International Journal of Gynecology and Obstetrics 118 (2012) 42–46

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International Journal of Gynecology and Obstetrics

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CLINICAL ARTICLE

Diagram to map the locations of endometriosis

Ricardo Bassil Lasmar ⁎, Bernardo Portugal Lasmar, Claudia PillarDepartment of Gynecology of Fluminense Federal University, Niteroi, Rio de Janeiro, Brazil

⁎ Corresponding author at: Department of GynecUniversity, Rua Marques do Paraná 303, Niteroi, Brafax: +55 21 25372321.

E-mail address: ricardo@lasmar.com.br (R.B. Lasmar

0020-7292/$ – see front matter © 2012 International Feddoi:10.1016/j.ijgo.2012.02.010

a b s t r a c t

a r t i c l e i n f o

Article history:

Received 4 November 2011Received in revised form 9 February 2012Accepted 20 March 2012

Keywords:ClassificationDiagramEndometriosisMapping

Objective: To develop and test a visual map that corresponds practically and objectively to the anatomical areasaffected by endometriosis.Method: The study comprised 150 questionnaires concerning 10 clinical cases of en-dometriosis presented as a visual diagram that were distributed at 3 different scientific events, among 3 groupsof 50 gynecologists. Data were analyzed to evaluate the diagram's ability to graphically represent the endome-triosis sites. Results: After presentation at the first event, the rate of correct answers on the site of endometriosiswas 84.7%; at the second event, after modifications implemented after feedback from the first event, the rateof correct answers was 97.4%; and at the third event, when all suggestions and modifications had been made,the rate was 99.7%. Conclusion: The diagram proposed to map the location of endometriosis lesions appearsto be an adequate and effective instrument to represent the site of the disease, with correlation at almost 100%.

© 2012 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Endometriosis affects about 10% of women of reproductive age. Itsprevalence ranges from 30%–50% in women diagnosed as infertile[1–4]. The disease is defined by the presence of endometrial glandsand stroma in ectopic sites [1,2,5]. Endometriosis is associated withvariable clinical outcomes and presents an insidious and progressiveevolution, interfering with the quality of life and daily activities ofthose affected [1,6–8].

The etiology and pathogenesis of endometriosis remain uncertain,including genetic, hormonal, and inflammatory aspects [2,8]. TheSampson theory, from 1927, which proposed retrogrademenstruationas the trigger for endometriosis, is the most widely accepted theory [2].Owing to gene expression involved in cell apoptosis, endometrialcells can survive in the peritoneal cavity. When activated macrophagesare present, neoangiogenesis begins, leading to implantation andinvasion of ectopic tissue, which is sustained and grows under estrogenstimulation [2].

From an anatomical and clinical viewpoint, endometriosis has3 forms: peritoneal or superficial, ovarian, and deep infiltrative.Multiple forms can be present in one patient. The peritoneal formtypically presents as pigmented or white, typical and atypical lesionsthroughout the surface of the peritoneum. Ovarian forms are charac-terized by the presence of chocolate cysts. The deep forms includelesions with larger-than-5-mm infiltrates that can involve pelvic andabdominal organs [5].

ology of Fluminense Federalzil. Tel.: +55 21 99875354;

).

eration of Gynecology and Obstetrics.

One of the major challenges of making a diagnosis in women withsuspected endometriosis is to assess the extent of the disease andits functional consequences for the pelvic or extra-pelvic organs.Moreover, it is difficult to create a common language among specialiststhat allows standardized diagnosis and treatment [9]. The endometri-osis classification systemproduced by the American Fertility Society, re-vised in 1985, has been helpful in documenting the disease, but it hasserious limitations in clinical use for predicting prognosis and treatmentof pain and infertility [10–12]. Many researchers have suggested classi-fications of endometriosis, but there is still no validated system thatmeets clinical needs and pregnancy rates [10–14].

