J Pediatr Adolesc Gynecol (1997) 10:199-202
Prevalence of Endometriosis in Adolescent Girls With Chronic Pelvic Pain Not Responding to Conventional Therapy M.R. Laufer, M.D. , 1- 3 ,5 L. Goitein , B.A. ,5 M. Bush , M.D. ,5 D.W. Cram缸, M.D. , M.P.H. ,4 ,5 and
S.l. Emans , M.D. 2 ,5 lDivision of Gynecology , Department of Surgery , 2Division of Adolescent/Young Adult Medicine , Department of Medicine , Children's Hospital; 3Division of Reproductive Endocrinology , 4Division of Epidemiology , Department of Obstetrics , Gynecology , and Reproductive Biology , Brigham and Women's Hospital; 5Harvard Medical School , Boston , 弘1assachusetts
Abstrac t. Study Objective: To evaluate adolescent girls with chronic pelvic pain not responding to conventional medical therapy , using advances in operative laparoscopy to determine endometriosis prevalence , clinical stage , and type of lesion. Design: A descriptive retrospective study of subjects who (1) were referred for the evaluation of chronic pelvic pain , (2) did not respond to a nonsteroidal anti-inflammatory drug and an oral contraceptive pill , and (3) underwent a laparoscopy to determine the etiology of the pelvic pain. Setting: Patients referred to a surgical gynecologist in a pediatric/adolescent gynecology and reproductive endocrine academic practice. Participants: All patients younger than 22 years of age with chronic pelvic pain. Intervention: Operative laparoscopy to determine the etiology of the chronic pelvic pain. Main Outcome Measures: Operative laparoscopy results including stage and description of endometriosis. Results: More than two thirds of the study population (69.6%) was found to have endometriosis. All subjects had either stage I or II as determined by the American Fertility Society' s classification system. The nature of the pain in the 32 subjects with endometriosis was both acyclic and cyclic in 20 (62.5%) , acyclic only in 9 (28.1 %), and cyclic only in 3 (9.4%). Other presenting symptoms included gastrointestinal in 11 (34.3%) , urinary in 4 (12.5%) , and irregular menses in 3 (9.4%). Conclusions: Adolescents with chronic pelvic pain not responding to medical therapy have a high rate of endometriosis and should be referred to a gynecologist who is experienced with the subtle laparoscopic findings of atypical endometriosis to diagnose the etiology of the pelvic pain and initiate appropriate therapy.
Key Words. Pelvic pain-Endometriosis-Adolescent
Introduction Endometriosis , the pathological presence of endometrial glands and stroma located outside of the normal intrauterine anatomic location , can cause symptoms during both adolescence and adulthood. I - 8 Primary care providers are often concerned about whether the adolescent with chronic pelvic pain has endometriosis or another pathological etiology. Prevalence rates of endometriosis in adolescents with chronic pelvic pain have previously been reported to range from 19%-47% .3,8 However, based on more recent descriptions of ‘ ι atypic al endometriosis ,' , 9- 15 it is possible that the previously reported prevalence rates may be understated. In addition , if only adolescents who have received and failed conventional treatment for dysmenorrhea with nonsteroidal antiinflammatory drugs (NSAIDs) and oral contraceptive pills (OCPs) undergo laparoscopy , the prevalence rates of endometriosis may be determined to be even higher. The purpose of this repolt is to determine the prevalence , stage , and typical appearance of endometriosis in young women who have failed conventional therapy and undergo laparoscopy with modem criteria for diagnosis of the disease.
Methods Address reprint requests to: Marc R. Laufer, M.D., Division of Gynecology, Department of Surge句 , Children's Hospital, 300 Longwood Avenue , Boston , Massachusetts 02115.
Presented in part at the Ninth Annual meeting of the North American Societyfor Pediatric and Adolescent Gynecology (NASPAG) , Toronto , Canada, 1995. 1083-3188 © 1997 Chapman & Hall
The study population consisted of all adolescent girls (less than age 22) from the Children' s Hospital and the Brigham and Women's Hospital in Boston who (1) were referred between 1990 and 1994 for the evaluation of
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Laufer et al. : Chronic Pelvic Pain and Endometriosis Table 1. Laparoscopic Findings of Adolescent Patients With Chronic Pelvic Pain Not Responding to OCPs and NSAIDs •• A
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chronic pelvic pain of longer than 3 months in duration, (2) had pelvic pain that did not respond to a regimen of an NSAID and a cyclic low-dose combination estrogen! progestin OCP (or for whom these therapies were contraindicated/not tolerated), and (3) underwent a laparoscopy , at which one of the authors (M.L.) was present, to determine the etiology of the pelvic pain. The patient population was identified from a computerized listing of all of the referred patients undergoing laparoscopy at which M.L. was present. Patients evaluated had been referred by prin1ary care providers who were unable to identify an etiology for the pelvic pain. Records of the study population were reviewed to establish demographic information , presenting symptoms , preoperative treatment, and operative findings. At laparoscopic evaluation, endometriosis was diagnosed on the basis of either visualization of gross lesions or microscopic evaluation of pelvic biopsy specimens. , 'Classic' , black-blue nodules and "atypical" lesions (white or opaque nodules , flame lesions, and clear vesicles) were identified as endometriotic lesions that were grossly visible laparoscopically and were classified by the same surgeon (M.L.) according to the American Fertility Society Revised Classification of EndometriOSiS. 16 Subjects with a grossly normal pelvis had random pelvic peritoneal biopsy specimens histologically evaluated to identify microscopic endometriosis. Characteristics of subjects with and without endometriosis were con1pared using X2 and Fischer' s exact tests for non1inal variables and Studen t' s I-tests for continuous variables.
