Skip to main content
Download PDF

Clinical diagnosis of pelvic endometriosis: a scoping review

BMC Women's Health volume 15, Article number: 39 (2015) Cite this article

Abstract

Background

Accurate and timely diagnosis of endometriosis is associated with confusion. Clinical manifestations, imaging techniques, biomarkers and surgical techniques are used as diagnostic approaches. This paper reviews current evidence on clinical manifestation in order to help practitioners and perhaps improve women’s health.

Methods

A review of the literature on clinical diagnosis of pelvic endometriosis that appeared in the English language biomedical journals was performed using PubMed, Science Direct and Google Scholar. The search strategy included the combination of key words ‘endometriosis’ and ‘diagnosis’ or ‘clinical diagnosis’ in the titles or abstracts of articles. The search included all papers published during the year 2000 to 2014. Then, the findings were classified in order to summarize the evidence.

Results

Using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement, in all 51 papers were found relevant and included in this review. In general we found three categories of diagnostic approaches for clinical manifestation including: i) diagnosis via symptoms obtained from history taking, ii) diagnosis via signs obtained from physical examination and iii) diagnosis via risk factors obtained from history taking.

Conclusion

Diagnosis of endometriosis is a matter of concern. Since the disease is associated with diverse clinical symptoms and signs, deeper and more comprehensive consideration according to patient’s history and clinical findings is recommended for early and more accurate detection in order to prioritize women for further investigation and contribute to its early management.

Peer Review reports

Background

Endometriosis is a disease with considerable prevalence. It has been estimated to affect 10% to 15% of women of reproductive age [1]. The disease has several impacts in general physical, mental, and social well-being. The annual cost for hospital admission is estimated to be in a total around 54 million euros [2]. Diagnostic delay of endometriosis is a problematic issue [3] and it takes 8 to 11 years to be diagnosed with long and expensive diagnostic methods [2,4]. Thus it is essential to contemplate diagnosis as an important topic. The best method for early diagnosis of endometriosis is still full of unknown issues. Research on the diagnosis of endometriosis currently interfaces with four areas including clinical manifestations, imaging techniques, biomarkers and surgical techniques [5]. Laparoscopy, which is considered as the golden standard in endometriosis diagnosis has considerable risks [5], and other diagnostic methods are presented as inaccurate and with some limitations [6]. Therefore it seems that for developing clinical and non-surgical approaches for early detection of disease, effort is needed to have a better understanding of signs and symptoms of the disease [7].

Although there are several useful overview papers on endometriosis, most published papers are unfocused and usually discuss about all aspects of the disease including pathophysiology, diagnosis and treatment. While there is not any internationally recognized noninvasive method for diagnosis, most presurgical diagnostic methods are clinical judgment based on medical history, symptoms and signs [8]. Thus, this study aimed to review the literature on clinical diagnosis of endometriosis in order to discover the clinical criteria for achieving broader and deeper insight on the topic. Clinical manifestations of endometriosis are very broad and diverse issue with a wide range of changes [9]. Particulalrly here we focus on current research on the history taking and physical examination of endometriosis. It is hoped that this review may help to bring more attention about clinical diagnosis of endometriosis and consequently aid in decreasing diagnostic delay and perhaps contribute to improved women’ health.

Methods

Definition

Endometriosis is defined as the presence of endometrial tissue (gland and struma) outside the uterus [10]. Endometriosis has been found in almost all of the tissues and organs of the body [11]. In this study we focused on pelvic endometriosis because pelvic endometriosis is the most common form of the disease, and it mostly affects women during their reproductive life [12].

Search engines

The search engines included PubMed, Science Direct and Google Scholar using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline [13].

Search strategy

The search strategy included the combination of key words ‘endometriosis’ and ‘diagnosis’ or ‘clinical diagnosis’ in the titles or abstracts of articles.

Inclusion and exclusion criteria

All qualitative and quantitative articles in English language biomedical journals from year 2000 to 2014 on pelvic endometriosis were included. Case reports and articles on non-pelvic endometriosis were excluded. The year 2000 was chosen because the intention was to include more recent literature in this systematic review. The initial search was carried out in January 2013 and updated twice in March 2014 and February 2015.

Data synthesis

The findings from each idivdual paper on clinical diagnosis were retrieved, and were classified. Then different tables were provided to summriaze and present the findings.

Results

Descriptive findings

A total of 2749 citations were identified and after exclusion of duplicates, the abstracts of 1272 citations were screened. Of these, 113 papers were found relevant. However, 51 articles met inclusion criteria and were included in this review. The study selection process is shown in Figure 1. Overall we found 16 overview/commentary publications [2,9,14-27], 33 original research articles [1,7,8,11,12,28-53], two meta-analysis [54,55] and 2 systematic reviews [56,57].

