Human Fertility

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Tubal pelvic damage: Prediction and prognosis

Valentine Akande

To cite this article: Valentine Akande (2002) Tubal pelvic damage: Prediction and prognosis,
Human Fertility, 5:sup1, S15-S20, DOI: 10.1080/1464727022000199861

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Published online: 03 Jul 2009.

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 Human Fertility (2002) 5 Supplement, S15S20
Tubal pelvic damage: prediction and prognosis
Valentine Akande
Division of Obstetrics and Gynaecology, University of Bristol, St Michaels Hospital, Bristol BS2 8EG, UK
Tubal pelvic damage is a common cause of infertility, and
laparoscopy is the accepted gold standard for its diagnosis.
However, laparoscopy is both costly and invasive. Chlamydia
is now recognized as the most common cause of tubal pelvic
damage. In contrast to laparoscopy, evidence of past chlam-
ydial infection using serology is readily available, and the
Downloaded by [University Library Utrecht] at 00:31 17 March 2016
test is simple and quick to perform. As such, serology can be
used as a screening test in infertile women. It is accepted
that screening tests may have higher margins of error and
may be less accurate than diagnostic tests. Screening is
most valuable when detecting a disease for which the
treatment is more effective when undertaken at the earliest
opportunity. Because there are justified constraints to the in-
discriminate use of laparoscopy, there is a need to minimize
the number of patients who do not have disease (false
positives) who are subjected to this diagnostic investigation.
An appropriate Chlamydia antibody titre that would dis-
tinguish women at risk of tubal pelvic damage should be
determined using diagnostic test analysis and clinical judge-
ment. Identification by serology of women who are likely to
have damage would enable these women to undergo a diag-
nostic test such as laparoscopy sooner, allowing treatment to
be provided earlier. However, the severity of tubal pelvic
damage varies, and the need to distinguish women with a
favourable or unfavourable prognosis after treatment using a
simple classification system is discussed.
Tubal pelvic damage involving pelvic adhesions, tubal occlu-
sion or tubal fibrosis is a major cause of infertility, and the inci-
dence in the infertile population ranges from 14 to 38% (Cates
et al., 1985; Hull et al., 1985) and up to 81% in developing coun-
tries (Blumenthal et al., 1984; World Health Organization, 1987).
The damage is most commonly due to ascending genital tract
infection although it may also occur after surgery and extra-
tubal infections arising in the abdomen and pelvis. In the de-
veloped world, the most common cause of tubal pelvic damage
is Chlamydia trachomatis (World Health Organization, 1995;
ESHRE, 1996). C. trachomatis, an important pathogen of humans,
is one of four species within the genus Chlamydia (Schachter,
1999) and is a small obligate intracellular, Gram negative bac-
terial pathogen (McGregor and French, 1991). This unique
bacterium is a true parasite and has a life cycle involving
extracellular and intracellular phases (Faro, 1991; Schachter,
1999).
Chlamydial infections of the genital tract have a worldwide
distribution, and are prevalent in both industrialized countries
and the developing world (Stamm, 1999). The exact mechanism
2002 The British Fertility Society
1464-7273/2002
that accounts for the adhesions, tubal damage or occlusion after
chlamydial infection in humans is unknown. However, it is
believed to be primarily immunologically mediated and not a
direct consequence of destruction of tissue by the organism
(Rice and Schachter, 1991; Beatty et al., 1994). Fallopian tube
tissue cultured in vitro with C. trachomatis shows little observ-
able damage (Witkin et al., 2000). As the organism is intracellu-
lar it is protected from humorally mediated host defences,
which may account for the low antibody concentrations in
uncomplicated infections and the prolonged persistence of un-
treated or latent infection (McGregor and French, 1991).