Choice of therapy depends on the symptoms of pelvic pain and in-fertility, the patient's goals, and the functional impairment assessedby clinical history, physical examination, and imaging [2]. Hormonetherapy and surgery are treatment options [2]. Laparoscopy is consid-ered the gold standard for diagnosis and offers a broader and moredetailed view of the pelvic organs, reduced risk of infection andabdominal wall complications, shorter hospitalization with fasterreturn to daily activities, and a higher likelihood of conservativesurgery [2,6,15]. The decision on indication for surgery must take latediagnosis into account, and the first surgical approach must be thebest possible to achieve the benefits and to reduce the risks of functionalimpairment [16]. Moreover, some studies have shown that recurrencerates for endometriosis are 20% at 2 years, and 40%–50% at 5 years. Forthis reason, experts avoid incomplete resections and carefully evaluatethe possibility of multifocality and multicentricity of lesions [6,15].

Since clinical data are essential for therapeutic management,mainly in complex surgeries, the topographic locations of lesions shouldbe accurately and objectively recorded [17]. Information is crucialto determine the appropriate treatment, coordinating the actionsof multidisciplinary clinical teams, and planning and obtaining the re-quired management and financial resources for every patient. To

Published by Elsevier Ireland Ltd. All rights reserved.

43R.B. Lasmar et al. / International Journal of Gynecology and Obstetrics 118 (2012) 42–46

be useful, clinical records must be clear and precise, organized andstandardized, and easily understood by team members [18]. A visualdiagram representing the sites affected by endometriosis may serve asa guide at the time of surgery and later during clinical follow up [17].

Several studies have described the most frequent locations of le-sions and the trend toward multifocality, which must be taken intoaccount when deciding upon management [17]. The aim of the presentstudy was to develop a visual map corresponding to the anatomicalareas affected by endometriosis in a practical and objective manner,to be included in patients’ clinical records and used in follow up.

2. Materials and methods

The present study is a descriptive study of a case series. A totalof 150 questionnaires concerning 10 clinical cases of endometriosispresented as visual diagrams were distributed during 3 scientific

LEGEND

Central

CER = cervix UTE = uterus

Around

VAG = vagina RTC = retrocervical SEP =VUS = vesicouterine septum OVA = ovary USC =

Distant

BLA = bladder URE = ureter SIG = sigmoid colon CEC = cecum

Rectum penetration

S = superficial M = medium or mus

Rectum height

L = low M = medium

Side

Right Left Anterior Po

BL

URER

USC

OVA( cm)

ROU

PAR

H

M

L

LEFT

Central

Around

Distant

SAN

ANT

POST

SIG

Fig. 1. Diagram to map the anatomica

gynecologymeetings held fromMarch to June, 2011, in Rio de Janeiro,Brazil. At each meeting, the questionnaires were handed out to 50different gynecologists, who voluntarily accepted to participate inthe study. All returned questionnaires were considered, includingthose that contained no answers or were incomplete. The study wasnot submitted to the ethics committee because it was not involvedin the direct care of patients.

The questionnaire requested open answers to questions concerning10 different cases of endometriosis that had been provided by 10specialists with extensive experience in treating the condition. Eachclinical case was interactively presented to the participants using anendometriosis-mapping diagram. Before presenting the cases, an exam-ple of how the diagram worked was given, and the meaning of eachabbreviation and the diagram's purpose were explained for 5 minutes.

As the clinical cases were presented, the participants were askedto record the areas affected by endometriosis. Each participant had

rectovaginal septum PAR = paracolpos/parametrium uterosacral ligament ROU = round ligament

RET = rectum SAN = sacral nervesAPE = appendix

cular D = deep or mucosa

H = high

sterior

A(cm)

ROU

USC

UREECTUM( cm)

OVA( cm)

VUS

RTC

PAR

VAG

VAG

UTE

CER

CECAPE

SEP

RIGHT

SAN

ERIOR

ERIOR

S M D

( cm)

l areas affected by endometriosis.

