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E.B. Janssen, A.C.M. Rijkers, K. Hoppenbrouwers, C. Meuleman, T.M. D'Hooghe, Prevalence of endometriosis diagnosed by laparoscopy in adolescents with dysmenorrhea or chronic pelvic pain: a systematic review, Human Reproduction Update, Volume 19, Issue 5, September/October 2013, Pages 570–582, https://doi.org/10.1093/humupd/dmt016
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Abstract
Endometriosis associated with pain symptoms in adolescents has been extensively reported, but the exact prevalence is unclear because pain symptoms may be atypical and endometriosis can only be diagnosed by laparoscopy. The aim of this paper is to provide a systematic review of the prevalence of endometriosis diagnosed by laparoscopy in adolescents.
A systematic literature search was carried out for relevant articles published between 1980 and 2011 in the databases PUBMED and EMBASE, based on the keywords ‘endometriosis’, ‘laparoscopy’, ‘adolescents’ and ‘chronic pelvic pain (CPP)’. In addition, the reference lists of the selected articles were examined.
Based on 15 selected studies, the overall prevalence of visually confirmed endometriosis was 62% (543/880; range 25–100%) in all adolescent girls undergoing laparoscopic investigation, 75% (237/314) in girls with CPP resistant to treatment, 70% (102/146) in girls with dysmenorrhea and 49% (204/420) in girls with CPP that is not necessarily resistant to treatment. Among the adolescent girls with endometriosis, the overall prevalence of American Society of Reproductive Medicine classified moderate–severe endometriosis was 32% (82/259) in all girls, 16% (17/108) in girls with CPP resistant to treatment, 29% (21/74) in girls with dysmenorrhea and 57% (44/77) in girls with CPP that is not necessarily resistant to treatment. Due to the quality of the included papers an overestimation of the prevalence and/or severity of endometriosis is possible.
About two-thirds of adolescent girls with CPP or dysmenorrhea have laparoscopic evidence of endometriosis. About one-third of these adolescents with endometriosis have moderate–severe disease. The value of early detection of endometriosis in symptomatic adolescents and the indications for laparoscopic investigation in adolescents require more research.
Introduction
Endometriosis is a gynecological disorder defined by the presence of endometrial glands and stroma outside the uterus, associated with pelvic pain (dysmenorrhea, non-menstrual pain and dyspareunia) and subfertility. Endometriosis can be chronic and progressive in a subset of patients (Reese et al., 1996; Doyle et al., 2009) but until now it has been unclear which patients are more likely to have a progressive disease. The prevalence of endometriosis is ∼10–15% among women of reproductive age (Vigano et al., 2004; Crosignani et al., 2006; Mao and Anastasi, 2010) and up to 35–50% among women with pelvic pain and/or infertility (Treloar et al., 2010). The exact cause of endometriosis remains unknown, although many theories have been developed regarding the pathophysiology. No single theory can explain the variety of clinical presentations of endometriosis and most likely the etiology is multi-factorial. However, the most widely accepted theory is Sampson's hypothesis that during menstruation endometrial cells regurgitate through the fallopian tubes and implant on the surrounding pelvic viscera (Sampson, 1927). Other hypotheses suggest a multi-factorial etiology with immunological, anatomical and genetic mechanisms leading to dysfunction in the ectopic endometrium and/or immune system. These theories could explain why only a minority of women develop endometriosis despite retrograde menstruation occurring in almost all women (Fraser, 2008). Taking into account this multi-factorial etiology, various individual features (family history of endometriosis, early menarche and exposure to circulating steroid hormones, body mass index during late childhood and early adolescence), lifestyle characteristics and environmental factors are likely related to the development of endometriosis. A positive family history might be associated with endometriosis but it is unclear whether this association can be explained by genetic mechanisms, environmental elements or just an overall heightened awareness (Shah and Missmer, 2011). An early menarche is also positively associated with endometriosis (Treloar et al., 2010), possibly because of an association between early menarche and overweight (Kaplowitz et al., 2001; Nagle et al., 2009; Vitonis et al., 2010) and late childhood/early adolescence body size (Nagle et al., 2009). The reported positive association between endometriosis and body size in late childhood and early adolescence is possibly due to a higher level of circulating steroid hormones in an adolescent with a higher body mass index (Nagle et al., 2009). However, an inverse relation between childhood and early adolescence body size and the incidence of laparoscopically confirmed endometriosis has also been reported and may be explained by anovulation due to insulin resistance and hyperinsulinemia in obese pre-adolescent girls (Vitonis et al., 2010). Clearly, despite numerous studies, considerable questions remain regarding the pathogenesis and epidemiology of endometriosis.
Endometriosis can only be diagnosed by visual inspection during laparoscopy, ideally confirmed by histology and can present as peritoneal disease with typical or subtle lesions, ovarian endometriotic cysts (endometriomas) or deeply infiltrative disease (DIE) or as a combination of these features. The degree of endometriosis can be staged by laparoscopy as minimal, mild, moderate or severe according to the classification of the American Society of Reproductive Medicine [ASRM—former American Fertility Society (AFS), (Revised American Society for Reprocutive Medicine, 1997)]. Alternative or historical classification systems include the Endoscopic Endometriosis Classification I–IV by Semm (EEC I–IV, Semm, 1984), the Acosta classification (Acosta et al., 1973) or the staging system proposed by Kistner et al. (1977) with a scale of I–IV.
Endometriosis does not only affect adult women but also adolescent girls. Symptoms in adolescents may present as cyclic or acyclic pain, severe dysmenorrhea leading to missed school, dysmenorrhea not or poorly responding to medical therapy [non-steroidal anti-inflammatory drugs (NSAID) and/or oral contraceptive pills (OCPs)]; prolonged menstrual bleeding with premenstrual spotting, bowel and bladder problems depending on the location of the implants, dyspareunia (Goldstein et al., 1980; Reese et al., 1996; Laufer et al., 1997) and an early age of onset of dysmenorrhea (Treloar et al., 2010). The main manifestation of endometriosis among teenagers is chronic pelvic pain (CPP) (Vercellini et al., 1989; Kontoravdis et al., 1999; Attaran et al., 2002; Bourdel et al., 2006) and/or dysmenorrhea (Laufer et al., 1997; Propst and Laufer, 1999; Bourdel et al., 2006). The pattern of pelvic pain in adolescents with endometriosis may differ from that in adults. Most commonly in adults the pain precedes the onset of the menses and increases during menstruation. Adolescents indicate the pain is cyclic and/or acyclic (not menstruation-related) as seen in an earlier study (Laufer et al., 1997) in which 9.4% of adolescents had the typical cyclic pain with menses, whereas 62.5% had both acyclic and cyclic pain and 28.1% had acyclic pain. This pelvic pain can occur unpredictably and intermittently or continuously throughout the menstrual cycle. The pain can be either dull, throbbing or sharp, with possible exacerbation by physical activity (Broach et al., 2009; Giudice, 2010).
Because endometriosis can only be diagnosed at laparoscopy, the true prevalence of endometriosis among adolescents remains unknown (American College of Obstetricians and Gynecologists, 2005; Kalu et al., 2008; Pandis et al., 2009; Dovey and Sanfilippo, 2010; Gylfason et al., 2010).
Furthermore, there has been limited research on endometriosis in adolescents. Previous reviews have mainly focused on: (i) the management and approach of CPP due to endometriosis (Attaran et al., 2002; Greco, 2003; Solnik, 2006), (ii) the treatment recommendations (Sanfilippo, 1997; Laufer et al., 2003; Dovey and Sanfilippo, 2010), (iii) the approaches to diagnosis and management of endometriosis (Sanfilippo, 1997; Black and Jamieson, 2002; Laufer et al., 2003; Laufer, 2008), (iv) adenomyosis (Dietrich, 2010), (v) endometriosis in girls from thelarche to their sixteenth birthday (Batt and Mitwally, 2003) and (vi) the incidence and diagnosis of endometriosis in adolescents (Propst and Laufer, 1999). However, to the best of our knowledge, there has not been an effort to systematically assess the prevalence of endometriosis in adolescents. Therefore, the overall aim of this paper is to present a systematic review of the prevalence of laparoscopically confirmed endometriosis in adolescents based on studies reporting originally collected data only.
Materials and Methods
Search strategy
The literature review was conducted in two steps. First, an extensive search of the electronic databases including PUBMED and EMBASE at the Biomedical Libraries of the University Hospital of Leuven was performed for research articles published between January 1980 and December 2011. The following Medical Subject Heading (Agarwal and Fong, 2008) terms were used in different combinations: ‘endometriosis’, ‘adolescent’, ‘laparoscopy’ and ‘chronic pelvic pain’. We decided to use the keyword ‘adolescent’ because of the vague age limits for the term ‘youth’. The term ‘children’ combined with endometriosis-related topics resulted in a strong contamination of articles related to adult endometriosis and subfertility.
Additionally, a search with the terms ‘endometriosis’, ‘Afro-American’ and ‘Asian’ was done to look more specifically to other cultures than Caucasian.
Inclusion and exclusion of publications
The search was limited to articles in the English language that were published in full text and that addressed the research question at hand as the primary outcome variable (i.e. the prevalence of endometriosis diagnosed by laparoscopy in adolescents). Articles were only considered to be relevant if they reported original research. Therefore, manuscripts that did not contain empirical quantitative results, such as letters to the editor, brief reports, case studies, qualitative designs, opinions of experts, etc., were excluded. The reference lists of all selected articles were reviewed to identify additional relevant papers.
Outcome measures
The primary outcome measure was the prevalence of laparoscopically confirmed endometriosis in adolescent girls. The classification of endometriosis was a secondary outcome measure (Table I).
