Avian Pathology
ISSN: 0307-9457 (Print) 1465-3338 (Online) Journal homepage: https://www.tandfonline.com/loi/cavp20
Iron storage diseases in birds
Susan C. Cork
To cite this article: Susan C. Cork (2000) Iron storage diseases in birds, Avian Pathology, 29:1,
7-12, DOI: 10.1080/03079450094216
To link to this article: https://doi.org/10.1080/03079450094216
Published online: 17 Jun 2010.
Submit your article to this journal
Article views: 3164
View related articles
Citing articles: 9 View citing articles
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=cavp20
Avian Pathology (2000) 29, 7–12
Review
Iron storage diseases in birds
Susan C. Cork*
Harper Adams University College, Edgmond, Newport, Shropshire TF10 8NB, UK
Parenteral iron is toxic to many species but, because the uptake of iron from the diet is regulated in
the intestine, acute intoxication is not seen under natural conditions. Chronic ingestion of large
amounts of absorbable iron in the diet can lead to the storage of iron in the liver in many species,
including humans. The excess iron is stored within hepatocytes as haemosiderin and can be
quantitatively assessed by liver biopsy or at necropsy using special stains such as Perls iron stain and/or
biochemical tests. Iron may also be found within the Kupffer cells in the liver and the macrophage cells
of the spleen especially where concurrent diseases are present such as haemolytic anaemia,
septicaemia, neoplasia and starvation. Iron accumulation in the liver, also known as haemosiderosis,
may not always be associated with clinical disease although in severe cases hepatic damage may occur.
It is probable that concurrent disease conditions are largely responsible for the degree and nature of
the pathological changes described in most cases of haemosiderosis. In some human individuals there
may be a genetic predisposition to iron storage disease, haemochromatosis, associated with poor
regulation of iron uptake across the intestine. In severe cases iron pigment will be found in the liver,
spleen, gut wall, kidney and heart with subsequent development of ascites, heart failure and multisystem pathology. Clinical disease associated with accumulation of iron in the liver, and other tissues,
has been reported in many species of bird although it is most commonly reported in Indian hill mynas
(Gracula religiosa) and toucans (Ramphastos sp). It is likely that the tolerance to the build up of tissue
iron varies in individual species of bird and that the predominant predisposing factors may differ, even
within closely related taxonomic groups.
Introduction
Iron is required in the diet to prevent the development of anaemia and poor immune function. Iron is
an integral component, along with copper, in the
formation of the haem complex, which forms the
haemoglobin fraction of the red blood cells. In
mammals and birds this is essential for the maintenance and transport of oxygen around the tissues
(Butler, 1983; Dewar, 1986). Parenteral iron can be
toxic but because the uptake of iron from ingested
sources is generally limited, acute intoxication is
not usually seen unless intestinal absorption is
promoted above normal levels (Hartley et al.,
1959). Chronic ingestion of large amounts of
absorbable iron in the diet can lead to the storage of
iron in the liver in many vertebrate species,
including humans (MacDonald, 1972; Nhonoli,
1973; Borch-Ionson & Nilssen, 1987; BorchIohnson et al., 1989; Spelman et al., 1989; Miller et
al., 1997). The excess iron is stored within
hepatocytes as haemosiderin and can be quantitatively assessed by liver biopsy or at necropsy using
special stains such as Perls iron stain (Perls, 1867)
and/or biochemical tests (Gosselin & Kramer,
1983). Iron may also be found within the Kupffer
cells in the liver and the macrophage cells of the
spleen, especially where concurrent diseases are
present such as haemolytic anaemia, septicaemia
and starvation (Kochan, 1973; Weinberg, 1984;
Kincaid & Stoskopf, 1987; Cork et al., 1995). Iron
accumulation in the liver, also known as haemosiderosis, may not always be associated with clinical
disease although in severe cases hepatic damage
may occur (Alt et al., 1990; Bulte et al., 1997).
Lowenstine (1986) reports that accumulation of
iron pigment in the liver has been reported in many
species of bird although it is most commonly
reported in Indian hill mynas (Gracula religiosa)
and toucans (Ramphastos sp.). There have been
*Tel/Fax: +44 1952 815327. E-mail: scork@harper-adams.ac.u k
Received 6 August 1999. Accepted 21 September 1999.
ISSN 0307-9457 (print)/ISSN 1465-3338 (online)/00/010007-0 6
© 2000 Houghton Trust Ltd
8
S. C. Cork
isolated reports and broader studies which have
reported cases of haemosiderosis in a range of other
species including hornbills, some psittacines, and
birds of paradise (Wadsworth et al., 1984; Taylor,
1984; Frankenhuis & Assink, 1981; Gerlach et al.,
1998). However, Lowenstine (1986) reports that
haemosiderosis was not diagnosed in two birds of
paradise trapped in the wild, until after they had
been fed a pig starter ration high in iron. From this
it was concluded that the disease in birds of
paradise was associated with captivity, probably the
artificial diet. Taylor (1994) also concluded that the
severity of haemosiderosis in liver samples examined from a variety of bird species held at the Jersey
wildlife trust was greatest in individuals that had
been in captivity for the longest. However, much
more work is needed to clarify the relative significance of a range of predisposing factors in the
aetiology of iron storage diseases in different avian
species.
