ON THE PATHOGENESIS OF
SHOULDER IMPINGEMENT
SYNDROME
PEKKA
H YV ÖN E N
Division of Orthopaedic
and Trauma Surgery,
Department of Surgery,
University of Oulu
OULU 2003
PEKKA HYVÖNEN
ON THE PATHOGENESIS OF
SHOULDER IMPINGEMENT
SYNDROME
Academic Dissertation to be presented with the assent of
the Faculty of Medicine, University of Oulu, for public
discussion in the Auditorium 1 of the University Hospital
of Oulu, on May 2nd, 2003, at 12 noon.
O U L U N Y L I O P I S TO, O U L U 2 0 0 3
Copyright © 2003
University of Oulu, 2003
Supervised by
Professor Pekka Jalovaara
Reviewed by
Docent Jan-Magnus Björkenheim
Emeritus Professor Hiroaki Fukuda
ISBN 951-42-7025-8
(URL: http://herkules.oulu.fi/isbn9514270258/)
ALSO AVAILABLE IN PRINTED FORMAT
Acta Univ. Oul. D 725, 2003
ISBN 951-42-7024-X
ISSN 0355-3221
(URL: http://herkules.oulu.fi/issn03553221/)
OULU UNIVERSITY PRESS
OULU 2003
Hyvönen, Pekka, On the pathogenesis of shoulder impingement syndrome
Division of Orthopaedic and Trauma Surgery, Department of Surgery, University of Oulu, P.O.Box
5000, FIN-90014 University of Oulu, Finland
Oulu, Finland
2003
Abstract
The pathomechanism of the shoulder impingement syndrome has been under debat. Two main
theories of the pathogenesis of the disease exists; mechanical (extrinsic) and degenerative (intrinsic)
theory.
The purpose of this work was to evaluate the pathogenesis of impingement syndrome with five
studies that consentrate to aspects related to ethiopathology as outcome and recovery after surgery,
radiological diagnosis, immunohisto- and histopathology of subacromial bursa, and subacromial
mechanical pressures.
The good results of 14 shoulders of 96 operated with an open acromioplasty turned painful after
an average of 5 (2 - 10) years postoperatively and had developed 6 full-thickness and 4 partial rotator
cuff tears. Initially good result is not permanent in all cases, suggesting that a degenerative process is
involved in the pathogenesis of impingement syndrome.
Shoulder muscle strengths of 48 patients, who had undergone an open acromioplasty, restored to
near normal within one year after open acromioplasty, suggesting that mechanical compression plays
a role in the pathogenesis of impingement syndrome.
Variation in the shape of the acromion, evaluated in 111 patients and their matched controls by a
routine supraspinatus outlet view, is associated with impingement syndrome, but this association is
weak. Validity of this radiograph in the diagnosis of impingement syndrome is therefore a minor
adjunct to the other diagnostic methods.
The role of subacromial bursa in impingement syndrome was studied in 62 patients (33 tendinitis,
11 partial and 18 full-thickness RC tear) suffering from a unilateral impingement syndrome and 24
controls. Tenascin-C proved to be a more general indicator of bursal reaction compared to the
conventional histological markers, being especially pronounced at the more advanced stages of
impingement.
The local subacromial contact pressures measured in 14 patients and 8 controls with a
piezoelectric probe were elevated in the impingement syndrome, supporting the mechanical theory.
On the basis of this study, both mechanical and degenerative factors are involved in the
pathogenesis of impingement syndrome.
Keywords: ethiology, pathology, shoulder impingement syndrome, shoulder pain
To my loving wife and wonderful children
Acknowledgements
This study was carried out at the Division of Orthopaedic and Trauma Surgery with the
valuable assistance of the Departments of Radiology and Pathology at the University of
Oulu during the years 1996–2003.
I owe my deepest gratitude to Professor Pekka Jalovaara, M.D., Ph.D., for his touch
guidance and supervision, help in collecting the material and his phenomenal art of
writing research papers.
I am grateful to Docent Kari Haukipuro, M.D., Ph.D., Head of the Division of Surgery,
Anaesthesiology and Neurosurgery, Professor Tatu Juvonen, M.D., Ph.D., and the former
and present heads of the Department of Orthopaedic surgery, Professor Martti
Hämäläinen, M.D., Ph.D., and Docent Timo Niinimäki, M.D., Ph.D. They have given me
a chance to practise my scientific and clinical work in this clinic.
Docent Jaakko Puranen, M.D., Ph.D., has constantly inspired me with his comments
on the studies. His legendary skills in clinical and scientific work and strong character
have served as an example during my career.
I am indebted to my co-workers Sini Lohi, M.D., Docent Juhana Leppilahti, M.D.,
Ph.D., Tapio Flinkkilä, M.D., Physiotherapist Tuula Merinen, Harri Lehtiniemi, M.D.,
Docent Markku Päivänsalo, M.D., Ph.D., Docent Jukka Melkko, M.D., Ph.D., Professor
Veli-Pekka Lehto, M.D., Ph.D. and Professor Vilho Lantto D.Sc. (Tech). Their support,
co-operation and help have been invaluable during the studies.
My sincere thanks to Professor Hiroaki Fukuda, M.D., Ph.D., and Docent Jan-Magnus
Björkenheim, M.D., Ph.D., the official reviewers of this thesis for their most valuable
comments on the manuscript.
My orthopaedic colleagues and the registrars in our clinic have assumed responsibility
for clinical work during the time that I have spent on scientific work. I am deeply grateful
to them all, especially to my traumatologist friends Jukka Ristiniemi, M.D., and Martti
Lakovaara, M.D.
Vesa Jokinen, M.D., has stimulated my thinking and helped with many practical
matters during the studies and while writing the thesis.
My colleagues from the business world Teppo Linden, MD, Ph.D., and Olli Karhi,
M.D., and colleague from the private clinic Esa Jormakka M.D., have supported my
scientific work in practical ways. I am deeply grateful to them.
Physiotherapist Pekka Anttila, OMT, is my long-time friend, to whom I want to express
my gratitude for the valuable discussions on shoulder biomechanism.
Since the time we spent as commandos in the Finnish Army, my colleague Jukka
Kettunen, M.D., Ph.D., has been a source of inspiration with his magnificent art of
speech. In the same way has Antti Wäänänen, M.D. given to me his support. I thank you
both.
The name of this thesis is tangential to the ‘Humerus Club’. My partners in this club
have supported me mentally and encouraged me for years to complete my doctoral
studies honourably and in a good scientific manner. I owe my most humble gratitude to
them.
I am very much obliged to Sirkka-Liisa Leinonen, Lic.Phil., who carried out the
language check of the thesis with flexible service.
I am greatful to Pasi Ohtonen, M.Sc. for statistical anlyses and Ville Varjonen for
processing the final version of the manuscript.
Roope and Wille are my friends from Nokela. We grew up together and shared each
other’s lives. There is no way to think that you two have not been involved to this work. I
thank you both.
I thank the only true Finnish macho singer Reetu (Ilkka Sysimetsä), who has given me
the right tune during the late night hours at scientific work.
Mother, you have always believed in your son and given me your love. My deceased
father showed me the example of a hard-working man. I am grateful to you both as well
as to my brothers and sister.
My loving wife Sirpa has given me the true stars of our life — a wonderful son Otto
and a lovely little daughter Oona. This thesis has taken from us some valuable time of
being together, but it has never been more important to me than you three are. I dedicate
this work to you and will look into the future with devotion.
This work was supported by Finnish Foundation for Orthopaedic and Traumatologic
research, Foundation of Finnish Inventions and Oulu University.
Oulu, April 2003
Pekka Hyvönen
Abbreviations
CG
EGF
FVIII-RAG
Fi
Fr
FTG
HE
MRI
MW-U
PTG
RC
SOV
TG
control group
epidermal growth factor
factor VIII related antigen
Fischers exact test
Friedmans test
full-thickness tear group
hematoxylin eosinofil
magnetic resonance imaging
Mann-Whitney-U test
partial tear group
rotator cuff
supraspinatus outlet view
tendinitis group
List of original publications
This thesis is based on the following original articles, which are referred to in the text by
Roman numerals I–V:
I
Hyvönen P, Lohi S & Jalovaara P (1998) Open acromioplasty does not prevent the
progression of impingement syndrome to a tear. J Bone Joint Surg (Br) B-80:813–
816.
II
Hyvönen P, Flinkkilä T, Leppilahti J & Jalovaara P (2000) Early recovery of shoulder
isometric strengths after open acromioplasty in stage II impingement syndrome. Arch
Orthop Trauma Surg 120:290–293.
III
Hyvönen P, Päivänsalo M, Lehtiniemi H, Leppilahti J & Jalovaara P (2001)
Supraspinatus outlet view in diagnosis of stage II and III of impingement syndrome.
Acta Radiologica 42:441–446.
IV
Hyvönen P, Melkko J, Lehto V-P & Jalovaara P (2003) Involvement of subacromial
bursa as judged by Tenascin-C expression and histopathology in the impingement
syndrome of the shoulder. J Bone Joint Surg (Br) 85-B:299–305.
V
Hyvönen P, Lantto V & Jalovaara P (2003) Local pressures in the subacromial space.
(Submitted)
Contents
Abstract
Acknowledgements
Abbreviations
List of original publications
Contents
1 Introduction ...................................................................................................................17
2 Review of the literature .................................................................................................20
2.1 Anatomy of the shoulder.........................................................................................20
2.2 Impingement syndrome ..........................................................................................21
2.2.1 Anatomy of impingement syndrome ...............................................................21
2.2.2 Stages of impingement syndrome....................................................................23
2.2.3 Symptoms of impingement syndrome .............................................................23
2.2.3.1 Pain ...........................................................................................................23
2.2.3.2 Weakness and stiffness of the shoulder.....................................................24
2.2.4 Signs ................................................................................................................24
2.2.4.1 Impingement sign .....................................................................................24
2.2.4.2 Impingement test ......................................................................................24
2.3 Etiopathology of impingement syndrome...............................................................24
2.3.1 Biomechanical studies of impingement ...........................................................25
2.3.2 Factors of the intrinsic theory ..........................................................................25
2.3.2.1 Muscle dysfunction...................................................................................25
2.3.2.2 Overuse of the shoulder ............................................................................26
2.3.2.3 Degenerative tendinopathy .......................................................................26
2.3.3 Factors of the extrinsic (mechanical) theory....................................................27
2.3.3.1 Shape of the acromion ..............................................................................27
2.3.3.2 Glenohumeral instability ..........................................................................28
2.3.3.3 Disturbed scapulothoracic rhythm ............................................................28
2.3.3.4 Degeneration of the acromioclavicular joint.............................................29
2.3.3.5 Impingement by the coracoacromial ligament..........................................29
2.3.3.6 Coracoid impingement..............................................................................30
2.3.3.7 Os acromiale .............................................................................................30
2.3.3.8 Impingement on the posterosuperior aspect of the glenoid ......................30
2.3.4 Role of subacromial bursa in impingement syndrome.....................................31
2.3.4.1 Fibrosis .....................................................................................................31
2.3.4.2 Inflammation ............................................................................................32
2.3.4.3 Nerves and pain mediators........................................................................32
2.3.5 Surgery of the shoulder at stage II impingement syndrome ............................32
2.3.5.1 Operative technique of open acromioplasty .............................................32
2.4 Outcome after open acromioplasty .........................................................................33
2.5 Recovery of shoulder muscle strength after subacromial decompression ..............34
2.5.1 Measurement of shoulder muscle strengths.....................................................34
2.6 Plain radiography in the evaluation of acromial shape and subacromial space ......35
2.7 Tenascin-C as an indicator of tissue reactions ........................................................35
2.7.1 Tenascin-C expression in normal tissue...........................................................36
2.7.2 Tenascin-C expression in different pathological situations..............................36
2.8 Subacromial pressure..............................................................................................36
3 Aims of the study...........................................................................................................38
4 Material and methods ....................................................................................................39
4.1 Patients ...................................................................................................................39
4.1.1 Late results of open acromioplasty ..................................................................39
4.1.2 Recovery of shoulder muscle strengths ...........................................................39
4.1.3 Acromial morphology as analysed by supraspinatus outlet view ....................40
4.1.4 Bursal reaction in different stages of impingement syndrome evaluated
by tenascin-C expression and histology...........................................................40
4.1.5 Measurement of the subacromial pressure.......................................................40
4.2 Methods ..................................................................................................................41
4.2.1 Clinical follow-up and radiological examination of the rotator cuff ...............41
4.2.2 Measurement of shoulder muscle strengths.....................................................41
4.2.3 Technique of supraspinatus outlet view and true AP view...............................42
4.2.4 Analysis of roentgenograms ............................................................................43
4.2.5 Immunohistochemical and histological methods in the evaluation
of subacromial bursa........................................................................................46
4.2.5.1 Biopsies and preparation of samples.........................................................46
4.2.5.2 Tenascin-C expression ..............................................................................46
4.2.5.3 Thickness ..................................................................................................47
4.2.5.4 Fibrosis .....................................................................................................47
4.2.5.5 Vascularity ................................................................................................47
4.2.5.6 Hemorrhage ..............................................................................................47
4.2.5.7 Inflammatory cells ....................................................................................47
4.2.5.8 Evaluation of the samples .........................................................................47
4.2.6 Measurement of subacromial pressure ............................................................48
4.2.7 Statistical analysis............................................................................................48
5 Results ...........................................................................................................................49
5.1 Long-term results of open acromioplasty and rotator cuff pathology.....................49
5.2 Recovery of shoulder muscle strengths after open acromioplasty..........................50
5.2.1 Flexion.............................................................................................................50
5.2.2 Abduction ........................................................................................................51
5.2.3 External rotation ..............................................................................................51
5.3 Acromial morphology based on the supraspinatus outlet view...............................53
5.3.1 Length and thickness .......................................................................................53
5.3.2 Acromial slope and tilt.....................................................................................53
5.3.3 Types and acromial angle ................................................................................53
5.4 Reactions of subacromial bursa at the different stages of impingement
syndrome ................................................................................................................55
5.4.1 Tenascin-C expression .....................................................................................55
5.4.2 Fibrosis ............................................................................................................56
5.4.3 Thickness .........................................................................................................57
5.4.4 Vascularity .......................................................................................................58
5.4.5 Haemorrhage ...................................................................................................59
5.4.6 Inflammatory cells...........................................................................................59
5.4.7 Correlations between tenascin-C expression and histological findings ...........60
5.5 Pressures in different parts of the subacromial space .............................................60
6 Discussion .....................................................................................................................62
6.1 Methods ..................................................................................................................62
6.2 Long-term results of open acromioplasty and rotator cuff pathology.....................64
6.3 Pathogenesis of impingement syndrome ................................................................64
6.4 Recovery of shoulder muscle strengths after open acromioplasty..........................65
6.5 Acromial morphology evaluated by supraspinatus outlet view ..............................65
6.6 Reactions of subacromial bursa in different stages of impingement syndrome......66
6.6.1 Tenascin-C expression .....................................................................................66
6.6.2 Vascularity .......................................................................................................67
6.6.3 Fibrosis ............................................................................................................67
6.6.4 Inflammatory cells...........................................................................................68
6.6.5 Thickness .........................................................................................................68
6.6.6 Haemorrhage ...................................................................................................68
6.6.7 Subacromial bursa in the pathomechanism of the impingement syndrome.....69
6.7 Pressures in different locations of the subacromial space.......................................69
7 Conclusions ...................................................................................................................71
References
Original publications
1 Introduction
Over the past few decades, shoulder impingement syndrome has become an increasingly
common diagnosis (Uhthoff & Sarkar 1991). However, the syndrome was first described
in the early 20th century. In 1931, Meyer (Meyer 1931) proposed that tears of the rotator
cuff occurred secondary to attrition due to friction against the undersurface of the
acromion and described corresponding lesions on the undersurface of the acromion and
the greater tuberosity. However, he did not implicate the acromion directly. Codman, in
1934, defined the critical zone where most degenerative changes occur as the portion of
the rotator cuff located one centimetre medial to the insertion of the supraspinatus on the
greater tuberosity (Codman 1990). Armstrong introduced the term ‘supraspinatus
syndrome’ (Armstrong 1949).