Table 2Characteristics of the 150 participating gynecologists.a

Participants Group 1 Group 2 Group 3 P value(n=50) (n=50) (n=50)

Age, y a 39.6±12.6 39.6±12.0 40.6±10.0 0.318Laparoscopic experience b 48 (96) 47 (94) 48 (96) 0.874Endometriosis experience b 32 (64) 36 (72) 44 (88) 0.328

a Values are given as mean±SD and number (percentage).

44 R.B. Lasmar et al. / International Journal of Gynecology and Obstetrics 118 (2012) 42–46

2 minutes to look at the diagram representing the case and to writedown where the endometriosis was located. During the presentation,some gynecologists raised questions and these were answeredpromptly and then noted down, thus generating data for future revi-sions of the diagram to improve its understanding and interpretation.At completion, all data were tabulated for individual participants andfor the groups evaluated at different times. At the end of the thirdmeeting, a total of 150 gynecologists, divided into 3 groups of 50,had completed the questionnaire. Each physician could list 38 endo-metriosis sites over the 10 clinical cases, totaling up to 1900 answersper group of 50 gynecologists. These data were analyzed to evaluatethe diagram's ability to graphically and precisely represent the endo-metriosis sites. The answers were considered correct or incorrect.

The first group of 50 physicians showed some difficulty in under-standing the diagram (Fig. 1), which led to its modification by theaddition of one further letter to the abbreviations representing thesites affected by endometriosis—to indicate laterality. The central,peripheral, and distal involved areas of the uterus are representedby distinct patterns of colors. The sites represented in the diagramare the cervix and uterine body, uterosacral ligament, paracolpos,ovaries, round ligaments, vagina, rectovaginal septum, retrocervicalnodule, vesicouterine pouch, ureters, rectum, sigmoid colon, bladder,appendix, sacral nerve, and cecum.

Among the 10 clinical cases, 6 cases showed 4 affected sites each;3 cases showed 3 affected sites each; and 1 case showed 6 affectedsites. Involvement of the retrocervical area was described in 6 out of10 clinical cases and of the paracolpos area in 5 cases; the otherareas were involved less often (Table 1).

The frequency of hits and errors was established in all 3 groupsseparately for each item and across all items, and the results ofthe 3 groups were compared. For the total frequency of hits in thedifferent groups, the proportion test for K(3) samples was applied,assuming as the null hypothesis that the population proportions areequal, and as the alternative hypothesis that proportions among the3 populations are not equal. As expected, the frequency was differentin the last group tested. The confidence level was established at 1%,i.e. a significance of 0.01 with 2 degrees of freedom. The χ2 value wascalculated and compared with critical χ2 values to determine whetherthe null hypothesis was supported. Participant data on sex, age, andexperience with laparoscopy and other surgeries were collected.Based on these data, proportions, means, medians, standard deviations,coefficients of variation, and asymmetry indices were calculated.P value hypothesis testing was applied.

Table 1Sites of endometriosis in each of the 10 clinical cases.

Site Cases

1 2 3 4 5 6 7 8 9 10

Posterior vagina X XUterus X XRetrocervical X X X X X XRight uterosacral ligament XLeft uterosacral ligament X XRight paracolpus X XLeft paracolpos X X XRight round ligamentsLeft round ligaments X XRight ovary XLeft ovary X XRight ureter XLeft Ureter X XSigmoid colon X XRectum X X X X XCecum X XAppendix XVesicouterine pouch XBladder X

3. Results

Out of 150 questionnaires returned, only 5 had blank answersand these were interpreted as incorrect. The age of the participantsranged between 26 and 65 years. In the first group of 50 physicians,16 (32%) were aged under 30 years, and 14 (28%) were over 50 years.In the second group, 15 (30%) were aged under 30 years, 14 (28%)were between 41 and 50 years, and 11 (22%) were over 50 years. Inthe third group, 12 (24%) were under 30 years and 15 (30%) wereover 50 years. Of the 150 respondents, 84 (56%) were male.