Figure 1
figure 1

Study selection process.

Full size image

Review of overview papers

A summary of overview/commentary publications is presented in Table 1. In general, these articles focused mainly on symptoms and treatment of the endometriosis. The emphasis of most papers was on pain, infertility and chronic fatigue.

Table 1 A summary of overview/commentary papers on clinical symptoms and signs
Full size table

Clinical diagnosis

Clinical diagnosis was achieved by different approaches. We have classified these methods in three groups: i) clinical diagnosis by symptoms obtained from history taking, ii) clinical diagnosis by signs obtained from physical examination and iii) clinical diagnosis by risk factors obtained from history taking. These are summarized as follows:

Clinical diagnosis by symptoms obtained from history taking

By taking a careful history of patients and considering their symptoms, the disease may be greatly suspected. Many studies recognized symptoms, which were very common such as cyclic or perimenstrual symptoms [16]. A summary of findings on symptoms obtained from history taking are presented here:

Pain

Included dysmenorrhea (during and at the end of menstruation) [2,7-9,15-17,19-26,28,29,32-37,42,53,54], pelvic pain before and during menstruation [2,7,14,16-18,21,23,25,33,34], and pain during sexual intercourse or after sex (dyspareunia) [2,7-9,11,15-17,19-25]. Dyspareunia was occurred only with deep thrusting [23]. Lower abdominal pain or suprapubic pain, lower back pain [11,14,17,20,21,29] and loin pain [17,20] were also mentioned. Pelvic pain was present as chronic pelvic pain (lasting ≥6 months) and patients reported that they were suffering from intermenstrual pain (non-period pelvic pain) or ovulation pain [2,7,15,16,19-24,33,34,37,42]. Rectal pain was also mentioned [11,21]. Pain character was found to be throbbing [31,35], dull or sharp and exacerbated by physical activity [20]. Pain often worsened over time and changed in character [20].

Menstrual symptoms

Included hypermenorrhea, menorrhagia, premenstrual spotting for 2–4 days [7,9,11,15,22,23,29,32], mid cycle bleeding, irregular bleeding, and irregular periods [2,16,19,26,29].

Urinary problems

Included dysuria, hematuria, urinary frequency, urinary tract infection, and cystitis [11,14,17,18,21,23,29,32,34,36,42].

Digestive symptoms

Included abdominal bloating, diarrhea with period, painful bowel movements and painful defecation (dyschezia) during menses, hematochezia, nausea and stomach upset at the time of period, constipation, [11,14,16-20,22,24,25,28,29,34,35], irritable bowel syndrome (IBS) [7,32] and early satiety [20].

Gynecologic comorbidities

Included gynecological infections and low resistance to infection, candidiasis [11,29,33] infertility [2,7-9,16,17,19,21,23-25,29,34,36,37,42,45], pelvic inflammatory disease, ovarian cysts [7,32,33] and postcoital bleeding [7].

Comorbidities

Included a wide range of allergies and allergic disease, dizziness, migraines and headaches at the time of period or before [11,23,29,33,34], and mitral valve prolapse [29].

Social life symptoms

Some symptoms such as inability to carry on normal activities including work or school were reported by patients [29]. Depressed and anxious feelings [11], irritability or premenstrual tension syndrome [23], and psychoemotional distress and alexithymia were also mentioned [47].

Musculoskeletal symptoms

Included muscle/bone pain, joint pain and leg pain [11].

Other symptoms

Patients reported suffering from chronic fatigue, exhaustion, low energy and low-grade fever [2,11,16,18,21,29]. Women also reported burning or hypersensitivity, symptoms that were suggestive of a neuropathic component [20]. Mictalgia was also mentioned [22]. Previous surgery for endometriosis also was found a considerable factor [31,42]. The findings are presented in Table 2.

Table 2 Main diagnostic symptoms and signs obtained from history taking and physical examination respectively
Full size table

Clinical diagnosis by signs obtained from physical examination

Clinical signs of the disease that identified by physical examination (pelvic examination by inspection and palpation) included a broad range of signs. External genitalia and the vaginal surface were usually unremarkable [15]. Findings of physical examination are listed as follows:

External genitalia

Visible red, blue, or hemorrhagic nodules on the external genitalia [21].

Vagina

Visible red, blue, or hemorrhagic nodules on the vagina, and tender masses, nodules, and fibrosis on palpation of the upper vagina [8,15-17,21].

Cervix

Visible lesions on the cervix, tenderness on cervical movement, lateral cervical displacement, and cervical stenosis [15,16,19,21,37].

