{"paper_id":"cb7e682d-8051-4fad-af99-9471b55087a7","body_text":"Vol.:(0123456789)1 3\nQuality of Life Research (2020) 29:19–36 \nhttps://doi.org/10.1007/s11136-019-02326-2\nREVIEW\nHealth‑related quality‑of‑life among patients with premature ovarian \ninsufficiency: a systematic review and meta‑analysis\nX. T. Li1 · P . Y . Li2 · Y . Liu1 · H. S. Yang3 · L. Y . He1 · Y . G. Fang3 · J. Liu1 · B. Y . Liu1 · J. E. Chaplin2 \nAccepted: 1 October 2019 / Published online: 16 October 2019 \n© The Author(s) 2019\nAbstract\nPurpose To systematically review studies investigating health-related quality-of-life (HrQoL) in patients with premature \novarian insufficiency (POI), to examine questionnaires used and to conduct a meta-analysis of control studies with normal \novarian function.\nMethods Data sources: PubMed, Embase, Web of science, CNKI, and CQVIP, searched from inception until June 2018. \nThe search strategy was a combination of medical (e.g. POI), subjective (e.g. well-being) and methodological (e.g. ques-\ntionnaires) keywords. PRISMA guidelines were used to assess outcome data quality/validity by one reviewer, verified by a \nsecond reviewer. Risk of bias within studies was evaluated. A meta-analysis compared HrQoL in patients and non-patients. \nDue to measurement differences in the studies, the effect size was calculated as standard mean difference.\nResults We identified 6869 HrQoL studies. Nineteen geographically diverse studies met inclusion criteria, dated from \n2006, using 23 questionnaires. The meta-analysis included six studies with 645 POI participants (age 33.3 ± 5.47) and \n492 normal-ovarian control subjects (age 32.87 ± 5.61). Medium effect sizes were found for lower overall HrQoL (pooled \nSMD = − 0.73, 95% CI − 0.94, − 0.51; I\n2 = 54%) and physical function (pooled SMD = − 0.54, 95% CI − 0.69, − 0.39; \nI2 = 55%). Heterogeneity was investigated. Effect sizes varied for sexual function depending on the measure (SMD = − 0.27 \nto −  0.74), overall HrQoL (SF-36) had the largest effect size (−  0.93) in one study. The effect sizes for psychological and \nsocial HrQoL were small.\nConclusion POI is associated with low-to-medium effect size on HrQoL compared to normal ovarian controls. The greatest \neffects are found in general HrQoL and most sexual function areas. Condition-specific questionnaires and RCTs are recom-\nmended for further investigation.\nKeywords Surveys and questionnaires · Menstruation disturbance · Gynaecology · Women’s health\nAbbreviations\nCAMS-R  The Cognitive and Affective Mindful-\nness Scale V Revised\nCES-D  Epidemiologic Studies Depression \nScale\nDHEA  Dehydroepiandrosterone\nDISF-SR  Derogatis Interview for Sexual Func-\ntion—Female Version\nDOR  Diminished ovarian reserve\nDSM-IV (SCID)  Diagnostic and Statistical Manual of \nMental Disorders (fourth edition)\nFACIT-Sp-12  Functional Assessment of Chronic Ill-\nness Therapy—Spiritual Well-Being \nScale\nFACIT-Sp-Ex  Functional Assessment of Chronic Ill-\nness Therapy—Spiritual Well-Being \nScale Expanded\nElectronic supplementary material The online version of this \narticle (https ://doi.org/10.1007/s1113 6-019-02326 -2) contains \nsupplementary material, which is available to authorized users.\n * B. Y. Liu \n baoyanjournal@163.com\n1 Institute of Basic Research in Clinical Medicine, China \nAcademy of Chinese Medical Sciences, Beijing, China\n2 Department of Pediatrics, The Queen Silvia Children’s \nHospital, Institute of Clinical Sciences, Sahlgrenska \nAcademy, University of Gothenburg, 416 85 Gothenburg, \nSweden\n3 Institute of Acupuncture and Moxibustion, China Academy \nof Chinese Medical Sciences, Beijing, China\n\n20 Quality of Life Research (2020) 29:19–36\n1 3\nFANLTC  Functional Assessment of Non-Life-\nThreatening Conditions\nFertiQoL  International Fertility Quality of Life \nQuestionnaire\nFSFI  Female Sexual Function Index\nFSH  