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Improved quality of life (EHP-30) in patients with endometriosis after surgical treatment

SUMMARY

OBJECTIVE:

This study aimed to evaluate the quality of life of patients with endometriosis before and after surgical treatment.

METHODS:

An observational, longitudinal, and prospective study was conducted with 102 women with pelvic pain and endometriosis that was unimproved by clinical treatment and indicated for surgical treatment. The patients’ quality of life was assessed using the 30-item Endometriosis Health Profile (EHP-30) questionnaire before and 3 and 6 months after surgery. The statistical tests were analyzed using the Statistical Package for Social Sciences version 17.0, and the Friedman test was used.

RESULTS:

There was a reduction in EHP-30 scores 3 and 6 months after surgery compared to before surgery, as well as 6 months after surgery compared to 3 months after surgery, in the central questionnaire (PART 1) and in Sections A, B, C, E, and F (p<0.0001). For Section D, there was a reduction in scores 6 months after surgery compared to before surgery (p<0.0001).

CONCLUSION:

Surgical treatment of endometriosis improves quality of life in several areas assessed by the EHP-30 questionnaire.

KEYWORDS:
Endometriosis; Surgical procedure; Quality of life

INTRODUCTION

Endometriosis is a common benign gynecological disorder defined by the presence of fibrotic lesions outside the uterine cavity that are morphologically similar to the endometrium, most commonly in the organs of the female pelvis11 Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod. 2017;32(2):315-24. https://doi.org/10.1093/humrep/dew293
https://doi.org/10.1093/humrep/dew293...
,22 Chapron C, Marcellin L, Borghese B, Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666-82. https://doi.org/10.1038/s41574-019-0245-z
https://doi.org/10.1038/s41574-019-0245-...
. The clinical presentation of this pathology is mainly characterized by pelvic pain and infertility; its etiology is undefined, and its overall incidence is approximately 10% in women of reproductive age33 Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol Rep. 2017;6(1):34-41. https://doi.org/10.1007/s13669-017-0187-1
https://doi.org/10.1007/s13669-017-0187-...
,44 Gordts S, Koninckx P, Brosens I. Pathogenesis of deep endometriosis. Fertil Steril. 2017;108(6):872-85.e1. https://doi.org/10.1016/j.fertnstert.2017.08.036
https://doi.org/10.1016/j.fertnstert.201...
.

The delay in the diagnosis of endometriosis leads to chronic pelvic pain, centralization of pain, anxiety, and depression, with consequent suffering and loss of quality of life as the disease progresses55 Soto E, Luu TH, Liu X, Magrina JF, Wasson MN, Einarsson JI, et al. Laparoscopy vs. robotic surgery for endometriosis (LAROSE): a multicenter, randomized, controlled trial. Fertil Steril. 2017;107(4):996-1002.e3. https://doi.org/10.1016/j.fertnstert.2016.12.033
https://doi.org/10.1016/j.fertnstert.201...
,66 Laganà AS, Rosa VL, Rapisarda AMC, Valenti G, Sapia F, Chiofalo B, et al. Anxiety and depression in patients with endometriosis: impact and management challenges. Int J Womens Health. 2017;9:323-30. https://doi.org/10.2147/IJWH.S119729
https://doi.org/10.2147/IJWH.S119729...
. To assess the quality of life of patients with endometriosis, three instruments have been developed to date: the Endometriosis Health Profile Questionnaire (EHP-30) developed by Jones et al.; the instrument developed by Colwell et al. 1998; and the instrument developed by Bodner et al. in 199777 Jones G, Kennedy S, Barnard A, Wong J, Jenkinson C. Development of an endometriosis quality-of-life instrument: the endometriosis health profile-30. Obstet Gynecol. 2001;98(2):258-64. https://doi.org/10.1016/s0029-7844(01)01433-8
https://doi.org/10.1016/s0029-7844(01)01...
,88 Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of Brazilian Portuguese version of quality of life questionnaire for women with endometriosis (Endometriosis Health Profile Questionnaire--EHP-30). Rev Bras Ginecol Obstet. 2008;30(8):384-92. https://doi.org/10.1590/s0100-72032008000800003
https://doi.org/10.1590/s0100-7203200800...
. Of these, only the EHP-30 includes items that were generated directly from interviews with patients. The relevance of this method for the construction of its items arises from literature findings that indicate that patients’ evaluations of their health and well-being differ from those performed by health professionals77 Jones G, Kennedy S, Barnard A, Wong J, Jenkinson C. Development of an endometriosis quality-of-life instrument: the endometriosis health profile-30. Obstet Gynecol. 2001;98(2):258-64. https://doi.org/10.1016/s0029-7844(01)01433-8
https://doi.org/10.1016/s0029-7844(01)01...
,88 Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of Brazilian Portuguese version of quality of life questionnaire for women with endometriosis (Endometriosis Health Profile Questionnaire--EHP-30). Rev Bras Ginecol Obstet. 2008;30(8):384-92. https://doi.org/10.1590/s0100-72032008000800003
https://doi.org/10.1590/s0100-7203200800...
.

