Human Reproduction Vol.18, No.4 pp. 756±759, 2003
DOI: 10.1093/humrep/deg136
Time elapsed from onset of symptoms to diagnosis of
endometriosis in a cohort study of Brazilian women
M.S.Arruda1, C.A.Petta1,3, M.S.AbraÄo2 and C.L.Benetti-Pinto1
1
Department of Obstetrics and Gynaecology, Universidade Estadual de Campinas (UNICAMP), Campinas and 2Department of
Obstetrics and Gynaecology, Universidade de SaÄo Paulo (USP), SaÄo Paulo, Brazil
3
BACKGROUND: The study aim was to assess the time elapsed between onset of symptoms and diagnosis of endometriosis, and to identify the factors associated with diagnostic delay in a group of Brazilian women. METHODS:
In this retrospective cohort study, 200 women with surgically con®rmed endometriosis were interviewed at an endometriosis outpatient clinic. RESULTS: The median (interquartile range) time elapsed from onset of symptoms until
diagnosis of endometriosis was 7.0 (range 3.5±12.1) years. The younger the women at onset of symptoms, the longer
the period for diagnosis to be made: the median delay was 12.1 (range 8.0±17.2) years in women aged <19 years,
and 3.3 (range 2.0±5.5) years in women aged >30 years. The median time period between onset of symptoms and
diagnosis was 4.0 (2.0±6.0) years for women whose main complaint was infertility, but 7.4 (3.6±13.0) years for those
with pelvic pain. CONCLUSIONS: The delay in diagnosis of endometriosis was considered to be long, and especially
so for young women with pelvic pain. More information relating to endometriosis should be offered to general physicians and gynaecologists in order to reduce the time taken to diagnose this condition.
Key words: diagnosis/endometriosis/infertility/pain
Introduction
Despite the considerable amount of information published on
many different aspects of endometriosis, few studies have
evaluated the time which has elapsed between the onset of
symptoms and diagnosis of the condition.
An initial study provided a retrospective analysis of this
delay in women recruited from endometriosis self-help groups
in the UK and USA (Had®eld et al., 1996), and showed the
period to be ~12 years in the US and 8 years in the UK. These
authors also referred to two unpublished studies investigating
the same topic. One study which included data from a survey of
2102 members of the National Endometriosis Society of Great
Britain, carried out in 1993, showed an average delay of 6.8
years, while a second study conducted by the Australian
Endometriosis Association in 748 women showed a delay of
6.1 years. Subsequently, the delay was found by another group
to be 6.3 years in women complaining of chronic pelvic pain,
and 3.1 years for women with infertility (Dmowski et al.,
1997).
Women with symptomatic endometriosis contend that they
are strongly and adversely affected by the delay in making a
diagnosis, and that their general health is affected unnecessarily by such a delay (Kennedy, 1991). Bearing in mind the
adverse effects that endometriosis has on these women, and the
paucity of methods available in developing countries to
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evaluate the delay in diagnosis, the present study was instituted
in a group of Brazilian women with surgically con®rmed
endometriosis in order to verify this delay.
Material and methods
Between September 2000 and September 2001, a total of 200
consecutive women with surgically con®rmed endometriosis
was invited to reply to a questionnaire by private interview
during the ®rst consultation at the endometriosis outpatient
clinic at the Department of Obstetrics and Gynaecology,
School of Medicine, State University of Campinas
(UNICAMP), Campinas, Brazil. This study was approved by
the Ethical Committee of the University, and all subjects
signed an informed consent form before participating.
The questionnaire included data about sociodemographic
characteristics, gynaecological and obstetrical history, age at
which symptoms of pain and/or infertility were ®rst experienced, intensity of pain at the onset of symptoms, and age when
these symptoms were ®rst reported to a physician. The median
time between the surgical diagnosis and the interview was 26
months.
The date of the ®rst diagnostic surgical intervention
(laparoscopy or laparotomy) was registered, and the severity
of the disease at that time was scored according to the revised
ã European Society of Human Reproduction and Embryology
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To whom correspondence should be addressed at: Caixa Postal 6181 CEP 13084-971, Campinas, Brazil.