Uterus

A fixed (decreased or absent mobility) and retroverted uterus, and uterine motion tenderness in pelvic examination [8,15-17,19,21,24].

Adnexa

Tender or fixed adnexal masses resulting from endometriomas, adnexal enlargement, and pelvic masses [8,14,17,19,21].

Posterior vaginal fornix

Tender nodules in the posterior vaginal fornix, bluish implants typical of endometriosis or red, hypertrophic lesions bleeding on contact [15,17].

Pouch of Douglas

Fullness or mass or nodularity or pain in the pouch of Douglas, local tenderness or palpable tender nodules in cul de sac [8,14,16,19,30].

Rectovaginal septum

Tender masses, nodules, and fibrosis of the rectovaginal septum [15,19-21,37].

Uterosacral ligament

Thickening, pain or tenderness or nodularity in uterosacral ligament [8,14-16,19,21,24,30].

The most reported signs included changes in uterus, cervix, adnexa and uterosacral ligament palpation. The findings are shown in Table 2.

Clinical diagnosis by risk factors obtained from history taking

Although it was reported that the following risk factors alone are not enough, they could potentially direct physicians toward clinical diagnosis of pelvic endometriosis. All risk factors are presented in Table 3.

Table 3 Risk factors or characteristics of endometriosis patients
Full size table

Risk factors related to menstrual periods

Included early menarche (before age 11–13) or late menarche (menarche at ≥14 y) [12,15,20,33,39,54], short menstrual cycle (≤27 days) [15,17,20,32,58], longer menstrual flow (≥7 days) [15,30], and spotting before onset of menses [11,15,19,23,29,51]. Late menopause [20], early history of dysmenorrhea [12], obstruction of menstrual outflow for example mullerian anomalies and use of pads and tampons were other risk factors [17,20].

Risk factors related to patients’ characteristics

Patients who were taller, thinner and had lower body mass index, red hair [1,15,39,40,43] and dysplastic nevi [15] were found to be more prone to pelvic endometriosis. Higher education was considered as another risk factor [18]. Rh-negativity [46], severe teenage acne [48] and blue eye color [49] were also mentioned as risk factors for pelvic endometriosis.

Risk factors related to obstetrics and gynecologic history

These included not having a history of pregnancy or delivery, [15,39-42], late initiation of sexual activity (≥21 y) and never used OCPs [17,39].

Risk factors related to family history

Included family history of endometriosis for example mother or sister [15,17,36,38,44]. The relative risk of endometriosis in female siblings was found to be 5.7 [42].

Risk factors related to nutrition

Consumption of red meat and trans fats were associated with an increased risk of endometriosis, and eating fruits, green vegetables, and omega-3 long-chain fatty acids were associated with a decreased risk [20].

Risk factors related to embryonic factors

Included exposure to diethylstilbestrol in utero and low birth weight [20].

Risk factors related to patient’s habits

Consumption of one or more alcoholic drinks per week [17,39,40,55].

Risk factors related to race

Asian origin increased the risk of the disease [15].

However, prolonged lactation, multiple pregnancies, the combined oral contraceptive, smoking and exercise are reported as protective factors [20]. The most risk factors were related to menstrual periods, patients’ characteristics and family history.

Discussion

The emphasis of this review was on several aspects of the clinical diagnosis of pelvic endometriosis. All factors that could have been of any help in clinical diagnosis of the disease were reviewed and classified. These findings divided in three main categories. Moreover this article showed that there were many more symptoms than have traditionally associated with endometriosis.

Usefulness of clinical signs and symptoms in the diagnosis of pelvic endometriosis in women who present with infertility was shown in some studies [17]. In addition, it has been reported that some symptoms had greater predictive value. The most commonly reported symptoms leading to a diagnosis were dysmenorrhea and pelvic pain. Treloar et al. reported that dysmenorrhea was associated with a 2.5-fold increased risk of subsequent endometriosis [12]. Pelvic pain was reported by all patients in a study by Greene et al. [34]. Among the other symptoms leading to a diagnosis, subfertility and an ovarian mass were more commonly reported in stages 3–4, whereas dyspareunia was more common in stages 1–2 [41]. Women with endometriosis were 9 times as likely to report dyspareunia as compared to a control group [32]. In Nnoaham et al. study painful defecation during menstruation and a history of benign ovarian cysts strongly predicted any stages of the disease. The stage III and IV disease was predicted with good accuracy based on symptom-based model. They used several variables in their model including indications for surgery, menstrual history, dysmenorrhea, dyspareunia, pelvic pain, bowel/urinary symptoms, pregnancy/infertility history, personal characteristics and family history [36].