Evidence of previous chlamydial infection is common among
infertile women (Eggert-Kruse et al., 1997). Women found to
have scarred or occluded tubes usually have no history of
pelvic inflammatory disease (PID) (Kane et al., 1984; Anestad
et al., 1987), which is often due to previous silent chlamydial
infection (Cates et al., 1993). A few infected women may ex-
perience mild symptoms. However, most cases of chlamydial
PID are asymptomatic (Kelver and Nagamani, 1989) and the
sole manifestation is pelvic or tubal damage discovered during
the course of investigations for infertility (Kelver and Nagamani,
1989). This silent salpingitis, which is not easily recognized on
clinical grounds (Cates and Wasserheit, 1991), accounts for a
sizeable proportion of cases of tubal infertility (Westrom, 1987).
Chlamydia apparently causes more severe subclinical tubal in-
flammation and ultimately tubal damage than other agents
despite its more benign presentation (Cates and Wasserheit,
1991). C. trachomatis can also be found in apparently healthy
Fallopian tubes (Menchaca et al., 1988; Shepard and Jones,
1989; Marana et al., 1990; Stacey et al., 1990). Superficial in-
fections (for example cervicitis) are considered to provide a
weak stimulus for antibody formation, whereas infiltrating
disease leading to upper genital infections is associated with
sero-conversion. IgM production is often transient, whereas
serum IgG antibodies persist for years and can be used as a
marker of previous infiltrating chlamydial infection.
Screening for tubal pelvic damage
Owing to their cost and invasiveness, both laparoscopy and
hysterosalpingography, which are used in the diagnosis of tubal
pelvic damage, are unsuitable for large-scale screening for this
condition in infertile women. In addition, the overall sensitivity
of hysterosalpingography for the detection of tubal pelvic
damage is only 65% (Swart et al., 1995). Hysterosalpingography
is more specific in the detection of tubal occlusion than pelvic ad-
hesions (Swart et al., 1995). The sensitivity of Chlamydia serology
is similar to that of hysterosalpingography (Mol et al., 1997).
However, the non-invasive nature and lower cost of serology
enable its wide use in infertility practice to screen for tubal
 S16 V. Akande
pelvic damage (Mol et al., 2001). Screening is defined as a pro-
cedure that helps to identify a specified disease or condition.
As most screened individuals will be unaffected, the test must
be safe and acceptable. In contrast, a diagnostic test is defined
as the application of a variety of examinations or tests to
patients to identify the exact condition. The two approaches
are not mutually exclusive (Peters et al., 1996). In this context,
laparoscopy, possibly complemented by hysterosalpingogra-
phy, would serve as a diagnostic test. Tests have three main
uses: diagnosis of disease, screening, and patient management.
From a practical point of view a diagnostic test is useful only if
the test result influences patient management (Campbell and
Machin, 1993). Therefore, how effective is a blood test for
evidence of past chlamydial infection? The questions to ask are:
Can the blood test readily detect serum antibodies?
What is the prevalence of tubal pelvic damage in the
Downloaded by [University Library Utrecht] at 00:31 17 March 2016
population?
How reliably can the blood test detect tubal pelvic damage?
What is the relationship between antibody titre and severity
of damage?
How is a cut-off level (antibody titre) of predictive value
chosen?
Can antibody titres be used to predict the probability of live
birth?
Can the blood test readily detect serum antibodies?
The whole inclusion immunofluorescence test is a sensitive
and specific serological test for Chlamydia IgG antibody
(Richmond and Caul, 1975). Other serological tests used
differ in detection method and source of antigen. The micro-
immunoflourescence method detects primarily type-specific
antibodies and should have the highest specificity for detecting
the organism, although at the expense of sensitivity. In this
test, different serovars should be mixed to detect all possible
C. trachomatis serotypes. The micro-immunofluorescence test is
difficult to standardize and is technically demanding, and thus
its use has been restricted to a relatively small number of lab-
oratories. The other methods (enzyme-linked immunoassay
and immunoperoxidase assay) use antigens that react more
broadly and are not specific for the Chlamydia genus.
What is the prevalence of tubal pelvic damage in the population?
