Hum. Reprod. 2007 Vercellini 2359 67

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Asymmetry in distribution of diaphragmatic endometrioticlesions: evidence in favour of the menstrual reflux theory

P. Vercellini1,2,3

, A. Abbiati2

, P. Vigano2

, E.D. Somigliana1,2

, R. Daguati1,2

, F. Meroni1

and P.G. Crosignani1

1 Department of Obstetrics and Gynaecology, Istituto Luigi Mangiagalli, University of Milan, Milan, Italy; 2Center for Research

in Obstetrics and Gynecology (C.R.O.G.), Milan, Italy

3Correspondence address. Tel: 3902 55032917; Fax: 3902 50320252; E-mail:[email protected]

BACKGROUND: If the menstrual reflux or implantation theory of endometriosis is true, refluxed endometrial cel

could reach the right hypochondrium transported by the clockwise peritoneal fluid current and would implant mo

easily on the right diaphragmatic leaf as they are stuck there by the falciform ligament. METHODS: To investigate i

lateral asymmetry exists in diaphragmatic endometriotic lesion distribution, all articles on diaphragmatic endom

triosis identified by MEDLINE, EMBASE and PUBMED database searches were retrieved, and additional repor

were collected by systematically reviewing all references. The number of women and the side of the lesion wirespect to the falciform ligament of the liver were obtained from individual studies, and the combined frequency

right- and left-side diaphragmatic endometriosis was computed. In addition, seven personal cases were describe

RESULTS: There were 16 reports including 47 subjects selected. Diaphragmatic endometriosis was on the rig

side in 31 (66%) patients, on the left in 3 (6%) and bilateral in 13 (27%). In the personal series, lesions were o

the right side in five cases, on the left in one and bilateral in one. Considering only unilateral lesions, the observe

proportion of right-sided endometriotic implants (36/40) was 90% (95% CI 7697%; x21 32.6, P < 0.0001CONCLUSIONS: The observed major asymmetry in diaphragmatic endometriotic lesion distribution in favour

the right leaf supports the menstrual reflux theory.

Keywords: endometriosis; diaphragm; laparoscopic surgery

Introduction

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 deter-

mined mainly by anatomical and physiological variables,

whereas if coelomic metaplasia is the cause of endometriosis,

lesions should not be distributed in relation to factors influen-

cing the spreading and implantation of endometrial cells

(Jenkins et al., 1986; Vercellini et al., 1998b).

The pattern of involvement of bilateral and symmetricorgans has been studied to verify if the proportion of endome-

triotic foci is equal on the two sides, and a significant asymme-

try 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, 198

Candiani et al., 1991) and sciatic nerve (Vercellini et a

2003)]. This asymmetry constitutes indirect evidence again

the coelomic metaplasia theory (Chapron et al., 2006), whi

is more likely to be associated with an equal distribution, an

the laterality has been attributed to both a physiologic

factor (i.e. the clockwise peritoneal current that keeps the pe

itoneal fluid circulating) (Meyers, 1970, 1973; Rosenshe

et al., 1979; Foster et al., 1981) and an anatomical factor (i

the presence of the sigmoid colon).

Peritoneal fluid originates mainly from ovarian surfa

tissues exudation secondary to increased vascular permeabilitTransudation from blood plasma as well as transudatio

exudation from kidneys, liver, pancreas, intestine a

intra-abdominal fat may contribute to the overall peritone

fluid volume, which is greatest at mid-cycle and in the ear

luteal phase (mean, 8.7 ml; range, 121 ml) (Koninkx et a

1998; Hunter et al., 2007). The lymphatic lacunae on the pe

itoneal surface of the diaphragm and the lymphoid aggregat

on the greater as well as lesser omentum and omental appe

dages constitute specific sites of peritoneal fluid resorpti

# The Author 2007. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology.

All rights reserved. For Permissions, please email: [email protected]

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Human Reproduction Vol.22, No.9 pp. 23592367, 2007 doi:10.1093/humrep/dem2

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(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 fal-

ciform 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 pos-

ition 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 exceed-

ingly 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 ana-

tomical factor) determining a higher frequency of endometrio-

tic foci on the right leaf of the diaphragm compared with the

left one. According to this mechanistic theory, refluxed endo-

metrial 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 hypo-

chondrium 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 obser-

vation in 1954 (Brews, 1954) according to the MOOSE guide-

lines 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 diag-

nostic and treatment alternatives was not among the aims of the

study. For these purposes, the readers should consult the excel-

lent reviews by Nezhat et al. (1998) and Redwine (2002).