Main symptoms leading to laparoscopy . | Authors (year) . | Definition for pain . | n . | n patients with visually confirmed endometriosis/n (%) . | n with biopsied endometriosis/n with visually confirmed endometriosis (%) . | n with histologically proven endometriosis/n with biopsied endometriosis (%) . | Classification [n patients/total n patients with endo (%)] . | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
rAFS (%) . | Acosta (%) . | ||||||||||||
I . | II . | III . | IV . | Mild . | Moderate . | Severe . | |||||||
CPP | |||||||||||||
Goldstein et al. (1980) | ‘The criterion for admission was three separate visits to ER/clinic/consultation because of pain’ | 140 | 66/140 (47%) | 66/66 (100%) | 66/66 (100%) | aStaging system with Kistner | |||||||
Emmert et al. (1998) | NR | 105 | 37/105 (35%) | 14/37 (38%) | 6/14 (43%) | bEndoscopic endometriosis classification | |||||||
Kontoravdis et al. (1999) | ‘Lasts for over 6 months' | 98 | 24/98 (25%) | NR | NR | NR | |||||||
Bai et al. (2002) | NR | 39 | 39/39 (100%) | 39/39 (100%) | 39/39 (100%) | 4/39 (10%) | 17/39 (44%) | 11/39 (28%) | 7/39 (18%) | ||||
Vicino et al. (2010) | ‘Defined as the presence of non-cyclic pelvic pain for ≥6 months’ | 38 | 38/38 (100%) | 30/38 (79%) | 30/30 (100%) | 7/38 (18.4%) | 5/38 (13.2%) | 13/38 (34.2%) | 13/38 (34.2%) | ||||
Subtotal | 420 | 204/420 (49%) | 149/180 (83%)c | 141/149 (95%) | 11/77 (14%) | 22/77 (29%) | 24/77 (31%) | 20/77 (26%) | |||||
CPP unresponsive to medical therapy | |||||||||||||
Reese et al. (1996) | NR | 67 | 49/67 (73%) | 3/67 (5%) | 3/3 (100%) | 39/49 (80%) | 6/49 (12%) | 3/49 (6%) | 1/49 (2%) | ||||
Laufer et al. (1997) | ‘CPP of longer than 3 months in duration’ | 46 | 31/46d (67) | NR | NR (‘5 patients with grossly normal pelvis had at least 2 random biopsy specimens taken and 1 patient had pathologically proven endometriosis’) | 24/31 (77%)d | 7/31 (23%)d | 0/31 (0%)d | 0/31 (0%)d | ||||
Stavroulis et al. (2006) | NR | 31 | 11/31 (36%) | 10/11 (91%) | 8/10 (80%) | 5/11 (45.5%)e | 6/11 (54.5%) | ||||||
Ventolini et al. (2005) | NR | 52 | 28/52 (54%) | 28/28 (100%) | 28/28 (100%) | 4/28 (14%) | 11/28 (39%) | 12/28 (43%) | 1/28 (4%) | ||||
Kalu et al. (2008) | NR | 28 | 28/28 (100%) | NR | NR | NR | |||||||
Doyle et al. (2009) | NR | 90 | 90/90 (100%) | Not performed | 67/90 (74%) rASRM | NR | NR | NR | |||||
Subtotal | 314 | 237/314 (75%) | 41/106 (39%) | 39/41 (95%) | 134/198 (68%) | 24/108 (22%) | 15/108 (14%) | 2/108 (2%) | 5/11 (45.5%)e | 6/11 (54.5%) | |||
Dysmenorrheal | |||||||||||||
Chatman and Ward (1982) | NR | 43 | 28/43 (65%) | 18/28 (64%) | 13/18 (72%) | 14/28 (50%) | 11/28 (39%) | 3/28 (11%) | |||||
Vercellini et al. (1989) | ‘CPP is defined as constant or intermittent cyclic or acyclic pain that persists for six months or more and includes dysmenorrhea, deep dyspareunia and intermenstrual pain’ | 47 | 18/47 (38%) | 11/18 (61%) | 8/11 (72%) | 12/18 (67%) | 6/18 (33%) | 0/18 (0%) | 0/18 (0%) | ||||
Davis et al. (1993) | ‘Dysmenorrhea was defined as severe cramping uterine with concomitant abdominal pain’ | 36f | 36/36 (100%) | NR | NR | 10/36 (28%) | 8/36 (22%) | 7/36 (19%) | 11/36 (31%) | 13/36 (36%) | 7/36 (19%) | 16/36 (44%) | |
Roman (2010) | NR | 20 | 20/20 (100%) | 20/20 (100%) | 20/20 (100%) | 8/20 (40%) | 9/20 (45%) | 1/20 (5%) | 2/20 (10%) | ||||
Subtotal | 146 | 102/146 (70%) | 49/64(77%) | 41/49 (84%) | 30/74 (41%) | 23/74 (31%) | 8/74 (11%) | 13/74 (18%) | 27/64 (42%) | 18/64 (28%) | 19/64 (30%) | ||
Total of main Symptoms | 880 | 543/880 (62%) | 239/392 (61%) | 221/239 (93%) | 175/349 (50%) | 69/259 (27%) | 47/259 (18%) | 35/259 (14%) | 50/75 (67%) | 25/75 (33%) |
Main symptoms leading to laparoscopy . | Authors (year) . | Definition for pain . | n . | n patients with visually confirmed endometriosis/n (%) . | n with biopsied endometriosis/n with visually confirmed endometriosis (%) . | n with histologically proven endometriosis/n with biopsied endometriosis (%) . | Classification [n patients/total n patients with endo (%)] . | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
rAFS (%) . | Acosta (%) . | ||||||||||||
I . | II . | III . | IV . | Mild . | Moderate . | Severe . | |||||||
CPP | |||||||||||||
Goldstein et al. (1980) | ‘The criterion for admission was three separate visits to ER/clinic/consultation because of pain’ | 140 | 66/140 (47%) | 66/66 (100%) | 66/66 (100%) | aStaging system with Kistner | |||||||
Emmert et al. (1998) | NR | 105 | 37/105 (35%) | 14/37 (38%) | 6/14 (43%) | bEndoscopic endometriosis classification | |||||||
Kontoravdis et al. (1999) | ‘Lasts for over 6 months' | 98 | 24/98 (25%) | NR | NR | NR | |||||||
Bai et al. (2002) | NR | 39 | 39/39 (100%) | 39/39 (100%) | 39/39 (100%) | 4/39 (10%) | 17/39 (44%) | 11/39 (28%) | 7/39 (18%) | ||||
Vicino et al. (2010) | ‘Defined as the presence of non-cyclic pelvic pain for ≥6 months’ | 38 | 38/38 (100%) | 30/38 (79%) | 30/30 (100%) | 7/38 (18.4%) | 5/38 (13.2%) | 13/38 (34.2%) | 13/38 (34.2%) | ||||
Subtotal | 420 | 204/420 (49%) | 149/180 (83%)c | 141/149 (95%) | 11/77 (14%) | 22/77 (29%) | 24/77 (31%) | 20/77 (26%) | |||||
CPP unresponsive to medical therapy | |||||||||||||
Reese et al. (1996) | NR | 67 | 49/67 (73%) | 3/67 (5%) | 3/3 (100%) | 39/49 (80%) | 6/49 (12%) | 3/49 (6%) | 1/49 (2%) | ||||
Laufer et al. (1997) | ‘CPP of longer than 3 months in duration’ | 46 | 31/46d (67) | NR | NR (‘5 patients with grossly normal pelvis had at least 2 random biopsy specimens taken and 1 patient had pathologically proven endometriosis’) | 24/31 (77%)d | 7/31 (23%)d | 0/31 (0%)d | 0/31 (0%)d | ||||
Stavroulis et al. (2006) | NR | 31 | 11/31 (36%) | 10/11 (91%) | 8/10 (80%) | 5/11 (45.5%)e | 6/11 (54.5%) | ||||||
Ventolini et al. (2005) | NR | 52 | 28/52 (54%) | 28/28 (100%) | 28/28 (100%) | 4/28 (14%) | 11/28 (39%) | 12/28 (43%) | 1/28 (4%) | ||||
Kalu et al. (2008) | NR | 28 | 28/28 (100%) | NR | NR | NR | |||||||
Doyle et al. (2009) | NR | 90 | 90/90 (100%) | Not performed | 67/90 (74%) rASRM | NR | NR | NR | |||||
Subtotal | 314 | 237/314 (75%) | 41/106 (39%) | 39/41 (95%) | 134/198 (68%) | 24/108 (22%) | 15/108 (14%) | 2/108 (2%) | 5/11 (45.5%)e | 6/11 (54.5%) | |||
Dysmenorrheal | |||||||||||||
Chatman and Ward (1982) | NR | 43 | 28/43 (65%) | 18/28 (64%) | 13/18 (72%) | 14/28 (50%) | 11/28 (39%) | 3/28 (11%) | |||||
Vercellini et al. (1989) | ‘CPP is defined as constant or intermittent cyclic or acyclic pain that persists for six months or more and includes dysmenorrhea, deep dyspareunia and intermenstrual pain’ | 47 | 18/47 (38%) | 11/18 (61%) | 8/11 (72%) | 12/18 (67%) | 6/18 (33%) | 0/18 (0%) | 0/18 (0%) | ||||
Davis et al. (1993) | ‘Dysmenorrhea was defined as severe cramping uterine with concomitant abdominal pain’ | 36f | 36/36 (100%) | NR | NR | 10/36 (28%) | 8/36 (22%) | 7/36 (19%) | 11/36 (31%) | 13/36 (36%) | 7/36 (19%) | 16/36 (44%) | |
Roman (2010) | NR | 20 | 20/20 (100%) | 20/20 (100%) | 20/20 (100%) | 8/20 (40%) | 9/20 (45%) | 1/20 (5%) | 2/20 (10%) | ||||
Subtotal | 146 | 102/146 (70%) | 49/64(77%) | 41/49 (84%) | 30/74 (41%) | 23/74 (31%) | 8/74 (11%) | 13/74 (18%) | 27/64 (42%) | 18/64 (28%) | 19/64 (30%) | ||
Total of main Symptoms | 880 | 543/880 (62%) | 239/392 (61%) | 221/239 (93%) | 175/349 (50%) | 69/259 (27%) | 47/259 (18%) | 35/259 (14%) | 50/75 (67%) | 25/75 (33%) |
NR, not reported; CPP, chronic pelvic pain; PP, pelvic pain; APP, acute pelvic pain; OCP, oral contraceptive pills; NSAID, non-steroidal anti-inflammatory drugs; rAFS, revised American Fertility Society.
aThe Kistner classification system (Kistner et al., 1977): stage I (58% 38/66); stage II (38% 25/66); stage III (0% 0/66) and stage IV (4% 3/66) (Goldstein et al., 1980).
bEndometriosis Classification I–IV by Semm (EEC): stage I (92%, 34/37), stage II (8%, 3/37) and stage III–IV (0%, 0/37) (Emmert et al., 1998).
cThe denominator is 180 instead of 204 because we did not take into account 24 patients of Kontoravdis et al. (1999) due to the lack of information on histology.
dOf the 46 adolescents included 31 were determined to have grossly visible endometriosis and these cases were classified by rAFS; in 5 subjects with a visual normal pelvis, 1 patient was found to have pathologically proven endometriosis, but this case was not taken into account in the classification.
eMeasures: mild-and-moderate endometriosis were counted together.
fThirty-six patients were selected from 49 consecutive adolescents who underwent laparoscopic treatment of pelvic endometriosis.