The prevalence of women with evidence of previous chlam-
ydial infections is much higher than those with active or
current infection. It has been estimated that up to 40% of sexu-
ally active women have been exposed to C. trachomatis and
have positive antibodies for the organism (Faro, 1991). A large
population-based epidemiological study (Jonsson et al., 1995)
found that 2.7% of the population had (current) genital chlam-
ydial infection, whereas 24.7% of the population studied (611)
were sero-positive (previous infection) for C. trachomatis. Similar
findings were reported in sero-epidemiological studies (Eggert-
Kruse et al., 1997) of infertile couples and of women attending
venereal disease clinics (Schachter et al., 1979). The discrepancy
in genital infection isolation rates contrasted with high sero-
positivity rates as indices of previous infection probably re-
flects cumulative exposure to Chlamydia.
How reliably can the blood test detect tubal pelvic damage?
Despite wide variations in design, several studies have
consistently demonstrated a significant association between
high antibody titres to Chlamydia and the frequency of tubal
infective damage (Punnonen et al., 1979; Henry-Suchet et al.,
1981; Jones et al., 1982; Moore et al., 1982; Gump et al., 1983;
Conway et al., 1984; Kane et al., 1984; Guderian and Trobough,
1986; Anestad et al., 1987; Robertson et al., 1987; Kelver and
Nagamani, 1989; Cetin et al., 1992; Lucisano et al., 1992;
Kalogeropoulos et al., 1993; Spandorfer et al., 1999). After the
introduction of Chlamydia serology (immunofluorescence test)
in a study of over 1000 women who underwent diagnostic
laparoscopy, the relative risk (in relation to the whole study
population) for detecting tubal pelvic damage increased from
0.26 at a titre of < 1:64 to 11.37 in women with a titre of 1:2048
(Akande, 2001; Akande and Jenkins, 2001).
What is the relationship between antibody titre and severity of
damage?
The severity of tubal disease with regards to adhesions,
tubal occlusion (Tanikawa et al., 1996) and endosalpingeal
damage (Minassian and Wu, 1992) has been positively corre-
lated with increasing antibody titres to Chlamydia. The severity
of tubal damage despite mild or absent clinical symptoms is
probably the result of chlamydial salpingitis causing more
chronic inflammation than that caused by other organisms.
This hypothesis (Cates and Wasserheit, 1991) is supported by
the low prevalence of IgM antibody to Chlamydia among
women with acute salpingitis (Mardh et al., 1981).
How is a cut-off level (antibody titre) of predictive value chosen?
Approaches to dealing with the problem of a cut-off titre
have to take into account the quantitative nature of serology in
relation to frequency of disease. For each antibody titre the
sensitivity, specificity, and positive and negative likelihood
ratios should be calculated (Land et al., 1998; Akande et al.,
2000). These parameters can be used to dichotomize patients
into those who are at high risk and those who are at low risk of
being found with tubal pelvic damage using Chlamydia ser-
ology. The choice of antibody titre used to classify patients into
these two risk categories using serology is the cut-off titre.
However, three main issues need to be considered when de-
fining the cut-off titre (Coggon et al., 1993). Firstly, a cut-off titre
may be based on statistical analysis (for example diagnostic test
analysis), which may be acceptable as a simple guide to the
limits of what values are common. Secondly, a cut-off titre
based on the perceived or actual clinical importance may define
the antibody titre above which the identification of tubal pelvic
damage becomes more frequent. Finally, a cut-off titre may be
based on prognostic factors for which high Chlamydia antibody
titres may be associated with a greater severity of disease and a
lower chance of conception.
Each of these approaches is suitable for different purposes
and needs to be defined when being used (Coggon et al., 1993).
However, any value stated depends on whether the aim is
to make a diagnosis or a prognosis (Altman, 1991). Again this
is a clinical judgment and not a statistical issue. For example,
in screening for lethal disease, high sensitivity is desirable,
 Tubal pelvic damage
although the trade off is usually lower specificity. However,
when dealing with a non-life-threatening condition, such as
tubal pelvic damage, a high cut-off value (lower sensitivity)
may be chosen: although the cut-off value may miss some
cases of tubal pelvic damge it would lead to fewer women
who do not have the disease being subjected to invasive and
costly laparoscopy (high specificity). The use of prevalence-
independent likelihood ratios can also help to overcome this
problem; a suitable cut-off titre would have a positive likeli-
hood ratio > 5 and a negative likelihood ratio < 0.2 (Land et al.,
1998).