Materials and Methods

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 endome-

triosis, 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 endo-

metriosis 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 irre-

levant 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 investi-

gations and surgical details were recorded independently. Diaphrag-

matic endometriosis was defined as presence of typical puckered

black lesions and blueberry nodules. Superficial brown patches (hemo-

siderin 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 endo-

metriosis 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 endo-

metriosis 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 endo-

metriosis was documented photographically in all patients (Fig. 1).

Women with genital malformations and those who had undergone pre-

vious abdominal surgery, except appendectomy, were excluded. Indi-

cation for and age at surgery, parity, disease stage according to the

revised American Fertility Society classification (The American Ferti-

lity Society, 1985) and site and side of diaphragmatic lesions were

recorded.

ResultsA 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 endo-

metriotic 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 speci-

fied (Table 1). There were 16 reports finally included in the

analysis (Table 2), 14 of which were published in the English

Vercellini et al.

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literature, one in the Spanish literature, and one in the French

literature.

A total of 47 women were selected: 17 with histopathologi-

cal 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; Garca Leon 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 124), and the median age of the subjects was

31 (range 1850). 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; Garca Leon 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 availab

(Griffith et al., 1988; Cooper et al., 1999). Pelvic endometrio

stage according to the The American Fertility Society (198

was defined in only 6 of the 16 reports included in the analys

(Nezhat et al., 1992; Witte and Guilbaud, 1995; Nezhat et a

1998; Garca Leon et al., 1999; Kalapura et al., 2000; Redwin

2002). The disease was at stage I in 3 cases, II in 5 cases, III in

cases and IV in 26 cases.

Endometriosis of the diaphragm was on the right side in 3

patients, on the left in 3 patients and bilateral in 13 patient

Considering only the patients with unilateral diaphragma

endometriosis, the observed proportion of right-sided lesio

(31/34, 91.1%; 95% CI 76 98) significantly differed frothe expected proportion of 50% (x

2

1 26.2, P, 0.000

Among the 17 cases with histological demonstration of di

phragmatic endometriosis, 13 were on the right side, (76.4%

95% CI 5093; x21 4.69, P 0.0253), 4 were bilateral a

none were on the left side.

It is unclear if the patient described in 1992 by Nezhat et

has been included in the series published by Nezhat et a

(1998). However, exclusion of the above subject from t

analysis did not change the results substantially (data nshown).

With regard to the personal series, 2065 women underwe

first-line surgical treatment for endometriosis at laparoscop

or laparotomy during the decade considered. The vast majori

of them were women self-referring for various conditions to

tertiary care academic centre for the treatment of endometri

sis. There were seven subjects (0.34%) who had typic

nodular, diaphragmatic endometriotic lesions, which were

the right side in five cases, on the left side in one case and bila

eral in one case. Pelvic endometriosis was always present:

stage III in four cases, and at stage IV in three cases (Th

American Fertility Society, 1985). Considering only unilater

lesions and combining the personal figures with those reportin the literature, the observed proportion of right-sided end

metriotic implants (36/40) was 90% (95% CI 769x2

1 32.6, P, 0.0001). Inclusion of the bilateral endometrio

lesions as well gave a total of 50/68 (73.5%; 95% CI 618x2

1 14.6, P 0.0001) right-sided and 18/68 left-sided dphragmatic implants.

Discussion

The results of the present systematic literature review confir

that diaphragmatic endometriosis develops significantly mo

frequently on the right side than on the left (Nezhat et a

1998; Redwine, 2002). Diagnostic bias is unlikely becauwith the laparoscope inserted through an umbilical port, t

right diaphragmatic leaf can be inspected easily only in

anterior part, whereas the left leaf can be observed entirely

the left liver lobe is smaller than the contralateral one. Cons

quently, misdiagnosis most probably would have tipped t

balance in favour of left lesions and not right ones.