Chapron et al. showed that variables such as painful defecation during menses, severe dyspareunia, pain other than noncyclic, and previous surgery were considered as independent predictors for posterior deep infiltrating endometriosis. They showed a diagnostic model that used two independent predictors: painful defecation during menses and severe dyspareunia. The sensitivity of this model for diagnosing posterior deep infiltrating endometriosis was 74.5% and its specificity was 68.7%. They concluded that standardized evaluation of painful symptoms is useful for screening the disease [31]. Pelvic inflammatory disease and ovarian cysts were 6 and 12 times as likely to be made in women with endometriosis [14].

Although no test provides strong evidence for the presence of endometriosis, the symptom of uterosacral pain had the highest positive likelihood ratio for the diagnosis of endometriosis [20]. In addition to the classic symptom of pain, other symptoms such as fatigue, exhaustion, low energy, gastrointestinal problems, abdominal bloating, and a range of allergic diseases also showed a positive association with endometriosis. These are usually dismissed because they are not widely known. These symptoms are very important. A study by Lemaire showed that the three symptoms with highest total symptom distress were fatigue or weariness, menstrual cramping and nonperiodic pelvic pain [11].

Women with endometriosis were twice as likely to report urinary symptoms such as dysuria, cystitis, and urinary tract infections compared with control group [14]. Sinaii et al. did not report any significant relationship between endometriosis and regular, vigorous exercise, regular use of talc as body powder and cigarette smoking [43], but other studies have found a significant association between smoking and endometriosis [40]. In Hediger study, patients were more likely to be late maturers (menarche at ≥14 y) [39] while in other studies early menarche was often cited as a risk factor for endometriosis [12]. In Parazzini study age at menarche and lifelong type of menstrual cycles were not related to the risk of deep or pelvic and ovarian endometriosis [40]. So it seems that further studies are needed to clarify this relationship.

The risk of the disease raised by advancing age within the reproductive years, peaking among women aged 40–44 years [58]. The findings of the Ballweg’s study indicated that the disease was more severe with an early age of onset and thus it is necessary to pay more attention to girls suffering from menstrual pain [29]. Most studies have shown a significant relationship between endometriosis and length of menstrual cycle, menstrual volume, occurrence of irregular menstrual periods, recent pelvic pain or dyspareunia except one [39] which may be attributed to the small sample size of the study. In the Flores’s study among Puerto Rican women the diagnosis of endometriosis was significantly associated with dysmenorrhea, dyspareunia, and chronic pelvic pain, but not with menstrual cycle characteristics [33]. This was probably due to their study on Hispanic population. In Treloar et al. study no association was found between endometriosis and duration of natural menstruation, heaviness of flow, type of sanitary protection used and history of sexual intercourse during menstruation which may be due to recall bias or small size of control group [12]. Ballard and Mangubat showed that menorrhagia in women with endometriosis was 5 times higher that controls [32].

Lafay et al. showed that patients with the lowest BMI (≤18.5) were at a higher risk of deep infiltrating endometriosis. BMI was significantly lower in deep infiltrating endometriosis and ovarian endometrioma patients but not for the superficial endometriosis patients [43]. In Yi et al. study, women with advanced-stage endometriosis had lower BMI than those with minimal or mild disease, and BMI was significantly associated with disease severity [1]. These findings are in line with other studies [39,40], but in Kennedy study the risk of the disease was increased for women with greater peripheral fat [58]. Borghese et al. showed that Rh-negative women were twice as likely to develop endometriosis. [46]. However, there is controversy about the relationship between blood group and endometriosis [46,59,60] and further investigation is needed to determine the role of blood groups in the development of endometriosis. In a study by Xie et al. it was reported that women who had severe teenage acne had a 20% increased risk of endometriosis. Probable mechanisms for such observation might be due to genetic factors, sex hormones including estrogens and immune malfunction [48]. Blue eye color also was another factor. It is argued that perhaps genetic factors, and vitamin D deficiency due to photo-sensitivity might lead to a relationship between eye color and endometriosis [49]. Several studies have shown that the risk of allergic disease could be increased with endometriosis [56].

In Kashima et al. study the relative risk of endometriosis in female siblings of patients was 5.7 [38], which were consistent with other findings [17]. These findings propose a familial tendency and a genetic factor for endometriosis.

Endometriosis occurs more commonly in middle-aged, upper class, ambitious, white women. This may occur due to greater access to medical care and diagnostic tests such as laparoscopy in these women [58]. Several studies have shown different results about the relationship between physical activity and endometriosis so there is inconclusiveness regarding the benefits of physical exercise as a risk factor for the disease [57].

