The Relation between Patient-Centered Care and Quality of Life in Women with Endometriosis

Objective: The objective of this study was to examine the hypothesis that experiences with patient-centered endometriosis care are related to the endometriosis-specific quality of life dimensions “emotional well-being” and “social support.” Design: A secondary regression analysis of two cross-sectional studies was conducted. Participants/Materials: In total, data from 300 women were eligible for analysis. The participating women all had surgically proven endometriosis. Setting: The study was conducted in one secondary and two tertiary endometriosis clinics in the Netherlands. Questionnaires were disseminated between 2011 and 2016. Methods: Both included studies investigated patient-centeredness of endometriosis care and endometriosis-specific quality of life using, respectively, the ENDOCARE questionnaire (ECQ) and the Endometriosis Health Profile 30 (EHP-30). To increase power, the regression analysis focused on the previously found relation between the ten dimensions of the ECQ and the EHP-30 domains “emotional well-being” and “social support” rather than all five EHP-30 domains. After the Bonferroni correction to limit type 1 errors, the adjusted p value was 0.003 (0.05/20). Results: The participating women had a mean age of 35.7 years and had predominantly been diagnosed with moderate to severe endometriosis. None of the relations between patient-centered endometriosis care and the EHP-30 domain “emotional well-being” were significant. Three dimensions of patient-centered endometriosis care proved to be significantly related to the EHP-30 domain “social support”: “information, communication, and education” (p < 0.001, beta = 0.436), “coordination and integration of care” (p = 0.001, beta = 0.307), and “emotional support and alleviation of fear and anxiety” (p = 0.002, beta = 0.259). Limitations: This cross-sectional study identified relations rather than proving causality between experiencing less patient-centeredness of care and having lower quality of life. Nevertheless, it is very tangible that some causality exists, either directly or indirectly (e.g., through empowerment) and that by improving patient-centeredness, quality of life might be improved as well. Conclusion: “Information, communication, and education”; “coordination and integration of care”; and “emotional support and alleviation of fear and anxiety” as dimensions of patient-centered endometriosis care are related to the quality of life domain “social support” of women with endometriosis. Improving the patient-centeredness of endometriosis care was already considered an important goal, but even more so given its relation with women’s quality of life, which is increasingly considered the ultimate measure of health care quality. Quality improvement projects focusing on “information, communication, and education” are expected to impact women’s quality of life the most.

investigated patient-centeredness of endometriosis care and endometriosis-specific quality of life using, respectively, the ENDOCARE questionnaire (ECQ) and the Endometriosis Health Profile 30 . To increase power, the regression analysis focused on the previously found relation between the ten dimensions of the ECQ and the EHP-30 domains "emotional well-being" and "social support" rather than all five EHP-30 domains. After the Bonferroni correction to limit type 1 errors, the adjusted p value was 0.003 (0.05/20). Results: The participating women had a mean age of 35.7 years and had predominantly been diagnosed with moderate to severe endometriosis. None of the relations between patient-centered endometriosis care and the EHP-30 domain "emotional well-being" were significant. Three dimensions of patient-centered endometriosis care proved to be significantly related to the EHP-30 domain "social support": "information, communication, karger@karger.com www.karger.com/goi and education" (p < 0.001, beta = 0.436), "coordination and integration of care" (p = 0.001, beta = 0.307), and "emotional support and alleviation of fear and anxiety" (p = 0.002, beta = 0.259). Limitations: This cross-sectional study identified relations rather than proving causality between experiencing less patient-centeredness of care and having lower quality of life. Nevertheless, it is very tangible that some causality exists, either directly or indirectly (e.g., through empowerment) and that by improving patientcenteredness, quality of life might be improved as well. Conclusion: "Information, communication, and education"; "coordination and integration of care"; and "emotional support and alleviation of fear and anxiety" as dimensions of patient-centered endometriosis care are related to the quality of life domain "social support" of women with endometriosis. Improving the patient-centeredness of endometriosis care was already considered an important goal, but even more so given its relation with women's quality of life, which is increasingly considered the ultimate measure of health care quality. Quality improvement projects focusing on "information, communication, and education" are expected to impact women's quality of life the most.

