_Journal oj Epidemiology anzd Community Health 1993; 47: 84-88

REVIEW ARTICLE

Epidemiology of endometriosis

Punam Mangtani, Margaret Booth

Endometriosis is a cause of acquired dys-menorrhoea, dyspareunia, intermenstrual bleedingand menorrhagia, infertility, and pelvic pain ofvarying severity and location.' The disease is seenas one with obscure determinants, with littleknown about its distribution in the population, andwith poor response to treatment. This reviewevaluates the current knowledge on the epidem-iology of endometriosis.

Disease descriptionEndometriosis was recognised as a pathologicalentity only in the 1860s, and as a recognisableclinical problem in the 1920s.2 It is a condition inwhich tissue with the histological structure andphysiological responses of uterine mucosa occursin sites other than the uterus; commonly within thepelvis.2 The implants produce vesicles or haemor-rhages that are seen as blue, brown, or blacknodules on peritoneal surfaces of the pelvis. Ifsevere, the implants may go on to produce fibrosisand adhesions.3 It is not known why implants thatdo not cause physical distortion are associated withinfertility or cause disproportionate pelvis dis-comfort.4 Little is known about the natural historyof endometriosis.' 7 Because the physical findingsare non-specific, clinical findings can be confusedwith those of pelvic inflammatory disease, benignor malignant ovarian disease, fibroids, and gastro-intestinal or urinary problems.

Since the 1970s, diagnostic confirmation hasbeen possible by directly visualising the pelvisusing a laparoscope. Before this, laparotomy wasthe only confirmatory method possible.

Department ofEpidemiology andPopulation Sciences,London School ofHygiene and TropicalMedicine, KeppelStreet, London WC1E7HTP MangtaniM Booth

Correspondence to:Dr P Mangtani

Accepted for publicationNovember 1992

Burden of diseaseEndometriosis is not life threatening, but it is an

important cause of morbidity in women. In

England and Wales there are few routine data on

its contribution to the burden of ill health in thepopulation. The disease did not have a separatecode in the national Morbidity Studies fromGeneral Practice' or in Hospital In-PatientEnquiry data.9 Routine data from the UnitedStates (USA) for 1980 showed that the hospitaladmission rate for endometriosis was twice therate for ectopic pregnancy in 15-44 year oldwomen and accounted for half a million bed daysper year.'0 A population based study undertakenin Rochester, USA in 1979 suggested that theprevalence of endometriosis was 3-3%. 11

For the individual, the disease can cause

chronic pain or infertility that may require hospi-

tal admission, surgery, or long periods of treat-ment which may have unpleasant side effects.Treatment is often unsatisfactory, although it canresult in resolution of the symptoms.12 Radicalsuppression of ovarian function by treatment withdrugs such as danazol and gonadotrophinreleasing factors may still not achieve permanentcure.13 15 For extensive disease, surgicalcastration may be the only definitive treatment.'2An understanding of the aetiology of endo-metriosis is needed in order to reduce the burdenof morbidity in women. Little is presently knownabout its causes because of the problem of casedefinition and methodological flaws in studydesign.

Case definitionStandardised objective criteria for the reliablediagnosis of endometriosis are difficult to estab-lish as it has a variable, non-specific clinicalpresentation and natural history. Confirmation ofthe diagnosis requires laparoscopy. There are,however, few data on the repeatability oflaparoscopic findings. Validity may also be lessthan thought as atypical lesions and microscopicchanges can occur.'6There are criteria to stage the severity of disease

at laparoscopy based on morphology.'7 Criteriafor establishing whether a case is one of sickness,prognostic of infertility, or amenable to treatmentwould be useful but such systematic investigationhas only just begun.3 5 18 19More simple tests such as the serum ovarian

tumour marker CA-125 are being investigated.CA-125, however, may have a low specificity andsensitivity. In one survey of infertile women it wasraised in just over 50% of those with endo-metriosis but it was also high in women with otherpelvic disorders including pelvic inflammatorydisease.20 In another study of women with bothinfertility and pelvic symptoms, the sensitivity wasonly 16% (10 of 60) although the specificity was98% (85 of 87).21

Immunological markers of endometriosis, such asanti-endometriosis antibody, have been found.Using an immunohistochemical method to detectthe antibody, the sensitivity was 77-5% (31 of 40)and the specificity 42-5% (17 of 40).22 In anotherstudy using passive haemagglutination, the sen-sitivity was 74% (17 of 23) and the specificity 100%(28 of 28).23 The control samples in both studies,however, were either from men or from cord blood.Further work on larger numbers of women isneeded to determine the usefulness of these tests.