Two important signs must be considered: deep dyspareunia and nodules in the pouch of Douglas [23]. Findings of physical examination vary significantly with location of endometriotic lesions. They can be seen on speculum examination in only 14% of patients, and a classic, painful, spheric nodule can be palpated in only 43% [28]. In Chapron study a nodule was found in 80% of patients with vaginal endometriosis, this rate dropped to only 35% and 33% in those with deep infiltrating endometriosis of the digestive tract and uterosacral ligaments, respectively [28]. High locations of deep infiltrating endometriosis lesions at the level of uterosacral ligaments, bottom of the pouch of Douglas and upper one-third of the posterior vaginal wall explain why results of routine clinical examination are so poor. Cheewadhanaraks showed a positive predictive value of tenderness and/or nodularity of the cul-de-sac and/or uterosacral ligament(s) in diagnosis of the endometriosis [30]. In Howard study no findings on physical examination, including cervical deviation, cervical tenderness, or paracervical tenderness were predictive for the disease [61] but in Bazot et al. study the sensitivity of physical examination was 73.5% for uterosacral ligament endometriosis, 50% for vaginal endometriosis and 46% for intestinal endometriosis. The accuracy of physical examination is higher during menstruation [42].

Eskenazi et al. reported that ovarian endometriosis, but not nonovarian endometriosis, could be reliably predicted with noninvasive procedures. They used history, pain reports, physical examination and ultrasound for prediction and found that these procedures have moderate success in predicting a surgical diagnosis of endometriosis [8].

Attempts to diagnose women using symptoms, clinical findings or ultrasonography had disappointing findings except, possibly, for ovarian endometriosis in Hediger et al. study [39]. Women with endometriosis experience significantly more gynecological, urological and bowel symptoms than women without endometriosis [32], and that the risk of endometriosis increases in women with endometriosis-related symptoms [7].

Conclusion

Clinical diagnosis of pelvic endometriosis is difficult. Thus considerable efforts are needed to improve the clinical diagnosis of pelvic endometriosis because it could help to prioritize women for further investigation and contribute to its early diagnosis. However, this review provides integrated findings from the literature containing issues related to signs, symptoms and risk factors. The findings suggest that better diagnosis of pelvic endometriosis need a careful and comprehensive investigation about risk factors during history taking and clinical visits. Perhaps every notes during this period by clinicians and midwifes might lead to timely diagnosis and treatment. Further studies with much more focus on signs and symptoms of the disease are recommended for clarifying the present contradictions.

References

  1. Yi KW, Shin JH, Park MS, Kim T, Kim SH, Hur JY. Association of body mass index with severity of endometriosis in Korean women. Int J Gynaecol Obstet. 2009;105:39–42.

    Article  PubMed  Google Scholar 

  2. Luisi S, Lazzeri L, Ciani V, Petraglia F. Endometriosis in Italy: from cost estimates to new medical treatment. Gynecol Endocrinol. 2009;25:734–40.

    Article  CAS  PubMed  Google Scholar 

  3. Hudelist G, Fritzer N, Thomas A, Niehues C, Oppelt P, Haas D, et al. Diagnostic delay for endometriosis in Austria and Germany: causes and possible consequences. Hum Reprod. 2012;27:3412–6.

    Article  CAS  PubMed  Google Scholar 

  4. Rogers PA, D’Hooghe TM, Fazleabas A, Gargett CE, Giudice LC, Montgomery GW, et al. Priorities for endometriosis research: recommendations from an international consensus workshop. Reprod Sci. 2009;16:335–46.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Scarselli G, Rizzello F, Cammilli F, Ginocchini L, Coccia ME. Diagnosis and treatment of endometriosis. A review. Gynecol Endocrinol. 2009;25:734–40.

    Article  Google Scholar 

  6. Vodolazkaia A, El-Aalamat Y, Popovic D, Mihalyi A, Bossuyt X, Kyama CM, et al. Evaluation of a panel of 28 biomarkers for the non-invasive diagnosis of endometriosis. Hum Reprod. 2012;27:2698–711.

    Article  CAS  PubMed  Google Scholar 

  7. Abbas S, Ihle P, Köster I, Schubert I. Prevalence and incidence of diagnosed endometriosis and risk of endometriosis in patients with endometriosis-related symptoms: findings from a statutory health insurance-based cohort in Germany. Eur J Obstet Gynecol Reprod Biol. 2012;160:79–83.

    Article  PubMed  Google Scholar 

  8. Eskenazi B, Warner M, Bonsignore L, Olive D, Samuels S, Vercellini P. Validation study of nonsurgical diagnosis of endometriosis. Fertil Steril. 2001;76:929–35.