E-mail: cpetta@attglobal.net
Diagnostic delay in women with endometriosis
Statistical analysis
The median and the interquartile range were used to describe
the sample. Because of the asymmetric distribution of the
variables (time from onset of symptoms to the ®rst appointment; time from the ®rst appointment to a diagnosis; and total
time from onset of symptoms to a diagnosis of endometriosis)
and the presence of atypical values (outliers), the nonparametric Wilcoxon test was used to evaluate the association
between dependent and independent variables. The level of
signi®cance was set at P < 0.05. Although the infertility group
was small (n = 20) compared with the chronic pelvic pain
group (n = 180), after performing a power analysis (a = 5%; b
= 80%), the sample size was considered appropriate (P = 0.01)
for use of the non-parametric test (Noether, 1987).
Results
At the time of the interview, 100 (50%) women were aged
between 30 and 39 years, 41 (20.5%) were aged >40 years, and
only ®ve (2.5%) were aged <20 years. Half of the women were
nulligravida, 73% were white, and 62% had more than 8 years
of formal school education.
Dysmenorrhoea was the main complaint for 134 women
(67%), chronic pelvic pain for 35 (12.5%), and dyspareunia for
11 (5.5%). Twenty patients (10%) reported infertility as the
main complaint. A total of 177 women (88.5%) experienced
more than one symptom, and 126 women (70%) who suffered
from pelvic pain classi®ed their symptoms as severe. The
overall median time from the onset of symptoms to a diagnosis
of endometriosis was 7.0 years, with an interquartile range of
3.5 to 12.1 years.
The median age at the time of onset of symptoms was 20.5
years for those women whose main complaint was pelvic pain,
Table I. Median (interquartile range) age at onset of symptoms, at
reporting symptoms to a doctor, and at diagnosis in women presenting for
pelvic pain and infertility
Age at onset of symptoms (years)
Age at reporting symptoms (years)
Age at diagnosis (years)
Median delay from onset of
symptoms to diagnosis (years)
aWilcoxon
Pelvic pain
(n = 180)
Infertility
(n = 20)
20.5 (14.0±27.5)
23.0 (17.0±30.0)
33.0 (29.0±39.0)
7.4a
23.5 (20.0±25.5)
25.5 (22.5±28.0)
30.0 (29.0±32.0)
4.0a
test, P < 0.01.
Table II. Median time (years) elapsed from the ®rst symptoms to seeing a
doctor and to the surgical diagnosis according to age at onset of symptoms
Age at onset of Time from ®rst Time from seeing a Total time elapsed
symptoms (years) symptoms to
doctor to surgical
from ®rst symptoms
seeing a doctor diagnosis
to diagnosis
<19
20±29
>30
Pa
aWilcoxon
2.0
0.5
0.2
< 0.01
9.0
4.0
3.0
< 0.01
12.1
4.5
3.3
< 0.01
test.
Table III. Median (interquartile range) time (years) elapsed from ®rst
symptoms to seeing a doctor and to the diagnosis, according to the main
symptom
Main complaint
n
From ®rst
symptoms
to seeing a
doctor
From seeing
a doctor to
diagnosis
From ®rst
symptoms to
diagnosis
Chronic pelvic pain
Dysmenorrhoea
Dyspareunia
Infertility
Total
35
134
11
20
200
0.3
0.6
1.0
1.7
0.9
4.0
6.5
4.0
2.0
5.0
4.2
8.4
5.0
4.0
7.0
(0.2±1.0)
(0.3±3.0)
(0.2±3.0)
(1.0±2.0)
(0.2±2.0)
(2.0±6.0)
(3.0±11.0)
(1.0±11.0)
(0.7±3.5)
(2.0±9.5)
(2.2±6.3)
(5.0±14.0)
(2.2±15.2)
(2.1±6.0)
(3.5±12.1)
and 23.5 years for those with infertility complaints. The median
age at diagnosis was 33.0 years for the group with pelvic pain,
and 30.0 years for those who were infertile (Table I).
The median time elapsed between onset of symptoms and
diagnosis was shorter for women complaining of infertility [4.0
(range 2.0±6.0) years] than in those with pelvic pain [7.4 (range
3.6±13.0) years] (P < 0.01). In terms of seeking help, the
infertility group took a median of 1.7 (1.0±2.0) years, which
was signi®cantly longer than women with pelvic pain, who
took 0.5 (range 0.2±2.0) years.