Avian nutrition
Since there are no complete studies of the nutrient
requirements of exotic avian species commonly
maintained in captivity, the requirements of individual species must be judged on the basis of whatever
information is available (Donoghue & Stahl, 1997;
Harper & Skinner, 1998; Schoemaker et al., 1999).
Most of the research data available for avian
nutrient requirements is based on the requirements
of gallinaceous birds (Anonymous, 1984). Although
the basic physiological requirement for metabolisable energy and total protein can be estimated on
the basis of body mass, age and growth rate, the
individual species requirements for minerals, trace
elements, essential fatty acids, and vitamins may
vary. The dietary requirements of different bird
species may depend on the environment in which
the birds have evolved, the composition of the
natural diet and the level of nutrient demand. The
last of these will vary with metabolic state, breeding
season (Osborn, 1979; Osborn & Young, 1985;
Diez, 1986) and climatic conditions (BorchIonhson et al., 1989). No dietary element can be
considered in isolation and each must be assessed
with regard to the other nutrients in the ration; this
is especially important if pelleted feeds are to be
provided instead of a more natural diet. Some trace
element interactions are well reported in gallinaceous birds as are the results of vitamin and mineral
excess or deficiency. It is likely that the same basic
physiological interactions occur in the more exotic
bird species kept in captivity but the effect of
dietary components such as the level of tannins in
diets composed largely of leaves and bark, oxalates
and phytates in some forage, and high levels of
certain trace elements in berries and some fruits,
may affect the level of absorption of trace elements
and minerals from the diet (Chubb, 1982; Inan et
al., 1998; Spelman et al., 1989; Kim et al., 1995).
Roughage and tannin content will often affect the
degree to which minerals and trace elements are
available to the bird. In primates, elements such as
iron are more readily absorbed if the level of
ascorbic acid in the diet (i.e. vitamin C) is high
(Hunt et al., 1994) whereas absorption is reduced
where tannin levels are high (Spelman et al., 1989).
Other components in the diet such as the level of
calcium salts and other chelating agents may also
reduce the bioavailability of iron from a given
ration. When designing a diet for a bird species it is
important to monitor the growth and development
of birds that are given the new ration and to assess
the concentrations of key nutrients in the tissues of
any birds that die. It is important to maintain the
monitoring process throughout the year as requirements for elements such as calcium, phosphorus ,
iron, zinc and copper may vary. In cases of trace
element or mineral deficiencies, there will rarely be
a single component of the diet involved. Usually the
clinical picture of a dietary deficiency is complex
due to the nutrient interactions involved.
Aetiology and terminology
Iron-containing brown pigment occurs frequently in
the livers of birds of several orders and families
(Lowenstine & Petrak, 1980; Garcia et al., 1984;
Taylor, 1984; Cork et al., 1995; Gerlach et al.,
1998) and has been observed in both wild and
domestic birds in regions all over the world (Ward
et al., 1991). The distribution of this histologicall y
stainable iron is variable (Taylor, 1984; Roels et al.,
1996) indicating that a range of aetiological factors
are probably involved in the development of
haemosiderosis (Lowenstine & Petrak, 1980; Andre
& Delverdier, 1994). Haemosiderosis used as a
descriptive term, does not imply a particular
pathogenesis to the condition unlike the term
haemochromatosis, which refers to the primary
idiopathic disease in human patients which has a
genetic basis and results in iron overload secondary
to poor control of iron uptake at the level of the
intestinal epithelium (Nhonoli, 1973). In most of
the cases reported in birds, even when significant
pathology is present, the term haemosiderosis is
possibly more appropriate unless a specific aetiology can be identified.
In some species of bird, especially migratory
species, seasonal changes in tissue iron occur as
part of the normal physiological cycle and are
associated with the breeding season and the moult
(Osborn, 1979; Osborn & Young, 1985). In a study
by Ward et al. (1991), it was shown that the
regulation of iron uptake at the intestinal level in
some avian species was not as tightly regulated as it
is in mammals. However, although some authors
favour the hypothesis that dietary overload is
responsible for the development of haemosiderosis
in many avian species (Kincaid & Stoskopf, 1987;
Gerlach et al., 1998), the distribution of iron in the
Iron storage diseases in birds
liver is not the same as that seen in human dietary
overload (Iancu, 1982; Iancu et al., 1987) or in the
early stages of primary haemochromatosis (Powell
et al., 1980). There has not been any conclusive
evidence that the presence of stainable iron in the
liver of birds has any clinical significance although
it has been linked to the presence of concurrent
infectious (Lowenstine & Petrak, 1980) and neoplastic diseases (Hill et al., 1986). Although the
presence of histologically stainable iron in the livers
of birds is not generally associated with hepatic
disease, the possible exception to this is the
‘haemochromatosis syndrome’ seen in the Indian
hill myna (Gracula religiosa) (Gosselin & Kramer,
1983). The term haemochromatosis is used in this
context to describe an excessive accumulation of
iron in tissues other than the reticuloendothelia l
system. Although often associated with hepatic
fibrosis, the condition may follow hepatic disease
rather than be a cause of it (Morris et al., 1989).