on March 14, 2020 by guest. P

rotected by copyright.http://jech.bm

j.com/

J Epidem

iol Com

munity H

ealth: first published as 10.1136/jech.47.2.84 on 1 April 1993. D

ownloaded from

Epidemiology of Endometriosis

At present the clincal and epidemiological casedefinition for endometriosis requires laparos-copy, which has to be undertaken in a hospital.Cases identified in this way may be unrepre-sentative of cases in the general populationbecause of variation in the presenting symptoms,in the health seeking behaviour of patients, thereferral process, diagnostic practice, and differen-tial access to diagnostic facilities. Studies whichuse cases found when laparoscopy is performed forother reasons also suffer from this considerableascertainment bias.

It may be possible to avoid ascertainment bias insome hospital settings. For instance, samplingwomen with endometriosis who had presented witha pelvic mass or acute abdomen. All women withthese presenting conditions, although uncommon,24would have had direct visualisation of the abdomenor pelvis. To generalise the results to all women withendometriosis, however, would require greaterknowledge of the natural history of the disease.One study tried to reduce some of the ascer-

tainment bias in the use of hospital cases byconstructing operational definitions based onlevels of diagnostic certainty. " These weredefined as follows:

(1) Histologically proved endometriosis only.(2) Histologically proved or surgically visual-

ised disease.(3) The above and those with clinically prob-

able endometriosis.Bias was reduced in the last definition by includingwomen who had not yet undergone selection forlaparoscopy. The sensitivity and specificity ofthese operational definitions, however, have still tobe determined.

Descriptive epidemiologyINCIDENCE AND PREVALENCERoutinely collected data from the USA showedthat in 1980 there were 18-4 hospital admissionsfor endometriosis per 100 000 women aged 1 5-44years. 10 The data cannot, however, reflect the trueincidence of disease. Repeat admissions wouldhave been counted as separate episodes. Womenseen as outpatients, or who had not come to theattention of medical services, or who wereasymptomatic would not have been included.Only one study has measured disease incidence,

defined as newly diagnosed cases of endo-metriosis. 1l All these cases in women aged 15 to49 years in the population of Rochester, USA in1979, were able to be traced as only one medical

Prevalence of endonietriosis in studies of case-grouips

Clinzicalcase-groupinvestigatedLaparoscopicsterilisations

Infertility

Chronic pelvicpain

Authors and yearof studyLiu and Hitchcock, (1986) "Moen, (1987)48Kirshon and Poindexter, (1 988)4"Cates et al (1983)54

Hasson, (1976)"Strathy, (1982)55Hasson, (1976) "

Stuidy, regioni

NottinghamNorwayUSAWHO) niidlticepitrex stid5w

AfricaAsiaLatin AmericaEast MediterraneanWest Europe, North

America, andAustralia

USAUSAUSA

Prevalkuce% (110)

43 (108)51 (75)7 (566)

1 (842)10 (1992)3 (1228)1 (432)

6 (3904)23 (66)21 (100)15 (212)

facility existed for the study population. The at riskpopulation, 17 000 women in that age group, wasobtained from the decennial census. Interobserverreliability of case ascertainment was near 100%when checked by a repeat survey of the records.The incidence rates per 100 000 women years atrisk for decreasing levels of certainty of diagnosiswere as follows:

(1) Histologically proved endometriosis only-108-8.

(2) Histologically proved or surgically visual-ised disease- 160-4.

(3) The above, and those with clinically prob-able endometriosis-237-4.

The incidence of diagnosed endometriosis wasabout 0-3% in white 15 to 49 year old women eachyear. In assuming a 10 year duration of disease onaverage, the authors estimated that the periodprevalence would have been between 2-5-3-3%.As population studies are otherwise absent, thereare no accurate data on time trends or geo-graphical distribution of disease.The only other data are from cross sectional

prevalence surveys of case-groups from hospitalsettings. As can be seen in table I the prevalencevaries considerably both within and between thecase-group categories. True variations in preva-lence, however, cannot be distinguished fromchance effects, distortions caused by ascer-tainment bias or confounding. Geographical dif-ferences in prevalence would have been affectedby changes in diagnostic habits and differences inaccess to health care between countries. Studiesthat are able to identify, measure, and investigateincident cases in a defined population would, ofcourse, be of greater use.