This study aimed to evaluate in the most diverse ways the quality of life of women with endometriosis that was unsuccessfully clinically managed and who underwent surgical treatment.

METHODS

This is a longitudinal and prospective analytical study of the evolution of the quality of life of women with endometriosis who underwent surgical treatment between September 2020 and May 2022.

The inclusion criteria were as follows: patients from the chronic pelvic pain and endometriosis outpatient clinic of the São Domingos Hospital, São Luis, Maranhão, Brazil, who voluntarily sought treatment; had a clinical picture and imaging test results compatible with endometriosis of various forms; were clinically treated for more than 3 months with no improvement in pain; had indications for surgical treatment via laparoscopy with intraoperative confirmation and pathological anatomy consistent with endometriosis; and agreed to participate in the study and signed an informed consent form.

The following patients were excluded from the study: those with suspected endometriosis alone or with infertility without pain; those with suspected endometriosis with or without pelvic pain that was not confirmed during laparoscopy and/or histological analysis; those who did not return for outpatient follow-up; those with previous or ongoing neoplastic pathologies; those with incomplete surgeries, major uncontrolled psychiatric disorders, or surgical or spontaneous menopause; those who underwent robotic surgeries; and those who refused to participate in the study.

The validated Portuguese-language version of the EHP-30 questionnaire was administered on the day of admission for surgery and 3 and 6 months after the surgical procedure, at the outpatient level88 Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of Brazilian Portuguese version of quality of life questionnaire for women with endometriosis (Endometriosis Health Profile Questionnaire--EHP-30). Rev Bras Ginecol Obstet. 2008;30(8):384-92. https://doi.org/10.1590/s0100-72032008000800003
https://doi.org/10.1590/s0100-7203200800...
.

The EHP-30 consists of a central questionnaire comprising 30 items that evaluate 5 dimensions (pain, control and powerlessness, emotional well-being, social support, and self-image) and a modular questionnaire comprising 23 items distributed across 6 scales (sexual relations, work, medical profession, infertility, relationship with children, and treatment)88 Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of Brazilian Portuguese version of quality of life questionnaire for women with endometriosis (Endometriosis Health Profile Questionnaire--EHP-30). Rev Bras Ginecol Obstet. 2008;30(8):384-92. https://doi.org/10.1590/s0100-72032008000800003
https://doi.org/10.1590/s0100-7203200800...
. Each scale yields a score from 0 to 100, and lower scores indicate better quality of life77 Jones G, Kennedy S, Barnard A, Wong J, Jenkinson C. Development of an endometriosis quality-of-life instrument: the endometriosis health profile-30. Obstet Gynecol. 2001;98(2):258-64. https://doi.org/10.1016/s0029-7844(01)01433-8
https://doi.org/10.1016/s0029-7844(01)01...
. The prospective examination of the patients’ quality of life entailed three applications of the questionnaire: during the preoperative period and 3 and 6 months after surgery.