Species differences
It has been reported in a number of studies that the
domestic chicken (Gallus domesticus) has low
values of tissue iron compared with those reported
for many other species (Osborn, 1979). Cork et al.
(1995) reported that 2-week-old White Leghorn
chickens have hepatic iron values of 120 to 190
micromol/gram, a value similar to that reported by
Osborn (1979) for chickens, but significantly less (p
< 0.01) than the value recorded for pre or post-moult
starlings. Osborn (1979) noted that, in seasonal
breeding birds such as starlings, hepatic iron stores
rise in the autumn following the summer moult. It
was suggested that this increase may reflect the
increased haemopoietic activity of some birds at the
time of the moult and is associated with changes in
the levels of thyroid hormone (Diez et al., 1986). In a
review of pathology reports from the New Zealand
native pigeon (Hemisphagea novaeseelandia e) and
New Zealand native passeriforms, which feed on
plant material and fruits, Cork (1994) found that
these species had a significantly higher prevalence of
severe haemosiderosis (p < 0.01) than did birds such
as the feral rock pigeon (Columba livia) and
granivorous passerines such as the house sparrow
(Passer domesticus). Although there were insufficient data to determine the effect of diet on hepatic
iron stores, there are data in the literature available
on birds (Hill et al., 1977; Butler, 1983; Kincaid &
Stoskopf, 1987) and mammals (Hartley et al., 1959;
Borch-Ionhson & Nilssen, 1987; Borch-Iohnson et
al., 1989; Iancu et al., 1987) to indicate that the
amount and form of dietary iron is an important
factor in determining hepatic iron stores.
Gerlach et al. (1998) cite Dorrestein (1997) who
has described the process of iron uptake modulation
in the intestinal tract and pose the question that
species differences in susceptibility to iron toxicity
are at least partially explained by differences in gut
9
absorption. At this time there is still insufficient
information available on the normal iron metabolism of different avian species to fully explain
species differences in susceptibilit y. Current and
retrospective data continue to be collected on the
pathology and pathogenesis of haemosiderosis in
birds held at the Jersey Wildlife Trust (Cooper,
1999) and other collections (Roels et al., 1996;
Gerlach et al., 1998).
Clinical significance
Lowenstine & Petrak (1980) examined liver sections
from myna birds using electron microscopy and
found that the iron pigment was located within
membrane-bound lysosomal structures and free in
the cytosol as ferritin moieties and larger haemosiderin aggregates. Examination of periodic acid
Schiff (PAS) stained sections indicated that the
majority of the iron in the liver sections examined
was in lysosomal structures. In human haemochromatosis considerable research effort has been
directed towards the identification of a mechanism
of liver damage. Witzleben & Buck (1971) hypothesised that damage was secondary to peroxidation as
a result of the iron overload. Stainable iron is the
ferric form which is loosely associated with tissue
proteins as ferritin or haemosiderin. It is thought that
haemosiderin is a metabolite of ferritin and that a
build-up of the former is more frequently associated
with liver disease (MacDonald, 1972). It is probable
that there are numerous mechanisms that will result
in an alteration in iron metabolism in mammals and
in birds (Lowenstine & Petrak, 1980). What is clear
is that the normal hepatic mechanisms for metabolising iron are incompletely understood.
There is a lot of evidence from retrospective
clinical studies and from in vitro work that indicates
that iron availability is an important determining
factor in the outcome of host– pathogen interactions
(Kochan, 1973; Weinberg, 1984; Bullen, 1987;
Wilson, 1994). The limitations of retrospective
investigations are, however, apparent due to the
lack of information about the exact progress of the
concurrent disease processes and the lack of
knowledge of how microbial agents interact with
the iron metabolism of the host in vivo (Griffiths &
Bullen, 1987; De Sousa, 1989; Griffiths, 1993). The
availability of iron to micro-organisms will increase
in conditions where serum transferrin is saturated
(Weinberg, 1978). In these conditions liver iron
stores will also be increased with predominantly
Kupffer cells loading as described in a disease
model investigating the effect of increased iron
stores on the pathogenesis of Yersinia sp. infection
in chickens (Cork et al., 1998). From experimental
evidence and from numerous reports in the literature, it appears that although hepatic haemosiderosis is frequently a histological finding not
associated with overt liver disease, it is often
associated with concurrent infectious diseases (Hill
10
S. C. Cork
et al., 1986). Haemosiderosis has also been associated with neoplastic diseases in birds (Hill et al.,
1986; Cork & Stockdale, 1995; Cork et al., 1999).