We cannot exclude that our results were influenced by pu

lication bias (i.e. papers are more likely to have been submitt

by investigators aware of the hypothesis and to have be

accepted by editors). In this case, pooling all publish

Figure 1: (a) At laparoscopic inspection typical puckered blacklesions and blueberry nodules (arrows) are present on the rightdiaphragmatic leaf(b) Endometriotic lesions in the posterior part of the right diaphrag-matic leaf (arrow) are identified only after liver retraction by meansof a blunt probe

Asymmetry in diaphragmatic endometriotic lesio

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Table 1: Details of publications excluded from the review on diaphragmatic endometriosis. Literature data, 19582006.

Reference Year No. of cases Reason for exclusion

Maurer et al. 1958 1 Lesions on the pleural side at thoracotomyWeldon and Tumulty 1961 1 Lesions on the pleural side at thoracotomyKovarik and Toll 1966 1 Lesions on the pleural side at thoracotomyCrutcher et al. 1967 1 Lesions on the pleural side at thoracotomyDavies 1968 1 Lesions on the pleural side at thoracotomyReboud et al. 1972 1 Lesions on the pleural side at thoracotomyShearin et al. 1974 1 Lesions on the pleural side at thoracotomy

Casella 1976 8 Lesions on the pleural side at thoracotomySodeberg and Dahlquist 1976 1 Lesions on the pleural side onlyMcKnight and Marshall 1978 1 Affected side not specifiedMatsuda et al. 1979 1 Lesions on the pleural side at thoracotomyFurman et al. 1980 1 Lesions on the pleural side at thoracoscopyYamazaki et al. 1980 1 Lesions on the pleural side at thoracotomyFoster et al. 1981 2 Lesions on the pleural side at thoracotomyHinson et al. 1981 1 Lesions on the pleural side at thoracotomySlasky et al. 1982 3 Lesions on the pleural side at thoracotomyBalashingham et al. 1986 1 Lesions on the pleural side at thoracotomyFinkel et al. 1986 1 Hepatic lesion, no diaphragmatic involvementGrabb et al. 1986 1 Hepatic lesion, no diaphragmatic involvementGray et al. 1987 1 Lesions on the pleural side at thoracoscopyKnitza et al. 1987 1 No surgical explorationFonseca 1988 1 Lesions on the pleural side at thoracoscopyBreton et al. 1990 1 Lesions on the pleural side at thoracotomyRovati et al. 1990 1 Hepatic lesion, no diaphragmatic involvement

Pruijt and Roldaan 1991 1 Lesions on the pleural side at thoracoscopyShirashi 1991 1 Lesions on the pleural side at thoracotomyTanimura et al. 1991 1 Lesions on the pleural side onlyAmar et al. 1992 1 Lesions on the pleural side at thoracotomyOkada et al. 1992 1 Lesions on the pleural side at thoracotomyIto et al. 1994 1 Lesions on the pleural side at thoracotomyMaruoka et al. 1995 1 Lesions on the pleural side at thoracoscopyVerbeke et al. 1996 2 Hepatic lesions, no diaphragmatic involvementCravello et al. 1996 1 Hepatic lesion, no diaphragmatic involvementEckford and Westgate 1996 1 Lesions on the pleural side onlyJoseph and Sahn 1996 67 Lesions on the pleural side at thoracotomy or thoracoscopyVan Schil et al. 1996 1 Lesions on the pleural side at thoracoscopyYamashita et al. 1996 3 Lesions on the pleural side at thoracotomy or thoracoscopyBlanco et al. 1998 1 Lesions on the pleural side at thoracotomyChung et al. 1998 1 Hepatic lesion, no diaphragmatic involvementWeinfeld et al. 1998 1 Hepatic endometrioid adenosquamous carcinomaCowl et al. 1999 1 Lesions on the pleural side at thoracoscopy