Number
F3
Visible endometriosis Grossly normal pelvis Adhesions Prior surgery With endometriosis Without endometriosis No prior surgery With endometriosis Without endometriosis Functional cysts Paratubal cysts Mullerian anomalies With endometriosis Without endometriosis
31146 (67 .4) 5/46 (10.9) 11146 (23.9) 8
3 5 3 3 O 4/46 (8.7) 4/46 (8.7) 3/46 (6.5) 2
endometriosis. Thus, of the 46 adolescent study subjects, 32 (69.6%) were found to have endometriosis. Ofthe 31 subjects with endometriosis that was grossly visible by laparoscopy, 24 (77.4%) had stage I disease, 7 (22.6%) had stage II , and 0% had stage III or IV. As shown in Table 2, the mean age at laparoscopy for those subjects found to have endometriosis was 16.0 years (range, 13 to 20 years), whereas the mean age of those not diagnosed with endometriosis was 16.4 years (range , 14 to 20 years)~ a I-test revealed no statistical difference in mean ages. There was also no statistical difference in age of menarche, the time from menarche to
Table 2. Characteristics of Subjects With and Without Results Forty-six patients met study eligibility criteria and were selected for chart review. Forty-three study subjects had pelvic pain of longer than 3 months in duration that did not improve on a regimen of OCPs and NSAIDs. Three patients were identified who did not complete at least one full month of OCPs because of a history of hypertension (1 subject) or the inability to tolerate the side effects (2 subjects) but otherwise satisfied the entrance criteria and were included. The mean age of subjects at the time of laparoscopy was 16.1 years (range, 的to 21 years). Age at menarche was known for 43 (93.5%) study subjects and ranged fron1 9-15 years, with a mean of 12.3 years. The mean time from menarche to laparoscopy was 3.8 years (range, <1-8 years). Laparoscopic findings in the study population are shown in Table 1. Of the 46 adolescents included in the study, 31 (67.4%) were determined to have grossly visible endometriosis. The 5 subjects with a grossly normal pelvis had at least two random pelvic peritoneal biopsy specimens taken from the posterior cul-de-sac, and 1 patient (20%) was found to have pathologically proven
(%)
Characteristics
Endome 仕iosis
Patients With Endometriosis (n = 32)
Patients Without Endometriosis (n = 14)
7 (2 1.8) 20 (62.5) 5 (15.6) 12.3 3.7
1 (7.2) 10 (7 1.4) 3 (2 1.4) 12.3 3.9
17 (53.1) 9 (28 .1) 6 (1 8.8) 3 (9 .4)
5 (35.7) 6 (42.9) 3 (2 1.4) 5 (35.7)
20 (62.5) 9 (28. 1) 3 (9 .4) 11 (34.3) 4 (12.5) 3 (9 .4) 2 (6.3)
8 (57. 1) 3 (2 1.4) 3 (2 1.4) 6 (42.9) 4 (33.3) 6 (42.9)α 2 (14.3)
Age (y) 三 14
15-17 三 18
Mean age at menarche (y) Mean time at menarche (mo) Duration of OCPs (mo) 三3
4- 11 主 12
Pri or surgery Presenting symptoms
Acyclic andcyclic pain Acyclic pain Cyclic pain Gastrointestinal pain Urinary symptoms Irr egular menses Vaginal discharge
The values shown are the number of patients , with the percentages in parentheses. Q
p < 0.05
Laufer et al. : Chronic Pelvic Pain and Endometriosis laparoscopy , or the mean duration of preoperative treatment with OCPs and NSAIDs in the group of subjects with or without endometriosis. The presenting symptoms of the study subjects with endometriosis as compared with those without endometriosis are shown in Table 2. The percentage of subjects with endometriosis who were identified as having irregular menstrual cycles was 9.49人 comp征ed with 42.9% of subjects without endometriosis (p < 0.05). No other statistically significant differences were noted , but the number of subjects in each group was small.