Introduction
Endometriosis is a chronic gynecological disease characterized by endometrial-like tissue growing outside the uterine cavity. Etiology of endometriosis is still not fully understood. It is generally agreed that endometriosis is a multifactorial disease with genetic and epigenetic predisposition with retrograde menstruation and endometrial stem cells being a part of the basis for pathology [1][2][3][4]. Endometriosis is related to a variety of abdominal pain complaints including dysmenorrhea, dyspareunia, dysuria, dyschezia, and chronic pelvic pain [2]. Sexual function can be impaired in women with endometriosis [5]. In addition, endometriosis may cause infertility, fatigue, and decreased work productivity as well as a diminished quality of life [6][7][8].
Health-related quality of life in women with endometriosis can be investigated using different questionnaires, including generic and endometriosis-specific tools [9].
The quality of the provided endometriosis care might impact women's quality of life. Women with endometriosis recruited from secondary care centers reported better quality of life compared to women recruited from tertiary care centers [10]. Lukas and colleagues [11] found that nearly half of about 500 surveyed women with histologically proven endometriosis were dissatisfied with their medical support, and that (lack of) information was the most distinctive indicator of satisfaction with patient experience [11].
"Patient-centeredness" is one of the dimensions of quality of care [12]. Patient-centeredness in a certain patient group can be measured by assessing specific aspects of patient experiences with health care that are proven to be important to this group. In the related field of fertility care, experiences with patient-centered care proved to be correlated with women's quality of life [13,14]. Identifying the patient-centered care dimensions that impact women's quality of life most would help endometriosis clinics in prioritizing targets for quality improvement projects. This is specifically important as more and more attention is given to improving quality of life in women with endometriosis nowadays [15]. An explorative study identified the relation between patient-centered endometriosis care and two of five endometriosis-specific quality of life domains but concluded that a more focused and adequately powered study was needed [16]. The two related quality of life domains found were "emotional well-being" and "social support." As this study was underpowered, no firm conclusions could be drawn. In order to be able to adequately investigate the hypothesis of the relation between quality of care and quality of life in women with endometriosis, the sample size should be increased. This could be performed by combining the previous study with a new data set to increase power [16,17]. This study aimed to examine the hypothesis that experiences with patient-centered endometriosis care are related to women's endometriosis-specific quality of life dimensions of "social support" and "emotional well-being."

Methods
This study is a secondary analysis of two cross-sectional studies [16][17][18] conducted in three endometriosis clinics in the Netherlands: two tertiary care centers (Amsterdam UMC, Amsterdam, and Radboud University Medical Center, Nijmegen) and one secondary care hospital (Isala Clinics, Zwolle). Exploring the data of one of the three clinics indicated that experiences with patient-centered endometriosis care seem to impact the endometriosis-specific quality of life dimensions "emotional well-being" and "social support" but lacked the power to draw firm conclusions [16]. The two studies asked Dutch speaking women with surgically proven endometriosis to complete two reliable and validated questionnaires: the Endometriosis Health Profile 30 (EHP-30) and the ENDOCARE questionnaire (ECQ) [6,[18][19][20]. The EHP-30 is a widely used health-related quality of life questionnaire that is specifically designed to investigate quality of life in women with endometriosis (Jones et al. [20]). Besides three other domains, the EHP-30 assesses the domain "emotional well-being" with six questions (e.g., "during the last 4 weeks, how often because of your endometriosis have you felt miserable?') and the domain 'social support' with four questions (e.g., "during the last 4 weeks, how often because of your endometriosis have you felt others do not understand what you are going through?'), all to be rated on a 5-point Likert scale (Jones et al. [20]). Scores per domain range from 0 to 100 with 100 reflecting the worst quality of life.
The ECQ has been validated to investigate the patientcenteredness of endometriosis care across Belgium, Sweden, and the Netherlands [18,19,21]. The ECQ includes 38 care aspects, grouped into ten dimensions of patient-centered care, to be rated on two 4-point Likert scales: one for importance and one for experienced performance [18,19]. For this paper, we calculated the "experienced performance score (EPS)," as previously done by Apers and colleagues in line with a similar study from the field of fertility [13,16]. The EPS takes account of more nuances than the previous used percentage of negative performance, dichotomizing the 4-point performance scale [18,19]. The EPS per dimension can be calculated by using the ordinal scale of its aspects (0 = agree completely, 1 = agree, 2 = disagree, 3 = disagree completely) to calculate percentages per dimension {e.g., EPS dimension1 = [(S1 + S2 + S3)/9] * 100} [13]. This results in a score from 0 to 100 with 100 reflecting the worst experience [16].

