Hum. Reprod. Advance Access originally published online on July 18, 2007
Human Reproduction 2007 22(9):2359-2367; doi:10.1093/humrep/dem224
Asymmetry in distribution of diaphragmatic endometriotic lesions: evidence in favour of the menstrual reflux theory
1 Department of Obstetrics and Gynaecology, Istituto Luigi Mangiagalli, University of Milan, Milan, Italy 2 Center for Research in Obstetrics and Gynecology (C.R.O.G.), Milan, Italy
3 Correspondence address. Tel: +3902 55032917; Fax: +3902 50320252; E-mail: paolo.vercellini{at}unimi.it
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Abstract |
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BACKGROUND: If the menstrual reflux or implantation theory of endometriosis is true, refluxed endometrial cells could reach the right hypochondrium transported by the clockwise peritoneal fluid current and would implant more easily on the right diaphragmatic leaf as they are stuck there by the falciform ligament.
METHODS: To investigate if a lateral asymmetry exists in diaphragmatic endometriotic lesion distribution, all articles on diaphragmatic endometriosis identified by MEDLINE, EMBASE and PUBMED database searches were retrieved, and additional reports were collected by systematically reviewing all references. The number of women and the side of the lesion with respect to the falciform ligament of the liver were obtained from individual studies, and the combined frequency of right- and left-side diaphragmatic endometriosis was computed. In addition, seven personal cases were described.
RESULTS: There were 16 reports including 47 subjects selected. Diaphragmatic endometriosis was on the right side in 31 (66%) patients, on the left in 3 (6%) and bilateral in 13 (27%). In the personal series, lesions were on the right side in five cases, on the left in one and bilateral in one. Considering only unilateral lesions, the observed proportion of right-sided endometriotic implants (36/40) was 90% (95% CI 76–97%; 
21 32.6, P < 0.0001).
CONCLUSIONS: The observed major asymmetry in diaphragmatic endometriotic lesion distribution in favour of the right leaf supports the menstrual reflux theory.
Key words: endometriosis/diaphragm/laparoscopic surgery
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Introduction |
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The aetiology of endometriosis is controversial. Investigating the anatomical distribution of endometriotic lesions may provide insights into the pathogenesis of the disease (Jenkins et al., 1986
). If retrograde menstruation is the source of ectopic endometrium, the pattern of lesions should be determined mainly by anatomical and physiological variables, whereas if coelomic metaplasia is the cause of endometriosis, lesions should not be distributed in relation to factors influencing the spreading and implantation of endometrial cells (Jenkins et al., 1986; Vercellini et al., 1998b).
The pattern of involvement of bilateral and symmetric organs has been studied to verify if the proportion of endometriotic foci is equal on the two sides, and a significant asymmetry in lesion distribution has been demonstrated both in the pelvis [ovary (Vercellini et al., 1998b, 2002; Ghezzi et al., 2001; Prefumo et al., 2002; Al-Fozan and Tulandi, 2003; Ciavattini et al., 2004), peritoneum (Al-Fozan and Tulandi, 2003; Parazzini et al., 2003), utero-sacral ligaments (Chapron et al., 2001) and ureter (Vercellini et al., 2000)] and in the lower abdomen [lower intestinal tract (Vercellini et al., 2004), inguinal canal structures (Clausen and Nielsen, 1987; Candiani et al., 1991) and sciatic nerve (Vercellini et al., 2003)]. This asymmetry constitutes indirect evidence against the coelomic metaplasia theory (Chapron et al., 2006), which is more likely to be associated with an equal distribution, and the laterality has been attributed to both a physiological factor (i.e. the clockwise peritoneal current that keeps the peritoneal fluid circulating) (Meyers, 1970, 1973; Rosenshein et al., 1979; Foster et al., 1981) and an anatomical factor (i.e. the presence of the sigmoid colon).