Can antibody titres be used to predict the probability of live
birth?
Previous infection with C. trachomatis may influence the
potential of infertile women to conceive or have the desired
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favourable outcome of a live birth. This deduction is supported
by the frequency and severity of damage found in women
with previous infection (Minassian et al., 1990; Minassian and
Wu, 1992; Akande, 2001). The evidence associating chlamydial
infection with an increased risk of ectopic pregnancy is con-
vincing (Walters et al., 1988; Kihlstrom et al., 1990; Chrysostomou
et al., 1992). Infection with Chlamydia is associated with tubal
damage, which, in turn, is associated with an increased risk of
ectopic pregnancy. Women with high Chlamydia antibody titres
would be expected to have lower pregnancy rates than do
women with severe tubal damage. Furthermore, it is likely that
women with higher titres would have lower live birth rates as a
result of ectopic pregnancy loss.
Studies using assisted conception techniques, such as in vitro
fertilization (IVF), as models have revealed conflicting results
on outcome in relation to increased Chlamydia antibody titres.
Some studies (Rowland et al., 1985; Lunenfeld et al., 1989;
Sharara and Queenan, 1999) indicate that women with chlam-
ydial infection may have a lower implantation and pregnancy
rate. However, no study so far has considered Chlamydia ser-
ology as an independent variable for live birth rate in women
trying to conceive naturally.
Prognosis for fertility in tubal pelvic damage
Owing to the protean nature of lesions found in the damaged
female pelvis, accurate prognosis for fertility is difficult. Many
authors have attempted to group features found at laparoscopy
into classification systems with the aim of providing a progno-
sis (Caspi et al., 1979; Boer-Meisel et al., 1986; Mage et al., 1986;
American Fertility Society, 1988; Wu and Gocial, 1988; Wu and
Minassian, 1989; Marana et al., 1995). However, the current
classification systems are recognized as imperfect (American
Fertility Society, 1985; Buttram, 1985; Canis et al., 1993; Hull
and Fleming, 1995). The use of classifications for endometriosis
is well established (American Fertility Society, 1979, 1985;
American Society for Reproductive Medicine, 1997). However,
many of the conclusions drawn from these classification sys-
tems are not valid as the outcome (pregnancy) rarely follows
a doseresponse relationship to severity of endometriosis
(Schenken and Guzick, 1997). At present there is no widely
recognized, reliable way to provide precise prognostic infor-
mation for women with tubal pelvic damage that is not due
S17
to endometriosis. The need to distinguish women with a
favourable or unfavourable prognosis after surgery for tubal
pelvic damage is paramount in light of the advent of assisted
conception techniques (Lilford and Watson, 1990; Singhal et al.,
1991; Winston and Margara, 1991). A classification system for
tubal pelvic damage would need to be simple, logical and
evidence-based to be widely acceptable.