Main symptoms leading to laparoscopy . | Authors (year) . | Definition for pain . | n . | n patients with visually confirmed endometriosis/n (%) . | n with biopsied endometriosis/n with visually confirmed endometriosis (%) . | n with histologically proven endometriosis/n with biopsied endometriosis (%) . | Classification [n patients/total n patients with endo (%)] . | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
rAFS (%) . | Acosta (%) . | ||||||||||||
I . | II . | III . | IV . | Mild . | Moderate . | Severe . | |||||||
CPP | |||||||||||||
Goldstein et al. (1980) | ‘The criterion for admission was three separate visits to ER/clinic/consultation because of pain’ | 140 | 66/140 (47%) | 66/66 (100%) | 66/66 (100%) | aStaging system with Kistner | |||||||
Emmert et al. (1998) | NR | 105 | 37/105 (35%) | 14/37 (38%) | 6/14 (43%) | bEndoscopic endometriosis classification | |||||||
Kontoravdis et al. (1999) | ‘Lasts for over 6 months' | 98 | 24/98 (25%) | NR | NR | NR | |||||||
Bai et al. (2002) | NR | 39 | 39/39 (100%) | 39/39 (100%) | 39/39 (100%) | 4/39 (10%) | 17/39 (44%) | 11/39 (28%) | 7/39 (18%) | ||||
Vicino et al. (2010) | ‘Defined as the presence of non-cyclic pelvic pain for ≥6 months’ | 38 | 38/38 (100%) | 30/38 (79%) | 30/30 (100%) | 7/38 (18.4%) | 5/38 (13.2%) | 13/38 (34.2%) | 13/38 (34.2%) | ||||
Subtotal | 420 | 204/420 (49%) | 149/180 (83%)c | 141/149 (95%) | 11/77 (14%) | 22/77 (29%) | 24/77 (31%) | 20/77 (26%) | |||||
CPP unresponsive to medical therapy | |||||||||||||
Reese et al. (1996) | NR | 67 | 49/67 (73%) | 3/67 (5%) | 3/3 (100%) | 39/49 (80%) | 6/49 (12%) | 3/49 (6%) | 1/49 (2%) | ||||
Laufer et al. (1997) | ‘CPP of longer than 3 months in duration’ | 46 | 31/46d (67) | NR | NR (‘5 patients with grossly normal pelvis had at least 2 random biopsy specimens taken and 1 patient had pathologically proven endometriosis’) | 24/31 (77%)d | 7/31 (23%)d | 0/31 (0%)d | 0/31 (0%)d | ||||
Stavroulis et al. (2006) | NR | 31 | 11/31 (36%) | 10/11 (91%) | 8/10 (80%) | 5/11 (45.5%)e | 6/11 (54.5%) | ||||||
Ventolini et al. (2005) | NR | 52 | 28/52 (54%) | 28/28 (100%) | 28/28 (100%) | 4/28 (14%) | 11/28 (39%) | 12/28 (43%) | 1/28 (4%) | ||||
Kalu et al. (2008) | NR | 28 | 28/28 (100%) | NR | NR | NR | |||||||
Doyle et al. (2009) | NR | 90 | 90/90 (100%) | Not performed | 67/90 (74%) rASRM | NR | NR | NR | |||||
Subtotal | 314 | 237/314 (75%) | 41/106 (39%) | 39/41 (95%) | 134/198 (68%) | 24/108 (22%) | 15/108 (14%) | 2/108 (2%) | 5/11 (45.5%)e | 6/11 (54.5%) | |||
Dysmenorrheal | |||||||||||||
Chatman and Ward (1982) | NR | 43 | 28/43 (65%) | 18/28 (64%) | 13/18 (72%) | 14/28 (50%) | 11/28 (39%) | 3/28 (11%) | |||||
Vercellini et al. (1989) | ‘CPP is defined as constant or intermittent cyclic or acyclic pain that persists for six months or more and includes dysmenorrhea, deep dyspareunia and intermenstrual pain’ | 47 | 18/47 (38%) | 11/18 (61%) | 8/11 (72%) | 12/18 (67%) | 6/18 (33%) | 0/18 (0%) | 0/18 (0%) | ||||
Davis et al. (1993) | ‘Dysmenorrhea was defined as severe cramping uterine with concomitant abdominal pain’ | 36f | 36/36 (100%) | NR | NR | 10/36 (28%) | 8/36 (22%) | 7/36 (19%) | 11/36 (31%) | 13/36 (36%) | 7/36 (19%) | 16/36 (44%) | |
Roman (2010) | NR | 20 | 20/20 (100%) | 20/20 (100%) | 20/20 (100%) | 8/20 (40%) | 9/20 (45%) | 1/20 (5%) | 2/20 (10%) | ||||
Subtotal | 146 | 102/146 (70%) | 49/64(77%) | 41/49 (84%) | 30/74 (41%) | 23/74 (31%) | 8/74 (11%) | 13/74 (18%) | 27/64 (42%) | 18/64 (28%) | 19/64 (30%) | ||
Total of main Symptoms | 880 | 543/880 (62%) | 239/392 (61%) | 221/239 (93%) | 175/349 (50%) | 69/259 (27%) | 47/259 (18%) | 35/259 (14%) | 50/75 (67%) | 25/75 (33%) |
Main symptoms leading to laparoscopy . | Authors (year) . | Definition for pain . | n . | n patients with visually confirmed endometriosis/n (%) . | n with biopsied endometriosis/n with visually confirmed endometriosis (%) . | n with histologically proven endometriosis/n with biopsied endometriosis (%) . | Classification [n patients/total n patients with endo (%)] . | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
rAFS (%) . | Acosta (%) . | ||||||||||||
I . | II . | III . | IV . | Mild . | Moderate . | Severe . | |||||||
CPP | |||||||||||||
Goldstein et al. (1980) | ‘The criterion for admission was three separate visits to ER/clinic/consultation because of pain’ | 140 | 66/140 (47%) | 66/66 (100%) | 66/66 (100%) | aStaging system with Kistner | |||||||
Emmert et al. (1998) | NR | 105 | 37/105 (35%) | 14/37 (38%) | 6/14 (43%) | bEndoscopic endometriosis classification | |||||||
Kontoravdis et al. (1999) | ‘Lasts for over 6 months' | 98 | 24/98 (25%) | NR | NR | NR | |||||||
Bai et al. (2002) | NR | 39 | 39/39 (100%) | 39/39 (100%) | 39/39 (100%) | 4/39 (10%) | 17/39 (44%) | 11/39 (28%) | 7/39 (18%) | ||||
Vicino et al. (2010) | ‘Defined as the presence of non-cyclic pelvic pain for ≥6 months’ | 38 | 38/38 (100%) | 30/38 (79%) | 30/30 (100%) | 7/38 (18.4%) | 5/38 (13.2%) | 13/38 (34.2%) | 13/38 (34.2%) | ||||
Subtotal | 420 | 204/420 (49%) | 149/180 (83%)c | 141/149 (95%) | 11/77 (14%) | 22/77 (29%) | 24/77 (31%) | 20/77 (26%) | |||||
CPP unresponsive to medical therapy | |||||||||||||
Reese et al. (1996) | NR | 67 | 49/67 (73%) | 3/67 (5%) | 3/3 (100%) | 39/49 (80%) | 6/49 (12%) | 3/49 (6%) | 1/49 (2%) | ||||
Laufer et al. (1997) | ‘CPP of longer than 3 months in duration’ | 46 | 31/46d (67) | NR | NR (‘5 patients with grossly normal pelvis had at least 2 random biopsy specimens taken and 1 patient had pathologically proven endometriosis’) | 24/31 (77%)d | 7/31 (23%)d | 0/31 (0%)d | 0/31 (0%)d | ||||
Stavroulis et al. (2006) | NR | 31 | 11/31 (36%) | 10/11 (91%) | 8/10 (80%) | 5/11 (45.5%)e | 6/11 (54.5%) | ||||||
Ventolini et al. (2005) | NR | 52 | 28/52 (54%) | 28/28 (100%) | 28/28 (100%) | 4/28 (14%) | 11/28 (39%) | 12/28 (43%) | 1/28 (4%) | ||||
Kalu et al. (2008) | NR | 28 | 28/28 (100%) | NR | NR | NR | |||||||
Doyle et al. (2009) | NR | 90 | 90/90 (100%) | Not performed | 67/90 (74%) rASRM | NR | NR | NR | |||||
Subtotal | 314 | 237/314 (75%) | 41/106 (39%) | 39/41 (95%) | 134/198 (68%) | 24/108 (22%) | 15/108 (14%) | 2/108 (2%) | 5/11 (45.5%)e | 6/11 (54.5%) | |||
Dysmenorrheal | |||||||||||||
Chatman and Ward (1982) | NR | 43 | 28/43 (65%) | 18/28 (64%) | 13/18 (72%) | 14/28 (50%) | 11/28 (39%) | 3/28 (11%) | |||||
Vercellini et al. (1989) | ‘CPP is defined as constant or intermittent cyclic or acyclic pain that persists for six months or more and includes dysmenorrhea, deep dyspareunia and intermenstrual pain’ | 47 | 18/47 (38%) | 11/18 (61%) | 8/11 (72%) | 12/18 (67%) | 6/18 (33%) | 0/18 (0%) | 0/18 (0%) | ||||
Davis et al. (1993) | ‘Dysmenorrhea was defined as severe cramping uterine with concomitant abdominal pain’ | 36f | 36/36 (100%) | NR | NR | 10/36 (28%) | 8/36 (22%) | 7/36 (19%) | 11/36 (31%) | 13/36 (36%) | 7/36 (19%) | 16/36 (44%) | |
Roman (2010) | NR | 20 | 20/20 (100%) | 20/20 (100%) | 20/20 (100%) | 8/20 (40%) | 9/20 (45%) | 1/20 (5%) | 2/20 (10%) | ||||
Subtotal | 146 | 102/146 (70%) | 49/64(77%) | 41/49 (84%) | 30/74 (41%) | 23/74 (31%) | 8/74 (11%) | 13/74 (18%) | 27/64 (42%) | 18/64 (28%) | 19/64 (30%) | ||
Total of main Symptoms | 880 | 543/880 (62%) | 239/392 (61%) | 221/239 (93%) | 175/349 (50%) | 69/259 (27%) | 47/259 (18%) | 35/259 (14%) | 50/75 (67%) | 25/75 (33%) |
NR, not reported; CPP, chronic pelvic pain; PP, pelvic pain; APP, acute pelvic pain; OCP, oral contraceptive pills; NSAID, non-steroidal anti-inflammatory drugs; rAFS, revised American Fertility Society.