Peritoneal fluid originates mainly from ovarian surface tissues exudation secondary to increased vascular permeability. Transudation from blood plasma as well as transudation/exudation from kidneys, liver, pancreas, intestine and intra-abdominal fat may contribute to the overall peritoneal fluid volume, which is greatest at mid-cycle and in the early luteal phase (mean, 8.7 ml; range, 1–21 ml) (Koninkx et al., 1998; Hunter et al., 2007). The lymphatic lacunae on the peritoneal surface of the diaphragm and the lymphoid aggregates on the greater as well as lesser omentum and omental appendages constitute specific sites of peritoneal fluid resorption (Carmignani et al., 2003). The force of gravity operates to pool peritoneal fluid in the dependent peritoneal recesses. However, diaphragmatic respiratory movements combined with intestinal peristalsis result in hydrostatic pressure differences between the lower and upper abdomen capable of conveying peritoneal fluid from the pelvis to the subhepatic and subphrenic regions also in the upright position (Rosenshein et al., 1979). Under experimental conditions, direct passage from the right to the left subphrenic space across the midline is prevented by the falciform ligament (Meyers, 1970, 1973). Intraperitoneal fluid hydrodynamics influence even the distribution of surface intra-abdominal cancer metastases (Carmignani et al., 2003).
Endometriotic lesions in the upper abdomen are less frequent compared with those in the lower abdomen and in the pelvis, possibly because of the effect of gravity during the erect position on seeding of refluxed endometrial cells. We deemed it important to clarify if the factors that influence the distribution of endometriotic lesions on the diaphragm and in the pelvis are similar. If the menstrual reflux theory is true, the influence of physiological and anatomical determinants should be exceedingly evident on the 'roof' of the abdominal cavity. In fact, the clockwise peritoneal current (i.e. the physiological factor) should interact with the falciform ligament of liver (i.e. the anatomical factor) determining a higher frequency of endometriotic foci on the right leaf of the diaphragm compared with the left one. According to this mechanistic theory, refluxed endometrial cells are transported by the intra-abdominal current coming down from the left peritoneal gutter and flowing across the pelvic floor and up along the right peritoneal gutter (Drye, 1948; Foster et al., 1981), but once the right hypochondrium is reached, they are stuck by the falciform ligament, a crescentic fold of peritoneum extending to the surface of the liver from the diaphragm and anterior abdominal wall. This should greatly facilitate implantation on the right leaf of the diaphragmatic peritoneum.
To verify this hypothesis, we analysed all data published on the topic in the scientific literature since the original observation in 1954 (Brews, 1954) according to the MOOSE guidelines for systematic reviews of observational studies (Stroup et al., 2000). Moreover, we combined published findings with the data of a large series of women with endometriosis evaluated in our department in the last decade. A detailed description of the patients’ symptoms and signs and of the diagnostic and treatment alternatives was not among the aims of the study. For these purposes, the readers should consult the excellent reviews by Nezhat et al. (1998) and Redwine (2002).
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Materials and Methods |
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Several different strategies were adopted to identify all medical papers published on diaphragmatic endometriosis without regard to language of publication. We conducted a MEDLINE, EMBASE and PUBMED search using combinations of medical subject heading terms 'endometriosis', 'diaphragm', 'liver' and 'pleura'. All pertinent articles were retrieved and additional reports were then identified by systematically reviewing all references. In addition, books and monographs on endometriosis published in the last 25 years were consulted. Proceedings of scientific meetings were not included. No attempt was made to identify unpublished studies, as it is exceedingly difficult to gain reliable and comprehensive access to information regarding very rare cases.
Study selection
We considered articles in which the presence of an endometriotic lesion of the diaphragm was assessed, as well as the affected side. We decided to include reports with surgical evidence of diaphragmatic endometriosis but lacking histological examination, as biopsies are not routinely performed in these cases because of technical difficulties or danger of perforating lesions and iatrogenic pneumothorax (Nezhat et al., 1998).
Two investigators (A.A. and R.D.) abstracted data in an unblinded fashion on standardized forms. An initial screening of the title and abstract of all articles was performed to exclude citations deemed irrelevant by both observers (i.e. when endometriosis was found only on sites other than the diaphragm). The year of publication, clinical characteristics of subjects, results of preoperative diagnostic investigations and surgical details were recorded independently. Diaphragmatic endometriosis was defined as presence of typical puckered black lesions and blueberry nodules. Superficial brown patches (hemosiderin deposits), white opacified peritoneal areas and stellate scars were considered potentially healed lesions and were excluded because they cannot be considered definitively active, infiltrating disease (Nezhat et al., 1998; Redwine, 2002). The number of women with diaphragmatic endometriosis and the side of the implants with respect to the falciform ligament of the liver were obtained from individual studies, and the proportion of right side lesions (the main outcome of interest) was computed.