In both the first and second groups, 33 (66%) participants had lessthan 5 years of experience with laparoscopy, while 3 (6%) had morethan 21 years of experience. In the third group, 23 (46%) physicianshad less than 5 years of experience with laparoscopy, while 5 (10%)had more than 21 years of experience.

The majority of gynecologists in all 3 groups responded that theyhad performed surgery for endometriosis: 64% (n=32) in group 1;72% (n=36) in group 2; and 88% (n=44) in group 3.

The third group of physicians comprised a more homogeneouspopulation, exhibiting lower coefficients of variation comparedwith the other 2 groups for age range and years of experience withlaparoscopy. However, there were no significant differences in thesefeatures among the 3 groups (Table 2).

The average number of correct answers in each of the groups isshown in Table 3. Proportion tests were calculated using these data,and the χ2 value was 12.1. The critical χ2 value for α=0.01 and 2 de-grees of freedom was 9.2. Since the calculated χ2 value was higherthan the critical value, the null hypothesis was rejected, i.e., the resultsanalyzed differed among the groups. It was observed that group 3 hadmore correct answers than the other groups.

When evaluating the sites of endometriosis separately, correctanswers for retrocervical lesions were given by 86% of participantsin group 1, 86% in group 2, and 100% in group 3. For sigmoid sites,correct answers were given by 80%, 100% and 97% of participants ingroups 1, 2, and 3, respectively. For sites in the left ovary, the correctanswers varied between 88.6% and 100%. In group 1, 13.3% of partici-pants gave incomplete information about laterality in otherwisecorrect answers for ovarian sites.

Table 3Correct answers for site of endometriosis by group.

Site Group 1 Group 2 Group 3

No. (%) No. (%) No. (%)

Vagina 79 (79) 100 (100) 100 (100)Uterus 85 (85) 92 (92) 100 (100)Retrocervical 258 (86) 295 (86) 300 (100)Uterosacral ligament 132 (88) 146 (97) 150 (100)Paracolpos 214 (86) 250 (100) 250 (100)Round ligaments 81 (81) 92 (92) 100 (100)Ovary 174 (87) 197 (99) 200 (100)Ureter 83 (83) 96 (96) 100 (100)Sigmoid colon 120 (80) 150 (100) 146 (97)Rectum 220 (88) 243 (97) 250 (100)Cecum 42 (84) 47 (94) 50 (100)Appendix 44 (88) 50 (100) 50 (100)Vesicouterine pouch 39 (78) 45 (90) 48 (96)Bladder 38 (76) 49 (98) 50 (100)Total 1609 (84.7) 1852 (97.4) 1894 (99.7)

Site

Fig. 2. Correct answers for site of endometriosis by group.

45R.B. Lasmar et al. / International Journal of Gynecology and Obstetrics 118 (2012) 42–46

The mapped area with the least correct answers in group 1 wasthe bladder (76%), followed by the vesicouterine pouch (78%); ingroups 2 and 3, these rates varied between 90% and 100%. Clinicalcases 8 and 10 included lesions in the mid- and high rectum andtheir size was given in centimeters; the hit rates varied between88% and 100% in these sites in the 3 groups. However, participantsdid not describe the size of these lesions in centimeters in 42% to63.4% of otherwise correct answers. When lesions were located inthe uterus, group 1 participants answered correctly in 85% of cases,group 2 in 92%, and group 3 in 100%. Lesions located in the paracolposarea were associated with hit rates varying between 86% and 100%.Ureteral lesions were identified by 83% to 100% of participants inthe 3 groups.

