Epidemiology of Endometriosis Awareness in Turkey

Endometriosis is an estrogen-dependent, chronic, inflammatory disease diagnosed with the presence of endometrial glands and/or stroma outside the uterine cavity [ 1 ]. Beside from its physical effects, it can alter the quality of life, mental health, relationships, and sexuality. Around 10% of women will develop it at some point in their lives, and it typically affects them from menarche through menopause [ 2 ]. This chronic disease may affect all organ systems and may cause organ-related symptoms, including dysmenorrhea, dyspareunia, chronic fatigue, chronic pelvic pain, and subfertility, while only 20-25% of endometriosis carriers are asymptomatic. For patients with infertility, endometriosis prevalence increases by up to 30%, and for those with chronic pelvic pain, the prevalence increases by up to 45% [ 3 , 4 ]. Moreover, the delay in the diagnosis of endometriosis causes a loss of labor, a decrease in productivity, and excessive costs [ 5 ]. Most cases go undiagnosed due to the need for laparoscopy as the gold standard method for diagnosis, and not all cases have the opportunity for proper laparoscopic diagnosis. As expected, for all these reasons, the actual incidence of endometriosis in the population, including developed countries, is not known, and frequency studies are not adequate [ 6 ]. Previous studies from developed countries show women with endometriosis have lower annual incomes and higher short- or long-term workforce loss [ 7 , 8 ]. Furthermore, according to an Aotearoa New Zealand web-based survey, the education of 27% of school students is disrupted due to endometriosis-related symptoms. In addition, studies show that almost six years of delayed diagnosis contribute to 60% of lost productivity among endometriosis carriers [ 4 , 9 ]. There is a paucity of information about the prevalence of endometriosis in developing countries. This current study aims to evaluate the prevalence of endometriosis in Turkey and the impact of related symptoms on social, professional, medical, and daily life.

A total of 16,304 surveys were completed, with 15,673 being included in the study. A total of 631 surveys were excluded due to incomplete data, participation from outside Turkey (foreign countries), and not being between 18 and 50 years old. Also, patients who reported being diagnosed with endometriosis but without a confirmed histologic diagnosis (256 participants) were excluded. The average age of responders was 30 years. Istanbul had the most respondents, followed by Ankara, Izmir, Bursa, and Antalya. There was a strong positive correlation between the distribution of respondents by province and the population of cities according to the Turkish Statistical Institute (Spearman's correlation coefficient = 0.81, p = 0.001) (Figure 1 ). Original figure. This survey had 15,673 participants, and 2880 (18.3%) were diagnosed with endometriosis. The mean number of days of menstrual cramps differed significantly between the two groups (p < 0.001). The average number of days of menstrual cramps was 2.7 ± 1.9 days for endometriosis participants and 2.1 ± 1.6 days for non-endometriosis participants. While 30.2% of endometriosis individuals reported menstrual cramps lasting three to six days, 3.1% of participants reported menstrual cramps lasting more than seven days. However, the percentage of individuals in the non-endometriosis group who had stated menstrual cramps lasted three to six days and lasted more than seven days were 20.3% and 2.5%, respectively (p < 0.05). Furthermore, there was a significant difference in the duration of menstruation and the number of pads used during menstruation (4.5 ± 2.1 days and 3.9 ± 1.8 pads vs. 3.9 ± 1.7 days and 2.8 ± 1.5 pads, respectively) (p < 0.001). The percentage of participants with endometriosis (1.3%) who reported quitting work/school due to pain was statistically higher than the non-endometriosis population (0.6%) (p = 0.001). The average number of working days lost per month by endometriosis and non-endometriosis participants was 1.3 ± 0.6 and 1.1 ± 0.7, respectively (p = 0.001). Among those diagnosed with endometriosis (2880 participants, 18.3%), 38 (1.3%) reported being unable to work owing to menstrual and/or continuous pain, while only 0.6% reported taking the day off for menstrual pain in the population with no surgical endometriosis diagnosis (p = 0.001) (Table 1 ). * Mean ± standard deviation. When endometriosis surgeries were questioned, 14% of participants with endometriosis reported having more than one endometriosis operation (Figure 2 ). Impact of endometriosis The proportion with difficulty getting pregnant was significantly higher in endometriosis patients (33.6 vs. 12.4%, p = 0.001). Brown spotting outside the menstrual cycle was significantly more common in endometriosis respondents (46.4 vs. 31.6, p = 0.001). Respondents with endometriosis reported urinary, neurological, and gastrointestinal disorders at statistically higher rates when compared to individuals without endometriosis diagnosis (54.2%, 84.5%, and 89.9% vs. 37.2%, 75.5%, and 81.1%, respectively; p = 0.001). Most respondents in both groups (73.4% of respondents with endometriosis and 66.1% without endometriosis) reported that abdominal bloating was the main gastrointestinal problem. Most respondents with endometriosis (80.1%) reported persistent fatigue, whereas only 59.5% of respondents without endometriosis reported fatigue as a problem. When asked, 21.2% of endometriosis participants reported feeling socially isolated related to their condition (p = 0.001) (Table 2 ). * Mean ± standard deviation. According to 1820 (63.2%) participants with endometriosis, people did not believe their pain or symptoms. The average number of physician visits was four before diagnosis. The average duration from symptom onset and initial attendance visiting a clinician was eight months (IQR = 2-24 months). In patients with endometriosis, the average period between the initial hospital attendance and the diagnosis was four years (IQR = 1-5 years). Most participants with endometriosis (77.9%) experienced financial difficulties due to their therapy. A total of 1152 individuals with endometriosis reported work/school difficulties (28.3%), and 224 (7.4%) respondents could not attend class/work due to endometriosis-related symptoms. In addition, most respondents with endometriosis (46.0%) reported problems in personal relationships. The survey showed that the most common symptom that caused hospital attendance in the beginning was a complaint happening during the menstrual period, and persistent groin pain was the next most-common complaint. Painkillers were the most commonly used medical treatment for respondents with endometriosis (73.3%), while 15% needed more than three treatment options. The majority of respondents with endometriosis (66.9%) had at least one additional disease (Table 3 ). Data on symptoms caused by endometriosis are summarized in Figures 3 - 5 . * Median (IQR).