Neer described subacromial impingement syndrome as a distinct clinical entity and
hypothesised that the rotator cuff is impinged upon by the anterior one third of the
acromion, the coracoacromial ligament and the acromioclavicular joint rather than by
merely the lateral aspect of the acromion. He also suggested that the part of the rotator
cuff that is impinged upon is at the insertion of the supraspinatus tendon on the greater
tuberosity (the impingement zone). The clinical diagnosis of impingement syndrome is
commonly based on findings called the impingement sign and the impingement test (Neer
& Welsh 1977). The patient’s history typically includes pain at night and positional
discomfort called ’painful arc’ (Calvert 1997). The clinical presentation may be
confusing, and it is important to differentiate subacromial impingement syndrome from
other conditions that may cause symptoms in the shoulder. Especially in young patients
and athletes who perform repeated overhead motions, the diagnosis of impingement
should be made with caution. In many cases, the primary diagnosis is subtle
glenohumeral instability, even though impingement and subacromial bursitis may be
evident (Uhthoff & Sarkar 1991).
Armstrong and Diamond (Diamond 1964) proposed that the condition should be
treated with total acromionectomy as described by Watson-Jones (Watson-Jones 1960).
McLaughlin and Asherman (McLaughlin 1994) developed lateral acromionectomy.
However, this procedure does not involve removal of the anterior portion of the
acromion, which is nowadays considered to be responsible for impingement, and it
necessitates detachment of a substantial portion of the deltoid origin (Bigliani & Levine
18
1997). Partial or complete resection of the acromion has also been reported to be a
promising method in the treatment of ‘rotator cuff syndrome’ (Michelsson & Bakalim
1977). On the other hand, the disappointing results of complete acromionectomy and
lateral acromionectomy prompted Neer to focus on the undersurface of the acromion as
the offending area (Neer 1972). He developed the technique of anterior acromioplasty,
which includes acromioclavicular resection arthroplasty when indicated, to correct
impingement by decompressing the subacromial space. This procedure has become the
’golden standard' for the treatment of impingement and has been associated with a high
percentage of satisfactory results (Neer 1972, Ha'eri & Wiley 1982, Neviaser et al. 1982,
Thorling et al. 1985, Post & Cohen 1986, McShane et al. 1987, Hawkins et al. 1988,
Bigliani et al. 1989, Sahlstrand 1989, Jalovaara et al. 1989, Bjorkenheim et al. 1990,
Stuart et al. 1990, Fu et al. 1991, Van Holsbeeck et al. 1992, Lindh & Norlin 1993,
Rockwood & Lyons 1993, Sachs et al. 1994, Frieman & Fenlin, Jr. 1995, Hartwig &
Burkhard 1996).
The fact that acromioplasty relieves the impingement pain suggests the importance of
the acromion in the aetiology of this disease. The shape and certain morphological angles
of the acromion have been presented to be associated with the pathogenesis of
impingement syndrome (Neer 1983, Aoki M et al. 1986, Bigliani et al. 1986, Toivonen et
al. 1995, Tuite et al. 1995). On the other hand, the mechanical aetiology of impingement
might be related to several other factors (Gruber 1863, Neer 1972, Kessel & Watson
1977, Gerber et al. 1985, Uhthoff et al. 1988, Jobe et al. 1989, Walch et al. 1992). These
numerous aspects are attributed to the extrinsic theory of impingement aetiology,
according to which the lesion appears purely mechanically.
The alternative for the mechanical theory of the aetiology of impingement syndrome is
called the intrinsic theory. Its central idea is that impingement syndrome occurs due the
degeneration of the rotator cuff tendons (Ozaki et al. 1988, Ogata & Uhthoff 1990,
Uhthoff 1996). Shoulder muscle dysfunction (Nirschl 1989) and overuse of the shoulder,
which causes microtrauma of the rotator cuff tendons (Uhthoff et al. 1987), are also
factors included in the intrinsic theory.
The relief of pain after subacromial decompression and the weakness of the shoulder
muscle suggest that mechanical pressure is an important factor in the pathogenesis of
impingement syndrome. Consequently, if impingement syndrome is due to increased
subacromial pressure (extrinsic force), the good outcome of subacromial decompression
should be permanent.
Shoulder muscle weakness is one of the signs associated with impingement syndrome.
It has been suggested that shoulder muscle strength is restored gradually after
subacromial decompression (Leroux et al. 1995), which could support the mechanical
aetiology of this disease. The recovery process has not been completely clear.
It is not known whether the primary cause of symptoms is associated with a lesion in
the tendon or a reaction in the bursa. At the microscopic level, increased cellularity and
vascularity in the bursa near the rotator cuff tear and increased fibrosis and presence of
inflammatory cells in the bursa in supraspinatus tendinitis have been reported (Uhthoff &
Sarkar 1991, Santavirta et al. 1992, Rahme et al. 1993, Kronberg & Saric 1997). Thus,
inflammation of the bursa has been suggested to be of importance as a source of pain in
this clinical entity (Thornhill 1985, Santavirta et al. 1992). However, the role of the
subacromial bursa in the pathology of impingement syndrome is not totally clear.
19
Widening of the subacromial space by acromioplasty (Neer 1972) relieves the
impingement pain, suggesting that increased subacromial pressure is involved in the
pathogenesis of impingement syndrome. Some studies have revealed high pressures in
the subacromial space (Sigholm et al. 1988, Regan & Richards 1990, Wuelker et al.
1995). Acromioplasty has been found to decrease the pressure (Nordt, III et al. 1999).
However, it has not been clear where exactly in the subacromial space the maximal
pressure occurs.
The purpose of our studies was to find out, firstly, how permanent the effect of
operative treatment for impingement syndrome is. Secondly, we wanted to discover how
the shoulder muscles recover during the first year after subacromial decompression. The
third matter of interest was the validity of the supraspinatus outlet view in the evaluation
of the acromial shape. The role of the subacromial bursa in the pathology of impingement
syndrome was studied in the fourth substudy, and in the last study, we tested the
assumption that subacromial pressure is elevated under the anterolateral acromion in
patients with impingement syndrome.
2 Review of the literature
2.1 Anatomy of the shoulder
The shoulder consists of three real joints. Most of the range of motion of the shoulder
occurs at the glenohumeral joint. The acromioclavicular and sternoclavicular joints
connect the shoulder to the trunk. In addition to these, the scapulothoracic space forms an
articular-like posterior connection to the trunk and the subacromial space, which consist
of the subacromial and subdeltoid bursa, acts like a joint (Fig.1.). The clavicle and the
scapula together suspend the upper limb from the trunk (Carr & Wallace 1997).
The three most visible structures of the scapula are the acromion, the coracoid process
and the spine. They are insertion areas for certain muscles of the shoulder. The trapezium
and deltoid muscles insert to the scapular spine and the acromion. Pectoralis minor,
coracobrachialis and the short head of biceps brachii insert to the coracoid process.
Supraspinatus, infraspinatus and subscapularis fossas are the scapular insertion areas of
muscles with corresponding names. Together with the teres minor muscle, their tendons
form the rotator cuff, which covers the humeral head. The medial margin of the scapula
includes the insertions of the levator scapulae and rhomboid muscles. The inferior angle
and lateral margin of the scapula serve as insertions of the latissimus dorsi, teres major
and minor and the long head of the triceps brachii muscle. The insertion of the long head
of the biceps brachii muscle is located intra-articularly in the superior part of glenoid rim.
The lateral third of the clavicle includes the insertions of the trapezium and deltoid
muscles and the trapezoid and coronal ligaments, which together form the
coracoclavicular ligament.
In addition to the articular surface, the humeral head has insertions of the rotator cuff
tendons, the greater tubercle for the supraspinatus tendon and the lesser tubercle for the
subscapularis tendon. The infraspinatus and teres minor muscles insert to the posterior
surface of the humeral head, and the tendon of the long head of the biceps brachii muscle
passes through the intertubercular groove over the humeral head.
21
2.2 Impingement syndrome
Impingement arises from mechanical compression of the rotator cuff centred primarily on
the supraspinatus tendinous insertion onto the greater tuberosity against the undersurface
of the anterior one third of the acromion (Neer 1983, Speer et al. 1991).
2.2.1 Anatomy of impingement syndrome
To understand the etiopathology of subacromial impingement, it is necessary to be
familiar with the anatomical characteristics of the subacromial space. Within this space, a
number of soft-tissue structures are situated between two rigid structures, of which the
inferior structures glide relative to the superior structures. The superior border (the roof)
of the space is the coracoacromial arch, which consists of the acromion, the
coracoacromial ligament and the coracoid process. The acromioclavicular joint is directly
superior and posterior to the coracoacromial ligament. The inferior border (the floor)
consists of the greater tuberosity of the humerus and the superior aspect of the humeral
head (Fig.1.).
22
Fig. 1. Coronal section of shoulder anatomy.
The mean height of the space between the acromion and the humeral head is 1.1
centimetres at 0 degree as seen on radiographs (Ellman 1990, Flatow et al. 1994).
Interposed between the two osseous structures are the rotator cuff (mostly the
supraspinatus tendon), the long head of the biceps tendon, the bursa and the
coracoacromial ligament. Therefore, the true height of this space is considerably less than
that seen on radiographs. Normally, the bursa facilitates the motion of the rotator cuff
beneath the arch.
23
2.2.2 Stages of impingement syndrome
Neer described the classical three stages of impingement (Neer 1983). Stage I with
oedema and haemorrhage of the bursa and cuff is typical in persons under twenty-five
years old. Stage II involves irreversible changes, such as fibrosis and tendinitis of the
rotator cuff, and typically occurs in patients who are twenty-five to forty years old. Stage
III is marked by partial or complete tears of the rotator cuff and usually is seen in patients
over forty years of age. Later, Neer divided impingement into outlet and non-outlet
lesions (Neer 1990). Outlet impingement occurs when the coracoacromial arch
encroaches on the supraspinatus outlet and non-outlet secondarily to thickening or
hypertrophy of the bursa or the rotator cuff tendons. Subsequently, Ellman {Ellman 1990
72 /id} described a new classification based on the depth of the lesion in the rotator cuff
tendons. A modification of Neer’s staging, presented by some other authors {Fukuda,
Mikasa, et al. 1983 224 /id}{Fukuda, Craig, et al. 1987 225 /id}{Olsewski & Depew
1994 68 /id}{Wright & Cofield 1996 227 /id}, correlates more with the treatment
options. This system classifies tendinitis and fibrosis with oedema and haemorrhage as
stage I, partial tears as stage II and full-thickness tears as stage III.
2.2.3 Symptoms of impingement syndrome
Most symptoms of impingement begin insidiously and have a chronic component that
progresses gradually during a period of several months. However, acute traumatic bursitis
may not completely resolve and may develop into an impingement lesion (Bigliani &
Levine 1997). Pain, muscle weakness, restricted ranges of motion and soft tissue crepitus
are generally present (Neer 1983).
2.2.3.1 Pain
Pain is the most common symptom of the shoulder impingement syndrome (Neer 1983,
Rockwood & Lyons 1993, McLaughlin 1994, Bigliani & Levine 1997). Night pain is
typical, and daytime pain is related to overhead activities (Calvert 1997). Pain that
originates from pathology in the subacromial region tends to be difficult to localise, is
usually felt in the deltoid region and often radiates to the arm as far as the elbow (Calvert
1997). It is usually elicited between 70 and 120 degrees of abduction (Bigliani & Levine
1997). This sector is called the ’painful arc’ (Calvert 1997).
24
2.2.3.2 Weakness and stiffness of the shoulder
Weakness and stiffness of the shoulder may also be present, but these symptoms are
usually secondary to pain (Bigliani & Levine 1997, Calvert 1997). Pain caused by the
impingement may also propagate weakness by reflex inhibition of the muscles and
wasting in the same fashion as the quadriceps becomes weak and wasted as the result of a
painful knee (Duke & Wallace 1997). However, it has been verified by isokinetic strength
measurements that prolonged impingement syndrome leads to a real decrease in shoulder
muscle strength (Leroux et al. 1994, Leroux et al. 1995).
2.2.4 Signs
2.2.4.1 Impingement sign
The impingement sign, as described by Neer (Neer 1983), is elicited by performing
passive shoulder flexion while preventing scapular rotation by pressing with a hand on
the acromion. This causes pain, as the greater tuberosity of the humerus impinges against
the acromion. Hawkins and Abrams modified this manoeuvre by rotating the humeral
head at 90° of anterolateral elevation to produce a similar effect (Hawkins & Abrams
1987).
2.2.4.2 Impingement test
In the impingement test, which is a continuation to the impingement sign, 5–10 millilitres
of local anaesthetic (Xylocain) is injected into the subacromial bursa. This causes relief
of the pain when the impingement sign is repeated (Neer 1983).