aThe Kistner classification system (Kistner et al., 1977): stage I (58% 38/66); stage II (38% 25/66); stage III (0% 0/66) and stage IV (4% 3/66) (Goldstein et al., 1980).
bEndometriosis Classification I–IV by Semm (EEC): stage I (92%, 34/37), stage II (8%, 3/37) and stage III–IV (0%, 0/37) (Emmert et al., 1998).
cThe denominator is 180 instead of 204 because we did not take into account 24 patients of Kontoravdis et al. (1999) due to the lack of information on histology.
dOf the 46 adolescents included 31 were determined to have grossly visible endometriosis and these cases were classified by rAFS; in 5 subjects with a visual normal pelvis, 1 patient was found to have pathologically proven endometriosis, but this case was not taken into account in the classification.
eMeasures: mild-and-moderate endometriosis were counted together.
fThirty-six patients were selected from 49 consecutive adolescents who underwent laparoscopic treatment of pelvic endometriosis.
Critical appraisal
The studies (see the section Results) were subsequently assessed independently by the first authors (E.J. and A.R.) for methodological quality using the Critical Appraisal Skills Programme (CASP) for cohort studies (The NHS Public Health Resource Unit Critical Appraisal Skills Programme, Oxford, UK.). This CASP is a key instrument required to evaluate the quality of cohort studies to make evidence-based decisions. It is based on three major questions (divided into subquestions) to systematically consider the following issues (Table II): (i) are the results of the study valid and is the bias limited? (ii) what are the results? (iii) will the results help me locally? The appraisal questions were graded ‘+’ when the criterion was fulfilled, ‘+/−’ when the criterion was unclear and ‘−’ when the criterion was not fulfilled. CASP is meant to be used as a guide and not to replace personal judgment and considered thought. Both first authors (E.J. and A.R.) decided to define an article as valid if a ‘yes’ answer was present in at least four out of the six questions related to the validity.
(A) Are the results of the study valid? . | (B) What are the results? . | (C) Will the results help me locally? . | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
. | Did the study address a clearly focused issue? . | Did authors use a appropriate method to answer their question? . | Was/were the cohort /cases recruited in an acceptable way? . | Was the outcome accurately measured to minimize bias? . | Is the disease status of the tested population clearly described? . | Have they taken account of the confounding factors in the design and/or analysis? . | Are the results of this study clear? . | Were results precisely presented? . | Do you believe the results? . | Can the results be applied to the local population? . | Were all important outcomes considered (policy-makers, professional family)? . |
Goldstein et al. (1980) | + | + | + | + | + | + | + | + | + | + | + |
Chatman and Ward (1982) | + | + | + | + | + | + | + | − | + | − | + |
Vercellini et al. (1989) | + | + | + | + | + | + | + | −/+ | + | + | + |
Davis et al. (1993) | + | + | + | + | + | + | + | + | + | + | + |
Reese et al. (1996) | + | + | + | + | + | + | + | + | + | + | + |
Emmert et al. (1998) | + | + | + | + | + | − | + | − | −/+ | + | + |
Laufer et al. (1997) | + | + | + | + | + | + | + | −/+ | + | + | + |
Kontoravdis et al. (1999) | + | −/+ | + | −/+ | + | −/+ | −/+ | − | −/+ | + | + |
Bai et al. (2002) | + | + | + | −/+ | + | + | −/+ | −/+ | −/+ | − | + |
Stavroulis et al. (2006) | + | + | + | + | + | − | + | − | −/+ | + | + |
Ventolini et al. (2005) | + | + | + | + | + | + | + | − | + | + | + |
Kalu et al. (2008) | + | + | + | − | + | + | + | + | −/+ | −/+ | + |
Doyle et al. (2009) | + | + | + | −/+ | + | + | − | + | −/+ | + | + |
Roman (2010) | + | + | + | + | + | + | + | + | + | + | + |
Vicino et al. (2010) | + | + | + | + | + | + | + | + | + | + | −/+ |
(A) Are the results of the study valid? . | (B) What are the results? . | (C) Will the results help me locally? . | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
. | Did the study address a clearly focused issue? . | Did authors use a appropriate method to answer their question? . | Was/were the cohort /cases recruited in an acceptable way? . | Was the outcome accurately measured to minimize bias? . | Is the disease status of the tested population clearly described? . | Have they taken account of the confounding factors in the design and/or analysis? . | Are the results of this study clear? . | Were results precisely presented? . | Do you believe the results? . | Can the results be applied to the local population? . | Were all important outcomes considered (policy-makers, professional family)? . |
Goldstein et al. (1980) | + | + | + | + | + | + | + | + | + | + | + |
Chatman and Ward (1982) | + | + | + | + | + | + | + | − | + | − | + |
Vercellini et al. (1989) | + | + | + | + | + | + | + | −/+ | + | + | + |
Davis et al. (1993) | + | + | + | + | + | + | + | + | + | + | + |
Reese et al. (1996) | + | + | + | + | + | + | + | + | + | + | + |
Emmert et al. (1998) | + | + | + | + | + | − | + | − | −/+ | + | + |
Laufer et al. (1997) | + | + | + | + | + | + | + | −/+ | + | + | + |
Kontoravdis et al. (1999) | + | −/+ | + | −/+ | + | −/+ | −/+ | − | −/+ | + | + |
Bai et al. (2002) | + | + | + | −/+ | + | + | −/+ | −/+ | −/+ | − | + |
Stavroulis et al. (2006) | + | + | + | + | + | − | + | − | −/+ | + | + |
Ventolini et al. (2005) | + | + | + | + | + | + | + | − | + | + | + |
Kalu et al. (2008) | + | + | + | − | + | + | + | + | −/+ | −/+ | + |
Doyle et al. (2009) | + | + | + | −/+ | + | + | − | + | −/+ | + | + |
Roman (2010) | + | + | + | + | + | + | + | + | + | + | + |
Vicino et al. (2010) | + | + | + | + | + | + | + | + | + | + | −/+ |
+, Yes; −/+, cannot tell; −, No.
(A) Are the results of the study valid? . | (B) What are the results? . | (C) Will the results help me locally? . | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
. | Did the study address a clearly focused issue? . | Did authors use a appropriate method to answer their question? . | Was/were the cohort /cases recruited in an acceptable way? . | Was the outcome accurately measured to minimize bias? . | Is the disease status of the tested population clearly described? . | Have they taken account of the confounding factors in the design and/or analysis? . | Are the results of this study clear? . | Were results precisely presented? . | Do you believe the results? . | Can the results be applied to the local population? . | Were all important outcomes considered (policy-makers, professional family)? . |
Goldstein et al. (1980) | + | + | + | + | + | + | + | + | + | + | + |
Chatman and Ward (1982) | + | + | + | + | + | + | + | − | + | − | + |
Vercellini et al. (1989) | + | + | + | + | + | + | + | −/+ | + | + | + |
Davis et al. (1993) | + | + | + | + | + | + | + | + | + | + | + |
Reese et al. (1996) | + | + | + | + | + | + | + | + | + | + | + |
Emmert et al. (1998) | + | + | + | + | + | − | + | − | −/+ | + | + |
Laufer et al. (1997) | + | + | + | + | + | + | + | −/+ | + | + | + |
Kontoravdis et al. (1999) | + | −/+ | + | −/+ | + | −/+ | −/+ | − | −/+ | + | + |
Bai et al. (2002) | + | + | + | −/+ | + | + | −/+ | −/+ | −/+ | − | + |
Stavroulis et al. (2006) | + | + | + | + | + | − | + | − | −/+ | + | + |
Ventolini et al. (2005) | + | + | + | + | + | + | + | − | + | + | + |
Kalu et al. (2008) | + | + | + | − | + | + | + | + | −/+ | −/+ | + |
Doyle et al. (2009) | + | + | + | −/+ | + | + | − | + | −/+ | + | + |
Roman (2010) | + | + | + | + | + | + | + | + | + | + | + |
Vicino et al. (2010) | + | + | + | + | + | + | + | + | + | + | −/+ |
(A) Are the results of the study valid? . | (B) What are the results? . | (C) Will the results help me locally? . | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
. | Did the study address a clearly focused issue? . | Did authors use a appropriate method to answer their question? . | Was/were the cohort /cases recruited in an acceptable way? . | Was the outcome accurately measured to minimize bias? . | Is the disease status of the tested population clearly described? . | Have they taken account of the confounding factors in the design and/or analysis? . | Are the results of this study clear? . | Were results precisely presented? . | Do you believe the results? . | Can the results be applied to the local population? . | Were all important outcomes considered (policy-makers, professional family)? . |
Goldstein et al. (1980) | + | + | + | + | + | + | + | + | + | + | + |
Chatman and Ward (1982) | + | + | + | + | + | + | + | − | + | − | + |
Vercellini et al. (1989) | + | + | + | + | + | + | + | −/+ | + | + | + |
Davis et al. (1993) | + | + | + | + | + | + | + | + | + | + | + |
Reese et al. (1996) | + | + | + | + | + | + | + | + | + | + | + |
Emmert et al. (1998) | + | + | + | + | + | − | + | − | −/+ | + | + |
Laufer et al. (1997) | + | + | + | + | + | + | + | −/+ | + | + | + |
Kontoravdis et al. (1999) | + | −/+ | + | −/+ | + | −/+ | −/+ | − | −/+ | + | + |
Bai et al. (2002) | + | + | + | −/+ | + | + | −/+ | −/+ | −/+ | − | + |
Stavroulis et al. (2006) | + | + | + | + | + | − | + | − | −/+ | + | + |
Ventolini et al. (2005) | + | + | + | + | + | + | + | − | + | + | + |
Kalu et al. (2008) | + | + | + | − | + | + | + | + | −/+ | −/+ | + |
Doyle et al. (2009) | + | + | + | −/+ | + | + | − | + | −/+ | + | + |
Roman (2010) | + | + | + | + | + | + | + | + | + | + | + |
Vicino et al. (2010) | + | + | + | + | + | + | + | + | + | + | −/+ |
+, Yes; −/+, cannot tell; −, No.