AGE DISTRIBUTIONThe risk of endometriosis may not increaselinearly with age. In Houston's study the inci-dence rate of clinically probable cases rose sharplywith age up to 35 years and then fell rapidly onlyafter age 44.11 Other incidence studies thatmeasure age specific rates would be useful toconfirm these findings.

SOCIOECONOMIC STATUSIt is often stated that endometriosis is seen morefrequently in higher socioeconomic groups.25 26The evidence comes historically from case groupstudies. For instance, a higher prevalence wasseen in a study of white private gynaecologypatients compared with white or black non-private patients.27 Differential access to healthcare by socioeconomic group was, however,likely.Two recent case-control studies also suggested

an association with higher socioeconomicstatus.28 29 In the former study differential accessby cases compared with controls may also havebeen operating; the cases having a mostly chroniccondition and the controls coming from a hospitalgroup requiring laparoscopies for a variety ofoften acute conditions. The latter study, con-ducted in the USA using population based con-trols, showed a positive socioeconomic associationonly in those presenting with infertility, not inthose with pelvic symptoms.2" It is possible that inthe USA, access to infertility services is more

85

on March 14, 2020 by guest. P

rotected by copyright.http://jech.bm

j.com/

J Epidem

iol Com

munity H

ealth: first published as 10.1136/jech.47.2.84 on 1 April 1993. D

ownloaded from

Punam Mangtani, Margaret Booth

influenced by socioeconomic status than investi-gations for pelvic symptoms.

ETHNICITY

An association with ethnicity has also been sug-gested in case-group studies in the USA. In the1 930s it was taught that endometriosis was rare inblack people.2 Prevalence was noted to be lowerin black compared with white non-privatepatients.27 30 This was also remarked upon morerecently, but it was also suggested that the highestprevalence occurred in South-East Asianpatients.3' However, little account was taken oflikely confounding factors such as socioeconomicstatus.32 In a study of private white and blackgynaecological surgery patients there was nodifference. 33A high prevalence of endometriosis in Japanese

women has been suggested.34 The evidence isbased on one cross sectional survey ofgynaecological admissions to hospitals in Hawaiiin 1974 in which fewer than four cases withendometriosis were Japanese.35 Thus little data ofsufficient rigor exist to show socioeconomic orethnic differences in disease risk.

AetiologyMENSTRUAL IRREGUIARITIES, EXERCISE, ANI)

SMOKINGRetrograde menstruation is a well recognised34and plausible pathogenetic explanation of howviable endometrial cells are seeded in the abdomi-nal cavity. This has been documented in 57 of 75(76%) of women who underwent laparoscopicsterilisation while menstruating. Fifty per cent ofthose with retrograde menstruation had endo-metriosis compared with 5% of those withoutretrograde flow.36Two case-control studies have investigated risk

factors for endometriosis mediated via retrogrademenstruation. In one, using women on deliverywards as control subjects, an increased risk wasassociated with increased duration ofbleeding andwith dysmenorrhoea. These may, however, havemerely been symptoms of disease. This study alsosuggested that exercise ofmore than two hours perweek was protective (odds ratio (OR) 0-6, 95%confidence interval (CI) 0 4, 0 8). The types ofexercise most strongly related to decreased riskwere conditioning exercises, including jogging or

calisthenics. Smoking more than one packet ofcigarettes per day from the age of 17 years was alsoprotective (OR 0-5, 95% CI 0 3, 0_9).37The other case-control study of endometriosis

used population based control subjects. The studypopulation was analysed as two separate groups,those cases with infertility and those with pelvicsymptoms, because various factors includingsocioeconomic status, race, age, and marital status

were found to be very different between the two

groups. An association was found between endo-metriosis and dysmenorrhoea but not with dur-ation of bleeding in both cases with infertility andcases with pelvic symptoms. As with the previousstudy, the case-control design did not allow separ-ation of risk factors from what were likely to besymptoms of disease. Exercise was not associatedwith disease in the infertility group but was