The surgical procedures entailed the removal of all endometriotic lesions, according to Koninckx et al.99 Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98(3):564-71. https://doi.org/10.1016/j.fertnstert.2012.07.1061
https://doi.org/10.1016/j.fertnstert.201...
, and the Working Group of the ESGE, ESHRE, and WES et al.1010 Working group of ESGE, ESHRE and WES. Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis †‡¶. Facts Views Vis Obgyn. 2020;11(4):269-97. PMID: 32322824. The endometriomas were treated according to the Working Group of the ESGE, ESHRE, and WES et al.1111 Working group of ESGE, ESHRE and WES, Saridogan E, Becker CM, Feki A, Grimbizis GF, Hummelshoj L, et al. Recommendations for the surgical treatment of endometriosis. Part 1: ovarian endometrioma. Hum Reprod Open. 2017;2017(4):hox016. https://doi.org/10.1093/hropen/hox016
https://doi.org/10.1093/hropen/hox016...
.

The data were organized using Microsoft Excel 2010® software for the preparation of databases, tables, and graphs. The statistical tests were analyzed using the Statistical Package for Social Sciences (SPSS) version 17.0. Absolute and relative frequency measurements were used to quantify the numerical and categorical variables. The Kolmogorov-Smirnov test was used to assess the normality of the EHP-30 questionnaire data. Since the distribution of the data was nonnormal, nonparametric data are expressed as the median (25th–75th percentile). For the comparisons among the different time points (before and 3 and 6 months after surgery), the Friedman test was used, followed by the Dunn posttest. Spearman's correlation was used to assess the correlation between the degree of endometriosis and the EHP-30 scores.

This study was evaluated and approved by the Research Ethics Committee of São Domingos Hospital through the Brazil Platform, with the Research Ethics Appraisal Certificate (CAAE) number 11808919.2.0000.5085, process approval number 3.334.498.

RESULTS

The final sample consisted of 102 patients with a mean age of 35.96±6.309 years of whom 34 (33.3%) were single and 68 (66.6%) were married. Regarding color, 18 (17.6%) patients were white, 70 (68.6%) were brown, and 14 (13.8%) were black. Regarding the classification of endometriosis according to the rASRM, 9 (8.8%) patients had minimal endometriosis, 18 (17.6%) had mild endometriosis, 35 (34.3%) had moderate endometriosis, and 40 (39.3%) had severe endometriosis (Table 1).

Table 1
Characteristics of patients before and 3 and 6 months after laparoscopic surgical treatment of all forms of endometriosis.

The types of surgery that the patients underwent were as follows: 21 (20.5%) underwent endometriosis, 30 (29.5%) underwent endometriosis+myomectomy, 23 (22.6%) underwent endometriosis+hysterectomy, 23 (22.5%) underwent endometriosis+rectosigmoidectomy+hysterectomy, and 5 (4.9%) underwent endometriosis+myomectomy+rectosigmoidectomy (Table 1).

The EHP-30 data are shown in Table 2. There were reductions in the scores 3 and 6 months after surgery compared to presurgery, and at 6 months after surgery compared to 3 months after surgery, on the questionnaire (Part 1) and on Sections A, B, C, E, and F (p<0.0001). For Section D, there was a reduction 6 months after surgery compared to before surgery (p<0.0001).

Table 2
Evaluation of quality of life (EHP-30) in patients before and 3 and 6 months after laparoscopic surgical treatment of all forms of endometriosis.

There was no moderate or strong correlation between the degree of endometriosis and the EHP-30 quality of life scores before surgery and 3 and 6 months after surgical treatment (Spearman's correlation).