Results
Characteristics of studies
The process of literature identification and selection is shown in Fig. 1. A PUBMED and EMBASE search with the above-mentioned MESH terms provided 1014 hits. Based on title and abstract content, 98 papers were kept for further analysis. After reading the articles, 83 more articles were excluded for the following reasons: no inclusion of specific data on adolescents (n = 18), review or no primary study (n = 27), case report (n = 8), case series (n = 2), descriptive study and/or opinion paper without a laparoscopic intervention (n = 8), containing information not relevant to the research question (n = 14) or not published as a full text paper (n = 5) or published as a brief report (n = 1). Finally, 15 articles were included in this review (Fig. 1, Table III). No additional papers were identified after checking the reference lists of these selected papers.
Author (year) . | Range of ages (mean age) in years . | Menarche (mean age in years) . | Sample (n) . | Study objective . | Period of study . | Design . | Care setting . | Outcome measure . |
---|---|---|---|---|---|---|---|---|
Goldstein et al. (1980) | 10–19.25 | 11.8 | n = 140 | To describe the experience in adolescents who have endometriosis | 1974 1979 | Prospective | Boston Children's Hospital Medical Center | Symptoms Surgical findings |
Chatman and Ward (1982) | 12–19 | NR | n = 43 | To outline the magnitude of the problem of endometriosis | NR | Prospective | Department of Obstetrics and Gynecology, University of Chicago | Stage, SymptomsSurgical findings |
Vercellini et al. (1989) | 11–19 (18.7) | NR | n = 47 | To determine the value of laparoscopy in the differential diagnosis of CPP | 1983 1987 | Retrospective | First Department Obstetrics and Gynecology, University, Milan | Stage, Lesion type Surgical findings |
Davis et al. (1993) | 13–20 (16.6) | NR | n = 36a | To describe the appearance, stage and treatment of endometriosis in adolescents | NR | Retrospective | Phoenix integrated residency program in obstetrics and gynecology, Arizona | Lesion type Stage infiltration |
Reese et al. (1996) | 11–19 | 12.5 | n = 67 | To determine the incidence, clinical stage and lesion type of endometriosis in adolescents | 1992 1994 | Retrospective | Emory University Affiliated Hospital Atlanta, Georgia | Lesion type, stage, symptoms |
Emmert et al. (1998) | 11–19 (17.3) | 12.2 | n = 105 | To determine the incidence, type, clinical stage of endometriotic lesions | 1996 1997 | Retrospective | Carl Thiem-Clinic and Gynecological Endoscopy Training Center, Cottbus, Germany | Age, incidence Lesion type Stage, symptoms |
Laufer et al. (1997) | 13–21 (16.1) | 12.3 | n = 46 | To evaluate adolescent girls with CPP not responding to medical therapy | 1990 1994 | Descriptive retrospective | Children's Hospital and the Brigham and Women's Hospital in Boston | Stage Lesion type |
Kontoravdis et al. (1999) | 16–19 | NR | n = 98 | To evaluate the role of laparoscopy in the diagnosis and treatment of CPP in adolescents | 1993 1997 | Prospective | University of Athens, Areteion Hospital, Athens | Role of laparoscopy |
Bai et al. (2002) | 14–21 (20.1) | 14.2 | n = 39 | To evaluate the age distribution, diagnosis, clinical stage, treatment of endometriosis in adolescents | 1990 1999 | Retrospective | Severance Hospital, Yonsei University Medical College, Korea | Age, stage, symptoms |
Stavroulis et al. (2006) | 13–20 (16.5) | NR | n = 31 | To determine the frequency and severity of endometriosis in adolescents with CCP unresponsive to medical treatment | 2001 2003 | Retrospective | Elizabeth Garrett Anderson and Obstetric Hospital, London | Stage surgical |
Ventolini et al. (2005) | 12–18 | NR | n = 52 | To compare mild-and-severe forms of endometriosis and to follow up their fecundability on long term | 1993 1995 | Prospective | Department of Obstetrics and Gynecology, University, Wright University, Ohio | Future fecundability Stage |
Kalu et al. (2008) | 15–21 | NR | n = 28 | To describe the clinical features and treatment outcome following the laparoscopic treatment of endometriosis | 2000 2005 | Retrospective | The Chelsea and Westminster Hospital, London | Symptom Recurrence |
Doyle et al. (2009) | 12–24 | NR | n = 90 | To evaluate the effect of combined surgical–medical treatment on endometriosis progression in adolescents | 1995 2007 | Retrospective | Two academic medical centers, Boston | Stage changing Adhesions |
Roman (2010) | (17.4) | NR | n = 20 | To describe the experience with laparoscopic excision in adolescents and to compare with a non-adolescent population | 2003 2009 | Comparative cohort | Braemar Hospital, Hamilton, New Zealand | Surgical findings Stage |
Vicino et al. (2010) | 10–21 | NR | n = 38 | To analyse the clinical manifestations of endometriosis in adolescents | 2005 2006 | Prospective | University and General Hospitals, Milan, Italy | Stage, age |
Total | 10–24 | 11.8–14.2 | n = 880 | Experience, magnitude, severity, clinical manifestations, incidence, stage, role of laparoscopy, age, lesion type among adolescents with endometriosis | 1974 2009 | Prospective (n = 5) Retrospective (n = 9) Comparative (n = 1) | Symptom (n = 6); stage (n = 12); surgical findings (n = 4); lesion type (n = 5); age (n = 3); adhesions (n = 1); recurrence (n = 1); future fecundability n = 1; role of laparoscopy (n = 1); incidence (n = 1) |
Author (year) . | Range of ages (mean age) in years . | Menarche (mean age in years) . | Sample (n) . | Study objective . | Period of study . | Design . | Care setting . | Outcome measure . |
---|---|---|---|---|---|---|---|---|
Goldstein et al. (1980) | 10–19.25 | 11.8 | n = 140 | To describe the experience in adolescents who have endometriosis | 1974 1979 | Prospective | Boston Children's Hospital Medical Center | Symptoms Surgical findings |
Chatman and Ward (1982) | 12–19 | NR | n = 43 | To outline the magnitude of the problem of endometriosis | NR | Prospective | Department of Obstetrics and Gynecology, University of Chicago | Stage, SymptomsSurgical findings |
Vercellini et al. (1989) | 11–19 (18.7) | NR | n = 47 | To determine the value of laparoscopy in the differential diagnosis of CPP | 1983 1987 | Retrospective | First Department Obstetrics and Gynecology, University, Milan | Stage, Lesion type Surgical findings |
Davis et al. (1993) | 13–20 (16.6) | NR | n = 36a | To describe the appearance, stage and treatment of endometriosis in adolescents | NR | Retrospective | Phoenix integrated residency program in obstetrics and gynecology, Arizona | Lesion type Stage infiltration |
Reese et al. (1996) | 11–19 | 12.5 | n = 67 | To determine the incidence, clinical stage and lesion type of endometriosis in adolescents | 1992 1994 | Retrospective | Emory University Affiliated Hospital Atlanta, Georgia | Lesion type, stage, symptoms |
Emmert et al. (1998) | 11–19 (17.3) | 12.2 | n = 105 | To determine the incidence, type, clinical stage of endometriotic lesions | 1996 1997 | Retrospective | Carl Thiem-Clinic and Gynecological Endoscopy Training Center, Cottbus, Germany | Age, incidence Lesion type Stage, symptoms |
Laufer et al. (1997) | 13–21 (16.1) | 12.3 | n = 46 | To evaluate adolescent girls with CPP not responding to medical therapy | 1990 1994 | Descriptive retrospective | Children's Hospital and the Brigham and Women's Hospital in Boston | Stage Lesion type |
Kontoravdis et al. (1999) | 16–19 | NR | n = 98 | To evaluate the role of laparoscopy in the diagnosis and treatment of CPP in adolescents | 1993 1997 | Prospective | University of Athens, Areteion Hospital, Athens | Role of laparoscopy |
Bai et al. (2002) | 14–21 (20.1) | 14.2 | n = 39 | To evaluate the age distribution, diagnosis, clinical stage, treatment of endometriosis in adolescents | 1990 1999 | Retrospective | Severance Hospital, Yonsei University Medical College, Korea | Age, stage, symptoms |
Stavroulis et al. (2006) | 13–20 (16.5) | NR | n = 31 | To determine the frequency and severity of endometriosis in adolescents with CCP unresponsive to medical treatment | 2001 2003 | Retrospective | Elizabeth Garrett Anderson and Obstetric Hospital, London | Stage surgical |
Ventolini et al. (2005) | 12–18 | NR | n = 52 | To compare mild-and-severe forms of endometriosis and to follow up their fecundability on long term | 1993 1995 | Prospective | Department of Obstetrics and Gynecology, University, Wright University, Ohio | Future fecundability Stage |
Kalu et al. (2008) | 15–21 | NR | n = 28 | To describe the clinical features and treatment outcome following the laparoscopic treatment of endometriosis | 2000 2005 | Retrospective | The Chelsea and Westminster Hospital, London | Symptom Recurrence |
Doyle et al. (2009) | 12–24 | NR | n = 90 | To evaluate the effect of combined surgical–medical treatment on endometriosis progression in adolescents | 1995 2007 | Retrospective | Two academic medical centers, Boston | Stage changing Adhesions |
Roman (2010) | (17.4) | NR | n = 20 | To describe the experience with laparoscopic excision in adolescents and to compare with a non-adolescent population | 2003 2009 | Comparative cohort | Braemar Hospital, Hamilton, New Zealand | Surgical findings Stage |
Vicino et al. (2010) | 10–21 | NR | n = 38 | To analyse the clinical manifestations of endometriosis in adolescents | 2005 2006 | Prospective | University and General Hospitals, Milan, Italy | Stage, age |
Total | 10–24 | 11.8–14.2 | n = 880 | Experience, magnitude, severity, clinical manifestations, incidence, stage, role of laparoscopy, age, lesion type among adolescents with endometriosis | 1974 2009 | Prospective (n = 5) Retrospective (n = 9) Comparative (n = 1) | Symptom (n = 6); stage (n = 12); surgical findings (n = 4); lesion type (n = 5); age (n = 3); adhesions (n = 1); recurrence (n = 1); future fecundability n = 1; role of laparoscopy (n = 1); incidence (n = 1) |
NR, not reported or not clearly described; CPP, chronic pelvic pain.
a36 patients were selected from 49 consecutive adolescents who underwent laparoscopic treatment of pelvic endometriosis.