Lasmar

Diagram to Map Endometriosis

Case

• 2 cm left ovarian endometriosis

• Left uterosacral ligament

• Right uterosacral ligament

BB L A (c m )

SIG ( cm)

URERET ( c

VUP

RTCUSC

OVA ( 2cm)

ROU

PAR

VAG

VAG

CER

UTE

H

M

L

S M

LEFT

SNE

Lasmar

Diagram to Map Endometriosis

Case

• 3 cm right ovarian endometriosis

• Right uterosacral ligament

• Retrocervical endometriosis

• Right round ligament endometriosis

• 2 cm bladder endometriosis

• 2 cm deep endometriosis in high rectum

RET

B L A (2 c m

SIG (

URE

VUP

USC

OVA ( cm)

ROU

PAR

VAG

VAG

CER

UTE

H

M

L

S

LEFT

SNE

RTC

Fig. 3. Diagrams representing t

Separate correct rates for mid- and high rectum sites variedbetween 88% and 100% in all 3 groups, but in up to 63% of correctanswers, the size of lesions in centimeters was not included. Thismay have resulted from too brief a presentation of the clinical cases,or it might indicate that participants did not consider the size oflesions to be an important piece of information. On the other hand,after including laterality, identification of sites improved; for exam-ple, the correct answers for lesions in the left ovary increased from88.6% in group 1 to 100% in group 2.

Correct answers for the vesicouterine pouch site increased from 78%in group 1 to 90% in group 2. Some other terms, such as vesicouterineseptum and anterior bladder, were used by physicians in reference tothe vesicouterine pouch, which might indicate a flaw in the uniformityof terminology; nevertheless, after modifications to the abbreviations,correct answers increased to 96% in group 3 (Fig. 2).

4. Discussion

A graphic mapping system of areas affected by endometriosis canbe used as the basis for therapeutic decision making and follow up ofpatients. The present study proposed amapping diagram for everydayclinical practice, both at the initial approach before surgery and atfollow up. The primary aim of the study was to verify whether thiskind of presentation is reproducible and easily understood.

The interactive method employed allowed us to detect somedifficulties in the understanding of cases, which led to minor modifi-cations in the abbreviations and inclusion of laterality indicators toimprove the final version of the diagram.

Lasmar

ROU

USC

UREm)

OVA ( cm)PAR

DCEC0APP

SEP

Diagram to Map Endometriose

RIGHT

SNE

Lasmar

B L A (c m )

SIG ( cm)

URE

ROU

USC

URERET ( cm)

OVA ( cm)

VUP

RTCUSC

OVA ( 2cm)

ROU

PAR PAR

VAG

VAG

CER

UTE

H

M

L

S M DCEC0APP

SEP

Diagram to Map Endometriose

LEFT RIGHT

SNESNE

( 2 cm)

Lasmar

)

cm)

USC

URE

OVA ( 3 cm)PAR

M DCEC0APP

SEP

Diagram to Map Endometriose

RIGHT

SNE

ROU

RET ( 2 cm)

Lasmar

BLA(2 c m )

SIG ( cm)

URE

USC

URE

OVA ( 3 cm)

VUP

USC

OVA ( cm)

ROU

PAR PAR

VAG

VAG

CER

UTE

H

M

L

S M DCEC0APP

SEP

Diagram to Map Endometriose

LEFT RIGHT

SNESNE

RTC

ROU

wo of the cases presented.

46 R.B. Lasmar et al. / International Journal of Gynecology and Obstetrics 118 (2012) 42–46

When comparing the correct answer and error rates among the3 groups, a progressive increase in hit rates was observed, especiallyfor the third group. This increase was statistically significant, andwas most likely due to the modifications made after the first presen-tation of the diagram, which facilitated correspondence betweenthe mapping information and the sites affected by endometriosisin each clinical case (Fig. 3). Another factor that contributed to betterunderstanding was an indicator of lesion distribution within theaffected area: central, peripheral, and distal.

It is not known whether a longer duration of presentation of theclinical cases or more repetitions of the instructions for reading themapping would decrease the number of blank answers. Another as-pect to be considered is that some groups comprised heterogeneouselements, such as gynecologists who had less experience or whohad not participated in endometriosis surgery.

The analysis of the responses showed that the endometriosismapping diagram is easily understood and can describe the locationof the affected sites in an objective and clear way. It may prove to bea useful tool for gynecologists because it reproduces the clinical dataand images, is helpful in management and follow up of endometriosispatients, and can act as a map for surgical purposes. It will be usefulin patient's referred to an endometriosis specialist and could be usedin multicenter studies and investigations.