significantly protective in the pelvic symptomsgroup even after adjustment for educational level,dysmenorrhoea, age at menarche, body massindex, and smoking (relative risk (RR) in theinfertility group 1-35, 95% CI 0-84, 2 16, RR inthe pelvic symptom group 0 36, 95% CI0 19, 0-69). A protective effect of smoking wasfound after adjustment for the level of education,age at menarche, dysmenorrhoea, body massindex, exercise, and oral contraceptive use. Theprotective effect was greatest in those with primaryinfertility (OR 0-18, CI 0 07, 0 47), followed bythose with pelvic symptoms (OR 0 53, 95% CI0-24, 1-19) and least in those with secondaryinfertility (OR0 73, CI0 27, 1.98).29 The reasonsfor this gradient are unclear.There is a suggestion that smoking and exercise

are associated with oestrogen deficiency38 and, ifendometriosis is oestrogen sensitive, findings ofsmoking or exercise protecting against endo-metriosis may be plausible.

UNOPPOSED OVARIAN FUNCTION

Unopposed cyclic ovarian hormone secretion haslong been thought to encourage proliferation ofendometrial tissue.'9 34 It is well known thatremoval of the ovaries reduces risk ofdisease39 andthat disease risk falls with the onset of themenopause. Oestrogen receptors have beendetected in endometriosis tissue but at lower levelsthan in endometrial tissue.4" In a trial ofmaintenance of endometrial implants placed inthe peritoneal cavities of monkeys, only oestrogenprolonged growth of the ectopic tissue comparedwith progesterone or placebo.42 The idea thatwomen may be protected against endometriosiswhen ovulation is interrupted by pregnancy or useofcombined oral contraception25 43 44 is thereforeplausible. Evidence to confirm this hypothesis is,however, scarce.

Histological regression of endometriotic de-posits has not been seen consistently in preg-nancy.'5 In a follow up study, 19 of 50 (38%)women with endometriosis who became pregnantre-attended with symptoms of the disease within 5years.46 Anovulation in over 1O0% of a case-seriesofwomen with endometriosis has also been repor-ted.47 Prospective data would be useful to confirmthat anovulation preceded the onset of endo-metriosis. If this were shown it would suggest thatthe presence of oestrogen may not be essentialfor disease to occur, though such results would notexclude its role as a predisposing factor.The relationship of combined oral contra-

ception and endometriosis was studied in a case-group of women undergoing laparoscopicsterilisation.48 Nineteen of 98 (19%) were foundto have endometriosis on laparoscopy. Nodifference was seen between those with or withoutdisease in their age, their age at menarche, age atfirst pregnancy, number of deliveries, and type ofcontraception used. There was, however, a signifi-cant difference between cases and controls in themean time of unopposed ovulation (cases 11 2years, controls 8-4 years (p<0 02)). The durationof combined oral contraceptive use may haveexplained this finding but the data were not

presented. A similar larger study of 566 patients(42 of whom had endometriosis) compared the

86

on March 14, 2020 by guest. P

rotected by copyright.http://jech.bm

j.com/

J Epidem

iol Com

munity H

ealth: first published as 10.1136/jech.47.2.84 on 1 April 1993. D

ownloaded from

Epidemiology of Endometriosis

proportions with or without disease in combinedoral contraceptive users and in users of barriermethods or of no contraception. No associationwith any one type of contraception was seen.49Apart from sampling error selection bias may haveresulted in an underestimate of the effect ofovarian suppression on disease risk. Cases andcontrols obtained from women havinglaparoscopic steriiisations under-representedinfertile women, who have a higher prevalence ofendometriosis.The effect of increasing age and higher socio-

economic status on the risk of disease has beenthought to be mediated by delaying pregnancy andhaving fewer children.25 There is, however, poorevidence of an association between pregnancy,socioeconomic status, and endometriosis. Adetailed hospital based case-control study did notshow this even in the late 1940s.30 A total of 646women with histologically proved endometriosiswere compared with 600 women admitted tohospital with pneumonia. Fertility rates in bothprivate and non-private cases were similar withinthe strata of time since marriage and age atmarriage. The same was seen in the controlpatients. Fertility rates were lower in the casesthan in the control subjects, suggesting only thatendometriosis reduces fertility.

IMMUNOLOGICAL FINDINGSResearch into the immunology of endometriosismay be useful in delineating further thepathogenesis of the disease. In one case-controlstudy, a twofold increased risk (95% CI, 0-6, 6 8)of endometriosis was found in patients with sys-temic lupus erythematosus.50 Newly diagnosedcases of systemic lupus erythematosus dischargedfrom hospital were compared with controls ran-domly selected from hospital discharges otherthan from obstetric and gynaecology specialities.The sample size was, however, too small toexclude chance given the wide confidence interval.