DISCUSSION

Due to the lengthy diagnostic process and consequent loss of quality of life for women with endometriosis, it is necessary to evaluate the quality of life of patients with symptomatic endometriosis along several parameters to improve their prognosis and offer both medical and multidisciplinary care33 Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol Rep. 2017;6(1):34-41. https://doi.org/10.1007/s13669-017-0187-1
https://doi.org/10.1007/s13669-017-0187-...
,1212 Römer T. Long-term treatment of endometriosis with dienogest: retrospective analysis of efficacy and safety in clinical practice. Arch Gynecol Obstet. 2018;298(4):747-53. https://doi.org/10.1007/s00404-018-4864-8
https://doi.org/10.1007/s00404-018-4864-...
,1313 Souza CA, Oliveira LM, Scheffel C, Genro VK, Rosa V, Chaves MF, et al. Quality of life associated to chronic pelvic pain is independent of endometriosis diagnosis--a cross-sectional survey. Health Qual Life Outcomes. 2011;9:41. https://doi.org/10.1186/1477-7525-9-41
https://doi.org/10.1186/1477-7525-9-41...
. As the results of this study show, in addition to providing a good prognosis for clinical symptomatology, surgical management led to a significant improvement in the quality of life 3 and 6 months after surgical treatment of endometriosis for the women who participated in this study.

Most of the participants were between 30 and 40 years old, reflecting a delay in diagnosis and treatment similar to what has been reported worldwide66 Laganà AS, Rosa VL, Rapisarda AMC, Valenti G, Sapia F, Chiofalo B, et al. Anxiety and depression in patients with endometriosis: impact and management challenges. Int J Womens Health. 2017;9:323-30. https://doi.org/10.2147/IJWH.S119729
https://doi.org/10.2147/IJWH.S119729...
. The participants were predominantly brown, compatible with the mixed ethnicities of the region where the study was conducted (the extreme north of Brazil), and the most common marital status was married.

Regarding the classification of endometriosis according to the rASRM, approximately 73.6% of the cases were moderate and severe, showing that the more advanced forms of this pathology are difficult to control with clinical treatment; this finding is reinforced by the fact that most of the patients required more comprehensive surgeries, such as myomectomies, hysterectomies, or rectosigmoidectomies.

Next, we will analyze other endometriosis studies that assessed quality of life with the EHP-30 questionnaire. Our study did not aim to compare clinical and surgical treatments, as the failure of clinical treatment was an inclusion criterion; however, it seems that both surgery and clinical treatment are valuable options to improve the harmful impact of dysmenorrhea associated with endometriosis1414 Vercellini P, Frattaruolo MP, Somigliana E, Jones GL, Consonni D, Alberico D, et al. Surgical versus low-dose progestin treatment for endometriosis-associated severe deep dyspareunia II: effect on sexual functioning, psychological status and health-related quality of life. Hum Reprod. 2013;28(5):1221-30. https://doi.org/10.1093/humrep/det041
https://doi.org/10.1093/humrep/det041...
.

Among the prospective studies that evaluated the treatment of intestinal endometriosis with surgeries performed by a multidisciplinary team experienced with the management of endometriosis, the results indicated significant improvement in quality of life 1 year after the surgical procedure, with no difference between the types of intestinal approach1515 Kent A, Shakir F, Rockall T, Haines P, Pearson C, Rae-Mitchell W, et al. Laparoscopic surgery for severe rectovaginal endometriosis compromising the bowel: a prospective cohort study. J Minim Invasive Gynecol. 2016;23(4):526-34. https://doi.org/10.1016/j.jmig.2015.12.006
https://doi.org/10.1016/j.jmig.2015.12.0...
. In a study that included only patients with deep endometriosis with or without intestinal resection, both groups showed a significant improvement in quality of life after surgery1616 Meuleman C, Tomassetti C, Wolthuis A, Cleynenbreugel B, Laenen A, Penninckx F, et al. Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study. Ann Surg. 2014;259(3):522-31. https://doi.org/10.1097/SLA.0b013e31828dfc5c
https://doi.org/10.1097/SLA.0b013e31828d...
,1717 Turco LC, Scaldaferri F, Chiantera V, Cianci S, Ercoli A, Fagotti A, et al. Long-term evaluation of quality of life and gastrointestinal well-being after segmental colo-rectal resection for deep infiltrating endometriosis (ENDO-RESECT QoL). Arch Gynecol Obstet. 2020;301(1):217-28. https://doi.org/10.1007/s00404-019-05382-8
https://doi.org/10.1007/s00404-019-05382...
.