The combined frequency of right- and left-side diaphragmatic endometriosis in published reports was analysed with the chi-squared test to compare observed and expected events. The confidence interval (CI) of the proportion of endometriosis of the right diaphragmatic leaf was computed using the normal approximation.
Personal series
Clinical records were retrieved from consecutive women with endometriosis undergoing first-line conservative or definitive surgery in the decade 1996–2005 at the First Department of Obstetrics and Gynaecology of the University of Milan, Italy. Diaphragmatic endometriosis was documented photographically in all patients (Fig. 1). Women with genital malformations and those who had undergone previous abdominal surgery, except appendectomy, were excluded. Indication for and age at surgery, parity, disease stage according to the revised American Fertility Society classification (The American Fertility Society, 1985) and site and side of diaphragmatic lesions were recorded.
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Results |
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A total of 61 studies were initially identified by computerized database searches as potentially relevant, and a further 38 studies were identified by manual searching and by checking bibliographies. There were 19 reports excluded because endometriotic lesions at different sites not definitely affecting the diaphragm were observed, 60 were excluded because only lesions on the pleural side of the diaphragm were described and 4 were excluded because the affected side was not specified (Table 1). There were 16 reports finally included in the analysis (Table 2), 14 of which were published in the English literature, one in the Spanish literature, and one in the French literature.
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A total of 47 women were selected: 17 with histopathological demonstration of infiltrating diaphragmatic endometriosis (Norenberg et al., 1977
; Posniak et al., 1990; Nezhat et al., 1992; Chinegwundoh et al., 1995; Kalapura et al., 2000; Redwine, 2002; Wolthuis et al., 2003; Nahir et al., 2004; Takeuchi et al., 2005); 26 with biopsy-confirmed diagnosis of pelvic or genital endometriosis but with no diaphragmatic specimen examined (Nezhat et al., 1998; Garcìa Léon et al., 1999) and 4 cases where the information was not available (Brews, 1954; Griffith et al., 1988; Mangal et al., 1996; Cooper et al., 1999). The median number of cases described was 1 (range 1–24), and the median age of the subjects was 31 (range 18–50). Pelvic lesions in addition to diaphragmatic endometriosis were observed in 43 women (Brews, 1954; Norenberg et al., 1977; Posniak et al., 1990; Nezhat et al., 1992; Chinegwundoh et al., 1995; Witte and Guilbaud, 1995; Mangal et al., 1996; Nezhat et al., 1998; Garcìa Léon et al., 1999; Kalapura et al., 2000; Redwine, 2002; Takeuchi et al., 2005), whereas diaphragmatic lesions alone were observed in two women (Wolthuis et al., 2003; Nahir et al., 2004). In the remaining two patients the information was not available (Griffith et al., 1988; Cooper et al., 1999). Pelvic endometriosis stage according to the The American Fertility Society (1985) was defined in only 6 of the 16 reports included in the analysis (Nezhat et al., 1992; Witte and Guilbaud, 1995; Nezhat et al., 1998; Garcìa Léon et al., 1999; Kalapura et al., 2000; Redwine, 2002). The disease was at stage I in 3 cases, II in 5 cases, III in 3 cases and IV in 26 cases.
Endometriosis of the diaphragm was on the right side in 31 patients, on the left in 3 patients and bilateral in 13 patients. Considering only the patients with unilateral diaphragmatic endometriosis, the observed proportion of right-sided lesions (31/34, 91.1%; 95% CI 76–98) significantly differed from the expected proportion of 50% (21 26.2, P < 0.0001). Among the 17 cases with histological demonstration of diaphragmatic endometriosis, 13 were on the right side, (76.4%; 95% CI 50–93; 21 4.69, P = 0.0253), 4 were bilateral and none were on the left side.
It is unclear if the patient described in 1992 by Nezhat et al. has been included in the series published by Nezhat et al. (1998). However, exclusion of the above subject from the analysis did not change the results substantially (data not shown).
With regard to the personal series, 2065 women underwent first-line surgical treatment for endometriosis at laparoscopy or laparotomy during the decade considered. The vast majority of them were women self-referring for various conditions to a tertiary care academic centre for the treatment of endometriosis. There were seven subjects (0.34%) who had typical, nodular, diaphragmatic endometriotic lesions, which were on the right side in five cases, on the left side in one case and bilateral in one case. Pelvic endometriosis was always present: at stage III in four cases, and at stage IV in three cases (The American Fertility Society, 1985). Considering only unilateral lesions and combining the personal figures with those reported in the literature, the observed proportion of right-sided endometriotic implants (36/40) was 90% (95% CI 76–97; 21 32.6, P < 0.0001). Inclusion of the bilateral endometriotic lesions as well gave a total of 50/68 (73.5%; 95% CI 61–83; 21 14.6, P = 0.0001) right-sided and 18/68 left-sided diaphragmatic implants.