Fukunaga 1999 1 Lesions on the pleural side at thoracoscopyKadry et al. 1999 3 Lesions on the pleural side at thoracoscopyTsunezuka et al. 1999 1 Lesions on the pleural side at thoracoscopyYoshida et al. 1999 1 Lesions on the pleural side at thoracoscopyCoimbra et al. 2000 1 Lesions on the pleural side at thoracotomyInal et al. 2000 1 Hepatic lesion, no diaphragmatic involvementNSenda et al. 2000 1 Hepatic adenosarcomaNwosu et al. 2000 1 Lesions on the pleural side at thoracoscopyShibata et al. 2000 1 Lesions on the pleural side at thoracotomyBohra and Diamond 2001 1 Hepatic lesion, no diaphragmatic involvementHuang et al. 2001 1 Hepatic lesion, no diaphragmatic involvementBhaumik and Hefni 2002 3 Hepatic lesions, no diaphragmatic involvementChoong et al. 2002 3 Lesions on the pleural side at thoracotomyJeanes et al. 2002 1 Hepatic lesion, no diaphragmatic involvementPerrotin et al. 2002 1 Lesions on the pleural side at thoracoscopyRoth et al. 2002 1 Lesions on the pleural side at thoracoscopyYu et al. 2002 1 No surgical exploration

Bagan et al. 2003 3 Lesions on the pleural side at thoracotomy or thoracoscopyHasumi et al. 2003 1 Lesions on the pleural side at thoracoscopyGroves et al. 2003 1 Hepatic lesion, no diaphragmatic involvementIshikawa et al. 2003 1 Lesions on the pleural side at thoracoscopyLaursen et al. 2003 1 Lesions on the pleural side at thoracoscopyReid et al. 2003 1 Hepatic lesion, no diaphragmatic involvementRoberts et al. 2003 1 Lesions on the pleural side at thoracoscopySakamoto, Ket al. 2003 1 Lesions on the pleural side at thoracoscopySakamoto, S et al. 2003 1 Lesions on the pleural side at thoracoscopyTuech et al. 2003 1 Hepatic lesion, no diaphragmatic involvementBasama 2004 1 Affected side not specifiedHausdorf and Hausdorf 2004 1 Lesions on the pleural side at thoracoscopy

Continued

Vercellini et al.

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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 indepen-

dent 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 diagno-

sis, 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

moist surfaces, and gravity may have variable effects on o

circulation model. Furthermore, a trail of ectopic implan

along the path of ascending colonic peristalsis has not be

observed systematically in women undergoing surgic

exploration for endometriosis. This could be explained

difficulties in cell attachment to intestinal surfaces that are co

tinuously moving and rubbing against each other (Carmigna

et al., 2003).

Alternatively, as both pleura and peritoneum develop fro

coelomic epithelium, it cannot be excluded that diaphragmat

endometriosis originates from coelomic metaplasia. Unknow

intrinsic embryogenetic processes of the coelomic epitheliu

may underlie the unequal distribution of endometrio

behind apparent anatomical and physiological explanation

Moreover, if the falciform ligament interrupts the flow of end

metrial cells, diaphragmatic lesions would be expected to occ

clustered along the ligament, rather than distributed along t

posterior margin of the diaphragm.Despite this, the observation of equal proportions of end

metriosis on the right and left diaphragmatic leafs wou

have rendered plausible this possibility of coelomic metaplas

but the finding of a 3:1 ratio in the pattern of lateral distributio

of lesions argues against it. Interestingly, the magnitude of th

asymmetry is greater than that observed in the organs of t

lower abdominal cavity (Clausen and Nielsen, 1987; Candian

et al., 1991; Vercellini et al., 1998b, 2000, 2002, 2003, 200

Chapron et al., 2001; Ghezzi et al., 2001; Prefumo et a

2002; Al-Fozan and Tulandi, 2003; Parazzini et al., 200

Ciavattini et al., 2004). Gravity, which may interfere in the di

tribution of pelvic endometriotic lesions limiting potent

differences, has by definition a reduced effect in the uppabdomen (Drye, 1948). Moreover, the falciform ligament

the liver constitutes a definite barrier to the clockwi

peritoneal fluid current. This current appears to be caus

by changes in hydrostatic pressure due to diaphragma

movements and large bowel peristalsis (Meyers, 1970, 197

Rosenshein et al., 1979; Foster et al., 1981). Mesenteric attac

ments would channel the fluid flow, and variations in intrape

itoneal pressure would direct this flow clockwise (Foster et a

1981). However, the current may need to be interpreted ca

tiously as the findings by Meyers (1970, 1973) were obtain

Table 2: Details of publications included in the review on diaphragmaticendometriosis. Literature data, 19542005.