2.3 Etiopathology of impingement syndrome
Many causes have been proposed for subacromial impingement syndrome (Aoki M et al.
1986, Bigliani et al. 1986, Codman 1990, Bigliani et al. 1991, Edelson & Taitz 1992,
Burns & Whipple 1993, Hutchinson & Veenstra 1993, Davidson et al. 1995). These
factors can be broadly classified as intrinsic or intratendinous factors, which are related to
the intrinsic theory on the origin of impingement, and extrinsic or extratendinous factors,
which are related to the mechanical theory. They can be further characterised as primary
or secondary. A primary aetiology — either intrinsic or extrinsic — causes the
impingement process by decreasing the subacromial space or by causing a degenerative
25
process of the rotator cuff tendons (Duke & Wallace 1997). A secondary aetiology is the
result of another process, such as instability, neurological injury, tight posterior capsule of
the glenohumeral joint and muscle dysfunction (Bigliani & Levine 1997, Duke &
Wallace 1997). The net effect of secondary causes is usually an anterosuperior translation
of the humeral head, which causes impingement of the cuff against the coracoacromial
arch (Duke & Wallace 1997). The next chapters on the etiopathology of impingement
syndrome are in line with the review article of Bigliani and Levine (Bigliani & Levine
1997).
2.3.1 Biomechanical studies of impingement
Anatomical specimens (Nasca et al. 1984) and cadaveric models {Jerosch, Castro, et al.
1989 120 /id}(Wuelker et al. 1995) have been used to investigate the contact areas of the
subacromial space. However, the use of anatomical specimens by Nasca et al did not
allow direct clinical correlation. Wuelker et al (Wuelker et al. 1995) found that the peak
forces under the acromion occurred between 85 and 136 degrees of elevation, which
corresponds to the ‘painful arc’ sign. Equal results was detected in a stereophotogrammetric analysis of cadaveric shoulders by Flatow et al (Flatow et al. 1994).
They demonstrated that the acromial undersurface and the rotator cuff tendons are in
closest proximity between 60 degrees and 120 degrees of elevation at the anteroinferior
part of the acromion. With three-dimensional computer modelling, Zuckerman et al
(Zuckerman et al. 1992) showed that the volume of the subacromial space decreased
when the anterior part of the acromion was more prominent.
2.3.2 Factors of the intrinsic theory
2.3.2.1 Muscle dysfunction
It has been suggested that an intrinsic contractile tension overload on the muscle rather
than primary impingement is the major factor in the aetiology of rotator cuff tendinitis
(Nirschl 1989). When the arm is in the overhead position, eccentric contraction of the
supraspinatus decelerates internal rotation and adduction of the arm, causing an overload
(Bigliani & Levine 1997). This phenomenon is most dramatic in persons who go in for
overhead sports, and it may also occur in manual labourers who use overhead motions in
their work (Bigliani & Levine 1997). The proximal migration of the humeral head has
also been associated with muscle fatigue, injury and degenerative changes in the rotator
cuff tendons (Jerosch et al. 1989, Leroux et al. 1994). Bigliani et al (Bigliani & Levine
1997) point out that resection of the coracoacromial ligament should be avoided in this
26
situation because it may not relieve the impingement, but may allow for additional
proximal migration of the humeral head.
Decrease in proprioceptive sense with muscle fatigue may play a role in decreasing
athletic performance and in fatigue-related shoulder dysfunction (Carpenter et al. 1998).
Some functional analysis of rotator cuff muscles has shown disturbances in strength in
different pathological conditions, including impingement syndrome (Nirschl 1989,
Warner et al. 1990, Leroux et al. 1994). Imbalance of the rotator cuff muscles in athletes,
who have developed it as a result of training or sport activities, has generally been found
to be a predisposing factor or a consequence of impingement syndrome (McMaster et al.
1991, Burnham et al. 1993, Ticker et al. 1995). Brox et al (Brox et al. 1993) reported that
surgery and supervised exercise improved equally and significantly rotator cuff disease
compared with placebo, suggesting the importance of considering this factor.
2.3.2.2 Overuse of the shoulder
The diagnosis of overuse syndrome can be made after possible extrinsic factors related to
the coracoacromial arch that may contribute to the process has been ruled out (Bigliani &
Levine 1997). This syndrome also occurs commonly in young competitive athletes and
manual labourers who use overhead motions in their work (Bigliani & Levine 1997).
Inflammation resulting from repetitive microtrauma increases the area occupied by soft
tissues in the subacromial space and leads to friction and wear against the coracoacromial
arch (Uhthoff et al. 1988, Jobe et al. 1989, Ark et al. 1992, McCann & Bigliani 1994).
However, inflammation of the subacromial bursa may also result from a systemic disease,
such as rheumatoid arthritis (Steinfeld et al. 1994, Reveille 1997). The findings of
Soslowsky et al (Soslowsky et al. 2000) described in animal tendons changes that result
from overuse activity, and they are believed to occur in rotator cuff tendons, too.
2.3.2.3 Degenerative tendinopathy
Ozaki et al (Ozaki et al. 1988) studied the pathological changes on the undersurface of
the acromion as associated with tears of the rotator cuff in 200 cadaveric shoulders. After
radiographic and histological analysis, they found that, in the specimens with a partial
tear of the cuff, the undersurface of the acromion was almost intact. Although a lesion in
the anterior one third of the undersurface of the acromion was always associated with a
tear of the cuff, the reverse was not true. They concluded that the pathogenesis of most
tears is probably a degenerative process. Ogata and Uhthoff (Ogata & Uhthoff 1990)
suggested that tendon degeneration is the primary etiology of partial tears of the rotator
cuff, and that they might allow proximal migration of the humeral head, which could
result in impingement and lead to complete tears of the rotator cuff.
27
2.3.3 Factors of the extrinsic (mechanical) theory
2.3.3.1 Shape of the acromion
Acromial morphology and differences in the shape and slope of the acromion as a
potential source of symptoms in the shoulder has been observed in early history
(Hamilton 1875, Goldthwait 1909). Neer (Neer 1972) focused on the cause-and-effect
relationship between acromial morphology and subacromial impingement. He proposed
that variations in the shape and slope of the anterior aspect of the acromion were
responsible for subacromial impingement and associated tears of the rotator cuff. A spur
that apparently had been caused by tensile forces on the coracoacromial ligament was
also found to be protruding into the subacromial space (Bigliani & Levine 1997). Bigliani
and Morrison (Bigliani et al. 1986) studied 139 shoulders from seventy-one cadavers and,
on the basis of direct observations and lateral radiographs, identified three types of
acromial morphology: I = flat, II = curved and III = hooked. A higher prevalence of fullthickness tears of the rotator cuff was noted in association with type III acromions. In
another study, they (Morrison D.S. & Bigliani L.U. 1987) evaluated supraspinatus outlet
radiographs and found that 80 per cent of the eighty-two patients who had a tear of the
rotator cuff visible an arthrogram had a type III acromion.
In a study of 420 cadaveric scapulae, Nicholson et al (Nicholson et al. 1996) found
acromial morphology to be a primary anatomical characteristic that does not change with
age. However, the prevalence of spur formation significantly increased after fifty years of
age.
The classification system described by Bigliani et al (Bigliani et al. 1986) has been
cited widely in the literature, but investigators have recently questioned its reliability.
Zuckerman et al (Zuckerman et al. 1997) reported low interobserver reliability during the
evaluation of 110 anatomic specimens to determine acromial shape according to the
classification of Bigliani et al (Bigliani et al. 1986). Jacobson et al. (Jacobson et al. 1995)
also reported low interobserver reliability when the system was used to evaluate acromial
morphology as seen on supraspinatus outlet radiographs. They also questioned the
correlation between acromial morphology and tears of the rotator cuff. The classification
of acromial morphology on the basis of a subacromial outlet radiograph has been said to
be difficult because of individual differences in the supraspinatus outlet angle (Duralde &
Gauntt 1999). Some investigators have stated that fluoroscopic control is necessary for a
proper supraspinatus outlet view (Kitay et al. 1995, Liotard et al. 1998).
Wuh and Snyder (Wuh & Snyder 1992) modified the classification system of Bigliani
et al (Bigliani et al. 1986) by addressing the thickness as well as the shape of the
acromion. Three types of acromion were identified: type A ( < 8 mm), type B (8–12 mm)
and type C ( > 12 mm).
Toivonen et al (Toivonen et al. 1995) presented the measurement of acromial angle
(Fig.5.), which is in accordance with the hypothesis proposed by Morrison and Bigliani
(Morrison D.S. & Bigliani L.U. 1987) that there is an association between type III
acromions and tears of the rotator cuff. Aoki et al (Aoki M et al. 1986) studied 130
cadaveric shoulders and found that acromions with spur formation had a flatter slope and
28
were associated with increased pitting on the surface of the greater tuberosity. They also
showed that the prevalence of spurs in the subacromial space increased with advancing
age and noted a decreased alpha angle ( = acromial tilt)(Fig.6.) in the patients who had
impingement.
Acromial slope (Fig.4.) and length (Fig.7) have been studied by Edelson and Taitz
(Edelson & Taitz 1992), who found that the more horizontal the acromion is, the greater
are the degenerative changes. They also noted that increased degenerative changes were
associated with increased length of the acromion.
Rockwood and Lyons (Rockwood & Lyons 1993) pointed out the importance of the
extended anterior part of the acromion in impingement syndrome. The authors developed
a modified acromioplasty that includes resection of the anterior prominence of the
acromion at the level of the clavicle and removal of bone from the antero-inferior surface
of the acromion. The findings of Zuckerman et al (Zuckerman et al. 1992) also support
the theory that the anterior projection of the acromion is an important factor in the
development of tears in the rotator cuff.
2.3.3.2 Glenohumeral instability
Especially in young competitive athletes with symptoms of impingement, it is necessary
to consider underlying glenohumeral instability as the primary source of the problem
(Jobe et al. 1989). Glenohumeral subluxation may cause disturbances in the mechanics of
overhead motion, which may lead to secondary impingement (Glousman 1993). This
concept may explain why certain throwing athletes do not show improvement after
anterior acromioplasty (Jobe et al. 1989, Fu et al. 1991, Glousman 1993). The underlying
instability needs to be treated either with an exercise program designed to strengthen the
dynamic stabilisers or with operative intervention if the exercise program fails (Bigliani
& Levine 1997). The rotator cuff muscles are important dynamic stabilisers of the
glenohumeral joint. Electromyographic analysis shows that they are all active throughout
the act of elevation (Matsen & Arntz 1990).
2.3.3.3 Disturbed scapulothoracic rhythm
Sportsmen, typically throwing athletes and swimmers, who suffer from impingement
syndrome have been demonstrated to have dysfunction of the scapulothoracic muscles
(Fu et al. 1991, McMaster et al. 1991, Warner et al. 1992, Kamkar et al. 1993, Kibler
2000). The dynamic effect of weakness on the scapular muscles is best seen when the
serratus anterior muscle is involved (Duke et al. 1997). The inability to protract the
scapula gives rise to winging of the scapula when the arm is raised (Weiser et al. 1999).
Weak or unbalanced scapular muscles alter the scapulohumeral rhythm and place a
greater strain on glenohumeral articulation, which results in secondary extrinsic
impingement (Duke & Wallace 1997).
29
2.3.3.4 Degeneration of the acromioclavicular joint
Neer proposed that degeneration of the acromioclavicular joint may contribute to
subacromial impingement (Neer 1972, Neer 1983), and a number of other authors have
supported this hypothesis (Kessel & Watson 1977, Watson 1978, Petersson & Gentz
1983). Osteophytes that protrude inferiorly from the undersurface of a degenerative
acromioclavicular joint can contribute to impingement when the cuff passes beneath the
joint (Petersson & Gentz 1983). Kessel and Watson (Kessel & Watson 1977) found that
one third of the patients in their study had lesions of the supraspinatus tendon, usually
associated with degeneration of the acromioclavicular joint. Penny and Welsh (Penny &
Welsh 1981) subsequently found that osteoarthritis of the acromioclavicular joint may
lead to failure after operative treatment of subacromial impingement. However, resection
of the acromioclavicular joint should be performed only if the patient has symptoms in
the joint region and if osteophytes contribute to the impingement (Bigliani & Levine
1997).
2.3.3.5 Impingement by the coracoacromial ligament
A number of investigators (Neer 1972, Neer 1983, Uhthoff et al. 1988, Ogata & Uhthoff
1990, Burns & Whipple 1993, McLaughlin 1994) have implicated also the
coracoacromial ligament as a source of impingement. McLaughlin and Asherman
(McLaughlin 1994) observed the condition called “snapping shoulder” and concluded
that the coracoacromial ligament was an offending structure in painful shoulders. Neer
(Neer 1972, Neer 1983) included resection of the ligament as an integral part of the
anterior acromioplasty procedure. Some other authors (Hawkins & Kennedy 1980, Penny
& Welsh 1981, Ha'eri & Wiley 1982, Burns & Turba 1992) have reported that the
coracoacromial ligament is a major component in the painful arc syndrome and have also
recommended resection of the ligament. Burns and Whipple (Burns & Whipple 1993)
studied five cadavers and saw that impingement occurred predominantly against the
lateral free edge of the coracoacromial ligament. In a study comparing rotator cuff tear
with normal specimens, Soslowsky et al (Soslowsky et al. 1996) found statistically
significant changes in the geometric dimensions of the lateral band of the coracoacromial
ligament, which is the region most likely to impinge on the rotator cuff. In another study,
they found significant changes in the material properties (Soslowsky et al. 1994) of the
ligament. Sarkar et al (Sarkar et al. 1990) and Uhthoff et al (Uhthoff et al. 1988) reported
that histological studies of specimens of the coracoacromial ligament from patients who
had impingement syndrome revealed only degenerative changes without thickening. They
proposed that the stiffness of the coracoacromial ligament might contribute to
impingement in patients who have swelling of the subacromial soft tissues.
30
2.3.3.6 Coracoid impingement
Coracoid impingement along the more medial aspect of the coracoacromial arch is less
common, but it has been reported (Gerber et al. 1985, Dines et al. 1990, Friedman et al.