The histological description of excess stainable iron
in the liver is probably a reflection of an altered iron
metabolism associated with increased turnover of
tissue iron. This alteration may occur following
starvation or trauma as well as changes in metabolism associated with seasonal physiological changes
(Osborn, 1979).
Similar treatment regimes which utilise the ironchelating capacity of Dessferioxamine have also
been used successfully in birds (Gosselin & Kramer, 1983; Cornelissen et al., 1995). Dietary
restriction of iron and phlebotomy have also been
used successfully in toucans (Roels et al., 1996).
However, although treatment is available, diagnosis
is not always made until necropsy and blood tests
have proved unsatisfactory (Gerlach et al., 1998).
Conclusions
Experimental models
The haemosiderosis –haemochromatosis complex
has been widely reviewed in the veterinary and
medical literature (Witzleben & Buck, 1971;
Bullen, 1981; Iancu, 1982: Gonzales et al., 1984;
Turlin & Deugnier, 1998), and there are several
retrospective studies describing avian haemosiderosis in the literature (Taylor, 1984; Lowenstine &
Petrak, 1980, Cork et al., 1995; Kübber-Heiss,
1994). Experimental models of the disease have
been developed in various species (Iancu et al.,
1987; Iancu 1993; Sayers et al., 1994; Miller et al.,
1997) including the domestic fowl (Gallus domesticus) (Cork et al., 1995).
Measurement of iron in tissues
Iron may be measured in liver sections taken by
biopsy methods antemortem or at necropsy (Gosselin & Kramer, 1983; Garcia et al., 1984; KübberHeiss, 1994; Turlin & Deugner, 1998); assessment
of iron levels in blood samples may be less useful
due to various factors which affect serum iron
levels (Planas et al., 1961; Weinberg, 1984; Gerlach
et al., 1998). It has been demonstrated, using a
chicken model, that there is a positive correlation
between the concentration of stainable iron measured in histological sections (log 10 image analysis
values) and the biochemically determined liver iron
concentration (-mol/g) (Cork et al., 1995). Image
analysis of histological sections can provide an
important research tool for current and retrospective
studies especially where biochemical tests are too
expensive for assessment of large numbers of
samples (Roels et al., 1996). Biochemical analysis
of liver iron is often not possible in retrospective
studies as fresh liver samples may not be available.
In addition, there is often insufficient hepatic tissue
from small birds for biochemical assessment.
Another advantage of using image analysis for the
assessment of hepatic iron is the ability to examine
the distribution of hepatic iron stores (Cork, 1994;
Roels et al., 1996).
Treatment of iron storage diseases
Treatment of iron overload in human patients has
been reviewed extensively (Strohmeyer & Stremmel, 1984; Kruger et al., 1984, Inan et al., 1998).
There is much literature available describing excessive levels of iron storage pigments in the livers of
birds and mammals but the terminology used is often
not uniform. A distinction should be made between
haemochromatosis, the genetic disorder seen in
humans and possibly some other species, and the
range of disorders which may lead to the build up if
iron pigments in hepatic tissue (haemosiderosis). It
is likely that the tolerance to the build-up of tissue
iron varies in individual species of bird and that the
predominant predisposing factors may differ, even
within closely related taxonomic groups. It is
probable that concurrent disease conditions are
largely responsible for the degree and nature of the
pathological changes described in most cases of
haemosiderosis. Neoplastic diseases, parasitism and
systemic bacterial infection may initiate disease
processes associated with haemosiderosis but may
also be potentiated by elevated levels of iron in the
tissues. The current challenge, therefore, is to gain a
better understanding of the aetiology of abnormal
iron storage and to develop nutritional and other
management guidelines for a range of avian species
to prevent the excessive uptake of iron.
References
Alt, E.R., Stemlib, I. & Goldfischer, S. (1990). The cytopathology of
metal overload. International Review of Experimental Pathology, 31,
165–188.
Andre, J.P. & Delverdier, M. (1994). Haemosiderosis or haemochroma tosis — a study in cage birds. Revue de Medecine Veterinaire, 145
(1), 37– 41.
Anonymous (1984). Nutrient Requirements of Poultry 8th revised edn.
Washington, DC: National Academy Press.
Borch-Iohnson, B. & Nilssen, K.J. (1987). Seasonal iron overload in
Svalbard Reindeer liver. Journal of Nutrition, 117, 2072– 2078.
Borch-Iohnsen, B., Olsson, K.S & Nilssen, K.J (1989). Seasonal
siderosis in Svalbard Reindeer. In Haemochromatosis, Proceedings
of the first international conference (pp. 355– 356). Annals of the
New York Academy of Sciences, 9, 526.