Raised non-specific IgG antibodies have beenfound in significantly more women with endo-metriosis compared with female blood donors5'and, as mentioned earlier, raised antiendometrialantibody levels were found in significantly morecases compared with control male or cord bloodsamples (p<0-001).22 23

GENETIC PREDISPOSITIONIt has been suggested that a genetic predispositionfor endometriosis may exist.'2 26 An associationwith a positive family history was found in twostudies. Design flaws exist, however, in bothstudies and may have introduced bias producingan overestimate of the magnitude of the associa-tion. In one ofthe studies, 6-9% ofcases comparedwith 0 9% of controls were found to have affectedrelatives. The controls used were the patients'husbands. Recall bias by women with disease waspossible and the husband controls may have beenless able or motivated to know about ill health intheir own families. Interviewer bias was alsopossible as the family history in both groups wasobtained by an interviewer not blind to the diag-

52nosis.52The second study found cases from the mailing

list of an endometriosis support group who had

volunteered a positive family history on the appli-cation form. The study used 'best friends' ascontrols. Because of the method of selection ofcases, it is inappropriate to make a case-controlcomparison. However, of the 43 women withendometriosis who reported other family mem-bers with the disease, most involved the maternalline.53

ConclusionsThus far, the data on the distribution anddeterminants of endometrisosis in the populationare limited. The disease occurs in reproductive agegroups but a linear increase with age has not beenshown and the quoted socioeconomic and ethnicdifferences in disease prevalence are not wellfounded. Knowledge of time trends and geo-graphical differences in disease risk is lacking.

Menstrual regurgitation may be a pathogenicfactor, and risk factors that increase the likelihoodof regurgitation into the pelvic cavity need to beinvestigated further. There may be an increasedrisk with unopposed ovarian function but it is notyet adequately documented to properly give pre-ventive advice such as encouraging pregnancy orthe use of combined oral contraception. Othertentative findings that might be followed up arethe role of smoking and exercise on disease risk.

Until a simple test that may be safely applied at a

population level becomes available, care withstudy design is needed to reduce ascertainmentbias. For instance, Houston used an operationalepidemiological definition for all clinically prob-able symptomatic endometriosis presenting tomedical services in a defined population.'" Itavoided a part ofthe ascertainment bias in hospitalbased studies by including probable cases who hadnot yet undergone selection for laparoscopy. Thestudy was also able to measure incidence ratherthan prevalence. In some studies the selection ofthe control groups may have introduced bias.Population based or hospital control subjectsother than obstetric or gynaecology patientsmaybe more appropriate than women known to befertile. If attention is also given to confoundingand power based calculations of sample size, itshould be possible to test more accurately theaetiological hypotheses suggested so far.

We thank George Davey-Smith for helpful commentsand Evelyn Middleton for typing help. Punam Mangtaniis a Medical Research Council Fellow in Health ServicesResearch and Margaret Booth is funded by a MedicalResearch Council Programme Grant.

I Galle PC. Clinical presentation and diagnosis ofendometriosis. Obstet Gvynaecol CGiU North Am 1989; 16(1):29-42.

2 Houston DE. Evidence for the risk ofpelvic endometriosis byage, race and socioeconomic status. Epideiniol Rev 1984; 6:167-91.

3 Brosens IA, Puttemans P. Endometriosis-currentconcepts. Horml Res 1989; 32(suppl 1): 103-5.

4 Fedele L, Parazzini F, Bianchi S, Arcaini L, Candiani GB.Stage and localisation of pelvic endometriosis and pain.Fertil Steril 1990; 53(1): 155-8.

5 Thomas EJ, Cook ID. Successful treatment ofasvmptomaticendometriosis, does it benefit infertile women? Br Aled JCliol Res 1987; 294: 1117-9.

6 Bancroft K, Vaughan-Williams CA, Elstein M. Minimal/mild endometriosis. A review. Br J Obster Gwiaecol 1989;96(4): 454-60.