According to our knowledge, this is the first high-attendee survey study to question the prevalence of endometriosis in Turkey. Studies from different regions of the world report that approximately one in seven or 10 women are diagnosed with endometriosis. The current study based on self-reported data revealed one in six of all women of reproductive age in Turkey has an endometriosis diagnosis. In this study, the numbers of the participants according to cities were correlated with the demographic distribution of populations in the cities according to data from the Turkish Statistics Institute [ 12 ]. This survey showed that most women with endometriosis differ from healthy women in terms of general health conditions, daily quality of life, personal relationship issues, and working and educational difficulties. The most frequent complaints at the time of diagnosis were cyclic menstrual problems and persistent groin pain. Participants with a diagnosis of endometriosis stated they had painful menstrual days, more days of heavy bleeding, and sanitary pad numbers used during each menstruation with statistically significant higher numbers. According to a recent study about menstrual health and costs for Turkish women, around 77% reported difficulty reaching menstrual products [ 13 ]. Thus, when including social and financial parameters about women with endometriosis, even this little step is something that must be dealt with. According to the study findings, women with endometriosis quit work and school due to being unable to manage pain, with 1.3% of participants with endometriosis stating that they could not work due to menstrual pain, while this rate was 0.6% in the undiagnosed group. In a study conducted in New Zealand, over 70% of respondents mentioned alterations in their employment status, such as losing their jobs, changing their profession, or reducing their working hours due to endometriosis-related symptoms [ 5 ]. In a study conducted on 931 women, 16% of participants declared that they had missed time in education due to endometriosis symptoms, and in their working careers, 48% had missed hours and 11% had lost their jobs [ 14 ]. As cultural variations might cause the differences in percentages, the loss of productivity is still two times higher in endometriosis patients when compared to the rest of the population. There was a significant increase in symptoms for women with endometriosis, including difficulty getting pregnant, heavy bleeding, urinary disorders, migraines and peripheral nerve pain, and gastrointestinal complaints such as gas and bloating. Along with menstrual pain, bowel complaints, sexual intercourse problems, and persistent fatigue were the leading problems at the time of diagnosis. In a survey-based study conducted in the United States of America (USA), similar to the current results, the respondents revealed the most common symptoms were pelvic pain, gastrointestinal symptoms, fatigue, anxiety, and stress [ 15 ]. The rate of fatigue in the endometriosis population was 80.1%, which is very high when compared to the worldwide rate of 2.83% [ 16 , 17 ]. A study analyzing endometriosis-related complaints among Polish women found that pain and infertility were the most common symptoms [ 18 ]. In a study of the Israeli population, the incidence of infertility was reported as 36.9% while it was 33.6% in the current study, which is also consistent with the difficulty conceiving rates for women with endometriosis globally [ 19 , 20 ]. When it comes to infertility, pain causing partners to avoid intercourse should also be considered, along with endometriosis-related infertility mechanisms [ 21 ]. Also when analyzed together, it can be seen that not only menstruation-related symptoms are associated with endometriosis; thus, healthcare providers should be educated about possible relationships between general health problems and endometriosis. In addition to physical problems, the social lives of women were also obstructed. With rates varying between 20% and 30%, the participants reported problems with their work/school life, partners, or children. Most importantly, 21.2% reported feeling socially excluded and 63.2% stated they were not believed about their complaints by their friends or family members, which is similar to results reported from Western countries [ 22 ]. The costs of endometriosis treatments have always been a topic of interest for studies all around the world. In a review questioning the economic burden of endometriosis, the authors found there were indirect costs related to absenteeism and presenteeism (lost productivity at work) [ 15 ]. In the current study, 77.9% of women with endometriosis reported that treatment costs burdened their budget, which included at least four doctor visits until diagnosis, an average of four years of delay until diagnosis, and loss of productivity. Additionally, 66.9% of women diagnosed with endometriosis stated they had at least one more medical condition, which means additional costs. These results are in parallel with the endometriosis burden in the USA and Australia [ 23 , 24 ]. Thus, provisions in healthcare policies, insurance coverage, and business plans are urgently required. This study is a pioneering study in which not only participants with a diagnosis of endometriosis but also Turkish women without diagnosis reported complaints related to menstruation, and comparisons were made between the two groups. It is also a pioneering study among examples worldwide due to the number of participants and statistically reliable results. The limitations of the current study firstly come from obtaining self-reported data. Also, due to the fact that endometriosis can only currently be diagnosed by being aware of symptoms, finding appropriate healthcare, and having surgery, there may be undiagnosed cases that remain in the non-endometriosis group. Third, while nurses working with family medicine specialists in rural areas also shared the surveys, some responses were obtained through online social media platforms, and there may be sample bias related to social media interests since social media may not be as widely used by the 40-50 age group. Fourth, while the study was designed to determine the current prevalence of the disease in Turkey reaching as many people as possible and, additionally, the results were consistent with national demographic statistics, still the subjects were not randomized. The survey used was a version of the WERF EndoCost tool, but it was not validated for the Turkish language.