Bullen, J.J. (1981). The significance of iron in infection. Review of
Infectious Diseases, 3, 1127–1138.
Bullen, J.J. (1987). Iron and the antibacterial function of polymorpholeucocytes. In J.J. Bullen & E. Griffiths (Eds), Iron and
Infection, molecular, physiological and clinical aspects (chapter 6).
Chichester: John Wiley & Sons.
Bulte, J.W.M., Miller, G.F., Vymazal, J., Brooks, R.A. & Frank, J.A.
(1997). Hepatic hemosiderosis in non-human primates: Quantification of liver using different field strengths. Magnetic Resonance in
Medicine, 37, 530– 536.
Butler, E.J. (1983). Role of trace elements in metabolic processes. In
B.M. Freeman (Ed.), Physiology and Biochemistry of the Domestic
Fowl, vol. 4 (chapter 10). London: Academic Press.
Iron storage diseases in birds
Chubb, L.G. (1982). Anti-nutritive factors in animal feedstuffs. In W.
Haresign (Ed.), Recent Advances in Animal Nutrition (chapter 2).
London: Butterworths.
Cooper, J.E. (1999) Personal communication .
Cork, S.C (1994). Yersinia pseudotuberculosi s, iron and disease in birds.
PhD Thesis, Massey University, Palmerston North, New Zealand.
Cork, S.C. & Stockdale, P.H.G. (1995). Adenocarcinoma with concurrent haemosiderosis in an Australian Bittern. Avian Pathology, 24
(1), 207–213.
Cork, S.C., Alley, M.R. & Stockdale, P.H.G. (1995). A quantitative
assessment of haemosiderosis in wild and captive birds using image
analysis. Avian Pathology, 24, 225– 239.
Cork, S.C., Marshall, R.B. & Fenwick, S.G. (1998) The effect of
parenteral iron dextran, with or without desferrioxamine, on the
development of experimental pseudotuberculosis in the domestic
chicken. Avian Pathology, 27, 394– 399.
Cork, S.C., Collins-Emerson, J.M., Alley, M.R. & Fenwick, S.G.
(1999). Visceral lesions caused by Yersinia pseudotuberculosi s
serotype II, in different species of bird. Avian Pathology, 28,
393– 399.
Cornelissen, H., Ducatelle, R. & Roels, S. (1995). Successful treatment
of a Channel-billed Toucan (Ramphastos vitellinus) with iron storage
disease by chelation therapy: Sequential monitoring of the iron
content of the liver during the treatment period by quantitative
chemical and image analysis. Journal of Avian Medicine & Surgery,
9, 131–137.
De Sousa, M. (1989). The immunology of iron overload. In De Sousa,
M. & Brock, J.H. (Eds), Iron and Immunity, cancer and infection
(chapter 11). London: John Wiley & Sons.
Dewar, W.A. (1986). Requirements for trace minerals. In C. Fisher &
K.N. Boorman (Eds), Nutrient Requirements of Poultry and
Nutritional Research (chapter 10). Poultry Science Symposium No.
19, London: Butterworths.
Diez, J.M., Agapito, M.T. & Recio, J.M. (1986). The effect of estrogens
on serum ferritin levels in ducks. Revista Espanola Fisiologia, 42,
179–184.
Donoghue, S. & Stahl, S. (1997). Clinical Nutrition of Companion
Birds. Journal of Avian Medicine and Surgery, 11, 228– 246.
Dorrestein, G.M. (1997). Iron in organs: A pathologists view. In
Proceedings of the Fourth European Conference (P 145) London:
Association of Avian Veterinarians.
Frankenhuis, M. T. & Assink, J. A. (1981). Iron accumulation in the
livers of birds of paradise. British Veterinary Zoological Society
Newsletter, 12, 2.
Garcia, F., Ramis, J., & Planas, J. (1984). Iron content in Starlings
(Sturnus vulgaris). Comparative Biochemistry and Physiology, A.
77, 651– 654.
Gerlach, H., Enders, F. & Casares, M. (1998). Discussion of the
increased iron content in the liver of some bird species (particularly
parrots). In Midwest Avian Research expo (pp. 75–78). Toledo, OH:
MARE.
Gonzales, J., Benirschke, K., Saltman, P., Roberts, J. & Robinson, P.T.
(1984). Hemosiderosis in lemurs. Zoo Biology, 3, 255– 265.
Gosselin, S.J. & Kramer, L.W. (1983). Pathobiology of excessive iron
storage in myna birds . Journal of the American Veterinary Medical
Association, 183, 1238–1240.
Griffiths, E. (1993). Iron & Infection. Better understanding at the
molecular level but little progress on the clinical front (Editorial).
Journal of Medical Microbiology, 38, 389– 390.
Griffiths, E. & Bullen, J.J. (1987). Iron & Infection: Future prospects.
In J.J. Bullen & E. Griffiths (Eds), Iron & Infection (chapter 8).