Author (year) . | Range of ages (mean age) in years . | Menarche (mean age in years) . | Sample (n) . | Study objective . | Period of study . | Design . | Care setting . | Outcome measure . |
---|---|---|---|---|---|---|---|---|
Goldstein et al. (1980) | 10–19.25 | 11.8 | n = 140 | To describe the experience in adolescents who have endometriosis | 1974 1979 | Prospective | Boston Children's Hospital Medical Center | Symptoms Surgical findings |
Chatman and Ward (1982) | 12–19 | NR | n = 43 | To outline the magnitude of the problem of endometriosis | NR | Prospective | Department of Obstetrics and Gynecology, University of Chicago | Stage, SymptomsSurgical findings |
Vercellini et al. (1989) | 11–19 (18.7) | NR | n = 47 | To determine the value of laparoscopy in the differential diagnosis of CPP | 1983 1987 | Retrospective | First Department Obstetrics and Gynecology, University, Milan | Stage, Lesion type Surgical findings |
Davis et al. (1993) | 13–20 (16.6) | NR | n = 36a | To describe the appearance, stage and treatment of endometriosis in adolescents | NR | Retrospective | Phoenix integrated residency program in obstetrics and gynecology, Arizona | Lesion type Stage infiltration |
Reese et al. (1996) | 11–19 | 12.5 | n = 67 | To determine the incidence, clinical stage and lesion type of endometriosis in adolescents | 1992 1994 | Retrospective | Emory University Affiliated Hospital Atlanta, Georgia | Lesion type, stage, symptoms |
Emmert et al. (1998) | 11–19 (17.3) | 12.2 | n = 105 | To determine the incidence, type, clinical stage of endometriotic lesions | 1996 1997 | Retrospective | Carl Thiem-Clinic and Gynecological Endoscopy Training Center, Cottbus, Germany | Age, incidence Lesion type Stage, symptoms |
Laufer et al. (1997) | 13–21 (16.1) | 12.3 | n = 46 | To evaluate adolescent girls with CPP not responding to medical therapy | 1990 1994 | Descriptive retrospective | Children's Hospital and the Brigham and Women's Hospital in Boston | Stage Lesion type |
Kontoravdis et al. (1999) | 16–19 | NR | n = 98 | To evaluate the role of laparoscopy in the diagnosis and treatment of CPP in adolescents | 1993 1997 | Prospective | University of Athens, Areteion Hospital, Athens | Role of laparoscopy |
Bai et al. (2002) | 14–21 (20.1) | 14.2 | n = 39 | To evaluate the age distribution, diagnosis, clinical stage, treatment of endometriosis in adolescents | 1990 1999 | Retrospective | Severance Hospital, Yonsei University Medical College, Korea | Age, stage, symptoms |
Stavroulis et al. (2006) | 13–20 (16.5) | NR | n = 31 | To determine the frequency and severity of endometriosis in adolescents with CCP unresponsive to medical treatment | 2001 2003 | Retrospective | Elizabeth Garrett Anderson and Obstetric Hospital, London | Stage surgical |
Ventolini et al. (2005) | 12–18 | NR | n = 52 | To compare mild-and-severe forms of endometriosis and to follow up their fecundability on long term | 1993 1995 | Prospective | Department of Obstetrics and Gynecology, University, Wright University, Ohio | Future fecundability Stage |
Kalu et al. (2008) | 15–21 | NR | n = 28 | To describe the clinical features and treatment outcome following the laparoscopic treatment of endometriosis | 2000 2005 | Retrospective | The Chelsea and Westminster Hospital, London | Symptom Recurrence |
Doyle et al. (2009) | 12–24 | NR | n = 90 | To evaluate the effect of combined surgical–medical treatment on endometriosis progression in adolescents | 1995 2007 | Retrospective | Two academic medical centers, Boston | Stage changing Adhesions |
Roman (2010) | (17.4) | NR | n = 20 | To describe the experience with laparoscopic excision in adolescents and to compare with a non-adolescent population | 2003 2009 | Comparative cohort | Braemar Hospital, Hamilton, New Zealand | Surgical findings Stage |
Vicino et al. (2010) | 10–21 | NR | n = 38 | To analyse the clinical manifestations of endometriosis in adolescents | 2005 2006 | Prospective | University and General Hospitals, Milan, Italy | Stage, age |
Total | 10–24 | 11.8–14.2 | n = 880 | Experience, magnitude, severity, clinical manifestations, incidence, stage, role of laparoscopy, age, lesion type among adolescents with endometriosis | 1974 2009 | Prospective (n = 5) Retrospective (n = 9) Comparative (n = 1) | Symptom (n = 6); stage (n = 12); surgical findings (n = 4); lesion type (n = 5); age (n = 3); adhesions (n = 1); recurrence (n = 1); future fecundability n = 1; role of laparoscopy (n = 1); incidence (n = 1) |
Author (year) . | Range of ages (mean age) in years . | Menarche (mean age in years) . | Sample (n) . | Study objective . | Period of study . | Design . | Care setting . | Outcome measure . |
---|---|---|---|---|---|---|---|---|
Goldstein et al. (1980) | 10–19.25 | 11.8 | n = 140 | To describe the experience in adolescents who have endometriosis | 1974 1979 | Prospective | Boston Children's Hospital Medical Center | Symptoms Surgical findings |
Chatman and Ward (1982) | 12–19 | NR | n = 43 | To outline the magnitude of the problem of endometriosis | NR | Prospective | Department of Obstetrics and Gynecology, University of Chicago | Stage, SymptomsSurgical findings |
Vercellini et al. (1989) | 11–19 (18.7) | NR | n = 47 | To determine the value of laparoscopy in the differential diagnosis of CPP | 1983 1987 | Retrospective | First Department Obstetrics and Gynecology, University, Milan | Stage, Lesion type Surgical findings |
Davis et al. (1993) | 13–20 (16.6) | NR | n = 36a | To describe the appearance, stage and treatment of endometriosis in adolescents | NR | Retrospective | Phoenix integrated residency program in obstetrics and gynecology, Arizona | Lesion type Stage infiltration |
Reese et al. (1996) | 11–19 | 12.5 | n = 67 | To determine the incidence, clinical stage and lesion type of endometriosis in adolescents | 1992 1994 | Retrospective | Emory University Affiliated Hospital Atlanta, Georgia | Lesion type, stage, symptoms |
Emmert et al. (1998) | 11–19 (17.3) | 12.2 | n = 105 | To determine the incidence, type, clinical stage of endometriotic lesions | 1996 1997 | Retrospective | Carl Thiem-Clinic and Gynecological Endoscopy Training Center, Cottbus, Germany | Age, incidence Lesion type Stage, symptoms |
Laufer et al. (1997) | 13–21 (16.1) | 12.3 | n = 46 | To evaluate adolescent girls with CPP not responding to medical therapy | 1990 1994 | Descriptive retrospective | Children's Hospital and the Brigham and Women's Hospital in Boston | Stage Lesion type |
Kontoravdis et al. (1999) | 16–19 | NR | n = 98 | To evaluate the role of laparoscopy in the diagnosis and treatment of CPP in adolescents | 1993 1997 | Prospective | University of Athens, Areteion Hospital, Athens | Role of laparoscopy |
Bai et al. (2002) | 14–21 (20.1) | 14.2 | n = 39 | To evaluate the age distribution, diagnosis, clinical stage, treatment of endometriosis in adolescents | 1990 1999 | Retrospective | Severance Hospital, Yonsei University Medical College, Korea | Age, stage, symptoms |
Stavroulis et al. (2006) | 13–20 (16.5) | NR | n = 31 | To determine the frequency and severity of endometriosis in adolescents with CCP unresponsive to medical treatment | 2001 2003 | Retrospective | Elizabeth Garrett Anderson and Obstetric Hospital, London | Stage surgical |
Ventolini et al. (2005) | 12–18 | NR | n = 52 | To compare mild-and-severe forms of endometriosis and to follow up their fecundability on long term | 1993 1995 | Prospective | Department of Obstetrics and Gynecology, University, Wright University, Ohio | Future fecundability Stage |
Kalu et al. (2008) | 15–21 | NR | n = 28 | To describe the clinical features and treatment outcome following the laparoscopic treatment of endometriosis | 2000 2005 | Retrospective | The Chelsea and Westminster Hospital, London | Symptom Recurrence |
Doyle et al. (2009) | 12–24 | NR | n = 90 | To evaluate the effect of combined surgical–medical treatment on endometriosis progression in adolescents | 1995 2007 | Retrospective | Two academic medical centers, Boston | Stage changing Adhesions |
Roman (2010) | (17.4) | NR | n = 20 | To describe the experience with laparoscopic excision in adolescents and to compare with a non-adolescent population | 2003 2009 | Comparative cohort | Braemar Hospital, Hamilton, New Zealand | Surgical findings Stage |
Vicino et al. (2010) | 10–21 | NR | n = 38 | To analyse the clinical manifestations of endometriosis in adolescents | 2005 2006 | Prospective | University and General Hospitals, Milan, Italy | Stage, age |
Total | 10–24 | 11.8–14.2 | n = 880 | Experience, magnitude, severity, clinical manifestations, incidence, stage, role of laparoscopy, age, lesion type among adolescents with endometriosis | 1974 2009 | Prospective (n = 5) Retrospective (n = 9) Comparative (n = 1) | Symptom (n = 6); stage (n = 12); surgical findings (n = 4); lesion type (n = 5); age (n = 3); adhesions (n = 1); recurrence (n = 1); future fecundability n = 1; role of laparoscopy (n = 1); incidence (n = 1) |
NR, not reported or not clearly described; CPP, chronic pelvic pain.
a36 patients were selected from 49 consecutive adolescents who underwent laparoscopic treatment of pelvic endometriosis.