Power
Examining the relation between on the one hand 10 dimensions of patient-centered endometriosis care and on the other hand two endometriosis-specific quality of life domains using regression analysis, required a sample size of at least 200 patients (10 for each of the included variables [22]). This exceeds the minimal sample sizes for multiple regression according to Green [23] of at least 104 subjects, which increased with the amount of predictors. Combining the datasets of both studies resulted in a sample size of 300 patients, which allows detecting a small to moderate effect size corresponding to a standardized regression coefficient of 0.22 with 80% power. Calculation is based on testing using a two-sided significance level of 5% and a Bonferroni correction to account for multiple testing of 20 relations and limit type 1 errors.

Analysis
The datasets of both studies were merged. Only patients who completed >50% of both questionnaires were included. Missing data was processed as advised in the manuals of the questionnaires. First, possible confounding patient characteristics for the endometriosisspecific quality of life outcomes "emotional well-being" and "social support" were identified using univariate regression analysis as they would need to be considered when examining the relation between patient-centered care and endometriosis-specific quality of life. The regression analyses with "emotional well-being" as dependent variable had to be corrected for the following determinants: clinic, educational level, having seen other specialists for endometriosis complaints, ever been pregnant, member of patient organization, severity of endometriosis, having seen >1 gynecologist for a second opinion, and >10 GP visits before referral. The regression analyses with "social support" as a dependent variable had to be corrected for the following determinants: clinic, educational level, having seen other specialists for endometriosis complaints, ever been pregnant, having children, having ever tried to conceive >12 months, being in relationship, diagnostic delay, being a member of patient organization, severity of endometriosis, having seen >1 gynecologist for a second opinion, and >10 GP visits before referral. Next, several (n = 20) linear regression models examined the relation between on the one hand the EPS for all 10 ECQ dimensions as independent variable and on the other hand the outcomes for the two EHP-30 domains "emotional well-being" and "social support" as dependent variables, while controlling for confounders. All ECQ dimensions found to be related to the EHP-30 domain investigated were further analyzed in multivariable regression analysis. As quality of life in women with endometriosis differs between secondary and tertiary clinics, all analyses were corrected for clinic [10]. Finally, in order to limit the chance of type 1 errors, the Bonferroni correction for multiples testing was applied (α = 0.05/20 = 0.003).

Results
The characteristics of the 300 studied women are shown in Table 1. The mean age of respondents was 35.7 years; the majority reported moderate to severe endometriosis and most respondents were in an intimate partner relationship. Table 2 presents the median scores on the endometriosis-specific quality of life domains emotional well-being and social support and the median EPS on the 10 patient-centered care dimensions.

Patient-Centered Care and the QoL Domain Emotional
Well-Being No significant relation was found between one of ten dimensions of patient-centered endometriosis care and the EHP-30 domain "emotional well-being" using the regression analysis (all p ≥ 0.010, which exceeds the Bonferroni-corrected p value).
For both "emotional well-being" and "social support," the highest beta coefficient was found in relation to "information, communication, and education." Overall, the beta coefficients were higher for the relations with "social support" compared to the relations with "emotional well-being.  Schreurs et al.