Chichester: John Wiley & Sons.
Harper, E.J. & Skinner, N.D. (1998). Clinical Nutrition of Small
Psittacines and Passerines. Seminars in Avian and Exotic Pet
Medicine, 7, 116–127.
Hartley, W.J., Mullins, J. & Lawson, B.M. (1959). Nutritional siderosis
in the bovine. New Zealand Veterinary Journal, 7, 99–105.
Hill, J.E., Burke, D.L. & Rowland, G.N. (1986). Hepatopathy and
lymphosarcoma in a myna bird with excessive iron storage. Pet bird
medicine; case report. Avian Diseases, 30, 634– 636.
Hill, R., Smith, I.M., Mohammadi, H. & Licence, S.T. (1977). Altered
absorption and regulation of iron in chickens with acute Salmonella
gallinarum infection. Research in Veterinary Science, 22, 371– 375.
11
Hunt, J.R., Gallagher, S.K. & Johnson, L.K. (1994). Effect of ascorbic
acid on apparent iron-absorption by women with low iron stores.
American Journal of Clinical Nutrition, 59, 1381–1385.
Iancu, T.C. (1982). Iron overload. Molecular Aspects of Medicine, 6,
1–100.
Iancu, T.C., Ward, R.J. & Peters, T.J. (1987). Ultrastructural observations in the carbonyl iron-fed rat, an animal model for haemochro matosis. Virchows Archives B, 53, 208– 217.
Iancu, T.C. (1993). Animal models in liver research – iron overload.
Advances in Veterinary Science and Comparative Medicine, 37,
379– 401.
Inan, C., Kilinc, K., Kotiloglu, E., Akman, H.O., Kilic, I. & Michi, J.
(1998). Antioxidant therapy of cobalt and vitamin E in hemosiderosis. Journal of Laboratory and Clinical Medicine, 132, 157–165.
Kim, M., Lee, D.T. & Lee, Y.S. (1995). Iron-absorption and intestinal
solubility in rats are influenced by dietary proteins. Nutrition
Research, 15, 1705–1716.
Kincaid, A.L. & Stoskopf, M.K. (1987). Passerine dietary iron overload
syndrome. Zoo Biology, 6, 79– 88.
Kochan, I. (1973). The role of iron in bacterial infections, with special
consideration of host-tubercule bacillus interaction. Current Topics
in Microbiology and Immunology, 60, 1– 30.
Kruger, N., Kiejewski, H., Konig, R., Schroter, W. & Tillman, W.
(1984). Desferrioxamine in hemosiderosis-proportion of faecal iron
excretion. Blut, 49, 246.
Kübber-Heiss, A. (1994). Zur Morphologie der Lebersiderose bei
Vögeln. Wiener Tierärztliche Monatsschrift, 82, 173–178.
Lowenstine, L.J. & Petrak, M.L. (1980). Iron pigment in the livers of
birds. In R.J. Montali & G. Migaki (Eds), The Comparative
Pathology of Zoo Animals (pp. 127–135). Washington, DC: Symposium of the National Zoological Park, Smithsonian Institute Press.
Lowenstine, L.J. (1986). Nutritional disorders of birds. In M.E. Fowler
(Ed.), Zoo & Wild Animal Medicine. 2nd edn (pp. 202– 205).
Philadelphia: W.B.Saunders & Co.
Miller, G.F., Barnard, D.E., Woodward, R.A., Flynn, B.M. & Bulte,
J.W.M. (1997). Hepatic hemosiderosis in common marmosets
(Callithrix jacchus). Effect of diet on incidence and severity.
Laboratory Animal Science, 47, 138–142.
MacDonald, R.A. (1972). Abnormal tissue iron. Methods and Achievments in Experimental Pathology, 6, 193– 206.
Morris, P.J., Avgeris, S.E. & Baumgartner, R.E. (1989). Haemochromatosis in a greater indian hill myna (Gracula religiosa). Journal of the
American Veterinary Medical Association, 3, 87– 92.
Nhonoli, A.M. (1973). Haemochromatosis /Haemosiderosis, a review
article. East African Medical Journal, 50, 229– 231.
Osborn, D. (1979). Seasonal changes in the fat, protein and metal
content of the liver of the starling (Sturnus vulgaris). Environmental
Pollution, 19, 145–155.
Osborn, D. & Young, W. (1985). Inter-relation between toxic and
essential metals in the livers of wild starlings. In C.F. Mills, I.
Brenner & J.K. Chester (Eds). Trace Elements in Man and Animals
(pp. 864– 866). Wallingford: CAB.
Perls, M. (1867). Nachweis von eisonxyd in geweissen pigmentation.
Virchows archive für Pathologische anatomie und physiologie für
klinische medizin, 39, 42.
Planas, J., de Castro, S. & Recis, J.M. (1961). Serum iron and its
transport mechanisms in the fowl. Nature, 189, 668– 669.