1998). In patients with coracoid impingement, the pain is usually located on the
anteromedial aspect of the shoulder and is referred to the arm and the forearm. Forward
elevation and internal rotation may elicit pain (Bigliani & Levine 1997). Friedman et al
(Friedman et al. 1998) used cine magnetic resonance imaging to measure the interval
between the coracoid process and the lesser tuberosity. In a symptomless control group,
the average interval between the coracoid process and the lesser tuberosity was eleven
millimetres, while in symptomatic patients, the interval was found to be six millimetres.
Gerber et al (Gerber et al. 1985) reported that coracoid impingement can be idiopathic,
iatrogenic or traumatic. As a choice for operative treatment, Dines et al (Dines et al.
1990) recommended coracohumeral decompression by excision of the lateral 1.5 cm of
the coracoid with re-attachment of the conjoined tendon.
2.3.3.7 Os acromiale
Os acromiale is an unfused distal acromial epiphysis, and it was first described in 1863
by Gruber (Gruber 1863). Folliasson (Folliasson 1933) classified the lesion into four
distinct types on the basis of anatomical location, with mesoacromion being the most
common type. The prevalence of os acromiale, as reported in both radiographic and
anatomical studies (Mudge et al. 1984, Edelson et al. 1993), has varied a great deal, with
a range of 1 to 15 per cent. It is difficult to detect an os acromiale on a routine
anteroposterior radiograph, and an axillary radiograph may thus be needed (Bigliani &
Levine 1997). An association between os acromiale and impingement syndrome (Bigliani
et al. 1983, Hutchinson & Veenstra 1993) and rotator cuff tears (Mudge et al. 1984) has
been reported. Impingement may occur because the unfused epiphysis on the anterior
aspect of the acromion may be hypermobile and may tilt anteriorly as a result of its
attachment to the coracoacromial ligament (Mudge et al. 1984). Hertel et al (Hertel et al.
1998) recommended stable fusion of a sizeable and hypermobile os acromiale.
2.3.3.8 Impingement on the posterosuperior aspect of the glenoid
During the past decade, another form of impingement seen in athletes who engage in
overhead activities has been reported (Walch et al. 1992, Davidson et al. 1995, Jobe
1995). Especially when the arm is placed in the throwing position (extension, abduction,
and external rotation), the rotator cuff is impinged on the posterosuperior edge of the
glenoid. Although this impingement is probably physiological, it becomes pathological in
these athletes because of the repetitive nature of the overhead activities and the potential
for increased contact secondary to fatigue of the muscles of the rotator cuff (Bigliani &
31
Levine 1997). The abnormal finding at arthroscopy is impingement on the
posterosuperior aspect of the glenoid (Davidson et al. 1995). Jobe (Jobe 1995) suggested
that anterior instability may contribute to posterosuperior impingement syndrome and
that this situation may injure one or more of the following: (1) superior labrum, (2)
rotator cuff tendon, (3) greater tuberosity, (4) inferior glenohumeral ligament or labrum
and (5) superior glenoid bone. Recently, Riand et al (Riand et al. 2002) noticed that
professional athletes, or ones competing at the international level, were not very satisfied
with the outcome of arthroscopic debridement.
2.3.4 Role of subacromial bursa in impingement syndrome
The subacromial bursa is commonly thought of as the culprit in impingement pain (Duke
& Wallace 1997). Codman stated at the beginning of the 19th century that ‘bursa like
peritoneum is secondarily involved’ (Codman 1990). The pain caused by intractable
impingement syndrome is often alleviated by a local cortisone injection into the
subacromial bursa, suggesting that inflammation of this tissue could be a source of the
impingement pain (Blair et al. 1996). Gotoh et al (Gotoh et al. 1998) found that an
increased amount of substance P in the subacromial bursa appears to correlate with the
pain caused by rotator cuff disease. At surgery, there are occasional signs of thickening,
inflammation, fibrosis or oedema in the subacromial bursa (Duke & Wallace 1997). At
the microscopic level, increased cellularity and vascularity in the bursa near the rotator
cuff tear and increased fibrosis and presence of inflammatory cells in the bursa in
supraspinatus tendinitis have been reported (Uhthoff & Sarkar 1991, Santavirta et al.
1992, Rahme et al. 1993, Kronberg & Saric 1997). Ide et al (Ide et al. 1996) stated that
the subacromial bursa is the major component of the subacromial gliding mechanism, and
they also concluded that the subacromial bursa receives nociceptive stimuli and
proprioception and seems to regulate appropriate shoulder movement. However, it is not
fully known whether the primary cause of impingement symptoms is associated with a
lesion in the tendon or a reaction in the bursa.
2.3.4.1 Fibrosis
The presence of increased subacromial bursal fibrosis has been found to correlate with
impingement syndrome and its removal has also predicted a better outcome after open
acromioplasty (Rahme et al. 1993, Kronberg & Saric 1997).
32
2.3.4.2 Inflammation
Inflammation of the bursa has been suggested to be of importance as a source of pain in
impingement syndrome (Thornhill 1985, Santavirta et al. 1992, Fukuda et al. 1994).
However, Uhthoff and Sarkar (Uhthoff & Sarkar 1991) showed no true acute
inflammatory changes in microscopical samples of bursa from patients with
impingement.
2.3.4.3 Nerves and pain mediators
Substance P is contained in primary afferent nerves, and its quantity increases during
chronic pain (Lembeck et al. 1981). Gotoh et al (Gotoh et al. 1998) noticed that patients
with an intact rotator cuff had more severe impingement pain than those with a torn
rotator cuff, and they also had increased amounts of substance P in the subacromial bursa.
Using special immunohistochemical stains and electron microscopy, Soifer at al (Soifer et
al. 1996) identified neural elements within the subacromial bursa, rotator cuff tendon,
biceps tendon and tendon sheath and transverse humeral ligament. There was a
significantly richer supply of free nerve fibres in the bursa compared with the other
tissues. Scattered free nerve endings were found throughout the subacromial bursae by
Vangsness et al (Vangsness, Jr. et al. 1995). They suggested that removal of symptomatic,
inflamed bursae might decrease pain signals from this part of the shoulder.
2.3.5 Surgery of the shoulder at stage II impingement syndrome
From the early 20th century until the 7th decade, the surgical procedure included quite
radical resection of the acromion. (Armstrong 1949, Watson-Jones 1960, Diamond 1964,
McLaughlin 1994) In the recent years, however, excessive removal of acromial bone has
been associated with complications and unsatisfactory clinical results (Neer & Marberry
1981, Bigliani et al. 1992). The development of surgical techniques has led to open (Neer
1972) or arthroscopic (Ellman 1987) anterolateral acromioplasty. If non-operative
treatment fails to reduce symptoms within six months, operative intervention may be
indicated. Anterior acromioplasty with resection of the coracoacromial ligament is the
preferred treatment (Neer 1972, Bigliani & Levine 1997).
2.3.5.1 Operative technique of open acromioplasty
Two types of incisions are recommended: bra-strap (or sabre) incision or coronal plane
incision along the deltoid muscle fibres (Duke et al. 1997). The first of these is more
cosmetic, while the second provides better access to the acromioclavicular joint and the
33
acromion. Deltoid split can be simple or more radical (Rockwood & Lyons 1993) if better
exposure of the acromion or concomitant acromioclavicular resection is needed. The
important thing is to leave enough good tissue to reattach the deltoid insertion (Bigliani &
Levine 1997, Duke et al. 1997). The coracoacromial ligament is most commonly divided
and partly resected, but because it has been thought to be an important superior support
structure, some recommend reconstruction or minor detachment during acromioplasty
(Duke et al. 1997). Neer proposed that the inferior part of the anterolateral acromion
should be resected (Neer 1972). It can be done with either a saw or an osteotome.
Rockwood modified acromial resection and recommends that the anterior projection of
the acromion should also be removed from the level of the anterior border of the clavicle
(Rockwood & Lyons 1993). It has been recommended (Kronberg & Saric 1997) that the
fibrotic, thickened bursa, which is the probable origin of the impingement pain (Gotoh et
al. 1998), should be removed (Rahme et al. 1993). However, the bursa may have a role in
regenerative processes, and it has been suggested therefore to be preserved (Codman
1990). Resection of the acromioclavicular joint is not routinely performed as part of
subacromial decompression and is indicated only when the joint is tender or when
inferiorly protruding excrescences or osteophytes contribute to the impingement (Bigliani
& Levine 1997). At the end of the operation, before the wound is closed, it is vital to
obtain good reattachment of the deltoid to the acromion (Duke et al. 1997).
2.4 Outcome after open acromioplasty
The results of open acromioplasty are difficult to interpret, partly because the criteria for
publication had not been carefully delineated at the time that many of the earlier studies
were conducted (Bigliani & Levine 1997). In the basic study of Neer (Neer 1972), the
outcome was considered satisfactory if the patient was satisfied with the operation, had
no pain and had less than 20 degrees of limitation of overhead elevation and at least 75
per cent of normal strength. A number of other investigators have also reported high
percentages of satisfactory results ranging from 85% to 95% in association with anterior
acromioplasty (Ha'eri & Wiley 1982) (90%) (Post & Cohen 1986) (89%) (Hawkins et al.
1988) (87%) (Daluga & Dobozi 1989) (94%) (Frieman & Fenlin, Jr. 1995) (97%)
(Rockwood & Lyons 1993) (87%). Some reports suggest that the outcome may be related
to the worker’s compensation status or pending litigation (Post & Cohen 1986, Hawkins
et al. 1988, Ogilvie-Harris et al. 1990). The same factor has also been found to be
predictive in cases with rotator cuff repair (Vastamaki 1986).
A higher percentage of unsatisfactory results has been reported in some other studies
(Thorling et al. 1985, Sahlstrand 1989, Bjorkenheim et al. 1990). Thorling et al (Thorling
et al. 1985), after an average follow-up of twenty months (range six to forty-two months),
reported that thirty-nine patients (76%) were satisfied with the outcome. The authors also
concluded that the prognosis is worse for patients who undergo concomitant resection of
the acromioclavicular joint. This tendency was not reported in another study (Daluga &
Dobozi 1989), in which resection of the acromioclavicular joint had also been performed
in every fourth of the cases. Sahlstrand (Sahlstrand 1989) reported, using another rating
34
scale after an average follow-up of only eleven months, that 77% of 52 cases had an
excellent or good outcome. Bjorkenheim et al (Bjorkenheim et al. 1990) used the
functional assessment of Neer (Neer 1972) and reported excellent or satisfactory results
in 73% of the cases after an average follow-up of forty-eight months. Tibone et al
(Tibone et al. 1985) reported, in a study of thirty-three athletes (thirty-five shoulders)
who were less than forty years old, an excellent or good outcome for only fourteen
patients (42%). The outcome was even worse for the athletes who were involved in
pitching or throwing, which may be due to primary instability of the shoulder (Jobe et al.
1989, Glousman 1993). However, Bigliani et al (Bigliani et al. 1989) reviewed
retrospectively twenty-six patients who were less than forty years old with an average of
33 months of follow-up after anterior acromioplasty for the treatment of subacromial
impingement syndrome. 96% of them reported subjective improvement after the
procedure. Seven of the ten recreational athletes had a satisfactory outcome.
2.5 Recovery of shoulder muscle strength after subacromial
decompression
Recovery of strength in the shoulder muscles after operative treatment of rotator cuff
tears has been found to be a slow process lasting for up to one year according to
isokinetic studies (Walker et al. 1987, Rabin & Post 1990, Rokito et al. 1996). Rabin and
Post (Rabin & Post 1990), who evaluated both rotator cuff tear patients (52) and subjects
with an intact rotator cuff (21), showed that muscle recovery does not correlate fully with
the clinical assessment, which shows early improvement. Endurance of the muscles may
decrease for a longer period. The results of Leroux et al (Leroux et al. 1995) indicate that
surgery restores the normal muscular balance between shoulder rotator muscles affected
by impingement syndrome.
2.5.1 Measurement of shoulder muscle strengths
Most studies have involved measurement of the strength of the rotator cuff muscles
isokinetically with slow (60°/sec) and fast (180°/sec) torque arm speed (Ivey, Jr. et al.
1985, Walker et al. 1987, Leroux et al. 1994, Holm et al. 1996). Leroux et al (Leroux et
al. 1995) made their measurements of postoperative scapular muscle functions after a
long (mean 44.5 months) period of follow-up following surgery for stage II and III
impingement syndrome, to avoid the possible effect of pain. Pain inhibition has turned
out to be significant in the isokinetic shoulder muscle testing (Ben Yishay et al. 1994).
Hand dominance does not have any significant effect on shoulder muscle strengths in
isometric measurements (Ivey, Jr. et al. 1985). Isometric measurement has been
considered an equally valid method of measuring the strength of the shoulder muscles as
isokinetic measurements (Gore et al. 1986, Kuhlman et al. 1992). Gore et al (Gore et al.
35
1986) carried out the measurements of internal and external rotation at abduction angles
of 0° and 90° (if possible), and measurements of abduction at angles of 45° and 90° (if
possible. However, Kuhlman et al (Kuhlman et al. 1992) recommended that the isometric
strength of external rotation should be measured at 45° of abduction and 45° of internal
rotation, and the strength of abduction in the scapular plane with the shoulder at 45° of
abduction.
2.6 Plain radiography in the evaluation of acromial shape and
subacromial space
Anteroposterior radiographs may help in identifying abnormalities, such as osteoarthritis
of the acromioclavicular joint, calcific tendinitis, evidence of glenohumeral instability
(osseous Bankart lesion or Hill-Sachs lesion), tumours and osteoarthritis of the
glenohumeral joint (Bigliani & Levine 1997). In making the diagnosis of subacromial
impingement, anteroposterior radiographs may show subchondral cysts or sclerosis of the
greater tuberosity with corresponding areas of sclerosis or spur formation on the anterior
edge of the acromion (Cone, III et al. 1984, Gold et al. 1993). An axillary radiograph
may be needed to diagnose an unfused acromial epiphysis (Os acromiale) (Edelson et al.
1993). Neer and Poppen (Neer & Poppen 1987) described the supraspinatus outlet view
(SOV), which is a lateral radiograph taken in the plane of the scapula with the x-ray beam
directed 10 degrees caudal. The supraspinatus outlet radiograph has been widely used in
the diagnosis of subacromial impingement. However, the findings may be difficult to
reproduce consistently because of thoracic kyphosis or superimposition of adjacent
osseous structures, such as the clavicle, ribs or scapular body (Bigliani & Levine 1997).