Furthermore, in a prospective study that evaluated quality of life in 22 patients with deep endometriosis who underwent surgical treatment, the EHP-30 results showed significant improvement for the items pain, control and powerlessness, emotional well-being, social relationships, sexual relations, and relationships with medical providers, but no significant changes in self-image, work, or relationships with the children1818 Tan BK, Maillou K, Mathur RS, Prentice A. A retrospective review of patient-reported outcomes on the impact on quality of life in patients undergoing total abdominal hysterectomy and bilateral salpingo-oophorectomy for endometriosis. Eur J Obstet Gynecol Reprod Biol. 2013;170(2):533-8. https://doi.org/10.1016/j.ejogrb.2013.07.030
https://doi.org/10.1016/j.ejogrb.2013.07...
,1919 Selvi Dogan F, Cottenet J, Douvier S, Sagot P. Quality of life after deep pelvic endometriosis surgery: evaluation of a French version of the EHP-30. J Gynecol Obstet Biol Reprod (Paris). 2016;45(3):249-56. https://doi.org/10.1016/j.jgyn.2015.06.007
https://doi.org/10.1016/j.jgyn.2015.06.0...
. Although both that study and our study were prospective and had equivalent study durations, our study had a larger sample and included patients with all forms of endometriosis, not just deep endometriosis, and we observed significant improvement in all areas except relations with medical providers; in this area, improvement was noted only between the preoperative scores and the scores 6 months after surgery.

Studies have shown that removal of the unaffected uterus does not seem to improve the quality of life of patients with endometriosis1818 Tan BK, Maillou K, Mathur RS, Prentice A. A retrospective review of patient-reported outcomes on the impact on quality of life in patients undergoing total abdominal hysterectomy and bilateral salpingo-oophorectomy for endometriosis. Eur J Obstet Gynecol Reprod Biol. 2013;170(2):533-8. https://doi.org/10.1016/j.ejogrb.2013.07.030
https://doi.org/10.1016/j.ejogrb.2013.07...
,2020 Rindos NB, Fulcher IR, Donnellan NM. Pain and quality of life after laparoscopic excision of endometriosis. J Minim Invasive Gynecol. 2020;27(7):1610-17.e1. https://doi.org/10.1016/j.jmig.2020.03.013
https://doi.org/10.1016/j.jmig.2020.03.0...
. A study that evaluated the quality of life of 61 patients who underwent surgical treatment that included the removal of the foci of endometriosis, hysterectomy, and oophorectomy compared with that of a group without hysterectomy and ovarian preservation found significant improvement on all 5 scales of the EHP-30 at 4 weeks postsurgery, and this improvement persisted for up to 6.8 years2020 Rindos NB, Fulcher IR, Donnellan NM. Pain and quality of life after laparoscopic excision of endometriosis. J Minim Invasive Gynecol. 2020;27(7):1610-17.e1. https://doi.org/10.1016/j.jmig.2020.03.013
https://doi.org/10.1016/j.jmig.2020.03.0...
. Although this was a longer observation period than that of our study, the results are in agreement with our findings.

In a multicenter, randomized clinical trial, we investigated the differences between the conventional robotic and laparoscopic pathways in the surgical treatment of endometriosis. Patients with all forms of endometriosis were evaluated. One of the comparison variables was quality of life, measured with the EHP-30 questionnaire; we found no difference between these two pathways, and both groups showed improved quality of life55 Soto E, Luu TH, Liu X, Magrina JF, Wasson MN, Einarsson JI, et al. Laparoscopy vs. robotic surgery for endometriosis (LAROSE): a multicenter, randomized, controlled trial. Fertil Steril. 2017;107(4):996-1002.e3. https://doi.org/10.1016/j.fertnstert.2016.12.033
https://doi.org/10.1016/j.fertnstert.201...
. In the present study, our sample included patients with all forms of endometriosis, and the results were similar, but we did not include patients who underwent robotic surgery.