Powell, L.W., Basset, M.L. & Halliday, J.W. (1980). Hemochromatosis :
1980 Update. Gastroenterology, 78, 374– 381.
Roels, S., Ducatelle, R. & Cornelissen, H. (1996). Quantitative image
analysis as an alternative to chemical analysis for follow-up of liver
biopsies from a toucan with hemochromatosis – A technique with
potential value for the follow-up of hemochromatosis in humans.
Analytical and Quantitative Cytology and Histology, 18, 221– 224.
Sayers, M.H., English, G. & Finch, C. (1994). Capacity of the iron
store-regulator in maintaining iron balance. American Journal of
Hematology. 47, 194–197.
Schoemaker, N.J., Lumeij, G.M., Dorrestein, G.M. & Beynen, A.C.
(1999). Voedingsgerelateerde problemen bij gezelschaps-vogels .
Tijdschrift voor Diergeneeskund e, 124, 39– 43.
Spelman, L.H., Osborn, K.G. & Anderson, M.P. (1989). Pathogenesis of
hemosiderosis in lemurs – role of dietary iron, tannin, and ascorbic
acid. Zoo Biology, 8, 239– 251.
12
S. C. Cork
Strohmeyer, G. & Stremmel, W. (1984). Treatment of hemosiderosis
with desferioxamine. Deutsche Medizinische Wochenschrift, 109,
1669– 1670.
Taylor, J.J. (1984). Iron accumulation in avian species in captivity. Dodo.
Journal of the Jersey Wildlife Preservation Trust, 21, 126–131.
Turlin, B. & Deugnier, Y. (1998). Evaluation and interpretation of iron in
the liver. Seminars in Diagnostic Pathology, 15, 237– 245.
Wadsworth, P.F., Jones, D.M.& Pugsley, S.L. (1983). Hepatic haemosiderosis in birds at the Zoological Society of London. Avian Pathology,
12, 321– 330.
Ward, R.J., Smith, T., Henderson, G.M. & Peters, T.J. (1991).
Investigation of the aetiology of haemochromatosis in Starlings
(Sturnus vulgaris). Avian Pathology, 20, 225– 232.
Weinberg, E.D. (1978). Iron & Infection. Microbiological Reviews, 42,
45– 65.
Weinberg, E.D. (1984). Iron withholding. A defence against infection
and neoplasia. Physiological Reviews, 64, 65–102.
Wilson, R.B. (1994). Hepatic hemosiderosis and klebsiella bacteremia in
a Green Aracari (Pteroglossus viridis). Avian Diseases, 38, 679– 681.
Witzleben, C. L. & Buck, B.E. (1971). Iron Overload Hepatotoxicity: A
postulated pathogenesis. Clinical Toxicology, 4, 579– 583.
RÉSUMÉ
Maladies dues au stockage du fer chez les oiseaux
L’administration parentérale de fer est toxique pour de nombreuses
espèces mais, du fait que la consommation de fer à partir de la ration
alimentaire est régulée par l’intestin, des intoxications aigus ne sont pas
observées dans les conditions naturelles. Une ingestion chronique de
quantités importantes de fer assimilable dans la ration alimentaire peut
conduire à un stockage du fer dans le foie de nombreuses espèces y
compris l’homme. L’excès de fer est stocké dans les hépatocytes sous
forme d’hémosidérine et peut être évalué quantitativement par une
biopsie du foie ou lors d’autopsie par l’utilisation d’une coloration
spécifique comme la coloration du fer de Perls et/ou par des tests
biochimiques. Le fer peut également être trouvé dans les cellules de
Kupffer au niveau du foie et des macrophages de la rate principalement
quand des maladies concomitantes sont présentes telles que l’anémie
hémolytique, une septicémie, une néoplasie et en cas de sousalimentation. L’accumulation de fer dans le foie connue sous le nom de
hémosidérose n’est pas forcément associée à une maladie clinique bien
que dans des cas graves des lésions du foie peuvent être observées. Il
est probable que les maladies concomitantes sont fortement responsables de la nature et de l’intensité des changements pathologiques
décrits dans la plupart des cas d’hémosidérose. Chez quelques
individus humains, il peut y avoir une prédisposition génétique à
l’accumulation de fer, l’hémochromatose associée à une mauvaise
régulation de la consommation du fer au long de l’intestin, dans les cas
graves des pigments ferriques peuvent être observés au niveau du foie,
de la rate, de la paroi intestinale, des reins et du cœur avec
développement ultérieur d’ascite, de crise cardiaque et de pathologi e
multisystémique. La maladie associée à une accumulation de fer dans
le foie et dans les autres tissus a fait l’objet de rapport chez de
nombreuses espèces d’oiseaux bien que plus communément rapportée
chez les ménates religieux (Gracula religiosa). Il est probable que la
tolérance varie en fonction des espèces aviaires et que les facteurs
prédisposant majeurs peuvent varier même au sein de groupes très
proches sur le plan taxonomique .