Variations of the supraspinatus outlet angle (Duralde & Gauntt 1999) and a high rate of
interobserver error (Jacobson et al. 1995) have been reported, suggesting inaccuracy of
SOV. Ono et al (Ono et al. 1992) described a 30-degree caudal tilt anteroposterior
radiograph that demonstrates the anteroinferior projection of the acromion. Andrews et al
(Andrews et al. 1991) suggested the use of a profile radiograph to facilitate evaluation of
the lateral aspect of the acromion.
2.7 Tenascin-C as an indicator of tissue reactions
Tenascin-C is a disulfide-bonded hexamer composed of subunits with molecular
weights in the range of 120–300 kD, depending on the expression of different
isoforms in different species. The subunits contain epidermal growth factor
(EGF)-like and fibronectin-like repeats commensurate with the growth-promoting
properties of tenascin-C (Engel 1989, Swindle et al. 2001).
36
2.7.1 Tenascin-C expression in normal tissue
Tenascin-C, the proteotypical tenascin, was originally isolated from embryonic tissues
(Chiquet-Ehrismann et al. 1986, Erickson & Bourdon 1989). It is the most widely
distributed tenascin and is typically seen only at sites of epithelial-mesenchymal
interaction in mature tissues. It is involved in various cellular functions, such as growth
promotion, hemagglutination, immunosuppression of T-cells, promotion of angiogenesis
and chondrogenesis. It also has an anti-adhesive effect on many cell types (Fischer et al.
1997).
2.7.2 Tenascin-C expression in different pathological situations
A high level of expression of tenascin-C in acute injury is well established, and it may
possibly play an important role in ensuring both inflammatory and reparative processes at
the site of injury (Mackie et al. 1988, Dalkowski et al. 1999). Prominent induction of
tenascin-C expression is seen in diverse reactive conditions, such as inflammation and
wound healing (Koukoulis et al. 1991), and in the stroma of various carcinomas (Mighell
et al. 1996, Riley et al. 1996, Kostianovsky et al. 1997, Lohi et al. 1998). The expression
of tenascin-C in different tissues varies, depending on the developmental stage of the
organism analyzed. It changes dramatically under various pathological conditions, such
as tumours, tendon degeneration, synovitis, colitis, colon adenoma and colorectal
carcinoma, pathological bone marrow and interstitial pneumonia (Erickson & Bourdon
1989, McCachren & Lightner 1992, Riedl et al. 1992, Soini et al. 1993, Riley et al. 1996,
Kaarteenaho-Wiik et al. 1996). Elevated expression of tenscin-C is seen in active
reparative processes, such as in wound healing, inflammatory lung diseases and keloids
(Mackie et al. 1988, Dalkowski et al. 1999, Kaarteenaho-Wiik et al. 2000).
2.8 Subacromial pressure
Subacromial contact pressure has been studied in cadaveric experiments {Jerosch, Castro,
et al. 1989 120 /id}(Regan & Richards 1990)(Wuelker et al. 1995). They found increased
pressures under the acromion and coracoacromial arch upon forward elevation, but few
clinical correlations emerged.
Sigholm et al (Sigholm et al. 1988) evaluated with the microcapillary infusion (MCI)
technique the pressure in the subacromial bursa in 30 shoulders in healthy volunteers.
Elevated bursal pressure was detected upon lifting up the arm, and it was more prominent
when a 1kg weight was held up. They found the MCI method also suitable for recording
pressure in the subacromial bursa during exercise. This method has not got much support,
because the subacromial space is not enclosed and the fluid pressure does not necessarily
37
reflect contact pressure (Nordt, III et al. 1999). Further, no local pressures can be
measured with this method.
The study of Nordt et al (Nordt, III et al. 1999) presents that subacromial pressures
were highest in the patients who had type III acromial morphology. They also pointed out
that fully abducted and cross-reach positions generate the highest impingement pressures.
Acromioplasty decreased significantly the anterolateral edge subacromial pressures.
There were technical difficulties with the catheter placement, and no measurement was
possible in active movements.
3 Aims of the study
The studies of the thesis focused on the pathogenesis of impingement syndrome. The aim
was:
1. to assess whether the outcome of open acromioplasty is permanent in the long run,
supporting the mechanical theory, or whether the outcome deteriorates over time,
indicating a degenerative pathomechanism.
2. to evaluate if the strength of the shoulder muscles is restored soon after open
acromioplasty, indicating the relief of mechanical or pain inhibition, or whether the
muscles remain deteriorated, indicating a more permanent lesion.
3. to study if the shape of the acromion evaluated by plain radiography is related to the
impingement syndrome and its stages, which would be in line with the mechanical
theory.
4. to investigate the role of the subacromial bursa in the pathogenesis of impingement
syndrome using tenascin-C expression and histological findings as parametres of
tissue reaction.
5. to study if the pressure conditions and distribution in subacromial space are altered in
shoulders with impingement in accordance with the mechanical theory.
4 Material and methods
4.1 Patients
4.1.1 Late results of open acromioplasty
The study population consisted of the 102 patients who had had open acromioplasty
during 1977–1986 for chronic (6–180 months, mean 39 months) impingement syndrome
(Neer 1983, Hawkins et al. 1988, Jalovaara et al. 1989). Two of them subsequently died,
and 7 patients could not be reached for the study. Thus, 96 shoulders (36 female, 60 male;
62 right, 34 left; 67 dominant, 23 non-dominant, 6 ambidextrous, 3 bilateral) of 93
patients with a mean age at operation of 45 years (26–69) were available for the study.
4.1.2 Recovery of shoulder muscle strengths
Recovery of the strength of the shoulder muscles was studied in 48 patients (21 female,
27 male). Their mean age was 44 years at operation (range 18–58), and they had
undergone open acromioplasty because of stage II impingement syndrome between 1989
and 1994. No prior surgery or pain in the opposite shoulder was reported. All patients (45
right-handed, 3 ambidextrous, 31 dominant, 17 non-dominant) had a positive
impingement test (Neer 1983) and an aggravated impingement sign (Neer 1983, Hawkins
et al. 1988) preoperatively. There were no signs of rotator cuff tear in ultrasonographic
examination (35 cases), arthrography (17 cases), MRI (3 cases) and open surgery.
40
4.1.3 Acromial morphology as analysed by supraspinatus outlet view
Supraspinatus outlet view (Neer & Poppen 1987) and standard shoulder roentgenograms
were taken before surgery from 137 shoulders (133 patients) with stage II or stage III
impingement syndrome. None of the patients had had prior subacromial surgery. Staging
of the impingement syndrome was based on findings in open (111 cases) or arthroscopic
surgery (28 cases). Ninety cases presented with tendinitis-stage impingement syndrome
(stage II) and 47 with a full-thickness rotator cuff (RC) tear (stage III). Twenty-six SOVs
(16 in the tendinitis group and 10 in the RC tear group) were excluded because of
inadequate quality. Thus, 111 shoulders (74 stage II and 37 stage III) were available for
study. For controls, similar roentgenograms were obtained from both shoulders of 75
voluntary patients and 84 members of hospital staff who had had no shoulder problems or
shoulder surgery. After excluding 5 control SOVs because of inadequate quality, the
SOVs of 313 shoulders were available for matching.
4.1.4 Bursal reaction in different stages of impingement syndrome
evaluated by tenascin-C expression and histology
Tissue samples were taken from the subacromial bursa during open subacromial surgery
of 62 patients (39 males, mean age 47, range 26 to 70 years, and 23 females, mean age
50, range 37 to 70 years) suffering from unilateral impingement syndrome. Thirty-three
of these patients had tendinitis (11 females and 22 males, mean age 43, range 26 to 54
years, tendinitis group = TG). Eleven had a partial (2 joint side, 7 bursal side and 2
intratendinous) tear (3 females and 9 males, mean age 50, range 35 to 70 years, partial
tear group = PTG). Eighteen had a full-thickness rotator cuff tear (9 females and 9 males,
mean age 55, range 45 to 67 years, full-thickness tear group = FTG). The preoperative
duration of symptoms of positional discomfort and night pain was more than six months
in all cases.
Tissue samples were also taken from 20 shoulders of 12 cadavers (10 males and 2
females, mean age 49, range 35 to 76 years). The samples from three shoulders were
excluded due to a partial joint side tear and one due to a shoulder prosthesis. In addition,
bursal biopsies were taken from the shoulders of four males operated on for traumatic
acromioclavicular joint dislocation (mean age 36, range 26 to 44 years) who had not had
any previous shoulder problems. The samples of these two groups were combined and
served as a control group = CG (N = 24, mean age 46, range 26 to 76 years).
4.1.5 Measurement of the subacromial pressure
Measurement of local subacromial contact pressures was done on 14 patients (7 male, 7
female; mean age 45 years; range: 33 to 55 years) who underwent acromioplasty for stage
41
II impingement syndrome (Neer 1983). Eight patients (7 male, 1 female; mean age 36,
range 27 to 45 years) undergoing surgery for complete acromioclavicular dislocation
{Jalovaara, Paivansalo, et al. 1991 195 /id}, of which 7 were acute and one chronic,
served as controls.
4.2 Methods
4.2.1 Clinical follow-up and radiological examination of the rotator cuff
At follow-up a mean of nine (6–15) years after open acromioplasty, a single investigator
performed the clinical examinations and interviewed the patients. The subjective outcome
was evaluated by using the method described by Thorling et al (Thorling et al. 1985).
Ultrasound examination and routine x-rays were performed on all shoulders. Magnetic
resonance imaging (MRI) and/or single contrast arthrography were performed if there
were any signs of RC pathology in the ultrasound examination or if the shoulder was
painful (subjective outcome poor or fair).
4.2.2 Measurement of shoulder muscle strengths
Isometric strengths of flexion (Fig. 2a), abduction (Fig. 2b) and external rotation (Fig. 2c)
were measured by a single physiotherapist at less painful 0° of flexion and abduction of
the shoulder and at 90° flexion of the elbow preoperatively (n = 25) and three months
(n = 33), six months (n = 13) and one year (n = 43) postoperatively. After warming up by
performing the maximal range of motions, the patient was familiarised with the
equipment and three attempts at maximal isometric contraction were made for each
muscle group, with a brief rest between the attempts. The means of these values were
used for analysis. In order to prevent associated movement of the trunk during strength
testing in an upright position, the patients were stabilised with a strap around the chest.
An isometric force meter was used (Newtest Force, Newtest Co. Oulu, Finland) (Fig.
2a–c).
42
Fig. 2. Force meter and the positions of measurements: a flexion, b abduction, c external
rotation (photography by Hannu Marjamaa)
4.2.3 Technique of supraspinatus outlet view and true AP view
The supraspinatus outlet view (Neer & Poppen 1987) was obtained in a standing position,
with the patient facing the film and the coronal shoulder line turned outwards 45 degrees.
The arm of the involved side was in a neutral position. The x-ray beam was pointed along
43
the scapular axis with a 15° caudal tilt (Rockwood et al. 1990). The tube-screen distance
was 100 cm, and the x-ray voltage was usually 60–65 kV.
The true anteroposterior radiographs were obtained by angling the x-ray beam 45°
from medial to lateral (Rockwood et al. 1990).
4.2.4 Analysis of roentgenograms
Supraspinatus outlet views were first classified for acromion morphology as type I (flat),
II (curved) or II (hooked) solely on the basis of the criteria established by Bigliani et al
(Bigliani et al. 1986) (Fig. 3).
Fig. 3. Three types of acromion. (From Bigliani L.U.: Impingement syndrome, Aetiology and
overview. In: Surgical disorders of the shoulder, p.237. Edited by M.S. Watson. Churchill
Livingstone, New York 1991.) A) Flat = Type I. B) Curved = Type II. C) Hooked = Type III.
44
The acromial shape (curvature) was also evaluated by measuring the acromial slope as
described by Bigliani et al (Bigliani et al. 1986) and Kitay et al (Kitay et al. 1995) (Fig.
4).
Fig. 4. Measurement of acromial slope (δ). A = anteroinferior point of the acromion.
B = posterioinferior point of the acromion. D = middle point of the inferior surface of the
acromion. δ = slope angle.
In addition as a method of quantitating the shape of the anteroinferior acromion, the
acromial angle (α) was measured as described by Toivonen et al (Toivonen et al. 1995)
Fig. 5. Measurement of the acromial angle (α). A and B as in fig. 3. C = turning point
(junction) of the inferior surface of the hooked acromion. α = acromial angle.
45
Measurement of acromial posture in relation to the scapula was based on the method
described by Aoki et al (Aoki M et al. 1986) and Kitay et al (Kitay et al. 1995) (Fig. 6).
Fig. 6. Measurement of acromial tilt angles (β and γ). A and B as in Figs. 3 and 4. E = inferior
coracoid curve. F = inferior tip of the coracoid process. β and γ = tilt angles.
The length of acromion was measured between the most anterior and posterior points of
the acromion, and the thickness of the acromion was measured from two points: the
anterior part and the middle acromial body (Fig. 7).
Fig. 7. Measurements of acromial dimensions. Length: Distance between the points A (most
anterior) and B (most posterior) of the acromion. Thickness of the anterior (line 1) and
middle (line 2) parts of the acromion.
The true AP views were examined to rule out malignancies, rotator cuff arthropathy and
advanced osteoarthritis of the glenohumeral and acromioclavicular joints, but no cases
had to be excluded for these.
46
4.2.5 Immunohistochemical and histological methods in the evaluation
of subacromial bursa
4.2.5.1 Biopsies and preparation of samples
The specimens for examinations of the subacromial bursa were take at open
acromioplasty (Neer 1983) during acromioclavicular reconstruction (Jalovaara et al.
1991) or at autopsy. The deltoid muscle was detached from the anterior part of the
acromion, and the samples were taken from the deltoid side of the subacromial bursa. For
histological and immunohistochemical investigations, the tissue samples were fixed in 10
percent neutral formalin and embedded in paraffin. 5-µm thick sections were cut and
stained with hematoxylin and eosin and Herovici stains.
4.2.5.2 Tenascin-C expression
Tenascin-C expression was determined by an immunohistochemical method. The 5-µm
thick sections were deparaffinised in xylene and rehydrated in graded alcohol. The
endogenous peroxidase was consumed by incubating the sections in 0.3% hydrogen
peroxide in absolute methanol for 30 min. The sections were then treated with 0.4%
pepsin (Merck, Darmstadt) at 37°C for 30 minutes. To visualise tenascin, a monoclonal
mouse antibody to human tenascin (143DB7) was employed (Tiitta et al. 1992). In order
to visualise the microvasculature, a rabbit antibody to human anti-factor VIII related
antigen (FVIII-RAG), a well-established marker for endothelial cells (Miettinen et al.