Younger women took a signi®cantly longer time to report
their symptoms to a doctor, and also had to wait for longer until
a de®nitive diagnosis was made (Table II). The time interval
from the ®rst symptoms to a diagnosis was not signi®cantly
different in the four stages of the disease, namely 7.0, 6.8, 7.4
and 6.7 years for stages I, II, III and IV respectively.
The delay from onset of symptoms to a ®rst consultation,
from the ®rst consultation to a diagnosis of endometriosis, and
the total time from onset of symptoms to diagnosis according to
the main complaint are detailed in Table III. No relationship
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American Society for Reproductive Medicine classi®cation
(American Society for Reproductive Medicine, 1997). These
data were obtained from the women's medical records or
surgical reports and/or video tapes of surgery sent by the
referring physician.
Women with more than one symptom were asked to point
out the main reason why they decided to seek help. Whenever
pain was the main complaint, whether chronic pelvic pain (pain
unrelated to menses and lasting for at least 6 months),
dysmenorrhoea or dyspareunia, women were asked to classify
their pain (at the time of the initial report) as either: (i) mild, if
there was mild interference with normal activities and usually
no medication was required; (ii) moderate, if there was
noticeable interference with normal daily activities and analgesics were usually required; or (iii) severe, if the patient was
unable to function normally or had to visit emergency units for
pain relief.
In order to obtain more precise data, attempts were made to
improve the patients' recall of the timing of the onset of
symptoms and the time they initially reported their symptoms
to a physician. They were asked about their age at menarche,
when they were married or became pregnant, the date they
delivered their children, their school and job activities, and
their use of analgesics or visits to emergencies rooms.
M.S.Arruda et al.
Discussion
The overall median time of 7.0 years from onset of symptoms
to a diagnosis of endometriosis observed in the present study
was similar to that reported by both The National
Endometriosis Society of Great Britain and the Australian
Endometriosis Association (Had®eld et al., 1996), and was also
in agreement with these authors' own ®ndings, which indicated
a mean delay in diagnosis of 11.7 and 7.9 years for women in
the USA and UK respectively. The delay in diagnosis in
infertile patients was shorter than that in patients with pelvic
pain, and was similar to that reported elsewhere (Dmowski
et al., 1997). This is most likely a consequence of a better
established protocol to investigate infertile women, which
includes diagnostic laparoscopy.
The age at onset of symptoms was inversely associated with
the delay in diagnosing endometriosis. Although 88 (44%) of
the present patients initially reported their symptoms to their
physicians before the age of 20, only seven (3.5%) were
diagnosed with endometriosis before that age. Unfamiliarity
with menstrual cramps during the ®rst years after menarche,
and the widespread notion that menstrual periods are painful,
are two possible reasons why these women took longer to seek
help. However, it is dif®cult to understand why the median
period from initial consultation to a diagnosis was 9.0 years
when symptoms started during adolescence, but only 3.0 years
when they started at the age of 30 years or more.
Physicians might consider painful menstruation a physiological condition, even when severe, subsiding with analgesics
or oral contraceptives. It is also possible that adolescents might
be less convincing and persuasive than older women when
reporting symptoms, and may also feel uncomfortable when
reporting the occurrence of pain during intercourse. Among the
adolescent patients interviewed, only one patient reported
dyspareunia spontaneously as the main complaint, and 49
758
reported it as a secondary complaint. In addition, a physical
examination may be more dif®cult in adolescents, especially if
they are not sexually active.
Although symptoms of pain are reported by almost one-third
of all gynaecological patients, and about 50% of menstruating
adolescents and young women suffer from painful menstruÈ zaksit et al., 1995), endometriosis should be suspected
ation (O
in adolescents because it is a common cause of pain and
dysmenorrhoea, affecting 45±70% of those with chronic pelvic
pain (Propst and Laufer, 1999). One study comparing
preoperative pelvic examination and ultrasonographic ®ndings
with laparoscopy in 45 adolescents with chronic pelvic pain
showed that when both, pelvic examination and ultrasound
were normal, 50% of these cases were abnormal at laparoscopy
È zaksit et al. 1995).
and 20% of them had endometriosis (O
Despite many limitations of the Brazilian public health
system, the time from an initial complaint to the diagnosis of
endometriosis was no longer than is observed in the UK and
USA (Had®eld et al., 1996).