    Article  CAS  PubMed  Google Scholar 

  9. Okeke TC, Ikeako LC, Ezenyeaku CC. Endometriosis. Niger J Med. 2011;20:191–9.

    CAS  PubMed  Google Scholar 

  10. Goshtasebi A, Nematollahzadeh M, Hariri F, Montazeri A. The short form endometriosis health profile (EHP-5): translation and validation study of the Iranian version. J Ovarian Res. 2011;4:11.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Lemaire GS. More than just menstrual cramps: symptoms and uncertainty among women with endometriosis. J Obstet Gynecol Neonatal Nurs. 2004;33:71–9.

    Article  PubMed  Google Scholar 

  12. Treloar SA, Bell TA, Nagle CM, Purdie DM, Green AC. Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol. 2010;202:534–6.

    Article  PubMed  Google Scholar 

  13. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.

    Article  PubMed  Google Scholar 

  14. Valle RF. Endometriosis: current concepts and therapy. Int J Gynaecol Obstet. 2002;78:107–19.

    Article  CAS  PubMed  Google Scholar 

  15. Spaczynski RZ, Duleba AJ. Diagnosis of endometriosis. Semin Reprod Med. 2003;21:193–208.

    Article  PubMed  Google Scholar 

  16. Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod. 2005;20:2698–704.

    Article  PubMed  Google Scholar 

  17. Mounsey AL, Wilgus A, Slawson DC. Diagnosis and management of endometriosis. Am Fam Physician. 2006;74:594–600.

    PubMed  Google Scholar 

  18. Denny E, Mann CH. A clinical overview of endometriosis: a misunderstood disease. Br J Nurs. 2007;16:1112–6.

    Article  PubMed  Google Scholar 

  19. Amer S. Endometriosis. Obstet, Gynecol Reprod Medicine. 2008;18:126–33.

    Article  Google Scholar 

  20. Giudice LC. Clinical practice. Endometriosis. N Engl J Med. 2010;362:2389–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Altman G, Wolcyzk M. Endometriosis: overview and recommendations for primary care nurse practitioners. J Nurse Pract. 2010;6:427–34.

    Article  Google Scholar 

  22. Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98:564–71.

    Article  PubMed  Google Scholar 

  23. Acién P, Velasco I. Endometriosis: a disease that remains enigmatic. ISRN Obstet Gynecol. 2013;17:1–12.

    Article  Google Scholar 

  24. Carneiro MM, Filogônio ID, Costa LM, de Ávila I, Ferreira MC. Clinical prediction of deeply infiltrating endometriosis before surgery: is it feasible? a review of the literature. Biomed Res Int. 2013;2013:1–8.

    Article  Google Scholar 

  25. Schrager S, Falleroni J, Edgoose J. Evaluation and treatment of endometriosis. Am Fam Physician. 2013;2:107–13.

    Google Scholar 

  26. Mehedintu C, Plotogea MN, Ionescu S, Antonovici M. Endometriosis still a challenge. J Med Life. 2014;7:349.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Bhattacharjee AK, Choudhury AP. Clinical and non-clinical presentations of endometriosis. Int J Clin Surg Adv. 2014;2:120–47.

    Google Scholar 

  28. Chapron C, Dubuisson JB, Pansini V, Vieira M, Fauconnier A, Barakat H, et al. Routine clinical examination is not sufficient for diagnosing and locating deeply infiltrating endometriosis. J Am Assoc Gynecol Laparosc. 2002;9:115–9.

    Article  PubMed  Google Scholar 

  29. Ballweg ML. Impact of endometriosis on women’s health: comparative historical data show that the earlier the onset, the more severe the disease. Best Pract Res Clin Obstet Gynaecol. 2004;18:201–18.

    Article  PubMed  Google Scholar 

  30. Cheewadhanaraks S, Peeyananjarassri K, Dhanaworavibul K, Liabsuetrakul T. Positive predictive value of clinical diagnosis of endometriosis. J Med Assoc Thi. 2004;87:740–4.

    Google Scholar 

  31. Chapron C, Barakat H, Fritel X, Dubuisson JB, Bréart G, Fauconnier A. Presurgical diagnosis of posterior deep infiltrating endometriosis based on a standardized questionnaire. Hum Reprod. 2005;20:507–13.

    Article  CAS  PubMed  Google Scholar 

  32. Ballard KD, Mangubat MC. Can symptomatology provide clues to the diagnosis of endometriosis?: a national case–control study of 5,544 women with endometriosis. J Minim Invasive Gynecol. 2007;14:S10–S154.

    Article  Google Scholar 

  33. Flores I, Abreu S, Abac S, Fourquet J, Laboy J, Ríos-Bedoya C. Self-reported prevalence of endometriosis and its symptoms among Puerto Rican women. Int J Gynaecol Obstet. 2008;100:257–61.