1983) (Dako A/S, Glostrup, Denmark), was used. The sections were incubated with the
primary antibody at 4°C overnight, followed by biotinylated rabbit anti-mouse IgG
antibody (to visualise tenascin) and biotinylated goat anti-rabbit IgG (to visualise FVIIIRAG). As a further amplification step, the avidin-biotin peroxidase complex (Dako A/S,
Glostrup, Denmark) was applied. The peroxidase reaction was developed with
diaminobenzidine. Thereafter, the sections were counterstained with a light hematoxylin
stain, mounted in an aqueous medium and overlaid with glass coverslips for viewing
under a light microscope. Agfapan 400 film was used for recording the images. The
amount of tenascin-C in the tissue was determined by analysing anti-tenascin-stained
tissue sections. The evaluation was done on a semiquantitative scale ranging from 1 to 3,
corresponding to the abundance of tenascin-C seen in the samples with a minimum
amount ( = 1, < 33% of the area of the specimen), an intermediate amount ( = 2, 33–66%)
and a maximal amount ( = 3, > 66%).
47
4.2.5.3 Thickness
The thickness of the bursal tissue was estimated visually under a microscope by using a
semiquantitative scale: 1 = normal, 2 = moderately thickened, 3 = markedly thickened.
4.2.5.4 Fibrosis
A semiquantitative scale ranging from 0 = no fibrosis to 1 = moderate and 2 = extensive
fibrosis was used to estimate the extent of fibrosis in the bursa. This was based on an
evaluation of the histological sections in which reactive fibrosis could be identified,
especially in Herovici stain.
4.2.5.5 Vascularity
The assessment of the degree of vascularity and neovascularisation was based on
immunohistochemical staining with anti-FVIII-RAG antibodies. The abundance of
vasculature was estimated based on the number of FVIII-RAG-positive vascular profiles
projected on a semiquantitative scale of 1 to 3, as described for tenascin.
4.2.5.6 Hemorrhage
The degree of hemorrhage was estimated based on a microscopic examination of HEstained sections on a scale of 1 to 3, as described for tenascin.
4.2.5.7 Inflammatory cells
The degree of inflammatory cell reaction was based on an examination of HE-stained
sections and evaluation on a scale ranging from 1 to 3, as described for tenascin.
4.2.5.8 Evaluation of the samples
Two pathologists evaluated the immunohistochemical stainings independently, and a
consensus was negotiated in the cases where their opinions differed.
48
4.2.6 Measurement of subacromial pressure
The pressures of the subacromial space were recorded from four locations in the
subacromial space (Fig.8.). 1) Anterolateral; tip of the acromion as close to the borders as
possible, 6 mm from the lateral and anterior borders. 2) Anteromedial; 6 mm distal to the
acromioclavicular joint and posterior to the anterior border of the acromion. 3)
Posterolateral; 25 mm posterior to point 1. 4) Posteromedial; 25 mm posterior to point 2.
Fig. 8. Points of subacromial pressure measurements.
At each measurement point, the recordings were made with the arm abducted in the
coronal plane at 0°, 30°, 60° and 90°. An assisting person achieved the positions of the arm
passively without any traction.
4.2.7 Statistical analysis
The results were analysed by SPSS versions 8.0 (I–IV) or 10.0 (V) for Windows (SPSS
Inc., Chicago, Illinois). Student's t-test (I–III and V) for paired samples, Fisher’s exact
test (IV and V), Mann-Whitney U-test (V) and Friedman’s non-parametric test (V) were
used in the statistical analysis. Non-parametric Kendall’s correlation coefficient was
calculated in the bivariate correlation analysis (IV). Because the data of study V included
excess zeros, the two-part model described by Lachenbruch {Lachenbruch 2002 229 /id}
was applied. Fisher’s exact (Fi) test was used for dichotomous data and Student’s t-test or
Mann-Whitney U-test (MW-U) for continuous data. Friedman’s non-parametric test (Fr)
was used to compare the differences between different locations, where the recordings at
all abduction angles were considered. A level of p < 0.05 was used to determine
significant differences.
5 Results
5.1 Long-term results of open acromioplasty and rotator cuff
pathology
The overall subjective outcome was excellent in 45, good in 24, fair in 18 and poor in 9
shoulders. Nineteen (20%) RC tears were found (Table 1.), twelve of which were
complete. Six cases were diagnosed by using MRI + ultrasound, 2 cases by using MRI +
ultrasound + arthrography, 3 cases by using ultrasound + arthrography and 1 case by
using MRI + arthrography. The 5 joint side partial RC tears and the 2 bursal side partial
RC tears were diagnosed by ultrasound and MRI. Rotator cuff tears were more common
in men (25%) (N = 60, mean age at operation 45 (26 to 69) years) than in women (11%)
(N = 36, mean age at operation 46 (27 to 61) years) (Table 1.). The tear rate was higher in
the groups with fair and poor results than in those with good and excellent results, being
4% in excellent, 25% in good, 33% in fair and 55% in poor cases (Table 1). Ultrasound
showed signs of partial RC tear in 4 more shoulders with a good or excellent outcome.
Three subjects refused further examination (not counted as RC tear here), and one had no
pathological findings in MRI. The mean age at the time of the operation in the 12 cases
with a total RC tear had been higher (mean 50, range 37–58) compared to the 7 cases
with a partial RC tear (mean 45, range 37–54) (p = 0.090) or to the remaining 77 affected
shoulders (mean 45, range 26–69) (p = 0.034).
Fourteen shoulders initially symptom-free after acromioplasty (mean age at operation
46 years (range 34 – 57) turned painful at an average of 5 (2 – 10) years postoperatively.
The subjective outcome for 6 of these shoulders was still good, however, while 6 had a
fair and 2 a poor outcome. Six shoulders (3 good, 3 fair) had a complete tear and 4 (2
good, 2 poor) a partial tear (71%) (Table I).
In 4 patients, no rotator cuff tear could be detected in US. Two of them refused further
examinations and the reason for impairment thus remained obscure. One shoulder (fair)
displayed a marked spur at the inferior margin of the acromion and thinning of the
supraspinatus tendon in MRI, while the other (fair) had developed marked osteoarthritis
and the patient had had shoulder hemiarthroplasty 8 years after acromioplasty.
50
Table 1. Mean (range) Constant functional shoulder scores and ages of the patients in
the different groups and respective pain-free unaffected shoulders (controls).
Affected shoulders
Mean Constant score
Number of
(range)
cases
All cases
Gender
Male
Female
Rotator cuff tear
None
Partial
Total
Surgical technique
Excision of
distal clavicle
No clavicular
resection
Initial outcome
Excellent
Good
Fair
Poor
Late outcome
Deteriorated
Unaffected shoulders
Mean Constant score
Number of
(range)
controls
70 (24–100)
96
84 (74–98)
48
74 (26–100)
64 (24–90)
60
36
87 (74–98)
80 (76–86)
30
18
73 (24–100)
64 (26–91)
59 (33–88)
77
7
12
85 (77–98)
85 (81–92)
83 (74–98)
40
4
7
61 (32–100)
21
81 (76–87)
12
72 (24–98)
75
85 (74–98)
36
82 (55–100)
66 (33–86)
52 (26–71)
49 (24–87)
45
24
18
9
86 (77–98)
84 (74–94)
83 (76–96)
82 (79–84)
20
14
10
4
60 (36–84)
14
87 (79–96)
6
5.2 Recovery of shoulder muscle strengths after open acromioplasty
5.2.1 Flexion
The mean preoperative flexion strength of the involved shoulder was 72.6% of that of the
uninvolved shoulder and increased to 77.1% by the third postoperative month, to 88.3%
by the sixth and by the 12th month (Table 2.). The difference was statistically significant
between the preoperative condition and that at 12 months (p = 0.04). Recovery was more
distinct when the poor cases (n = 7) were not included in the analysis, the difference
being significant at six (p = 0.02) and 12 months (p = 0.01). The strengths of male
shoulders showed no statistically significant recovery, but in the female shoulders the
difference between the preoperative condition and that at six months (p = 0.02) and 12
months (p = 0.01) was statistically significant.
51
5.2.2 Abduction
The recovery of abduction strength in the whole group showed a similar trend compared
to flexion (Table 2.). The difference between the preoperative and 12-month results was
statistically significant (p = 0.01). Here, too, recovery was more distinct and already
significant after three months, when the poor cases (n = 7) were excluded from analysis.
No significant recovery was observed in the male shoulders. In the female shoulders, the
difference in abduction strength between the preoperative condition and that at six
months (p = 0.01) and 12 months (p = 0.00) was statistically significant.
5.2.3 External rotation
In the whole group, the recovery of external rotation strength was statistically significant
between the preoperative condition and that at six months (p = 0.04) and 12 months
(p = 0.03), (Table 2.). Again, recovery was more distinct when only the cases with
satisfactory outcome (n = 41) were considered. The recovery of male shoulders was not
statistically significant, but female shoulder strength increased significantly between the
preoperative condition and that at 12 months (p = 0.02).
52
Table 2. Shoulder strengths in the different groups preoperatively and at different times
postoperatively. Values are percentages of the uninvolved sides. (n = number of
observations)
n
mean
Flexion
SD
mean
Abduction
SD
External rotation
mean
SD
25
14
11
22
72.6%
82.8%
60.5%
68.6%
31.4
27.9
32.7
29.3
68.4%
78.9%
55.0%
63.7%
30.0
29.2
26.5
26.7
75.1%
77.5%
72.1%
72.1%
29.9
25.4
35.8
30.5
3
10.,7%
36.3
102.6%
35.9
97.6%
8.9
33
20
14
29
77.1%
83.2%
68.3%
78.0%
26.4
20.1
31.5
24.3
80.4%
86.2%
72.9%
84.0%
40.0
43.8
31.6
(p = 0.05) 40.0
77.4%
82.2%
69.9%
76.4%
26.7
18.7
33.9
26.0
4
71.6%
37.9
61.9%
32.3
82.2%
30.7
13
7
6
11
88.3%
80..0%
98.0% (p = 0.02)
90.7% (p = 0.03)
21.0
22.2
16.2
18.5
88.7%
80.7%
98.0%
94.0%
33.4
41.0
(p = 0.01) 21.4
(p = 0.01) 33.4
95.15
88.4%
102.8%
99.2%
(p = 0.04) 20.5
21.4
18.2
(p = 0.01) 19.5
2
74.8%
38.3
59.1%
12.8
72.6%
8.4
43
23
20
39
88.3% (p = 0.04)
86.6%
90.3% (p = 0.01)
92.7% (p < 0.01)
27.4
27.4
27.8
24.3
91.0%
86.3%
96.5%
92.7%
(p = 0.01) 34.4
39.4
(p < 0.01) 27.6
(p < 0.01) 24.3
95.5%
87.5%
100.4%
99.3%
(p = 0.03) 27.4
31.0
(p = 0.02) 27.3
(p < 0.01) 24.0
4
45.8% (p = 0.04) 17.7
40.3%
(p = 0.02) 13.9
36.5%
(p = 0.01) 16.5
Preoperative
All cases
Male
Female
Poor not
considered’
Poor
3 month
All cases
Male
Female
Poor not
considered’
Poor
6 month
All cases
Male
Female
Poor not
considered’
Poor
12 month
All cases
Male
Female
Poor not
considered’
Poor
p-values indicate the significance in comparison with the preoperative percentage
* = Cases with at least satisfactory outcome
53
5.3 Acromial morphology based on the supraspinatus outlet view
5.3.1 Length and thickness
The mean values of the length of the acromion varied from 47.1 to 50.3 mm, showing no
differences between the patients and the controls (Table 3.). The mean thickness of the
acromion was 7.8 mm in the patients with the tendinitis stage and 7.6 mm in their
controls and 8.0 mm and 7.8 mm in the patients with the tear stage and in their controls,
the differences being not significant (Table 3.).
5.3.2 Acromial slope and tilt
The mean acromial slope was 29.2° in the tendinitis stage group, 30.1° in the respective
controls and 30.4° and 31.2° in the tear stage group and their controls, but the differences
were not significant (Table 3.). The mean acromial tilt values varied from 31.7° to 33.5°,
displaying no significant differences between the study groups and their controls (Table
3.).
5.3.3 Types and acromial angle
There were no significant differences in the distribution of different types of acromion
between the groups evaluated according to Bigliani et al (Bigliani et al. 1986) (Table 4.).
However, there were more type III acromions in the patient groups than in their controls.
Type II acromion was the most common type in the patients and their controls,
accounting for 70.2–86.5%, whereas flat acromion was a rare finding. There was no
significant difference in the acromial angle between the tendinits group and the control
group, but the acromial angle was significantly greater in the rotator cuff tear group than
in the control group (p = 0.03) (Table 3.).
54
Table 3. Parameters of acromial morphology examined in the different groups.
Tendinitis stage group
(n = 74)
patients
controls
mean SD mean SD
Length (mm)
Thickness (mm)
Middle
Anterior
Slope (°)
Angle (°)
Tilt (γ angle) (°)
Tear stage group
(n = 37)
patients
controls
mean SD mean SD
All
(n = 111)
patients
controls
mean SD mean SD
47.7
6.9
47.7
5.9
50.3
6.6
47.1
6.2
48.6
6.9
47.5
6.0
7.8
10.3
29.2
33.2
33.5
1.7
2.0*
9.8
9.5
5.3
7.6
9.6
30.1
34.7
34.5
2.0
1.6
9.7
9.9
5.1
8.0
10.6
34.0
38.6
33.2
1.5
1.4
9.5
9.3**
4.7
7.8
10.4
31.2
33.9
31.7
1.7
2.0
7.8
8.2
6.3
7.9
10.0
30.8
35.1
33.4
1.7
1.6
9.9
9.8
5.1
7.9
10.3
31.0
34.5
33.5
1.6
2.0
9.1
9.3
5.6
*p = 0.02
**p = 0.03
Table 4. Types of acromions in the different groups
Tendinitis stage group
(n = 74)
n patients n controls
%
%
Flat
Curved
Hooked
5
52
17
6.8
70.2
23.0
2
64
8
2.7
86.5
10.8
n
0
29
8
Tear stage group
(n = 37)
patients n controls
%
%
0
78.4
21.6
0
32
5
0
78.4
13.5
n
5
81
25
All
(n = 111)
patients n controls
%
%
4.5
73.0
22.5
2
95
14
1.8
85.6
12.6
55
5.4 Reactions of subacromial bursa at the different stages of
impingement syndrome
5.4.1 Tenascin-C expression
In uninvolved tissue, tenascin-C was only seen around small arteries, which is its regular
site of native expression. No accumulation of tenascin was seen in the acellular matrix. In
tissue samples from involved bursas, on the other hand, variable degrees of tenascin were
also seen in the stroma. Tenascin was usually associated with fibrous and inflammatory
lesions. Its expression was significantly increased in FTG compared to CG, TG and PTG
(p ≤ 0.001) and almost significantly increased in TG compared to CG (p = 0.06) (Fig. 9).