Considering that the sample size was small, further studies mustbe performed in different countries to validate the diagram.

In conclusion, the diagram proposed to map the location of endo-metriosis lesions appears to be an adequate and effective instrumentto represent the site of the disease. In this study, the correlation wasalmost 100%.

Conflict of interest

The authors have no conflicts of interest to declare.

References

[1] Pugsley Z, Ballard K. Management of endometriosis in general practice: the pathwayto diagnosis. Br J Gen Pract 2007;57(59):470–6.

[2] Nácul AP, Spritzer PM. Current aspects on diagnosis and treatment of endometriosis[in Portuguese]. Rev Bras Ginecol Obstet 2010;32(6):298–307.

[3] Halis G, Mechsner S, Ebert AD. The diagnosis and treatment of deep infiltratingendometriosis. Dtsch Arztebl Int 2010;107(25):446–56.

[4] Abrao MS, Gonçalves MO, Dias Jr JA, Podgaec S, Chamie LP, Blasbalg R. Comparisonbetween clinical examination, transvaginal sonography and magnetic resonanceimaging for the diagnosis of deep endometriosis. Hum Reprod 2007;22(12):3092–7.

[5] Fritel X. Endometriosis anatomoclinical entities. J Gynecol Obstet Biol Reprod(Paris) 2007;36(2):113–8.

[6] Roman H. Guidelines for the management of painful endometriosis. J GynecolObstet Biol Reprod (Paris) 2007;36(2):141–50.

[7] Borguese B, Vaiman D, de Ziegler D, Chapron C. Endometriosis and genetics: whatresponsibility for the genes? J Gynecol Obstet Biol Reprod (Paris) 2010;39(3):196–207.

[8] Somigliana E, Vercellini P, Vigano' P, Benaglia L, Crosignani PG, Fedele L. Non-invasive diagnosis of endometriosis: the goal or own goal? Hum Reprod 2010;25(8):1863–8.

[9] Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of BrazilianPortuguese version of quality of life questionnaire for women with endometriosis(Endometriosis Health Profile Questionnaire–EHP-30). Rev Bras Ginecol Obstet2008;30(8):384–92.

[10] Roberts CP, Rock JA. The current staging system for endometriosis: does it help?Obstet Gynecol Clin North Am 2003;30(1):115–32.

[11] Hornstein MD, Gleason RE, Orav J, Haas ST, Friedman AJ, Rein MS, et al. The repro-ducibility of the revised American Fertility Society classification of endometriosis.Fertil Steril 1993;59(5):1015–21.

[12] Adamson GD. Endometriosis classification: an update. Curr Opin Obstet Gynecol2011;23(4):213–20.

[13] Coccia ME, Rizzelo F. Ultrasonographic staging: a new staging system for deependometriosis. Ann N Y Acad Sci 2011;1221:61–9.

[14] Chvatal R, Habelsberger A, Wurm P, Schimetta W, Oppelt P. Comparison of revisedAmerican Fertility Society and ENZIAN staging: a critical evaluation of classificationsof endometriosis on the basis of our patient population. Fertil Steril 2011;95(5):1574–8.

[15] Golfier F, Sabra M. Surgical management of endometriosis. J Gynecol Obstet BiolReprod (Paris) 2007;36(2):162–72.

[16] Kondo W, Bourdel N, Tamburro S, Cavoli D, Jardon K, Rabischong B, et al. Complica-tions after surgery for deeply infiltrating pelvic endometriosis. BJOG 2011;118(3):292–8.

[17] Chapron C, Fauconnier A, Vieira M, Barakat H, Dousset B, Pansini V, et al. Anatomicaldistribution of deeply infiltrating endometriosis: surgical implications and proposi-tion for a classification. Hum Reprod 2003;18(1):157–61.

[18] Marin HF. Health Information System: general considerations. J Health Inform2010;2(1):20–4.