ZUSAMMENFASSUNG
Eisenspeicherkrankheiten bei Vögeln
Parenterales Eisen ist für viele Spezies toxisch, weil aber die
Aufnahme von Eisen aus der Nahrung im Darm reguliert wird, gibt
es unter natürlichen Bedingungen keine akute Intoxikation. Die
dauernde Aufnahme großer Mengen von absorbierbarem Eisen in der
Nahrung kann bei vielen Spezies einschließlich der Menschen zur
Eisenspeicherung in der Leber führen. Das übersch üssige Eisen wird
als Hämosiderin in den Leberzellen gespeichert und kann mittels
Leberbiopsie oder bei der Sektion mit Hilfe von speziellen Färbungen
wie der Berliner-Blau-Reaktion und/oder biochemischen Tests quantitativ festgestellt werden. Eisen kann auch in den Kupffer-Sternzellen
in der Leber und in den Makrophagen der Milz gefunden werden,
insbesondere beim Vorliegen von gleichzeitigen Leiden wie hämolytische Anämie, Septikämie, Neoplasie und Hungern. Die Eisenakkumulation in der Leber, auch als Hämosiderose bekannt, mag nicht
immer mit einer klinischen Erkrankung verbunden sein, obgleich es
in schweren Fällen zu einem Leberschaden kommen kann. Es ist
wahrscheinlich, dass für den Grad und die Beschaffenheit der in den
meisten Hämosiderosefällen beschriebenen pathologischen Veränderungen größtenteils Begleiterkrankungen verantwortlich sind. Bei
manchen Menschen kann es eine genetische Prädisposition für eine
Eisenspeicherkrankheit, die Hämochromatose, geben, verbunden mit
einer mangelhaften Regulierung der Eisenaufnahme durch den Darm
hindurch; in schweren Fällen ist Eisenpigment in der Leber, Milz,
Darmwand, Niere und im Herzen nachweisbar, mit anschließender
Entwicklung von Aszites, Herzinsuffizienz und pathologische n
Befunden in mehreren Systemen. Klinische Erkrankungen in Verbindung mit der Akkumulation von Eisen in der Leber und in anderen
Geweben sind bei vielen Vogelarten festgestellt worden, am häufigsten jedoch bei Beos (Gracula religiosa) und Tukanen (Ramphastos
sp.). Es ist wahrscheinlich, dass die Toleranz gegen die Ansammlung
von Gewebeeisen bei den einzelnen Vogelarten variiert, und dass die
hauptsächlichen prädisponierenden Faktoren unterschiedlich sein können, sogar innerhalb eng verwandter taxonomischer Gruppen.
RESUMEN
Enfermedades por deposito de hierro en aves
El hierro administrado por v´õ a parenteral es tóxico en múltiples
especies aunque, debido a que la absorción de hierro a partir de la
dieta es regulada por el intestino, la intoxicación aguda no se da en
condiciones naturales. La ingestión crónica de grandes cantidades de
hierro absorbibles en la dieta puede dar lugar al depósito de hierro
en el h´õ gado en muchas especies, incluida la especie humana. El
exceso de hierro es acumulado por los hepatocitos como hemosiderina que puede ser cuantificada mediante biopsia hepática o en la
necropsia, utilizando técnicas especiales como la de tinción de hierro
de Perls y/o tests bioqu´õ micos. El hierro también se puede localizar
en las celulas de Kupffer del h´õ gado y en los macrófagos del bazo,
especialmente cuando se dan enfermedades concurrentes como la
anemia hemol´õ tica, septicemia, neoplasias o periodos largos de
inanición. El acumulo de hierro en el h´õ gado también conocido como
hemosiderosis, no esta siempre asociado con manifestaciones cl´õ nicas
de enfermedad, aunque en casos graves se puede producir un daño
hepático. Es probable que las condiciones de enfermedades concurrentes sean mayoritariamente responsables de la naturaleza y el
grado de los cambios patológicos descritos en la mayor´õ a de los casos
de hemosiderosis. En algunos individuos humanos puede haber una
predisposición genética a la enfermedad por depósito de hierro,
hemocromatosis, asociada a una mala regulación de la entrada de
hierro en el intestino; en casos graves el pigmento férrico se puede
detectar en h´õ gado, bazo, pared intestinal, riñón y corazón con el
consiguiente desarrollo de ascitis, fallo card´õ aco y patolog´õ a multistémica. La enfermedad cl´õ nica asociada a la acumulaci ón de hierro
en el h´õ gado y otros tejidos ha sido descrita en muchas especies
aviares aunque aparece mayoritariamente citada en mainate (Gracula
religiosa ) y tucanes (Ramphastos sp). Es probable que la tolerancia
a la acumulaci ón de hierro tisular var´õ e en las diferentes especies de
aves y que los factores predisponentes puedan diferir incluso entre
grupos taxonómicos muy próximos.