Fig. 9. Percentages of tenascin-C expression in controls and at different stages of
impingement syndrome. (For explanations of p-values, see text.)
56
5.4.2 Fibrosis
Fibrosis was a frequent finding (58%) in the tissue samples of the involved groups, but
rare in CG (8%) (Fig. 10). It was significantly increased in TG (64%), PTG (45%) and
FTG (56%) compared to CG (p = 0.001 vs TG, p = 0.05 vs PTG and p = 0.002 vs FTG).
No significant differences were seen between TG, PTG and FTG.
Fig. 10. Percentages of fibrosis in controls and at different stages of impingement syndrome.
(For explanations of p-values, see text.)
57
5.4.3 Thickness
The thickness of the bursa was evaluated as normal in the majority of cases in CG, but in
only 39% of the involved shoulders, but the differences between the groups were not
significant (Fig. 11). In general, a low degree of vascularity, mostly close to the surface,
was seen in the predominantly acellular bursal tissue.
Fig. 11. Percentages of the grade of thickness in controls and at different stages of
impingement syndrome. (For p-values, see text.)
58
5.4.4 Vascularity
A slight increase in vascularity was seen in the bursae of the involved groups (Fig. 12).
The increase was most marked in FTG, but the differences compared to the other groups
were not significant. Haemorrhages seen in the bursal wall were usually restricted to
small focal areas and only appeared here and there in the stroma.
Fig. 12. Percentages of the grade of vascularity in controls and at different stages of
impingement syndrome. (For p-values, see text.)
59
5.4.5 Haemorrhage
The lowest abundance of haemorrhage was a frequent finding in CG and FTG, whereas
TG and PTG presented with intermediate abundance (Fig. 13). An increase of
haemorrhage was a significant finding in TG compared to CG (p = 0.016). On the other
hand, haemorrhages were significantly less often found in FTG compared to CG
(p = 0.006) and PTG (p = 0.038).
Fig. 13. Percentages of haemorrhage in controls and at different stages of impingement
syndrome. (For p-values, see text.)
5.4.6 Inflammatory cells
In uninvolved tissue, no inflammatory cells were seen. They were also rare in involved
tissue. Variable amounts of lymphocytes were seen, usually close to the degenerative or
fibrotic areas in one sample in TG and in two samples in PTG and FTG. Statistical
comparison between the groups was not possible.
60
5.4.7 Correlations between tenascin-C expression and histological
findings
There were no significant correlations between tenascin-C and the histological
parameters, which suggests that tenascin-C reflects a different phase of the bursal
reaction than the conventional histological parameters. The same was true of the
intercorrelations between the histological parameters. Increased fibrosis tended to
correlate slightly with vascularity and thickness according to the stage of the
impingement syndrome in the samples taken from the patient groups (TG, PTG and
FTG).
5.5 Pressures in different parts of the subacromial space
The highest subacromial compressions in both groups were recorded under the
anterolateral part of the acromion (Fig. 8 and 14). These values were significantly
(p < 0.001, Friedman’s test) higher than those in the anteromedial, posterolateral and
posteromedial parts in the impingement group. No such differences were observed in the
control group.
The pressures were significantly higher in the impingement group than in the control
group under the anterolateral acromion at 60° (p = 0.016, MW-U test) and 90° (p = 0.015)
of abduction and under the anteromedial acromion at 90° (p = 0.046) of abduction.
The pressures under the anterolateral acromion increased during abduction in the
impingement group (Fig. 14). The differences were significant between 0° and 30°
(p = 0.007, Student’s t-test), 0° and 60° (p = 0.006) and 0° and 90° (p = 0.004). Similar
significant increases were seen under the anteromedial acromion between 0° and 60°
(p = 0.044) and 0° and 90° (p = 0.046). An increase of abduction angle had no significant
effect on subacromial pressures in the control group.
61
Fig. 14. Relative pressures in the A) anterolateral, B) anteromedial, C) posterolateral and D)
posteromedial parts of the acromion. (Median and 25% and 75% quartiles)
6 Discussion
6.1 Methods
We focused on the condition of the rotator cuff, examining all the operated shoulders by
using ultrasound and, in suspicious cases and symptomatic shoulders, by using
arthrography and/or MRI. These imaging methods, which have relatively high accuracy
rates, are routinely used in the diagnosis of RC tears, and our results therefore appear
reliable, especially in view of the fact that they were used as paired or triple. It must be
emphasised that, in some cases, the patient may have had a partial joint side or
intratendinous RC tear at the time of operation, which did not heal or which progressed to
a full-thickness tear. Shoulder joint arthroscopy and MRI were not in routine use at the
time when the operations were performed. Trial tenotomy, which is an accurate method to
diagnose intratendinous partial tears (Fukuda 2003), was not done routinely, but only in
suspected (by palpation of RC tendons) cases at the initial operations.
Most of the earlier studies have involved measuring the strength of the rotator cuff
muscles isokinetically with slow (60°/sec) and fast (180°/sec) torque arm speed (Ivey, Jr.
et al. 1985, Leroux et al. 1994, Leroux et al. 1995, Holm et al. 1996). We used only
isometric measurements, which have been shown to be equally valid for the measurement
of the strength of the external rotation and abduction of the shoulder as isokinetic
measurements (Gore et al. 1986, Kuhlman et al. 1992). Gore et al (Gore et al. 1986), who
used the isometric method, carried out measurements of internal and external rotation at
abduction angles of 0° and 90° (if possible) of the shoulder, and those of abduction at
angles of 45° and 90° (if possible), but did not record flexion. However, Kuhlman et al
(Kuhlman et al. 1992) recommended that the isometric strength of external rotation
should be measured at 45° of abduction and 45° of internal rotation, and the strength of
abduction in the scapular plane with the shoulder at 45° of abduction. We carried out all
our measurements at 0° of abduction and flexion, because this position is the least painful
preoperatively and even in the very early postoperative period. It has been shown that the
effect of pain on strength measurement is remarkable (Ben Yishay et al. 1994), and
isokinetic measurements were therefore not used here.
63
The strength values of the involved shoulder were given as percentages of those of the
uninvolved shoulder, as in some earlier studies (Walker et al. 1987, Kirschenbaum et al.
1993). This management was especially useful here due to the great number of lacking
recordings, which unfortunately prevented the use of repeated measures analysis of
variance (ANOVA) in statistical analysis. The variation of thein group size detracts from
the value of the information obtained from that study. However, we think that the
statistical values of the percentages of the opposite shoulder are still comparable to each
other, because the groups are homogenous for age and sex. We also believe that our
measurements are valid, as they were carried out in a consistent manner by a single
physiotherapist and give an accurate picture of the relative changes of shoulder muscle
strength preoperatively and in the early recovery period after decompressive surgery.
Proper projection is essential for an accurate evaluation of radiological acromial
morphology (Duralde & Gauntt 1999). Correct x-ray beam direction can be obtained by
fluoroscopic control as described by Liotard et al (Liotard et al. 1998) and Prato et al
(Prato et al. 1998). They pointed out that, for a good projection of SOV, the direction of
the x-ray beam varies between 5° cranial to 25° caudal. However, a proper technique for
obtaining traditional SOV can produce acceptable and reproducible SOVs, as suggested
by Duralde et al (Duralde & Gauntt 1999). We did not use fluoroscopy but only used
standard positioning of the patient, film and beam with 15° caudal tilt, which is the mean
of the values reported by Prato et al (Prato et al. 1998). Proper SOVs were also ensured
by selecting only the valid projections according to Liotard et al (Liotard et al. 1998) for
the study. Using this method, we found 10% of the x-rays inadequate. This figure is
clearly lower than that (23%) reported by Kitay et al (Kitay et al. 1995).
Our histological evaluation of bursal reactions in impingement syndrome was mainly
based on the same criteria as in some earlier studies (Chiquet-Ehrismann et al. 1986,
Uhthoff & Sarkar 1991, Rahme et al. 1993, Kronberg & Saric 1997). Therefore, reliable
and valid comparisons could be made with the previous results.
There are aspects in the study of subacromial pressures that may cause some bias. The
pressures between the acromion and the rotator cuff proved to be surprisingly high. It
must be considered that the sensor, although not more than 2 mm thick, interferes with
the recording by stretching the subacromial space, which may increase the real pressure
value. However, our sensor was markedly thinner than the balloon used in the study by
Nordt et al (Nordt, III et al. 1999), which was 4 mm thick. We give the measured
pressures in relative values, which are sufficient for our purposes. To obtain pressure
values near to the real, a transducer as thin as possible should be developed. The
measurements were performed under general anaesthesia. It is possible that, under
normal conditions, the co-ordination of muscle function and arm torque would have an
effect on the pressures in the subacromial space. It is, however, difficult to find a valid
control group for measurements of this kind. Here, we performed the control
measurements during repair of the dislocated acromioclavicular joint, which was the only
frequently performed operation in our hospital during which the subacromial space can
be reached without unnecessarily widening the approach. Some biomechanical error
might occur in the case of scapular poise (Rasyid et al. 2000). This must be accepted
because it is impossible to make the measurements used here in a completely nonaffected shoulder or under local anesthesia. This was also pointed out by Nordt et al
(Nordt, III et al. 1999) after some preliminary attempts at a study design similar to ours.
64
We believe that these sources of error are not decisive and that our results reflect the real
pressure conditions in the subacromial space.
6.2 Long-term results of open acromioplasty and rotator cuff
pathology
The subjective results of open acromioplasty are generally favourable, the percentage of
excellent and good outcomes ranging from 43% to 94% (Neer 1972, Thorling et al. 1985,
Tibone et al. 1985, Post & Cohen 1986, McShane et al. 1987, Hawkins et al. 1988,
Jalovaara et al. 1989, Bjorkenheim et al. 1990, Stuart et al. 1990, Rockwood & Lyons
1993, Hartwig & Burkhard 1996). The subjective outcomes in this study were similar to
those reported earlier. We observed a relatively high incidence of RC tears after open
acromioplasty in long-term follow-up, which has not been reported earlier. Most of the
earlier studies on the outcome of open acromioplasty have concentrated on the clinical
outcome, and the mean follow-up times have been mostly too short to show these late
failures (Neer 1972, Thorling et al. 1985, Tibone et al. 1985, Post & Cohen 1986,
McShane et al. 1987, Hawkins et al. 1988, Jalovaara et al. 1989, Bjorkenheim et al.
1990, Stuart et al. 1990, Rockwood & Lyons 1993, Hartwig & Burkhard 1996).
In our study with a long follow-up time, 15% of the shoulders showing a favourable
primary outcome deteriorated some years postoperatively, and the majority of these had
developed an RC tear. This suggests that the disease process sometimes continues in the
RC tendon after acromioplasty despite the disappearance of symptoms and the
elimination of subacromial compression. Cuff tears were also found in shoulders which
did not benefit from acromioplasty and in pain-free shoulders. Including these, nearly one
fifth of the operated shoulders displayed either a partial or a complete tear. However, it
has been shown in cadaveric, ultrasonic and MRI studies that partial and complete RC
tears also appear in the asymptomatic population, and they are age-related (Neer 1983,
Thorling et al. 1985, Sher et al. 1995).
6.3 Pathogenesis of impingement syndrome
Ozaki et al (Ozaki et al. 1988) suggested that RC tears or injuries are the result of
intrinsic rather than extrinsic causes associated with impingement, as advocated by Neer
(Neer 1983). They found that although a lesion in the anterior third of the undersurface of
the acromion was always associated with a RC tear, the reverse was not true, and they
concluded that the pathogenesis of most cuff tears was probably an intrinsic process. Our
results partially support the findings of Ozaki et al. (Ozaki et al. 1988). The majority of
the patients remained symptomless and showed no evidence of RC tear, suggesting that
the process in the tendon did not progress in these cases.
65
According to the extrinsic theory of the pathogenesis of impingement, the lesion in the
rotator cuff tendon is caused by mechanical compression by the coracoacromial arch.
Consequently, the disease process should come to a halt after decompressive
acromioplasty, and the surgical outcome should be permanent. On the other hand, if the
symptoms recur and the disease progresses to the tear stage despite acromioplasty,
intrinsic factors, i.e. a degenerative process in the RC tendons, might be significant.
6.4 Recovery of shoulder muscle strengths after open acromioplasty
It has been shown that shoulder muscle strength decreased by supraspinatus tendinitis and
rotator cuff tear is restored after surgical treatment (Leroux et al. 1994, Leroux et al.
1995). The recovery of shoulder strength after reconstruction of rotator cuff tear is a slow
process, lasting up to a year (Vastamaki 1986, Walker et al. 1987, Kirschenbaum et al.
1993, Rokito et al. 1996). However, strength does not always completely recover to the
level of the uninvolved opposite shoulder (Gore et al. 1986, Rabin & Post 1990). In this
regard, our findings are in agreement with those of earlier reports, but no report focusing
on the early recovery of isometric shoulder muscle strength after surgery of stage II
impingement syndrome could be found.
The recovery of strength was more marked in women, and this is at least partly due to
their more pronounced loss of strength preoperatively than seen in men. The favourable
outcome of surgery is reflected in the good recovery of strengths, suggesting that
mechanical aspects are involved in the pathogenesis of impingement syndrome. On the
other hand, in cases with a poor outcome at one year, strengths mostly decreased
compared with the preoperative situation, even though this group was too small for
statistical analysis. The finding that male shoulders did not show equally significant
recovery as female shoulders might provide some support to the intrinsic theory (overuse
syndrome). Dominance was not considered because its effect has been proved to be nonsignificant (Ivey, Jr. et al. 1985, Murray et al. 1985, Walker et al. 1987).