Discussion
This adequately powered study confirms that experienced patient-centeredness of care is related to women's quality of life in the domain "social support." This study could not confirm the hypothesis generated by the underpowered explorative study of Apers and colleagues that patient-centered care is also related to the quality of life domain "emotional support" [16]. Of the 3 patientcentered care dimensions related to the quality of life domain social support, "information, communication, and education" is the most interesting target for quality improvement projects as it has the strongest relation with quality of life.
This study presents secondary analyses of studies originally designed to assess quality of care. If we were to have designed a study to examine the relation between patient-centered care and the quality of life domains emotional well-being and social support, we would have designed a mixed method study. Conducting a follow-up qualitative study seeking to gain in-depth understanding of the causality of the relations between patient-centered care and quality of life would be of interest. Do better experiences with certain patientcentered care dimensions result in better quality of life? Or do women who receive less social support from their family and friends rate the patientcenteredness of their clinic as lower as their needs are simply not met? It would also be interesting to examine if women from other cultures may have different social support systems and health care experiences, which affect the identified relations [24,25]. Furthermore, it would be interesting to investigate the differences in quality of life and quality of care between pre-and postmenopausal women [26]. Focusing on location of endometriosis disease (e.g., ovarian, deep infiltrating endometriosis, or adenomyosis) in correlation with quality of life and quality of care should also be a goal for future research. An important strength of the current study is its power, achieved by: (i) increasing the sample by almost threefold compared to Apers and colleagues, (ii) focusing analyses on solely two QoL domains, and (iii) applying a Bonferroni correction [16,27].
Social support is an important quality of life domain for endometriosis research, as women with endometriosis have reported to experience social isolation due to the lack of understanding from family and friends related to the social stigma associated with gynecological conditions and chronic pelvic pain [28,29]. Communication, information, and education have previously been identified as an important improvement targets for endometriosis clinics, as they are very important to patients and are often experienced negatively by patients [11,17,18,[30][31][32][33]. In the allied field of fertility care, researchers demonstrated an indirect relation between on the one hand experienced information and communication from the clinic and on the other hand The lines represent the relations between EPS and "emotional well-being" and "social support" that remain after the Bonferroni correction. patient anxiety, depression, and even intended treatment compliance via lowering treatment concerns [14,34]. One can indeed imagine that patients who are empowered by patient information have less concerns about their condition and treatment, feel better supported by clinic staff and therefore rate the social support domain of their quality of life as better.
Improving quality of life in women with endometriosis should be the main treatment goal when deciding on endometriosis treatment. Newly introduced endometriosis treatments should be investigated primarily for their effect on quality of life. Moreover, focusing on improving sexuality as one of the aspects of quality of life should be a goal for the future [35,36]. As endometriosis does not only alter quality of life in women with endometriosis but also affects quality of life in their partners, it would be interesting if future research would take this into account when investigating improvement strategies for quality of life [37,38].
In conclusion, improving the patient-centeredness of endometriosis clinics was already considered an important improvement target and should now be even more so given its relation with women's quality of life, which is increasingly considered the ultimate measure of health care quality [15]. When resources are limited, focusing first on improving information, communication, and education to lower women's concerns about their condition and treatment is advised as it is expected to improve women's quality of life, besides improving their health care experience.

Statement of Ethics
An ethics statement is not applicable for this study as it is a secondary analysis based on published data. Primary studies were approved in their respective clinics. Apers et al. (2018): Ethical Review Board of the Radboud University Medical Center, Nijmegen, The Netherlands. Schreurs et al. (2020): Ethical Review Board of the Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands. Consent to participate was based on responses to the questionnaire, therefore no written informed consent was obtained from participants as discussed with the Ethical Review Boards.