Although laparoscopy has become a valuable tool in the
investigation of pelvic pain, laparotomy was found still to be
used as a diagnostic method, especially in public hospitals
where laparoscopy is still not widely available. Indeed, the high
cost of laparoscopy in private institutions may force women to
seek free-of-charge treatment at public hospitals, and this will
result in long waiting lists for scheduled appointments at
referral centres. In addition, gynaecologists might lack the skill
to perform a laparoscopy and would be reluctant to refer their
patients to a specialized centre. This is a phenomenon observed
in all parts of the world, even in developed countries (Jones
et al., 2002).
The high prevalence of moderate and severe disease among
the interviewed patients was expected because the present
investigation was carried out at a tertiary care centre, with
referred cases. As the University also has an infertility clinic to
which infertile couples are usually referred, few of the present
patients listed infertility as their main complaint. For these
reasons, the population investigated may not re¯ect the
situation of the general population with endometriosis.
The overall long delay in the present study to reach a
diagnosis of endometriosis corroborates with a previous
observation (Kennedy, 1991): ``Women frequently complain
that the diagnosis was made only after months and months of
being fobbed off or ignored by doctors''. Whether or not this
delay is associated with a progression of the disease stages is a
controversial issue. Although some publications have attempted to support the concept that endometriosis is a
progressive disease (Koninckx et al., 1991; Dmowski et al.,
1997), conclusive data are still lacking.
Consequently, it is impossible to be sure that an earlier
diagnosis would detect endometriosis at a less severe stage of
the disease, though the impact of endometriosis on the lives of
these women could be minimized. Appropriate medical
therapy would reduce absenteeism at school or work and
make sexual intercourse more enjoyable for those with pelvic
pain, while adequate therapy would be indicated for those with
infertility.
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between the intensity of pain and the stage of the disease was
found, however (data not shown).
A comparison was also made as to where the diagnosis was
carried out, the percentage of laparoscopic procedures performed, and the delay in diagnosis for each group. Diagnoses
were made at the authors' institution (a public university
centre) in 106 women (53%), in a private setting in 62 (31%),
and in other public hospitals in 32 (16%). The diagnosis
performed laparoscopically in 66% of women at the authors'
institution, and in 77 and 25% at private institutions and other
public hospitals respectively. The median delay from onset of
symptoms and diagnosis at the authors' hospital and other
public hospitals (6.3 years) was shorter than that at private
clinics (9.1 years).
No correlation was found between the patients' years of
formal school education and the time interval for a diagnosis of
endometriosis. Women with <7 years of formal education took
a median period of 0.8 years to report symptoms to a doctor,
whereas those with >7 years of education took 0.9 years (P =
NS). The total delay from onset of symptoms to a surgical
diagnosis in these patient groups was 6.2 and 7.2 years
respectively (P = NS).
Diagnostic delay in women with endometriosis
Acknowledgements
The authors thank Edson Zangiacomi Martinez and Gislaine Carvasan
for their assistance in the data analysis. These results were presented
as a poster at the VIII World Congress on Endometriosis, San Diego,
CA, United Sates, February 24±27, 2002.
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Submitted on January 29, 2002; resubmitted on November 19, 2002; accepted
on November 28, 2002
759
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The present study provides evidence of the situation
regarding the diagnosis of endometriosis in a less-developed
country. There are some methodological limitations to be
considered, however: the precise date of the onset of symptoms
and the date that these symptoms were reported to a physician
were totally dependent on the patients' ability to remember
facts that very often occurred a long time ago. Even with the
investigators' efforts to improve the patients' recollection of
dates and times, this may not be absolutely accurate.
In addition, it is dif®cult to assign a precise stage of the
disease retrospectively for patients referred to this service, on
the basis of surgical records alone. To minimize this limitation,
patients who could not have their disease stage assigned were
excluded from the study. Despite all of these possible biases,
personal interviews might provide more accurate information
than self-answered questionnaires sent by mail.
Another possible criticism of the present study is the very
small number of patients included in the infertility group.
Although pain and infertility have different starting points, and
also have different in¯uences on any decision to perform
laparoscopy, the statistical power of the non-parametric test
used enabled comparisons to be made between the two groups.
Hence, it was decided to retain this group in order to show the
important differences in the delay to a diagnosis of endometriosis in both groups.
In conclusion, the present study shows that the delay in
diagnosing endometriosis was considerably long, and especially so in young women with pelvic pain and in adolescents.
Clearly, more information about endometriosis must be made
available to general physicians and gynaecologists in order to
reduce the time taken to diagnose this condition.