It must be emphasised that rehabilitation mostly remained the personal responsibility
of the patient, based on guidance given by the physiotherapist at discharge from the
hospital, with no controlled supervision afterwards. In fact, supervised exercises have
been suggested to be as effective as surgery based on a prospective randomised study of
patients with stage II impingement syndrome (Brox et al. 1993). It is possible that
recovery may be improved and facilitated by effective controlled physiotherapy. The slow
recovery of shoulder muscle strengths should also be considered when prescribing a sick
leave for a heavy manual worker.
6.5 Acromial morphology evaluated by supraspinatus outlet view
Despite the potential value of correlating specific acromial forms with lesions of the
rotator cuff described by Bigliani and Morrison (Bigliani et al. 1986), some investigators
66
have been unable to reproduce these findings. They have questioned the reliability of
radiographic acromial morphology assessment in the sagittal plane (Jacobson et al. 1995,
Zuckerman et al. 1997, Bright et al. 1997, Liotard et al. 1998). Here, we found no
significant differences in the distribution of the different types of acromions between the
patients and controls. However, there was a tendency for type III acromions to appear
more frequently in patients than in controls. This tendency turned out significant when an
objective method of measurement was applied.
In an effort to objectively quantitate and standardise the classification of the curvature
of the anterior acromion, Toivonen et al (Toivonen et al. 1995) devised the measurement
of an acromial angle. They found it to range from 5° to 42°, which is comparable to the
values observed in our study, 3° to 67°. We also found an increased acromial angle to
associate with rotator cuff tears, which is in agreement with the findings of earlier studies
(Toivonen et al. 1995, Tuite et al. 1995, Banas et al. 1995).
There is some terminological confusion concerning the slant of the acromion in
relation to the scapula and the reference points used to determine it (Chambler & Emery
1997). This inclination has been called acromial tilt (Zuckerman et al. 1992, Kitay et al.
1995, Prato et al. 1998) and acromial slope (Aoki et al. 1986, Edelson & Taitz 1992,
Gohlke et al. 1993), and it has been evaluated by different methods. Kitay et al (Kitay et
al. 1995) and Aoki et al (Aoki et al. 1986) determined it as the angle formed by
connecting two lines from the posteroinferior undersurface (angulus acromialis) of the
acromion to the tip of the coracoid process and to the anteroinferior acromion. Some
other investigators (Edelson & Taitz 1992, Zuckerman et al. 1992, Mallon et al. 1992,
Gohlke et al. 1993, Prato et al. 1998) have evaluated the corresponding inclination in
relation to the scapular axis. Here, we used the method described by Kitay et al and Aoki
et al using the tip of the coracoid process as a reference point and called this inclination
acromial tilt. It was, however, emphasised that the tilt may vary because the length of the
tip of the coracoid is affected by the osteophytes pointing the conjoined tendon.
Therefore, we also measured the tilt by using the coracoid undersurface curve as a
reference point, but this did not alter the results. (Fig. 6.)
The dimensions of the acromion have been found to be different between sexes, but
not age-dependent (Nicholson et al. 1996). Here, we found no significant differences in
the acromial measures between the controls and the patients, and the measurement of
acromial dimensions is therefore a waste of time in view of the diagnosis.
6.6 Reactions of subacromial bursa in different stages of
impingement syndrome
6.6.1 Tenascin-C expression
The expression of tenascins in different tissues varies, depending on the developmental
stage of the organism analysed, and it changes dramatically under various pathological
67
conditions (Erickson & Bourdon 1989, McCachren & Lightner 1992, Riedl et al. 1992,
Soini et al. 1993, Riley et al. 1996, Kaarteenaho-Wiik et al. 1996). Elevated expression
of tenascin is seen in active reparative processes as wound healing, inflammatory lung
diseases and keloids (Mackie et al. 1988, Dalkowski et al. 1999, Kaarteenaho-Wiik et al.
2000). In bursal tissue, it also very probably characterises regeneration and, thus, a
different phase of reaction compared to fibrosis, being a late reaction. This is in good
accordance with our results showing a lack of intercorrelation between tenascin-C
expression and fibrosis.
Our study was the first to use the expression of tenascin-C as a marker of tissue
lesions in the subacromial bursa. Tenascin-C expression in the subacromial bursa was
significantly more pronounced in all of the involved groups than in the control group. It
was expressed weakly in the extracellular matrix in the controls, but was found in larger
quantities in the stroma of involved tissue. Riley et al (Riley et al. 1996) studied tenascinC expression in supraspinatus tendon affected by the impingement syndrome and found it
to be increased, especially in degenerative tendons, but not in healthy cadaveric tendons.
On the other hand, increased tenascin-C expression might be caused by a mechanical load
due to impingement, as it has been shown that the expression of tenascin-C responds to a
mechanical load in bone (Webb et al. 1997) and in the osteotendinous junction (Jarvinen
et al. 2000). Further support of the mechanical cause might be a lack of correlation
between tenascin-C expression and an inflammatory reaction or fibrosis in the bursa. It
thus seems that the reaction in the subacromial bursa is associated with the tendon lesion
regardless of whether it is degenerative or caused by a mechanical load or compression.
6.6.2 Vascularity
Ishii et al (Ishii et al. 1997) examined vascularity (angiogenesis) and cellularity (mostly
fibroblasts and occasionally lymphoblasts) as a combined measure of the “bursal
reaction”, while we evaluated and presented them as separate parameters of bursal
involvement. As far as we can see, this distinction allows a more refined analysis of the
course of the pathological and healing process at different stages of impingement
syndrome.
6.6.3 Fibrosis
The most significant difference in the histological parameters between the controls and
patients was that fibrosis was present significantly more frequently in the involved
groups. An increased amount of bursal fibrosis in impingement syndrome has also been
observed in the previous studies (Rahme et al. 1993, Kronberg & Saric 1997). Rahme et
al (Rahme et al. 1993) found bursal fibrosis in 80% of their patients with supraspinatus
tendinitis but in only 15% of cadaveric controls. Kronberg and Saric (Kronberg & Saric
1997) reported severe fibrosis in 10, moderate in 8 and no fibrosis in 1 of 19 patients with
68
tendinitis stage impingement syndrome and no fibrosis in 5 cadaveric control shoulders.
In the study of Ishii et al (Ishii et al. 1997), fibrosis was evaluated as part of the bursal
reaction and turned out to be more pronounced next to the rotator cuff tear than in
specimens obtained further away from the lesion. They also found the reactions to be
significantly slighter in tendinitis than in the presence of a rotator cuff tear. This was also
the case in our study, where the specimens were taken from the deltoid side of the bursa,
which probably reflects better the general reaction of the bursa than the specimens
obtained from lesion sites.
6.6.4 Inflammatory cells
Santavirta et al (Santavirta et al. 1992) found in their immunohistochemical study one
mild and six moderate inflammatory cell involvements in the 12 subacromial bursas
biopsied at acromioplasty for supraspinatus tendinitis or rotator cuff tear. They suggested
that inflammation of the subacromial bursa is a potentially important cause of pain in
impingement syndrome. In our study, inflammatory cells were seen only rarely. This is in
agreement with the findings reported by Ishii et al (Ishii et al. 1997), who observed no
plasma cells and only occasional lymphocytes in bursal specimens taken from patients
with tendinitis or a tear of the rotator cuff.
6.6.5 Thickness
The thickness of the bursa has not been used as a specific parameter of bursal reaction in
the earlier studies, probably because it is difficult to measure due to uncertainties in the
definition of the cutting plane. However, Rahme et al (Rahme et al. 1993) evaluated it as
part of fibrosis, and it proved to be increased. Fibrosis and bursal thickness also tended to
be related in the present study.
6.6.6 Haemorrhage
Previous reports have not paid much attention to the presence of hemorrhages in the
subacromial bursa. Ishii et al (Ishii et al. 1997) noticed hemorrhages in 15% of their cases
of tendinitis stage impingement syndrome. In this study, bursal hemorrhages occurred
most frequently in association with tendinitis and partial tears, but were uncommon in the
controls and in full-thickness tears.
69
6.6.7 Subacromial bursa in the pathomechanism of the impingement
syndrome
Our study sheds some light on the role of the reaction of the subacromial bursa in the
pathomechanism of the impingement syndrome. Based on histological studies, it has been
suggested that bursal involvement is secondary to the damage of the rotator cuff tendon
(Uhthoff & Sarkar 1991, Ishii et al. 1997) and the bursa is, similarly to the peritoneum,
only secondarily involved, as postulated by Codman (Codman 1990). We did not
examine the changes in tendons, but the fact that the increased tenascin-C expression
reflecting bursal reactions was more pronounced at the tear stage than at the tendinitis
stage of the disease supports the previous assumptions. However, the reaction of the
subacromial bursa may be the origin of the symptoms of impingement syndrome, as
suggested by some other studies, which focused on the origin and mediators of
impingement pain (Santavirta et al. 1992, Rahme et al. 1993, Gotoh et al. 1998).
The attitude to bursal resection during rotator cuff surgery has been under discussion.
Ishii et al (Ishii et al. 1997) recommended repair of the bursa during RC tear repair. On
the other hand, Kronberg and Saric (Kronberg & Saric 1997) and Rahme et al (Rahme et
al. 1993) reported a better outcome in the patients whose bursa had been removed at the
tendinitis stage. In this study, we observed that the fibrosis phase of the bursal reaction is
dominant compared to the regeneration phase, as indicated by tenascin-C expression at
the tendinitis stage of impingement. Thus, we feel that the resection of bursa is justified,
as it has been suggested that bursal fibrosis impairs the outcome (Rahme et al. 1993,
Kronberg & Saric 1997). At the tear stage, the regenerative process in the bursa,
determined by tenascin-C expression, is so notable as to be potentially important for the
healing of the tear. Its restoration is therefore recommended.
6.7 Pressures in different locations of the subacromial space
Our results suggest that subacromial pressure is highest under the anterolateral acromion,
increases during abduction in impingement patients and is elevated in shoulders suffering
from impingement. These findings further elaborate the earlier knowledge and are, by
and large, in agreement with the previous studies. Flatow et al (Flatow et al. 1994), using
stereo-photogrammetric analysis, demonstrated that the acromial undersurface and the
rotator cuff tendons are in closest proximity between 60 degrees and 120 degrees of
elevation in cadaveric shoulders and that the main area of increased contact is the
anteroinferior part of the acromion. Zuckerman et al (Zuckerman et al. 1992) evaluated
subacromial pressure indirectly, using three-dimensional computer modelling, which
showed that the volume of the subacromial space decreased when the prominence of the
anterior aspect of the acromion increased. However, they did not measure the pressure.
Wuelker et al (Wuelker et al. 1995a, Wuelker et al. 1995b), using a dynamic cadaveric
model, found that the peak forces under the coracoacromial arch occurred between 51°
and 82° of elevation and were most pronounced underneath the acromion. They pointed
70
out that measurements of anatomic specimens may not be fully applicable to the clinical
situation. Jerosch et al (Jerosch et al. 1989) suggested in their cadaveric study, where the
measurement was carried out with a compression film, that mechanical subacromial
compression only occurs in shoulder joints with a Bigliani acromion type III (Morrison &
Bigliani 1987) and/or in joints with imbalance of the deltoid/rotator cuff relation. In our
study, acromions were classified as type II and we could not consider the muscular
imbalance because of the anesthesia. Sigholm et al (Sigholm et al. 1988) studied
subacromial bursal pressures in healthy volunteers using a microcapillary infusion
method. The pressure, which averaged 8 mm Hg at rest, increased when the arm was
lifted to 39 mm Hg and, with a 1 kg weight, to 56 mm Hg. Their method reflects only the
total pressure of the bursal pouch (Nordt, III et al. 1999), not local pressures under the
acromion, as does our method. Nordt et al (Nordt, III et al. 1999) posted that fully
abducted and cross-reach positions generate the highest impingement pressures, while
acromioplasty decreased significantly (60%–100%) the anterior edge subacromial
pressures. These studies are very much in accordance with our findings showing that the
measured pressures were highest in 90° of abduction in the anterolateral part of the
subacromial space. These papers, in line with our findings, lend support to the use of
Neer´s acromioplasty in the treatment of impingement syndrome (Neer 1972). Excision
of the anterior undersurface of the acromion, under which the subacromial pressure is
concentrated, decreases the pressure and explains the good effect of acromioplasty in this
disease.
The steady increase in subacromial pressure observed under the anterolateral part of
the acromion during abduction at up to 90° in impingement syndrome shoulders fits very
well with the classical clinical symptom of this disease, i.e. a painful arc (Calvert 1997).
Our findings thus seem to support the "extrinsic" theory (Neer 1983, Morrison & Bigliani
1987, Bigliani & Levine 1997) of the pathogenesis of impingement pathology. It should
be considered, however, that increased subacromial pressure might also be of secondary
origin, i.e. caused by spur formation secondary to the primary degenerative process in the
cuff, as suggested by the supporters of the "intrinsic theory" (Uhthoff et al. 1987, Ozaki
et al. 1988).
Generally, the shoulder impingement syndrome can be manifested in many forms. It
seems that it has at least two different pathomechanisms, which we should be able to
differentiate. The diagnosis of the disease is still mostly clinical, and good criteria for
evaluating the precise need for surgery are lacking. As a treatment option, a tailored
rehabilitation program can help to avoid unnecessary surgery.
7 Conclusions
1. The good outcome after open acromioplasty is not permanent in all cases, suggesting
that a degenerative process is involved in the pathogenesis of impingement syndrome
2. Shoulder muscle strength is restored to near normal within one year after open
acromioplasty. This suggests that mechanical compression plays a role in the
pathogenesis of impingement syndrome.
3. Variation in the shape of the acromion, as evaluated by a routine supraspinatus outlet
view, is associated with impingement syndrome, but this association is weak and its
validity in the diagnosis of impingement syndrome is therefore a minor adjunct to the
other diagnostic methods.
4. Tenascin-C is a more general indicator of bursal reaction compared to the
conventional histological markers, being especially pronounced at the more
advanced stages of impingement. It seems that the bursal reaction is an essential part
of the impingement pathology at all stages, and that this reaction shows different
phases, as indicated by the different parameters used in this study.
5. Impingement pain may be caused by compression onto the inflamed subacromial
bursa or pressure ischaemia in the rotator cuff.
6. The local pressures in the subacromial space were elevated in impingement
syndrome, supporting the mechanical theory.
7. Mechanical (extrinsic) and degenerative (intrinsic) factors are involved in the
pathogenesis of impingement syndrome.
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