Discussion Adolescent girls frequently complain of dysmenorrhea and pelvic pain. A standard clinical approach to these complaints is the assessment of symptoms by history and physical examination followed by the prescription of OCPs and NSAIDs in an attempt to treat dysmenorrhea. 9 Some adolescents continue to describe persistent pain despite this medical therapy , and primary care providers must determine when referral to a gynecologist is appropriate for operative laparoscopy so that endometriosis or other entities can be diagnosed and treatment initiated. Symptoms are helpful but cannot precisely distinguish which adolescents will have endometriosis. One classically described symptom of endometriosis in adults is cyclic pain associated with menses. In our adolescent population , this classic adult symptom was found in only 9.4% of subjects , whereas 28.1% of subjects had acyclic pain , and the majority (65.5%) had both cyclic and acyclic pain; thus , 90.6% of adolescents with endometriosis had acyclic pain. This finding is important for the primary care provider and gynecologist because adolescent endometriosis may not present with the typical cyclic pain pattern that is found in adults with the disease. We also found that adolescents with endometriosis were more likely to have regular menses than those without endometriosis. Although this study does not con1pare menstrual cycles in women with chronic pelvic pain to normal adolescents , this finding may relate to Sampson' s Theory of retrograde menstruation17 leading to endometriosis. Based on laparoscopic findings , approximately 90% of adult women have regular exposure to retrograde menstrual flOW. 18 Adolescents with regular menses may have an increased oppol1unity for retrograde menstruation and , thus , a greater tendency for endometriosis to become established. Therefore , regular cycles in adolescents may lead to an earlier presentation of symptoms of endometriosis. In this study , we found a 69.6% prevalence of endometriosis in adolescents who presented with chronic pelvic pain that was unresponsive to OCPs and NSAIDs. In a previous study from Children' s Hospital ,3 endometriosis was identified in 66 of 140 adolescents (47%) with
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chronic pelvic pain. Wolfman and Kreutner5 described 48 adolescents with chronic pelvic pain and found a 19% prevalence of endometriosis; this study was conducted from 1972 to 1982, before atypical lesions 1 o一15 were widely recognized. It is likely that the study of Wolfman and Kreutner underestimated the prevalence of endometriosis because of the under-recognition of atypical lesions. Data from our center collected from 1974-1983 reported the prevalence of endometriosis in 282 adolescent girls with chronic pelvic pain to be 45%.8 A category of "serositis" was included in the diagnosis of these patients , and was reported at approximately 5%. This condition of "serositis" may represent the now recognized "clear" or "vesicular" lesions of "atypical" endometriosis. Studies by Martin et al. 11 and Stripling et al. 12 have documented an increase in laparoscopic diagnosis of endometriosis when atypical lesions are included with histological confirmation , and Mm1in et al. suggest that failure to recognize such lesions may have resulted in a missed diagnosis in 7% of patients with endometriosis and an underestimation of the extent of disease in at least 50% of cases. In a study conducted between 1983 and 1987, of 47 adolescents with chronic pelvic pain , Vercellini et al. 7 found a 38.8% prevalence of endometriosis; however, the investigators acknowledge that their classification of endometriosis expanded to include atypical lesions halfway through the study. After this change in protocol , the prevalence of endometriosis was 52%. "Atypical" or subtle lesions of endometriosis are the most common in adolescents. 10,15 Our study' s findings of an increased prevalence rate of 69.9% as compared with other studies could possibly be explained by a vigorous preoperative screening , the use of OCPs and NSAIDs to help exclude patients whose pelvic pain is caused by primary dysmenorrhea , and/or the recent advances in diagnostic operative laparoscopic techniques for the recognition of endometriosis that has an atypically gross appearance. A recent study from Emory University-affiliated hospitals revealed a 73% incidence of endometriosis in adolescents not responding to medical therapy. 19 There may be a natural progression of endometriosis , which evolves from atypicallesions in adolescents to the “ classic" lesions of adult women. Martin et al. 11 report a p
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Conclusion We found a 69.6% prevalence of endometriosis in adolescent girls with chronic pelvic pain that did not respond to conventional medical therapy. Our study supports the need for laparoscopy to determine the etiology of the chronic pain. Familiarity with atypical endometriotic lesions enables gynecologists to accurately diagnose , stage , and surgically treat the disease at the time of visualization. We found a high prevalence of acyclic pelvic pain in adolescents found to have endometriosis. Our study also demonstrates an earlier stage of endometriosis at the time of diagnosis as compared with an adult population that may support a theory of disease progression. Additional studies should further clarify the presenting symptoms in the adolescent population with endometriosis and allow the selection of a patient population that may maximally benefit from a surgical intervention. A more complete understanding of the prevalence and presentation of endometriosis will enable clinicians to improve care and treatment for young women with chronic pelvic pain.
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