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Discussion |
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The results of the present systematic literature review confirm that diaphragmatic endometriosis develops significantly more frequently on the right side than on the left (Nezhat et al., 1998
; Redwine, 2002). Diagnostic bias is unlikely because, with the laparoscope inserted through an umbilical port, the right diaphragmatic leaf can be inspected easily only in its anterior part, whereas the left leaf can be observed entirely as the left liver lobe is smaller than the contralateral one. Consequently, misdiagnosis most probably would have tipped the balance in favour of left lesions and not right ones.
We cannot exclude that our results were influenced by publication bias (i.e. papers are more likely to have been submitted by investigators aware of the hypothesis and to have been accepted by editors). In this case, pooling all published observations would magnify any publication bias. However, the hypothesis of an asymmetric distribution of diaphragmatic endometriosis has been formulated in a few isolated articles (Nezhat et al., 1998; Redwine, 2002) and does not seem to have gained popularity.
Various article search strategies were adopted. Data were abstracted from standardized forms compiled by two independent investigators who were not blinded. Rejected studies and the reason for their exclusion are described. Endometriosis infiltrating the peritoneum and muscle fibers was demonstrated histologically only in some of the considered cases. However, the asymmetry in favour of the right side was virtually similar in subgroups with presence or absence of a histological diagnosis, as well as in the personal surgical series, and was confirmed also after inclusion of women with bilateral lesions, which supports the consistency of the general results.
Admittedly, we have not accounted for several scarcely studied factors that may influence implantation of regurgitated endometrial cells. Peritoneal fluid cycle dynamics, strength and velocity of the intra-abdominal current, surface tension of moist surfaces, and gravity may have variable effects on our circulation model. Furthermore, a trail of ectopic implants along the path of ascending colonic peristalsis has not been observed systematically in women undergoing surgical exploration for endometriosis. This could be explained by difficulties in cell attachment to intestinal surfaces that are continuously moving and rubbing against each other (Carmignani et al., 2003).
Alternatively, as both pleura and peritoneum develop from coelomic epithelium, it cannot be excluded that diaphragmatic endometriosis originates from coelomic metaplasia. Unknown intrinsic embryogenetic processes of the coelomic epithelium may underlie the unequal distribution of endometriosis behind apparent anatomical and physiological explanations. Moreover, if the falciform ligament interrupts the flow of endometrial cells, diaphragmatic lesions would be expected to occur clustered along the ligament, rather than distributed along the posterior margin of the diaphragm.
Despite this, the observation of equal proportions of endometriosis on the right and left diaphragmatic leafs would have rendered plausible this possibility of coelomic metaplasia, but the finding of a 3:1 ratio in the pattern of lateral distribution of lesions argues against it. Interestingly, the magnitude of this asymmetry is greater than that observed in the organs of the lower abdominal cavity (Clausen and Nielsen, 1987; Candiani, et al., 1991; Vercellini et al., 1998b, 2000, 2002, 2003, 2004; Chapron et al., 2001; Ghezzi et al., 2001; Prefumo et al., 2002; Al-Fozan and Tulandi, 2003; Parazzini et al., 2003; Ciavattini et al., 2004). Gravity, which may interfere in the distribution of pelvic endometriotic lesions limiting potential differences, has by definition a reduced effect in the upper abdomen (Drye, 1948). Moreover, the falciform ligament of the liver constitutes a definite barrier to the clockwise peritoneal fluid current. This current appears to be caused by changes in hydrostatic pressure due to diaphragmatic movements and large bowel peristalsis (Meyers, 1970, 1973; Rosenshein et al., 1979; Foster et al., 1981). Mesenteric attachments would channel the fluid flow, and variations in intraperitoneal pressure would direct this flow clockwise (Foster et al., 1981). However, the current may need to be interpreted cautiously as the findings by Meyers (1970, 1973) were obtained under experimental conditions which may be dissimilar to the physiologic abdominal environment of menstruating women (e.g. adoption of Trendelenburg position, injections of radiopaque dye in volumes probably larger then those normally refluxed at menstruation, and induction of mild ascites due to high osmolality of the iodinated contrast media used).