Follicle-Stimulating Hormone\nGCS  Greene Climacteric Scale\nHrQoL  Health-related quality of life\nHRT  Hormone replacement therapy\nIHD  Ischaemic heart disease\nLEU  Life events scale\nNOS  Newcastle–Ottawa Scale\nPANAS  Positive and Negative Affect Schedule\nPCOS  Polycystic ovarian syndrome\nPM  The Pearlin Mastery Scale\nPOF  Premature ovarian failure\nPOI  Premature ovarian insufficiency\nPOR  Poor ovarian responders\nPRQ85  Personal Resource Questionnaire 1985\nQOL  Quality of life\nSF-36  The 36-Item Short Form Survey from \nthe RAND Medical Outcomes Study\nSMD  Standard Mean Difference\nSPEQ  Sexual Personal Experiences \nQuestionnaire\nSTAI  State-Trait Anxiety Inventory\nTABP/TCBP  Type A/C behavior pattern\nTCM  Traditional Chinese Medicine\nWHOQoL-BREF  World Health Organization Quality of \nLife\nYMA  Young Menopause Assessment\nIntroduction\nThanks to medical advances, the living condition of \nwomen with premature ovarian insufficiency (POI) has \ngained more attention in recent years [1 ]. POI is a clinical \nsyndrome defined by loss of ovarian activity before the \nage of 40, associated with menstrual disturbance, raised \ngonadotropins and low estradiol [2 ]. Although proper \ndiagnostic accuracy in POI is lacking, the European Soci-\nety of Human Reproduction and Embryology (ESHRE) \nhas developed guidelines on management of women with \npremature ovarian insufficiency [2 ] in which they recom-\nmend the following diagnostic criteria for POI: (i) oligo/\namenorrhea for at least 4 months, and (ii) an elevated \nFSH level > 25 IU/l on two occasions > 4 weeks apart. \nThe nomenclature has changed over the years and POI has \nbeen referred to as premature ovarian failure, premature \nmenopause, and premature ovarian dysfunction [3 ]. Ear-\nlier studies often used the term premature ovarian failure \n(POF) and more recent articles have used POI. It should \nalso be noted that in POI serum follicle-stimulating hor -\nmone (FSH) levels are often found to exceed the diag-\nnostic definition in studies of POI and are noted in sev -\neral studies to be above 40 IU/L [2 –4]. An earlier study \nreported the prevalence of POI in women under 30 years \nold estimated to be 0.1%, while the incidence of meno-\npause in women before the age of 40 is approximately 1% \n[5]. In recent years, studies have investigated the prev -\nalence of patients with POI in different countries. For \nexample, one article reported a higher prevalence (1.9%; \n95% CI 1.7–2.1) of POI in women before the age of 40 in \nSweden [6 ] and another article reported 0.91% (95% CI \n0.81–1.02%) in Estonia [7 ]. There has been a long-stand-\ning confusion over the various terms such as poor ovar -\nian responders (POR), premature menopause and dimin-\nished ovarian reserve (DOR) [2 , 3, 8, 9]. It is important \nto distinguish these conditions from POI because women \nwith POI face more challenges than diminished fertil-\nity, and have different management needs [2 , 10]. Only \n5–10% of women with POI may be able to spontaneously \nconceive and deliver a child [11]. In addition, women \nwith POI suffer from amenorrhea-related symptoms [12] \npsychological problems [13, 14], increased risk to car -\ndiovascular health [15, 16] and to bone health [17]. POI \nis a condition that is influenced by genitourinary and \nsexual function [18] and neurological dysfunction [19] \nin both the short- and long-term and can lead to prema-\nture death [20]. The best option to relieve symptoms and \nprotect POI patients against serious morbidity related to \nprolonged estrogen deficiency is hormone replacement \ntherapy (HRT). However, HRT is just a mimic of normal \nphysiological endocrinology, which has no evidence to \nimprove the ovary function [2 ]. Consequently, patients \nwith POI are at risk of poor health quality despite avail-\nable treatment options. Quality of life (QoL) is a broad \nmultidimensional concept that usually includes subjective \nevaluations of both positive and negative aspects of life \n[21]. While, health-related quality of life (HrQoL) focus \non the effects of a disease on an individual’s health and its \ntreatment [22– 25] encompassing physical, psychological, \nand social functioning [23, 26] and presents an avenue \nfor the evaluation of the consequences of experienc-\ning premature ovarian insufficiency. This review aimed \nto investigate studies of women with POI, which have \nincluded measures of HrQoL, in order to evaluate effect \nsizes and in addition to identify the measurement instru-\nments used. A meta-analysis was conducted of the studies \nthat reached quality standards and which compared the \nHrQoL outcomes among patients with POI with a control \ngroup consisting of normal ovary function women.\n\n21Quality of Life Research (2020) 29:19–36 \n1 3\nMaterials and methods\nThis study followed the Preferred Reporting Items for Sys-\ntematic Reviews and Meta-analyses (PRISMA) [27] report-\ning guideline (Online Resource ESM_1). A submission to \nthe ethics committee of the Clinical Basic Medicine Insti-\ntute, China Academy of Chinese Medical Sciences was \nsought. The Ethics committee judged that ethical approval \nwas not required for this research (ref 2019/1).\nSearch strategy and data selection\nAn electronic search of the six databases was undertaken \nfrom database inception to June 2018. PubMed/MEDLINE \nand ‘Web of science’ provided a broad coverage of the bio-\nmedical literature, including reproductive biology and clini-\ncal medicine. EMBASE was included because it has greater \ncoverage of European and non-English language publica -\ntions and topics such as alternative medicine. China National \nKnowledge Infrastructure (CNKI), WanFang database and \nChongqing VIP information (CQVIP) were included to \nensure that no Asian publications were missed. Searches \nwere conducted without restrictions with respect to publica-\ntion year, language, type or setting of study or accessibility \nto full-text articles. A combination of keywords and database \nspecific terms was used (premature ovarian insufficiency OR \npremature ovarian failure OR diminished ovarian reserve \nOR poor ovarian response OR premature menopause OR \nhyper-gonadotropic hypogonadism OR elevated gonado-\ntrophins OR triad of amenorrhea OR estrogen deficiency) \nAND (well-being OR health outcome OR quality-of-life \nOR health-related quality of life) AND (questionnaire OR \ninstrument OR patient reported outcome). Strategies differed \nin the different databases depending upon the information \nstructures. The details of the different search strategies are \nprovided in the online resource materials (online resource \nESM_2). The process of article selection is outlined in Fig. 1 \nwith a description of predefined criteria for selection. One \nauthor (XT Li) was mainly responsible for screening the \ntitles and abstracts. Articles identified were independently \nread and discussed with two more authors (HS Yang, PY Li) \nto ensure an unbiased selection. Some studies of post-men-\nopause have used instruments such as the MSQOL [28, 29] \nhowever this is not a measure of subjective quality-of-life \nand was therefore not included in this review. No additional \narticles were identified through the manual search. Stud -\nies describing the construction and validity of the HrQoL \nquestionnaires used in the studies were also evaluated. If \ninformation on construction and validity was sparse, contact \nwas attempted with the author responsible for the develop-\nment of the questionnaire.