7 Surrev ES, Halme J. Endometriosis as a cause of infertilitv.Obstet Gwaecol (Clin North Aii 1989; 16(1): 79-91.

87

on March 14, 2020 by guest. P

rotected by copyright.http://jech.bm

j.com/

J Epidem

iol Com

munity H

ealth: first published as 10.1136/jech.47.2.84 on 1 April 1993. D

ownloaded from

Punam Manigtanl, Margaret Booth

8 Roval College of General Practitioners, Office of PopulationCensuses and Surveys, Department of Health and SocialSecurity. Alorbidity statistics jromti genieral practice 1981-82:third national stuidy. London: HMSO, 1986.

9 Department of Health, Office of Population Censuses andSurveys. Hospital in-patient inquiryn 1979-85. London:HMSO, 1989.

10 McCarthy E. Inpatient utilisation of short stay hospitals bydiagnosis: Uniited States- -1980. Hyattsville, Maryland:DHHS publication no (PHS) 83-1735; 1982.

11 Houston DE, Noller KL, Melton LJ 3rd, Selwyn BJ, HardvRJ. Incidence of pelvic endometriosis in Rochester,Minnesota, 1970-1979. AmJEpideniiol 1987; 125: 959-69.

12 Anonymous. Endometriosis (Editorial). BAIR 1990; 301:189-90.

13 Candiani GB, Vercellini I', Fedele L, Bocciolone L, BianciC. Medical treatment of mild endometriosis in infertilewomen: analysis of a failure. Hunn Reprod 1990; 5(8): 901- 5.

14 Hull ME, Moghissi KS, Magyar DF, Hayes MF.Comparison of different treatment modalities ofendometriosis in infertile women. F'ertil Steril 1987; 47(1):40 4.

15 Thomas EJ, Cooke ID. Impact ofgestrinone on the course ofasvmptomatic endometriosis. BA13 1987; 294: 272-4.

16 Dmowski WP. Pitfalls in clinical, lapaoscopic andhistological diagnosis of endometriosis. Acta Obstet GyjnaecolScand 1984; 123(suppl): 61-6.

17 The American Fertility Society. Revised American FertilitySociety Classification of Endometriosis: 1985. Fertil Steril1985; 43: 351-2.

18 Weitzman GA, Buttram VC. Classification of endometriosis.Obstet Gvnaecol Clin North Ami 1989; 16(1): 61-77.

19 Thomas EJ. Preventive, symptomatic and expectantmanagement of endometriosis. Prog C'lini Biol Res 1990; 323:197-208.

20 Pittawav DE. CA 125 in women with endometriosis. ObstetGvnaecol Clipi North Am 1989; 16(1): 237-52.

21 Barbieri RL, NiloffJM, Bast Jr RC, Schaetzl E, Kistner RW,Knapp RC. Elevated serum concentrations of CA-125 inpatients with advanced endometriosis. Fertil Steril 1986; 45:630-4.

22 Kennedy SH, Sargent IL, Starkey PM, Hicks BR, BarlowDH. Localisation of anti-endometrial antibody binding inwvomen with endometriosis using a double-labellingimmunohistochemical method. Br 7 Obstet Gwnaecol 1990;97: 671-4.

23 Chihal HJ, Mathur S, Holtz GI, Wiliiamson HO. Anendometrial antibody assay in the clinical diagnosis andmanagement of endometriosis. Iertil Ste-il 1986; 46(3):408 11.

24 O'Connor 1). Clinical features and diagnosis. In: O'ConnorD, ed. Cur-rent reviews in Obstetrics and Gvnaecologs' 12.I'.ndomnetriosis. New York: Churchill Livingstone, 1987:68 84.

25 MeigsJV. An interest in endometriosis and its consequences.Ani]i Obstet (s'naecol 1960; 79: 625 35.

26 Editorial. Endometriosis continuing conundrum. BM.1980; 281: 889-90.

27 Scott RB, TeLinde RW. External endometriosis- -thescourge of the private patient. Annii Suirg 1950; 131: 697-720.

28 Obermeyer CM, Armenian HK, Azoury R. Endometriosis inLebanon. AinjEpidemiol 1986; 124: 762-7.

29 Hiller JE. A case-control stuidy of endonietinosis [PhD thesis].Baltimore, Maryland: Johns Hopkins University, 1987.

30 Cavanagh WV. Fertility in the etiology of endometriosis. Ani.7 Obstet Gvnaecol 195 1; 61: 539 47.

31 Hasson HM. Incidence of endometriosis in diagnosticlaparoscopy. 7 Reprod Med 1976; 16(3): 135-8.

32 Navarro V. Race of class versus race and class: mortalitydifferentials in the United States. Lancet 1990; 336: 1238-40.