It has been hypothesized that diaphragmatic endometriosis is the precursor of hepatic and pleural endometriosis (Rovati et al., 1990; Nezhat et al., 1998; Redwine, 2002). Extension to the liver capsule would be by contiguity (Redwine, 2002), whereas diffusion to the basal pleura would occur through small defects or cribiform fenestrations (Foster et al., 1981; Joseph and Sahn, 1996). This view is strongly supported by the impressive and almost identical preponderance of right-side lesions of both diaphragm and pleura (Foster et al., 1981; Joseph and Sahn, 1996). Along this line, the same pathogenetic mechanism could cause a sort of 'right hypochondrium endometriotic complex', involving the right diaphragm, liver, and right diaphragmatic pleura, which can be considered the counterpart of the 'left hemipelvis endometriotic complex', which is caused by the presence of the sigmoid and which may involve the left ovary, pelvic peritoneum, uterosacral ligament, ureter and the large bowel itself (Vercellini et al.,1998a, 2004; Chapron et al., 2006) (Fig. 2).
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The prevalence of diaphragmatic endometriosis in our surgical series seems relatively low. This could be partly explained by adoption of particularly conservative diagnostic criteria to avoid over diagnosis, as well as potential disease underestimation due to surgeons’ limited awareness of the condition. Moreover, diaphragmatic endometriosis could have been missed due to incomplete visualization. In fact many lesions have been reported to originate in the posterior leaf of the right diaphragm, which is hidden by the large bulk of the liver. This area can be explored only after liver retraction by means of a blunt probe, (Nezhat et al., 1998
; Fig. 1b) or by inserting the laparoscope beneath the costal margin with the operating table in steep reverse Trendelemburg position (Redwine, 2002). Consequently, it cannot be excluded that the true prevalence of diaphragmatic endometriosis is considerably higher than reported.
The occurrence of endometriotic implants on the diaphragm may constitute a serious event due to the elusive and sometimes severe pain syndrome (Nezhat et al., 1998; Redwine, 2002) as well as the risk of spread to the liver and pleura with potential major morbidity (Foster et al., 1981; Joseph and Sahn, 1996; Nezhat et al., 1998). Accordingly, systematic and as complete as possible inspection of the diaphragm, and specifically of the area included between the posterior edge of the liver, the right lateral chest wall, and the falciform ligament, should constitute an integral part of laparoscopic evaluation of women with endometriosis.
We have documented a consistent and almost systematic association between diaphragmatic and pelvic endometriosis in both published reports and our personal series. Overall, peritoneal or ovarian lesions were observed in 43/47 (91.4%) cases. This finding strongly suggests a common aetiology for the two disease forms. In fact, if a different and peculiar pathogenetic mechanism leading to diaphragmatic endometriosis exists, the frequency of pelvic endometriotic lesions in patients with diaphragmatic endometriosis should be similar to that observed in the general population, which has been reportedly estimated to be around 10% (Eskenazi and Warner, 1997; Somigliana et al., 2004).
Moreover, endometriosis of the diaphragm, like that of the ovary (Vercellini et al., 1998b, 2002; Ghezzi et al., 2001; Prefumo et al., 2002; Al-Fozan and Tulandi, 2003; Ciavattini et al., 2004), pelvic peritoneum (Al-Fozan and Tulandi, 2003; Parazzini et al., 2003), uterosacral ligaments (Chapron et al., 2001), ureters (Vercellini et al., 2000), round ligaments (Clausen and Nielsen, 1987; Candiani et al., 1991), lower intestinal tract (Vercellini et al., 2004) and sciatic nerve (Vercellini et al., 2003) develops asymmetrically. In our opinion, neither the coelomic metaplasia nor the embryonic cell rest theory explain such a clear-cut difference in frequency distribution of diaphragmatic lesions between the two sides. Indeed, our findings are compatible with the menstrual reflux theory, with the anatomical characteristics of the upper abdomen, and with the spreading of endometrial cells generated by a peritoneal fluid current.
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Acknowledgements |
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Supported in part by the University of Milan School of Medicine Research Grant FIRST no. 12-01-5068118-00 067. Photographs for Figure 1 are courtesy of Dr. Enrico Canducci.
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Submitted on November 13, 2006; resubmitted on June 12, 2007; accepted on June 21, 2007.
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