\nCriteria to select articles\nThe inclusion criteria for empirical investigation studies of \nadults with POI was that HrQoL was a primary or second-\nary outcome. Studies with participants from hospitals and \nlong-term care facilities or with specific conditions (e.g. \nTurner syndrome or anorexia) or where abstracts only were \nfound were included in the literature in order to be able to \nextract data on the questionnaires used but excluded from \nthe meta-analysis. No restrictions were placed on the geo-\ngraphic, soioeconoimic or ethinic backgrounds of any of the \nparticipants. There was no restriction in terms of treatment, \nboth randomized and non-randomized trials were included. \nExclusion criteria for the systematic review were duplicate \npublications or reviews, studies that did not include out-\ncomes from a HrQoL questionnaire. Exclusion criteria for \nthe meta-analysis were articles which lacked relevant data \nfor investigation and studies without a normal ovary func-\ntion control group.\nCritical appraisal: assessment of bias \nin the studies\nThe quality of eligible articles was assessed at the study \nlevel using the Newcastle–Ottawa Scale (NOS) for nonrand-\nomized cohort studies [30]. Each article was awarded a ‘star’ \nor score out of four for selection bias, two for comparability \nand three for bias in the outcome assessment, with a maxi-\nmum total score of nine points. The NOS score was used \nto assess differences in study quality scores > 6 high; 4–6 \nmedium, < 4 low [31]. The scoring system and evaluation \nis provided in the Online Resource ESM_3. Two authors \n(XT Li, PY Li) independently evaluated the findings of each \nstudy to ensure an unbiased assessment.\nMeta‑analysis\nA meta-analysis investigated the outcome of HrQoL in \npatients with POI compared with a normal ovary func -\ntion reference population. Review Manager (Version 5.3. \nCopenhagen: The Nordic Cochrane Centre, The Cochrane \nCollaboration, 2014) was used. The estimated value and \n95% confidence interval (95% CI) of the effect size was \ncalculated by Standard Mean Difference (SMD) [ 32]. The \nSMD is used as a summary statistic in meta-analysis when \nthe studies all assess the same outcome but measure it in a \nvariety of ways [33]. Cohen [34] suggested that d = 0.2 be \nconsidered a ‘small’ effect size, 0.5 represents a ‘medium’ \neffect size and 0.8 a ‘large’ effect size. The size of hetero -\ngeneity among studies after combination was determined \nvia I\n2 statistic: 0% to 40%: might not be important; 30% to \n\n22 Quality of Life Research (2020) 29:19–36\n1 3\n60%: may represent moderate heterogeneity; 50% to 90%: \nmay represent substantial heterogeneity; 75% to 100%: \nconsiderable heterogeneity [35]. If there was no hetero-\ngeneity among studies, a fixed effects model was applied \nfor meta-analysis; if there was statistical heterogeneity, \nthe sources of heterogeneity were further analyzed, and \na random effects model was adopted for meta-analysis. \nAccording to the same questionnaires used and same \nFig. 1  The article selection \nprocess and criteria for selection \nfor the literature review and \nmeta-analysis\n\n\n23Quality of Life Research (2020) 29:19–36 \n1 3\nspecific domain evaluated, the effect sizes were divided \ninto subgroups. This systematic review and meta-analysis \nwere performed and reported according to the PRISMA \nguidelines. The PRISMA checklist is included as Online \nResource_3.\nResults\nThirty-four studies matched the inclusion criteria and were \nincluded for review. Fifteen articles were related to treatment \nevaluation while 19 articles examined elements of HrQoL \n(Tables  1, 2). In five of these studies only the abstracts were \navailable for examination [36– 40]. These articles were all \npublished between 2006 and 2018. Eighteen articles were \ncross-sectional studies [36– 53] two of which included \ncase–controls [43, 51]. One article reported only case–con-\ntrol data [54]. Nine articles described HrQoL among patients \nwith the nomenclature of POI [36, 39, 40, 42, 47, 49, 51–53] \nand ten articles