33 Lloyd FP. Endometriosis in the negro woman: a five vearstudy. Anin Obstet Gynaecol 1964; 89: 468-9.

34 Haney AF. Etiology and histogenesis of endometriosis. ProgCli,, Biol Res 1990; 323: 1-14.

35 Miyazawa K. Incidence of endemetriosis among Japanesewomen. Obstet Gyniaecol 1976; 48(4): 407-9.

36 Liu DTY, Hitchcock A. Endometriosis: its association withretrograde menstruation, dysmenorrhoea and tubalpathology. Br_] Obstet Gvnaecol 1986; 93: 859-62.

37 Cramer DW, Wilson E, Stillman RJ, et al. The relation ofendometriosis to menstrual characteristics, smoking andexercise. JAMA 1986; 255: 1904 8.

38 Baron JA. Smoking and oestrogen-related disease. Anii 7IEpidemiol 1984; 119: 9-21.

39 Williams TJ, Pratt JH. Endometriosis in 1000 consecutiveceliotomies: incidence and management. Aiui 7 ObsltGvnaccol 1977; 129(3): 245 50.

40 Tamaya T, Motoyama TO, Ohono Y, Ide N, Tsurusaki T,Okada H. Steriod receptor levels and histology ofendometriosis and adenomyosis. Fertil Steril 1979; 31(4):396-400.

41 Janne 0, Kauppila A, Kokko E, Lantto T, Ronnberg L,Vihko R. Estrogen and progestin receptors in endometriosislesions: comparison with endometrial tissue. Anti .7 ObstetGvnaecol 1981; 141(5): 562-6.

42 Dizerega GS, Barber DL, Hodgen GD. Endometriosis: roleof ovarian steroids in intiation, maintenance andsuppression. Fertil Steril 1980; 33(6): 649-53.

43 Ranney B. The prevention, inhibition, palliation andtreatment of endometriosis. An .7 Obstet Gvnaecol 1975;123(8): 778-85.

44 Ranney B. Endometriosis: pathogenesis, symptoms andfindings. Clin Obstet Gynaecol 1980; 23(3): 865--74.

45 McArthur JW, Ulfelder H. The effects of pregnancy onendometriosis. Obstet Gynaecol Surv 1965; 20: 709-33.

46 Walton LA. A re-examination of endometriosis afterpregnancy. _Reprod Med 1977; 19(6): 341-4.

47 Soules MR, Malinak LR, Bury P, Poindexter A.Endometriosis and anovulation: a coexisting problem in theinifertile female. Ani.7 Obstet Gvnaecol 1976; 125(3): 412- 7.

48 Moen MH. Endometriosis in women at interval sterilisation.Acta Obstet (Gynaecol 'Scand 1987; 66(5): 451 4.

49 Kirshon B, Poindexter AN 3rd. Contraception: a risk factorfor endometriosis. Obstet Gvnaecol 1988; 71: 829 31.

50 Grimes DA, Lebolt SA, Grimes KR, Wingo PA. Systemiclupus erythematosus atid reproductive function: a casc-control studv. Ami 7 Obstet Gvnaecol 1985; 153: 179-86.

51 Gleicher N, EL-Roeiy A, Confino E, Friberg J. Isendometriosis an autoimmune disease? Obstet Gvnaecol1987; 70(1): 115-22.

52 Simpson JI, Elias S, Malinak ILR, Buttram VC. Heritableaspects of endometriosis. 1. Genetic studies. Antt 7 ObstetGvnaecol 1980; 137: 327 31.

53 Lamb K, Hoffman RG, Nichols TR. Family trait analysis: acase control study of43 women with endometriosis and theirbest friends. An,iY Obstet Gynaecol 1986; 154: 596 601.

54 Cates W, Farley TMM, Rowe PJ. Worldwide patterns ofinfertility: is Africa different? lIancet 1983; ii: 596-8.

55 Strathy JH, Molgaard CA, Coulam CS, Melton LU 3rd.Endometriosis and infertilitv: a laparoscopic study ofendometriosis among fertile and infertile women. IFertil Steril1982; 38(6): 667-72.

88

on March 14, 2020 by guest. P

rotected by copyright.http://jech.bm

j.com/

J Epidem

iol Com

munity H

ealth: first published as 10.1136/jech.47.2.84 on 1 April 1993. D

ownloaded from