A literature review showed that endometriosis impairs quality of life, especially in the domains of pain and psychological and social functioning, and that therapies alleviate symptoms and improve the quality of life of these patients, but further research is needed to evaluate the impact of endometriosis on patients’ lives2121 Gao X, Yeh YC, Outley J, Simon J, Botteman M, Spalding J. Health-related quality of life burden of women with endometriosis: a literature review. Curr Med Res Opin. 2006;22(9):1787-97. https://doi.org/10.1185/030079906X121084
https://doi.org/10.1185/030079906X121084...
. In this study, we confirmed that surgical treatment improves the quality of life of patients with surgical indications for the treatment of endometriosis that has not been relieved by clinical treatment. The cases were not separated by the type of surgical intervention performed. All patients who underwent the removal of peritoneal, ovarian, or deep endometriosis with or without hysterectomy or rectal, segmental, or shaving rectosigmoidectomy were included, providing an overview of all patients who require surgical therapy.

Based on the results obtained and analyzed, surgery offers a good prognosis for improving the quality of life of women with endometriosis, and it is justified to relieve the suffering, limitations of daily activities, and anxiety and depression that affect patients with endometriosis66 Laganà AS, Rosa VL, Rapisarda AMC, Valenti G, Sapia F, Chiofalo B, et al. Anxiety and depression in patients with endometriosis: impact and management challenges. Int J Womens Health. 2017;9:323-30. https://doi.org/10.2147/IJWH.S119729
https://doi.org/10.2147/IJWH.S119729...
.

In conclusion, when indicated for women with endometriosis, surgery generally improves their quality of life in several areas analyzed by the EHP-30 questionnaire.

  • Funding: none.