    Article  PubMed  Google Scholar 

  34. Greene R, Stratton P, Cleary SD, Ballweg ML, Sinaii N. Diagnostic experience among 4,334 women reporting surgically diagnosed endometriosis. Fertil Steril. 2009;91:32–9.

    Article  PubMed  Google Scholar 

  35. Ballard K, Lane H, Hudelist G, Banerjee S, Wright J. Can specific pain symptoms help in the diagnosis of endometriosis? a cohort study of women with chronic pelvic pain. Fertil Steril. 2010;94:20–7.

    Article  PubMed  Google Scholar 

  36. Nnoaham KE, Hummelshoj L, Kennedy SH, Jenkinson C, Zondervan KT. Developing symptom-based predictive models of endometriosis as a clinical screening tool: results from a multicenter study. Fertil Steril. 2012;98:692–r.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hadisaputra W. Clinical signs, symptoms and serum level of interleukin–6 and tumor necrosis factor in women with or without endometriosis. APJR. 2013;2:142–5.

    Google Scholar 

  38. Kashima K, Ishimaru T, Okamura H, Suginami H, Ikuma K, Murakami T, et al. Familial risk among Japanese patients with endometriosis. Int J Gynaecol Obstet. 2004;84:61–4.

    Article  CAS  PubMed  Google Scholar 

  39. Hediger ML, Hartnett HJ, Louis GM. Association of endometriosis with body size and figure. Fertil Steril. 2005;84:1366–74.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Parazzini F, Cipriani S, Bianchi S, Gotsch F, Zanconato G, Fedele L. Risk factors for deep endometriosis: a comparison with pelvic and ovarian endometriosis. Fertil Steril. 2008;90:174–9.

    Article  PubMed  Google Scholar 

  41. Sinaii N, Plumb K, Cotton L, Lambert A, Kennedy S, Zondervan K, et al. Differences in characteristics among 1,000 women with endometriosis based on extent of disease. Fertil Steril. 2008;89:538–45.

    Article  PubMed  Google Scholar 

  42. Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I, Daraï E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril. 2009;92:1825–33.

    Article  PubMed  Google Scholar 

  43. Lafay Pillet MC, Schneider A, Borghese B, Santulli P, Souza C, Streuli I, et al. Deep infiltrating endometriosis is associated with markedly lower body mass index: a 476 case–control study. Hum Reprod. 2012;27:265–72.

    Article  PubMed  Google Scholar 

  44. Chapron C, Lafay- Pillet MC, Monceau E, Borghese B, Ngo C, Souza C, et al. Questioning patients about their adolescent history can identify markers associated with deep infiltrating endometriosis. Fertil Steril. 2011;95:877–81.

    Article  PubMed  Google Scholar 

  45. Peterson CM, Johnstone EB, Hammoud AO, Stanford JB, Varner MW, Kennedy A, et al. Risk factors associated with endometriosis: importance of study population for characterizing disease in the ENDO Study. Am J Obstet Gynecol. 2013;208:451e1–451e11.

    Article  Google Scholar 

  46. Borghese B, Chartier M, Souza C, Santulli P, Lafay-Pillet MC, de Ziegler D, et al. ABO and Rhesus blood groups and risk of endometriosis in a French Caucasian population of 633 patients living in the same geographic area. Biomed Res Int. 2014;2014:618964.

  47. Cavaggioni G, Lia C, Resta S, Antonielli T, Benedetti Panici P, Megiorni F, et al. Are mood and anxiety disorders and alexithymia associated with endometriosis? A preliminary study. Biomed Res Int. 2014;2014:786830.

  48. Xie J, Kvaskoff M, Li Y, Zhang M, Qureshi AA, Missmer S A, et al. Severe teenage acne and risk of endometriosis. Hum Reprod. 2014;29:2592–9.

  49. Vercellini P, Buggio L, Somigliana E, Dridi D, Marchese M A, Viganò P. ‘Behind blue eyes’: the association between eye colour and deep infiltrating endometriosis. Hum Reprod. 2014:29:2171–2175.

  50. Tu Frank F, Hongyan DU, Goldstein GP, Beaumont JL, Zhou Y, Brown WJ. The influence of prior oral contraceptive use on risk of endometriosis is conditional on parity. Fertil Steril. 2014;101:1697–704.

    Article  CAS  PubMed  Google Scholar 

  51. Heitmann RJ, Langan KL, Huang RR, Chow GE, Burney RO. Premenstrual spotting of two or more days is strongly associated with histologically confirmed endometriosis in women with infertility. Am J Obstet Gynecol. 2014;211;4:358.e1–6.