The 15 selected articles were observational studies published between 1980 and 2010 and were conducted between 1974 and 2009. Seven studies were conducted in the USA (Goldstein et al., 1980; Chatman and Ward, 1982; Davis et al., 1993; Reese et al., 1996; Laufer et al., 1997; Ventolini et al., 2005; Doyle et al., 2009), six studies in Europe (Vercellini et al., 1989; Emmert et al., 1998; Kontoravdis et al., 1999; Stavroulis et al., 2006; Kalu et al., 2008; Vicino et al., 2010), one in New Zealand (Roman, 2010) and one in Asia (Bai et al., 2002). Data were retrospectively collected by reviewing medical records in nine studies (Vercellini et al., 1989; Davis et al., 1993; Reese et al., 1996; Laufer et al., 1997; Emmert et al., 1998; Bai et al., 2002; Stavroulis et al., 2006; Kalu et al., 2008; Doyle et al., 2009) and prospectively collected in five cohort studies (Goldstein et al., 1980; Chatman and Ward, 1982; Kontoravdis et al., 1999; Ventolini et al., 2005; Vicino et al., 2010). One comparative cohort study compared data from adolescents and adult women with endometriosis treated surgically during the same period (Roman, 2010).
Critical appraisal
All selected studies used a cohort study design to describe the prevalence of endometriosis among adolescent girls. This design gives rise to considerable biases like selecting the interesting cases due to a retrospective approach resulting in selection bias (Vercellini et al., 1989; Davis et al., 1993; Reese et al., 1996; Laufer et al., 1997; Emmert et al., 1998; Bai et al., 2002; Stavroulis et al., 2006; Kalu et al., 2008; Doyle et al., 2009) or the risk of confounding because of different levels of experience among the clinicians (Reese et al., 1996; Kalu et al., 2008).
All selected studies were interpreted with caution using CASP criteria for observational studies. The overall appraisal of selected studies was more than acceptable and gave answers to the three major questions (‘are the results valid’, ‘what are the results’ and ‘will the results help locally’). The results of the studies were valid with the exception of one paper (Kontoravdis et al., 1999) in which only three times a ‘yes’ answer was present instead of in four out of the six questions related to the validity. The results were clearly described with the exception of three studies (Kontoravdis et al., 1999; Bai et al., 2002; Doyle et al., 2009) and could be applied to the local population with the exception of two studies (Chatman and Ward, 1982; Bai et al., 2002). In three papers (Emmert et al., 1998; Kontoravdis et al., 1999; Stavroulis et al., 2006), the potential impact of confounders (e.g. age, culture) was not clearly mentioned.
A summary of the critical appraisal of the 15 included articles can be found in Table II.
General patient characteristics
Included subjects were adolescent girls (n = 880) with pelvic pain, aged 10–21 years, of Caucasian (n = 798/880, 91%), African (n = 43/880, 5%) or Asian (n = 39/880, 4%) ethnic origin. The number of patients included in the 15 studies varied between 20 (Roman, 2010) and 140 (Goldstein et al., 1980).
A total of 543 cases of endometriosis were found (184 in prospective studies, 339 retrospective studies and 20 in the comparative cohort study).
The term ‘adolescents’ was present in the title of all articles, except two (Stavroulis et al., 2006; Vicino et al., 2010), but was defined differently in each study, with age groups (Table III) varying between 10 and 19.25 years (Goldstein et al., 1980), between 16 and 19 years (Kontoravdis et al., 1999) and up to 21 years (Laufer et al., 1997; Bai et al., 2002; Kalu et al., 2008; Vicino et al., 2010) and 24 years (Doyle et al., 2009).
The main symptom leading to laparoscopic investigation was either CPP (Goldstein et al., 1980; Emmert et al., 1998; Kontoravdis et al., 1999; Bai et al., 2002; Vicino et al., 2010) or CPP not responding to medical therapy with NSAIDs and OCPs (Reese et al., 1996; Laufer et al., 1997; Ventolini et al., 2005; Stavroulis et al., 2006; Kalu et al., 2008; Doyle et al., 2009) or dysmenorrhea (Chatman and Ward, 1982; Vercellini et al., 1989; Davis et al., 1993; Roman, 2010) (Table I). Histological confirmation was reported in 10 of the 15 selected studies (Goldstein et al., 1980; Chatman and Ward, 1982; Vercellini et al., 1989; Vercellini et al., 1989; Reese et al., 1996; Emmert et al., 1998; Bai et al., 2002; Ventolini et al., 2005; Stavroulis et al., 2006; Vicino et al., 2010).
Details of the studies (authors, age group of study, age at menarche, sample size, study objective, study period and design, care setting and outcome measure) are summarized in Table III. The average age of menarche was mentioned very clearly in only five studies (Goldstein et al., 1980; Reese et al., 1996; Laufer et al., 1997; Emmert et al., 1998; Bai et al., 2002) and ranged between 11.8 and 14.2 years.
Prevalence of endometriosis
The prevalence of endometriosis was highly variable (25–100%) among the selected studies. The overall prevalence of endometriosis visually confirmed at laparoscopy in all patients included in all studies was 62% (n = 543/880). The prevalence appeared to be higher in girls with CPP resistant to treatment with OCPs/NSAIDs (75%; 237/314) and in girls with dysmenorrhea (70%; 102/146) than in those with CPP which is not necessarily resistant to treatment (49%; 204/420). However, due to an extensive heterogeneity on exploring these differences using Meta-regression in STAT 11, we did not find statistical evidence for significant differences between the subgroups.
Classification and stage of endometriosis
Endometriosis was staged laparoscopically according to different classification systems. The AFS/ASRM classification system (ASRM—former AFS, 1997) was used in 8 out of 15 studies (Vercellini et al., 1989; Reese et al., 1996; Laufer et al., 1997; Bai et al., 2002; Ventolini et al., 2005; Doyle et al., 2009; Roman, 2010; Vicino et al., 2010). The ACOSTA classification (Acosta et al., 1973) was used in only two studies (Chatman and Ward, 1982; Stavroulis et al., 2006), whereas one study applied a combination of the AFS/ACOSTA classification (Davis et al., 1993). The Semm Endoscopic Endometriosis Classification (Emmert et al., 1998) and the Kistner classification system (Goldstein et al., 1980) were each used in one paper. The classification of endometriosis was not mentioned in 2 of the 15 studies (Kontoravdis et al., 1999; Kalu et al., 2008).
When only the ASRM classification was taken into account, the adolescents with endometriosis, taken together from all studies, had either minimal (50%, 175/349), mild (27%, 69/259), moderate (18%, 47/259) or severe (14%, 35/259) endometriosis. The distribution of minimal, mild, moderate and severe endometriosis was different between the subgroup with CPP (14, 29, 31 and 26, respectively), the subgroup with CPP resistant to treatment with OCPs and NSAIDs (68, 22, 14 and 2, respectively) and the subgroup with dysmenorrhea (41, 31, 11 and 18%, respectively). The overall prevalence of ASRM classified moderate–severe endometriosis was 32% (82/259) and appeared to be higher in the subgroup with CPP (57%; 44/77) than in the girls with CPP resistant to treatment with OCPs/NSAIDs (16%; 17/108) and the girls with dysmenorrhea (29%; 21/74). However, as mentioned above, due to extensive heterogeneity, these differences were not significant after Meta-regression analysis.
The laparoscopic presentation of moderate-to-severe endometriosis was only noted in three studies (Goldstein et al., 1980; Davis et al., 1993; Stavroulis et al., 2006). In the first study (Davis et al., 1993), 50% (18/36) had moderate-to-severe endometriosis following the revised AFS classification (1997) and 64% (23/36) had moderate-to-severe endometriosis following the Acosta classification (Acosta et al., 1973). The presentation was marked by the presence of rectal lesions (severe endometriosis according to Acosta classification) and tubo-ovarian adhesions. In the second study (Goldstein et al., 1980), only 5% (3/66) of adolescents had stage IV endometriosis, based on the criteria of Kistner et al. (1977), and this was marked by extensive disease of the peritoneum, ovaries and tubes as well as involvement of surrounding structures. In the third study (Stavroulis et al., 2006), 54.5% (6/11) of the adolescents had severe endometriosis (Acosta classification; Acosta et al., 1973) associated with rectovaginal, uterovesical, bowel and ureteric endometriosis.
Discussion
According to our systematic review, nearly two-thirds of adolescents with CPP or dysmenorrhea have laparoscopic evidence of endometriosis, including moderate-to-severe disease in about one-third of those with endometriosis.
Our systematic review is characterized by several strengths. First, we only included studies documenting the prevalence of endometriosis in the investigated adolescents as the primary outcome variable and analysed these studies on the level of originally collected patient data. Other reviews on adolescent endometriosis were not based on a systematic approach and were focused on other endometriosis-related topics in adolescents such as those mentioned in the introduction. Secondly, all selected studies were largely comparable with regard to sex, age, pain symptoms and laparoscopic assessment of endometriosis (Tables I–III). Thirdly, a total of 880 adolescents with CPP or dysmenorrhea were included in this review, a number that is sufficiently large to draw meaningful conclusions with statistical analyses. We do recognize, however, that due to the limited current knowledge of clinical care for adolescents with suspected endometriosis, this number only represents a small portion of the adolescents with endometriosis. On account of only a minimal number of clinicians around the world who, on the one hand, perform laparoscopic surgery on adolescents and, on the other hand, who have the experience of surgical visualization to diagnose endometriosis properly, this number of adolescent patients would currently represent only the ‘tip of the iceberg’.