Endometriosis is a chronic, underestimated disease that affects at least 18% of Turkish women of reproductive age. Despite all the efforts and attempts to raise awareness about gender equality, the social and physical health of women with endometriosis is still depleted. There is a need for guidelines to inform healthcare providers, population professionals, and patients. This will not only provide a good quality of life but also will ensure the opportunity for new scientific studies about the diagnosis and treatment of the disease. Societies and governmental health sources must work together to resolve this public health problem.

Endometriosis-related problems were surveyed in this cross-sectional analysis. For this purpose, the World Endometriosis Research Foundation (WERF) EndoCost tool was utilized [ 10 ]. However, it was altered to be used with a Turkish demographic and healthcare background, and the survey was sent to applicants through Google Forms (Google, Mountain View, CA) [ 11 ]. The ethical approval has been taken from Istanbul Medipol University Ethics Committee (E-10840098-772.02-4247). The primary method of recruitment was dissemination using social media platforms (Facebook and Instagram), including social media accounts of influencers who have followers from all over the country, accounts of authors and women’s support organizations, and countywide student clubs in universities, and by delivering to regions by nurses working in family medicine all around the country. The online information and a consent sheet were given on the first page of the survey. The survey was open for 10 weeks, from September 15, 2022, to November 2022. Participants who reported a histopathologic diagnosis of endometriosis on the questionnaire form were included in the endometriosis group. Exclusion criteria for responders were not being 18-50 years old, incompletely filling the questionnaires, participating from outside Turkey (foreign countries), or being diagnosed only by gynecologic examination or ultrasound but without a histological diagnosis. Because this survey was meant to identify the prevalence of symptoms and women with endometriosis diagnosis rather than test a hypothesis, a power analysis was not conducted. Statistical analyses The Statistical Package for the Social Sciences (SPSS) version 20 program (IBM Corp., Armonk, NY) was used for statistical analysis. Normality distribution was evaluated by the Kolmogorov-Smirnov test. Data were described using mean and standard deviation, medians, and interquartile ranges. Categorical values and proportions are expressed as percentages and were compared using the chi-square test or Fisher's exact test between groups. Pearson's and Spearman's rank correlations were used to evaluate the relationship between the participants and the population of cities.