    Article  Google Scholar 

  52. Walch K, Kernstock T, Poschalko-Hammerle G, Gleiß A, Staudigl C, Wenzl R. Prevalence and severity of cyclic leg pain in women with endometriosis and in controls – effect of laparoscopic surgery. Eur J Obstet Gynecol Reprod Biol. 2014;179:51–7.

    Article  PubMed  Google Scholar 

  53. Barbosa JS, Yamamoto MMW, de Medeiros MAS, Kubiszeski EH, Banhara CR, de Medeiros SF. Clinical and endocrine features of Brazilian infertile women with or without endometriosis: A comparative cross-sectional study. APJR. 2014;3:275–81.

    Google Scholar 

  54. Nnoaham KE, Webster P, Kumbang J, Kennedy SH, Zondervan K. Is early age at menarche a risk factor for endometriosis? A systematic review and meta-analysis of case–control studies. Fertil Steril. 2012;98:702–12.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Parazzini F, Cipriani S, Bravi F, Bravi F, Pelucchi C, Chiaffarino F, et al. A metaanalysis on alcohol consumption and risk of endometriosis. Am J Obstet Gynecol. 2013;209:106.e1–10.

    Article  CAS  Google Scholar 

  56. Bungum HF, Vestergaard C, Knudsen UB. Endometriosis and type 1 allergies/immediate type hypersensitivity: a systematic review. Eur J Obstet Gynecol Reprod Biol. 2014;179:209–15.

    Article  PubMed  Google Scholar 

  57. Bonocher CM, Montenegro ML, Silva JC, Ferriani RA, Meola J. Endometriosis and physical exercises: a systematic review. Reprod Biol Edocrinol. 2014;12:4.

    Article  Google Scholar 

  58. Kennedy S. Who gets endometriosis? Women’s Health Med. 2005;2:18–9.

    Article  Google Scholar 

  59. Matalliotakis I, Cakmak H, Goumenou A, Sifakis S, Ziogos E, Arici A. ABO and Rh blood groups distribution in patients with endometriosis. Arch Gynecol Obstet. 2009;280:917–9.

    Article  PubMed  Google Scholar 

  60. Demir B, Dilbaz B, Zahran M. ABO and Rh blood groups distribution in patients with endometriosis. Arch Gynecol Obstet. 2010;281:373–4.

    Article  PubMed  Google Scholar 

  61. Howard FM. Clinical predictors of a surgical diagnosis of endometriosis. J Minim Invasive Gynecol. 2005;12:6–7.

    Article  Google Scholar 

Download references

Acknowledgments

This manuscript was originated from the PhD thesis of the first author at Department of Midwifery and Reproductive Health, Faculty of Medicine, Tarbiat Modares University.

Author information

Authors and Affiliations

  1. Department of Reproductive Health and Midwifery, Faculty of Medical Sciences, Tarbiat Modares University, Jalal-e Al Ahmad Highway, P.O Box 14115-331, Tehran, Iran

    Hedyeh Riazi, Najmeh Tehranian & Saeideh Ziaei

  2. Department of Nursing, Faculty of Medical Sciences, Tarbiat Modares University, Jalal-e Al Ahmad Highway, P.O Box 14115–331, Tehran, Iran

    Easa Mohammadi

  3. Department of Biostatistics, Faculty of Medical Sciences, Tarbiat Modares University, Jalal-e Al Ahmad Highway, P.O Box 14115-331, Tehran, Iran

    Ebrahim Hajizadeh

  4. Mental Health Research Group, Health Metrics Research Center, Iranian Institute for Health Sciences Research, ACECR, P.O Box 13185–1488, Tehran, Iran

    Ali Montazeri

  5. Faculty of Humanity Sciences, University of Science & Culture, ACECR, Tehran, Iran

    Ali Montazeri

Authors
  1. Hedyeh Riazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Najmeh Tehranian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saeideh Ziaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Easa Mohammadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ebrahim Hajizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ali Montazeri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Najmeh Tehranian or Saeideh Ziaei.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

HR was the main investigator and carried out the study. NT and SZ supervised the study. EM and EH were the study advisors and involved in data synthesis. AM contributed to conducting the systematic review, the writing process, responded to the reviewers’ comment and prepared the final draft. All authors read and approved the manuscript.

Rights and permissions

Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.

The Creative Commons Public Domain Dedication waiver (https://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Riazi, H., Tehranian, N., Ziaei, S. et al. Clinical diagnosis of pelvic endometriosis: a scoping review. BMC Women's Health 15, 39 (2015). https://doi.org/10.1186/s12905-015-0196-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12905-015-0196-z

Keywords

BMC Women's Health

ISSN: 1472-6874

Contact us