The results of our systematic review indicate a number of limitations in the selected papers. First, only a restricted number of articles (n = 15) met the inclusion criteria. Secondly, data were collected retrospectively by reviewing medical records in 9 of the 15 studies (Vercellini et al., 1989; Davis et al., 1993; Reese et al., 1996; Laufer et al., 1997; Emmert et al., 1998; Bai et al., 2002; Stavroulis et al., 2006; Kalu et al., 2008; Doyle et al., 2009). This retrospective method is prone to positive selection bias because of the risk of selecting the interesting cases, resulting in an overestimation of the prevalence and/or severity of endometriosis. Thirdly, taking into account the heterogeneity between the studies, we had difficulty performing validated statistics. We explored the difference across the main symptom groups (CPP, CPP resistant to treatment and dysmenorrhea) using Meta-regression in STATA 11. However, using this Meta-regression, we did not find evidence of a difference between the subgroups for any of the prevalence and classification groups. The pooled prevalence of endometriosis was not significantly different among the three different pain subgroups. Based on the limited and heterogeneous data, we suggest that the differences noted by pooling the data are only an indicator for a tendency. We hypothesize that in prospectively and correctly collected data, the difference between the subgroups would be statistically significant. Fourthly, CASP is not a validated tool for a measure of quality in observational studies. Unfortunately, there are no truly validated tools for critical appraisal available for prevalence studies. We therefore referred to it as a key instrument instead of a validated tool. Fifthly, included data were based largely on adolescents of Caucasian origin (n = 798/880, 91%). It is therefore impossible to conclude anything about the prevalence of endometriosis in adolescents of non-Caucasian origin as the total study population included only a small proportion of adolescents of African (n = 43/880, 5%) or Asian (n = 39/880, 4%) ethnic origin, presented in only two articles (Chatman and Ward, 1982; Bai et al., 2002). Sixthly, histological analysis of endometriosis biopsies obtained during laparoscopy was not noted or performed in 33% (5 of 15) of studies. The overall histological confirmation rate was 93% (221/239) but it is variable in the different studies (see Table I). Seventhly, the severity of endometriosis was classified in most studies (13/15) using variable systems. Most commonly, the staging system of the ASRM (1997) (9/13) was followed but other classification systems were used in a significant proportion (5 of 13) of other studies. Moreover, have these systems all been designed in an adult population where the appearance of the disease might be different when compared with adolescents. It appears that red, clear or white lesions are more frequently seen in adolescents than in adults (Kennedy et al., 2005 online updated 30 June 2007). Eighthly, selection bias was important because, in the absence of a standardized care protocol, patients were allocated to laparoscopy based on subjective criteria such as pain symptoms and the surgeon's personal discretion and experience. It is possible that a higher or lower level of experience in endometriosis surgery could lead to an increased or decreased recognition and prevalence of endometriosis (Katsuno et al., 2009; Markides et al., 2010). Ninthly, the term 'adolescents' was not defined in any of the included studies. It is interesting to note that the age of an adolescent is defined differently according to different sources: 13–18 years (PUBMED), 13–17 years (EMBASE), 10–19 years (WHO) or 15–20 years (Van Dale Large Dictionary of the Dutch Language). Tenthly, 3 of the 15 studies were published in the 1980s, at a time when the laparoscopic recognition of subtle endometriotic lesions was limited, which could have resulted in an underestimation of endometriosis in those studies (Koninckx et al., 1991). Eleventhly, CPP was not defined in most (7 of 11) studies, and differently defined in the other (4 of 11) studies (Table I).
In this systematic review, we noted that the overall prevalence of endometriosis in adolescents was 62% and that it was higher in girls with CPP resistant to treatment with OCPs and/or NSAIDs (75%) and in girls with dysmenorrhea (70%) than in girls with CPP that is not necessarily resistant to treatment (49%). We hypothesize that CPP, which is defined differently in the included studies, is a more heterogeneous clinical symptom which may be less specific for endometriosis than is dysmenorrhea (menstrual pain only) or CPP that is resistant to OCPs and/or NSAIDs as these are likely to be the 'worst cases'. This hypothesis is supported by recent evidence showing that dysmenorrhea at an early age is a risk factor for endometriosis in general (Treloar et al., 2010) and that both the incidence and duration of oral contraceptive use for severe primary dysmenorrhea during adolescence is higher in women who later develop deeply infiltrative endometriosis than in women without deeply infiltrative endometriosis (Chapron et al., 2011).
The proportion of girls with ASRM classified moderate–severe endometriosis was higher than expected (32%), as minimal-to-mild endometriosis according to the revised ASRM (rASRM) classification are the most common stages of the disease in adolescents (Kennedy et al., 2005 online updated 30 June 2007). Unfortunately, only three studies included some description of the type of lesions observed that led to their classification as moderate–severe endometriosis. While adhesions were reported in these studies, it is not clear if ovarian endometriotic cysts or DIE contributed to this classification. Furthermore, it is not clear why and also unexpected that the prevalence of moderate–severe endometriosis was lower in girls with CPP resistant to treatment with OCPs and/or NSAIDs (16%; 17/108) or those with dysmenorrhea (29%; 21/74) than in the subgroup with CPP that is not necessarily resistant to treatment (57%; 44/77). We speculate that treatment with OCPs and/or NSAIDs may not prevent the development of endometriosis, but may limit its progression to moderate–severe disease at least in some adolescents. Furthermore, we suggest that even CPP that is treatable in adolescents must be taken seriously, not only because they may have endometriosis, but especially because endometriosis may present as moderate–severe disease in more than 50% of cases (Table I). Of course, we do recognize that our presumption first needs to be confirmed by statistically significant data.
Overall, the high prevalence of endometriosis with a substantial proportion of moderate–severe disease demonstrated in our review in adolescents with CPP has important consequences for clinical practice. It is important to take young girls with dysmenorrhea or CPP seriously and to recognize their pain, rather than deferring it as ‘psychological’, with a potentially harmful effect on their self-esteem. The treatment with NSAIDs is the preferred initial treatment for adolescents with severe dysmenorrhea (American College of Obstetricians and Gynecologists, 2005; Harel, 2010) that impacts their daily life activities like going to school and playing with friends. If an NSAID of one class is not efficient it is a reasonable approach to switch to an NSAID of a different class. If NSAIDs alone are not sufficient, hormonal therapy, such as combined estrogen and progestin OCPs or progestin-only pills, can be combined with NSAIDs. If the pain persists after combined therapy of hormones and NSAIDS for 3–6 months, a definitive diagnosis is recommended and a laparoscopy is indicated to diagnose or exclude endometriosis (American College of Obstetricians and Gynecologists, 2005; Harel, 2010). There is insufficient evidence to recommend alternative approaches such as acupuncture, yoga or diet adjustments, although it has to be recognized that these can have a positive influence on pain perception.
In these adolescents with severe CPP and/or dysmenorrhea that is resistant to OCPs and/or NSAIDs, a diagnostic laparoscopy with simultaneous surgical treatment should be offered. Although there is no definitive evidence of the advantage of excision of the lesions in adolescents, it seems appropriate to perform resection at the same time to limit the surgical interventions for a teenage girl and also in the view of the ESHRE Guidline (Kennedy et al., 2005 online updated 30 June 2007) where it is mentioned as an ideal practice to diagnose and remove endometriosis surgically at the same time, provided that pre-operative adequate consent has been obtained. Adolescents and their parents need to be fully informed about potential risks and benefits before any surgical intervention. Prospective studies are needed to identify the adolescent population at risk for the development of endometriosis and to develop a clinical pathway to care for this specific group of teenagers in collaboration with health professionals based in schools, youth health centers and universities, family physicians and gynecologists specialized in endometriosis.
In order to advance research on endometriosis in adolescence, it would be ideal to record all information of laparoscopic confirmed endometriosis on teenagers concerning age, menarche, symptoms, age of onset of symptoms, description and location of lesions, previous treatment and management in endometriosis centers of expertise and to integrate this information in a large (inter)national database. In addition, center-specific long-term follow-up of adolescents is required to capture symptom changes, evaluate progression and document long-term influences on fertility. Furthermore, it is important to realize that, for various reasons, patients do not always return to the same center for follow-up visits. However, so far all published studies on progression of endometriosis are limited to those girls who return to the same surgeon for repeat surgery, which offers only a small window into what is really happening across time with endometriosis. Furthermore, international consensus is needed to develop a standardized system of longitudinal follow-up with respect to demographic, lifestyle, clinical, imaging, surgical and post-operative data, and regarding patient reported outcomes and assessment of patient centerdness
Most likely in daily practice the majority of teenagers with endometriosis or suspected endometriosis could be well managed symptomatically with medical treatment (NSAIDS and/or OCPs) and lifestyle measures during their adolescence. Further research needs to focus on the question of whether this management is sufficient to prevent further progression and to evaluate the impact on future quality of life regarding fertility and pain problems. With the current insights, it is not possible to propose definitive recommendations for diagnosis and treatment of endometriosis in adolescents. A first step could be to test the hypothesis that early laparoscopic diagnosis and excisional treatment of adolescent endometriosis combined with medical or expectant management and follow-up after the laparoscopy can prevent the progression to moderate–severe disease which can be associated with debilitating pain and infertility and long-term social and economic consequences.
Authors' roles
E.B.J, A.C.M.R.; K.H.; C.M.; T.H.: (i) Substantial contributions to conception and design, or acquisition of data, or analysis and interpretation of data; (ii) drafting the article or revising it critically for important content and (iii) final approval of the version to be published.
Funding
The first author of this review (E.J.) was sponsored by the Leuven University Hospital Research Fund and by funding received via the Merck Serono and Ferring Chairs in Reproductive Medicine held by the last author (T.D.).
Conflict of interest
The idea for this study originated from the Centre for Health Services and Nursing Research. There is no conflict of interest for the first author, the co-authors, the Centre for Health Services and Nursing Research, the Leuven University Fertility Center and the Department of Obstetrics and Gynaecology of the University Hospital Leuven, Belgium.
References
Author notes
Joined first authors.
Joined last authors.