REFERENCES

  • 1
    Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, et al. World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod. 2017;32(2):315-24. https://doi.org/10.1093/humrep/dew293
    » https://doi.org/10.1093/humrep/dew293
  • 2
    Chapron C, Marcellin L, Borghese B, Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666-82. https://doi.org/10.1038/s41574-019-0245-z
    » https://doi.org/10.1038/s41574-019-0245-z
  • 3
    Parasar P, Ozcan P, Terry KL. Endometriosis: epidemiology, diagnosis and clinical management. Curr Obstet Gynecol Rep. 2017;6(1):34-41. https://doi.org/10.1007/s13669-017-0187-1
    » https://doi.org/10.1007/s13669-017-0187-1
  • 4
    Gordts S, Koninckx P, Brosens I. Pathogenesis of deep endometriosis. Fertil Steril. 2017;108(6):872-85.e1. https://doi.org/10.1016/j.fertnstert.2017.08.036
    » https://doi.org/10.1016/j.fertnstert.2017.08.036
  • 5
    Soto E, Luu TH, Liu X, Magrina JF, Wasson MN, Einarsson JI, et al. Laparoscopy vs. robotic surgery for endometriosis (LAROSE): a multicenter, randomized, controlled trial. Fertil Steril. 2017;107(4):996-1002.e3. https://doi.org/10.1016/j.fertnstert.2016.12.033
    » https://doi.org/10.1016/j.fertnstert.2016.12.033
  • 6
    Laganà AS, Rosa VL, Rapisarda AMC, Valenti G, Sapia F, Chiofalo B, et al. Anxiety and depression in patients with endometriosis: impact and management challenges. Int J Womens Health. 2017;9:323-30. https://doi.org/10.2147/IJWH.S119729
    » https://doi.org/10.2147/IJWH.S119729
  • 7
    Jones G, Kennedy S, Barnard A, Wong J, Jenkinson C. Development of an endometriosis quality-of-life instrument: the endometriosis health profile-30. Obstet Gynecol. 2001;98(2):258-64. https://doi.org/10.1016/s0029-7844(01)01433-8
    » https://doi.org/10.1016/s0029-7844(01)01433-8
  • 8
    Mengarda CV, Passos EP, Picon P, Costa AF, Picon PD. Validation of Brazilian Portuguese version of quality of life questionnaire for women with endometriosis (Endometriosis Health Profile Questionnaire--EHP-30). Rev Bras Ginecol Obstet. 2008;30(8):384-92. https://doi.org/10.1590/s0100-72032008000800003
    » https://doi.org/10.1590/s0100-72032008000800003
  • 9
    Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98(3):564-71. https://doi.org/10.1016/j.fertnstert.2012.07.1061
    » https://doi.org/10.1016/j.fertnstert.2012.07.1061
  • 10
    Working group of ESGE, ESHRE and WES. Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis †‡¶. Facts Views Vis Obgyn. 2020;11(4):269-97. PMID: 32322824
  • 11
    Working group of ESGE, ESHRE and WES, Saridogan E, Becker CM, Feki A, Grimbizis GF, Hummelshoj L, et al. Recommendations for the surgical treatment of endometriosis. Part 1: ovarian endometrioma. Hum Reprod Open. 2017;2017(4):hox016. https://doi.org/10.1093/hropen/hox016
    » https://doi.org/10.1093/hropen/hox016
  • 12
    Römer T. Long-term treatment of endometriosis with dienogest: retrospective analysis of efficacy and safety in clinical practice. Arch Gynecol Obstet. 2018;298(4):747-53. https://doi.org/10.1007/s00404-018-4864-8
    » https://doi.org/10.1007/s00404-018-4864-8
  • 13
    Souza CA, Oliveira LM, Scheffel C, Genro VK, Rosa V, Chaves MF, et al. Quality of life associated to chronic pelvic pain is independent of endometriosis diagnosis--a cross-sectional survey. Health Qual Life Outcomes. 2011;9:41. https://doi.org/10.1186/1477-7525-9-41
    » https://doi.org/10.1186/1477-7525-9-41
  • 14
    Vercellini P, Frattaruolo MP, Somigliana E, Jones GL, Consonni D, Alberico D, et al. Surgical versus low-dose progestin treatment for endometriosis-associated severe deep dyspareunia II: effect on sexual functioning, psychological status and health-related quality of life. Hum Reprod. 2013;28(5):1221-30. https://doi.org/10.1093/humrep/det041
    » https://doi.org/10.1093/humrep/det041
  • 15
    Kent A, Shakir F, Rockall T, Haines P, Pearson C, Rae-Mitchell W, et al. Laparoscopic surgery for severe rectovaginal endometriosis compromising the bowel: a prospective cohort study. J Minim Invasive Gynecol. 2016;23(4):526-34. https://doi.org/10.1016/j.jmig.2015.12.006
    » https://doi.org/10.1016/j.jmig.2015.12.006
  • 16
    Meuleman C, Tomassetti C, Wolthuis A, Cleynenbreugel B, Laenen A, Penninckx F, et al. Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study. Ann Surg. 2014;259(3):522-31. https://doi.org/10.1097/SLA.0b013e31828dfc5c
    » https://doi.org/10.1097/SLA.0b013e31828dfc5c
  • 17
    Turco LC, Scaldaferri F, Chiantera V, Cianci S, Ercoli A, Fagotti A, et al. Long-term evaluation of quality of life and gastrointestinal well-being after segmental colo-rectal resection for deep infiltrating endometriosis (ENDO-RESECT QoL). Arch Gynecol Obstet. 2020;301(1):217-28. https://doi.org/10.1007/s00404-019-05382-8
    » https://doi.org/10.1007/s00404-019-05382-8
  • 18
    Tan BK, Maillou K, Mathur RS, Prentice A. A retrospective review of patient-reported outcomes on the impact on quality of life in patients undergoing total abdominal hysterectomy and bilateral salpingo-oophorectomy for endometriosis. Eur J Obstet Gynecol Reprod Biol. 2013;170(2):533-8. https://doi.org/10.1016/j.ejogrb.2013.07.030
    » https://doi.org/10.1016/j.ejogrb.2013.07.030
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Publication Dates

  • Publication in this collection
    14 Aug 2023
  • Date of issue
    2023

History

  • Received
    15 Mar 2023
  • Accepted
    21 May 2023
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