described HrQoL among patients with the \nprevious nomenclature of POF [37 , 38, 41, 43–46, 48, 50, \n54]. Thirteen articles had control groups [39–46, 48, 49, 51, \n53, 54] and nine of these had a control group of women with \nnormal ovarian function [41–46, 51, 53, 54], six of these had \nsufficient information to be included in the meta-analysis \n[41–45, 54]. None of the studies used proxy-reports from \nfamily members as part of the evaluation. Reported stud-\nies had varying sample sizes; the largest sample size was \n340 women [46]. The studies were geographically diverse \nincluding China [41, 44–46], UK [37, 38, 50], America [36, \n39, 40, 42, 49, 51–53], Brazil [43, 54], Australia [48] and \nmulti-national studies [47] (Fig.  1 and Tables  1, 2).\nDomains of HrQoL examined\nThe definition of HrQoL used in the studies is derived from \nthe domains of the questionnaires used to measure HrQoL. \nAmong the 19 articles examining HrQoL, seven studies \nincluded a measure of overall HrQoL as measured by either a \ngeneric questionnaire (SF-36, WHOQoL-BREF) [37, 43, 44, \n50, 54] or measured in relation to fertility or sexual function \n[42, 45, 50, 54]. Nine studies focused on psychiatric aspects \nincluding depression and meaning in life [36, 38–40, 49–53]. \nFour articles used the POI related symptom questionnaires \n[38, 47, 48] Only one of these [50] used a condition specific \ninstrument designed for POI (Young Menopause Assess-\nment (YMA) [50]). One study evaluated the aspect of social \nfunction: perceived social support [53]. The reduced HrQoL \namong patients with POI was mentioned in all 19 articles. A \nsummary of the studies is found in Tables  1, 2.\nOverall HrQoL\nThree articles described factors correlated with lower \nHrQoL in POI populations: one article reported that \norgasm and sexual satisfaction were correlated with all \nQOL domains [54]; a second article analysed charac-\nter traits of POI patients [45], which showed that older \npatients, with primary infertility and who had had chil-\ndren had lower HrQoL scores than patients who were of \nyounger age, secondary infertility or had previously given \nbirth. In one article [ 44] different Traditional Chinese \nMedicine (TCM) syndromes were considered as summa-\nries of symptoms of the pathogenesis of disease develop-\nment [55]. These syndromes included insufficiencies of \nliver and kidney or asthenia of both the spleen and kidney. \nIt was noted that patients with deficiency of liver and kid-\nney had the lowest overall QOL scores (Table  3).\nPhysical function and symptoms\nPhysical health of the women with POI was consistently \nreported to be significantly lower than controls. A number \nof physical function symptoms were explored including \nexperience of physical pain [43] sexual function [42, 54] \narousal, lubrication, orgasm and satisfaction, and sexual \nbehaviour/experiences [42, 50, 54]. In addition, meno-\npause symptoms such as vasomotor symptoms, mood \nswings and mental fog, hair loss, dry eyes, cold intoler -\nance, joint clicking, tingling in limbs and low blood pres-\nsure were found at a high rate in patients with POI [47].\nPsychological function and psychosocial \naspects\nWomen with spontaneous POI were reported to score \nadversely on all measures of psychological functioning [43, \n51] with higher negative feelings such as “blue mood” [56], \ndespair, anxiety, and depression or had a negative impact on \ntheir self-image and confidence [50 ]. This population also \nhad a high rate of mental health medication use and counsel-\nling [51] and a risk for depression [49]. Some articles ana-\nlysed the factors related to these negative feelings. Adverse \naffective symptoms were associated with a lower perceived \nlevel of control [39]. One article reported illness uncertainty \nand lack of purpose in life as a significant independent factor \nassociated with anxiety [51]. Scores on the Spiritual Well-\nBeing scale were also associate with POI and were found to \nreduce with increased age [52].