There is little doubt that prognosis for pregnancy is related
to severity of tubal pelvic damage (Wu and Minassian, 1989;
Hull and Fleming, 1995). Although difficult to compare because
of heterogeneity, studies indicate that the pregnancy rate in
patients with the most severe disease is < 10% (Caspi et al.,
1979; Boer-Meisel et al., 1986; Mage et al., 1986; Wu and Gocial,
1988; Surrey and Surrey, 1996). In the study of Boer-Meisel
et al. (1986) discriminant analysis was used to distinguish three
categories of good, intermediate and poor prognostic value in
predicting outcome, which was also suggested by Wu and
Gocial (1988). Other studies (Caspi et al., 1979; Boer-Meisel
et al., 1986; Donnez and Casanas-Roux, 1986; Mage et al., 1986;
Carey and Brown, 1987) reported pregnancy rates of > 4050%
in the most favourable groups. The best prognosis in cases of
infective tubal damage, however slight, does not exceed 60%,
therefore subclassification of the favourable group is not
worthwhile. Only reversal of sterilization leads to higher suc-
cess rates, but cannot be included in studies of infective tubal
damage. The group classified as intermediate or uncertain
prognosis (Hull and Fleming, 1995) is difficult to subclassify
and it may be unrealistic to attempt to do so, except to dis-
tinguish those who may fit better into the other main classes
(favourable or unfavourable). These patients will have an as-
sumed (or possibly later defined) 1040% chance of pregnancy
in 2 years; therefore, if other features are favourable, such as
age, sperm function and duration of infertility, surgery may be
preferred to IVF (Winston and Margara, 1991; Hull and
Fleming, 1995).
On the basis of this information and the best available
evidence, a classification system for tubal pelvic damage
that should distinguish women according to prognosis based
on the severity of pelvic findings at laparoscopy or laparotomy
has been proposed (Hull and Fleming, 1995; Table 1). The
classification, known as the Hull and Rutherford classification,
is published in full in this supplement (Rutherford and Jenkins,
2002).
The classification fulfills some of the previously stated
criteria that would seek to classify women with severe disease
into an unfavourable category and those with mild disease into
a favourable category. However, it would need to be studied
with regard to its real benefits in clinical practice in women
undergoing surgery. Notwithstanding the fact that surgery for
tubal pelvic damage is not without risks and hazards associ-
ated with laparotomy or laparoscopy, surgery could also be
detrimental by causing further adhesions and tubal occlusion,
particularly when post-operative infection or significant blood
loss occurs (Grainger, 1994). Therefore, it is likely that some
women benefit more from surgery than do others. However
polemical the issue of the benefit of surgery in women with
tubal pelvic damage (Watson et al., 2000), attempts at surgical
correction are still carried out on selected patients in tertiary
centres (Winston and Margara, 1991; Li and Cooke, 1994) and
in smaller units if no assisted reproductive technologies are
 S18
Table 1. Hull and Rutherford classification for tubal pelvic damage
1. Minor/grade I
Tubal fibrosis absent even if tube occluded (proximally)
Tubal distension absent even if tube occluded (distally)
Mucosal appearances favourable
Adhesions (peritubalovarian) are flimsy
2. Intermediate or moderate/grade II
Unilateral severe tubal damage (see below)
With or without contralateral minor disease
Limited (< 1/3) dense adhesions of tubes and/or ovaries
3. Severe/grade III
Bilateral tubal damage
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Tubal fibrosis extensive
Tubal distension > 1.5 cm
Abnormal mucosal appearance
Bipolar occlusion
Extensive dense adhesions
available to the patient (Watson et al., 1990, 2000). The proposed
classification (Rutherford and Jenkins, 2002) distinguishes
patients into prognostic categories (Akande, 2001; Akande and
Jenkins, 2001). Owing to its simplicity, validation by further
study could make this classification widely acceptable, not only
providing a pragmatic tool for description of the disease but
also prognosis.
Conclusion
Infertile women who are likely to have tubal pelvic damage can
be screened using Chlamydia serology. The choice of titre used
to determine who is at high risk of tubal pelvic damage should
be determined by prevalence of the condition, type of sero-
logical test used, availability of resources for confirmatory
diagnostic testing, such as laparoscopy, and whether the iden-
tification of disease would influence patient management.
Although there is a recognized relationship between increasing
Chlamydia antibody titres and increasing severity of disease, the
prognosis for fertility would best be determined by lap-
aroscopic assessment. In contrast to other classifications, which
are often complex and have so far not gained wide acceptance,
a simple classification is proposed which has the potential
to classify infertile women into prognostic groups based on
severity of findings at laparoscopy.
The concepts behind this article were conceived during my tenure
as a Clinical Research Fellow under the late Professor Mike Hull, and
led to the completion of a PhD thesis.
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