Reference Year No. of cases

Side involved Surgicalexploration

Brews 1954 1 Right LaparotomyNorenberg et al. 1977 1 Right LaparoscopyGriffith et al. 1988 1 Right LaparotomyPosniak et al. 1990 1 Right LaparoscopyNezhat et al. 1992 1 Right LaparoscopyChinegwundoh et al. 1995 1 Right Laparotomy

Witte and Guilbaud 1995 1 Bilateral LaparoscopyMangal et al. 1996 1 Bilateral LaparoscopyNezhat et al. 1998 24 Right, 14 Laparoscopy

Left 2Bilateral, 8

Cooper et al. 1999 1 Right LaparotomyGarca Leon et al. 1999 2 Right, 1 Laparoscopy

Left,1Kalapura et al. 2000 1 Bilateral LaparoscopyRedwine 2002 8 Right, 7 Laparoscopy

Bilateral, 1Wolthuis et al. 2003 1 Bilateral LaparotomyNahir et al. 2004 1 Right LaparotomyTakeuchi et al. 2005 1 Right Laparoscopy

Table 1: Continued

Reference Year No. of cases Reason for exclusion

Korom et al. 2004 3 Lesions on the pleural side at thoracotomy or thoracoscoJeffry et al. 2004 1 Affected side not specifiedJelovsek et al. 2004 1 Hepatic lesion, malignant transformationCarbone et al. 2004 1 Hepatic lesion, no diaphragmatic involvementAlifano et al. 2005 7 Lesions on the pleural side at thoracotomy or thoracoscoDevue et al. 2005 1 Lesions on the pleural side at thoracoscopyGirlanda et al. 2005 1 Hepatic lesions, no diaphragmatic involvement

Hiraoka et al. 2005 6 Lesions on the pleural side at thoracoscopyMarshall et al. 2005 5 Lesions on the pleural side at thoracoscopyNezhat et al. 2005 3 Affected side not specifiedPeikert et al. 2005 1 Lesions on the pleural side at thoracoscopyBagan et al. 2006 1 Lesions on the pleural side at thoracoscopyLee et al. 2006 1 Lesions on the pleural side at thoracoscopy


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under experimental conditions which may be dissimilar to the

physiologic abdominal environment of menstruating women

(e.g. adoption of Trendelenburg position, injections of radio-

paque 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 endo-

metriotic 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 liga-ment, ureter and the large bowel itself (Vercellini et al.,1998a,

2004; Chapron et al., 2006) (Fig. 2).

The prevalence of diaphragmatic endometriosis in our surgi-

cal 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 underestima-

tion due to surgeons limited awareness of the condition. More-

over, 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 dia-

phragm, 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 thelaparoscope beneath the costal margin with the operating

table in steep reverse Trendelemburg position (Redwine,

2002). Consequently, it cannot be excluded that the true preva-

lence 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 rightlateral 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, per-

itoneal 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 patho-

genetic 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 intes-

tinal 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.

Figure 2: Hypothesized pathogenesis of diaphragmatic endometrio-sisThick dashed arrows, clockwise peritoneal fluid current, Thin blackarrows, trans-diaphragmatic migration of endometrial cells as acause of secondary right pleural endometriosis; A, adnexa; C, des-cending colon; D, diaphragm; F, falciform ligament; L, left hepaticlobe; R, right hepatic lobe; S, sigmoid; RHEC, right hypocondriumendometriotic complex; LHEC, left hemipelvis endometrioticcomplex. Modified from Ingram (1984). Reproduced withpermission

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Acknowledgements

Supported in part by the University of Milan School of MedicineResearch Grant FIRST no. 12-01-5068118-00 067. Photographs forFigure 1 are courtesy of Dr. Enrico Canducci.

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Submitted on November 13, 2006; resubmitted on June 12, 2007; acceptedJune 21, 2007


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