\n\n24 Quality of Life Research (2020) 29:19–36\n1 3\nTable 1  Presentation of details of studies included in the systematic review and included in the meta-analysis\nAuthor, year [Ref]/\ncountry\nTitle Type of study Objective of the study Questionnaire [ref]/\ntype of questionnaire\nSample size/observation \ngroup (age range) and \npopulation\nControl group (size), \nmean (SD) and population\nNOS\nPang et al. 2007 [41]/\nChina\nInvestigations of person-\nality characteristics and \nmental health status in \npatients with premature \novarian failure\nCross-sectional study Analysis of personal-\nity characteristics and \nmental health status of \npatients with premature \novarian failure\nTABP/TCBP \n[57–59]/Behaviour \npattern\nN = 80 no description of \nage range\nHospital-based\nPCOS N = 80, Normal \nN = 81\nno description of age \nrange\nPopulation-based\n7 High\nKalantaridou et al. 2008 \n[42]/USA\nSexual function in young \nwomen with spontane-\nous 46, XX primary \novarian insufficiency\nCross-sectional study To assess sexual function \nin women with sponta-\nneous 46, XX primary \novarian insufficiency \nafter at least 3 months \nof a standardized \nhormone replacement \nregimen\nDISF-SR-Female \nVersion/[60, 61]/\nsexual function\nN = 143\n32 ± 5.5 years\nHospital-based\nWomen of healthy, non-\npregnant, and regularly \nmenstruating N = 70\n28.5 ± 7.3 years\nPopulation-based\n7 High\nBenetti-Pinto et al. 2011 \n[43]/Brazil\nQuality of life in women \nwith premature ovarian \nfailure\nCross-sectional and \nCase–control study\nEvaluate quality-of-\nlife in women with a \ndiagnosis of premature \novarian failure (POF)\nWHOQoL-\nBREF-100/[62–64]/\nGeneric QoL\nN = 58\n22–39 years 44.8%,\n40–51 years 55.2%\nHospital-based\nWomen with normal ovar-\nian function N = 58\n22–39 years 53.4%\n40–51 years 46.6%\nHospital-based\n7 High\nJi 2013 [44]/China Clinical study on the \nrelationship between \nsyndrome types dif-\nferentiation of TCM \nand quality-of-life in \npremature ovarian \nfailure\nCross-sectional study To understand the qual-\nity-of-life in patients \nwith premature ovarian \nfailure and to explore \nthe correlation between \nTCM syndrome types \nand quality of life\nSF-36/[65–67]/\nGeneric QoL\nN = 114\n34.5 ± 3.66 years\nHospital-based\nWomen with normal ovar-\nian function N = 90\n34.6 ± 3.2 years\nHospital-based\n7 High\nYang et al. 2017 [45]/\nChina\nStudy on quality of \nfertility in patients \nwith premature ovarian \nfailure\nCross-sectional study Investigation of repro-\nductive quality-of-life \nin patients with prema-\nture ovarian failure\nFertiQoL/[68, 69]/\nFertility specific\nN = 170\n31.2 ± 5.8 years\nHospital-based\nwomen with normal ovar-\nian function N = 113\n30.5 ± 5.3 years\nHospital-based\n7 High\nYela et al. 2018 [54]/\nBrazil\nInfluence of sexual \nfunction on the social \nrelations and quality \nof life of women with \npremature ovarian \ninsufficiency\nCase–control study To evaluate the impact \nof sexual function (SF) \nin the quality-of-life of \nwomen with premature \novarian insufficiency \n(POI)\n1. FSFI/[70–72]/\nSexual function\n2. WHOQoL-BREF \n[62–64]/Generic \nQoL\nN = 80\n38.4 ± 7.3 years\nHospital-based\nwomen matched by age \n(± 2 years) and present-\ning preserved gonadal \nfunction free of chronic \ndiseases N = 80\n38.1 ± 7.3 years\nHospital-based\n7 High\n\n25Quality of Life Research (2020) 29:19–36 \n1 3Table 2  Studies included in the systematic review not included in the meta-analysis due to insufficient data or non-normal ovarian function control group\nAuthor, year [ref], \ncountry\nTitle Type of study Objective of the study Questionnaire Sample size/observation \ngroup (age range) and \npopulation\nControl group(size) and \npopulation\nNOS\nPang 2006 [46],  China\na The demonstration study \nof the relationship \nbetween the social/\npsychology factors in \npatients with POF\nCross-sectional study To study the relationship \nbetween premature \novarian failure and \npsychosocial factors \nsuch as emotional \nstate, personality char-\nacteristics and negative \nlife events\n1. TABP/TCBP \n(reported 2007)\n2. STAI\n3. Life Events Scale\nN = 80\n33.3 ± 5.33 years\nHospital-based\nPCOS N = 60 \n25.6 ± 4.7 years, \nNormal N = 200 \n33.53 ± 5.29 years\nPopulation-based\nInsufficient data \nreported\n8 High\nDavis et al. 2010 [51], \nUSA\nThe psychosocial transi-\ntion associated with \nspontaneous 46, XX \nprimary ovarian insuf-\nficiency: illness uncer-\ntainty, stigma, goal \nflexibility, and purpose \nin life as factors in \nemotional health\nCross-sectional and \ncase–control study \nTo examine factors asso-\nciated with emotional \nwell-being in women \nwith spontaneous \nprimary ovarian insuf-\nficiency\n1. CES-D\n2. STAI\n3. PANAS\n4. Purpose in Life\nN = 99\n32.4 ± 5.2 years\nHospital-based\nHealthy control women \nof similar age N = 60 \n31.0 ± 6.9 years\nPopulation-based\nInsufficient data \nreported\n7 High\nOrshan et al. 2009 [53], \nUSA\nWomen with spontane-\nous 46, XX primary \novarian insufficiency \n(hypergonadotropic \nhypogonadism) have \nlower perceived social \nsupport than control \nwomen\nCross-sectional study To test the hypoth-\nesis that women with \nspontaneous POI differ \nfrom controls regard-\ning perceived social \nsupport and to inves-\ntigate the relationship \nwith self-esteem\n1. PRQ85\n2. Rosenberg’s Self \nEsteem Questionnaire\nN = 154\n32.2 ± 4.9 years\nHospital-based\nControl women: healthy, \nfree of chronic dis-\nease, not pregnant, and \nregularly menstruating \nN = 63\n29.9 ± 7.0 years\nPopulation-based\nInsufficient data \nreported\n7 High\nGibson-Helm et al. 2014 \n[48], Aus\nSymptoms, health \nbehavior and under-\nstanding of menopause \ntherapy in women with \npremature menopause\nCross-sectional study To explore symptoms, \nunderstanding of \nmenopausal therapies, \nmedication use and \nhealth-related behavior \nin women with and \nwithout premature \nmenopause\nGCS N = 25\n36 ± 8.0 years\nPopulation-based\nPremenopausal women \nN = 23,\n29 ± 13 years and \nwomen with \nmedically induced \npremature meno-\npause (MIPM)N = 29 \n38 ± 4.0 years\nPopulation-based\n6 Medium\n\n26 Quality of Life Research (2020) 29:19–36\n1 3\nSocial function\nMarital relationship and social support were reported to be \nsignificantly lower in POI patients [45]. Social relationships \nwere found to have a negative influence of sexual function \nsuch as arousal, orgasm, satisfaction and pain [53, 54]. How-\never, other articles reported no significant differences found \nwith respect to the social relationships or support [43, 46].\nQuestionnaires\nIn total, twenty-three different questionnaires had been used \nin the nineteen articles identified for review (Table  4). The \nmost frequently used questionnaires were the two generic \nHrQoL: World Health Organization Quality of Life (WHO-\nQoL-BREF) [62– 64], and the 36-Item Short Form Survey \nfrom the RAND Medical Outcomes Study (SF-36) [65–67] \nwhich were used in five studies. Between 1 and 4 question-\nnaires were used in each study, 50% of the studies only used \none questionnaire. Those studies that used four concentrated \non the psychological aspects of the condition and were \nmainly from the same research group at NIH in the US and \nreported in Abstract form. Other studies combined generic \nquestionnaires with condition specific issues e.g. sexual or \nmenopause specific questionnaires. Only one study [50] used \na POI specific questionnaire (Young Menopause Assessment \n(YMA) [Unpublished]. This was used in combination with a \nsexual function questionnaire (Sexual Personal Experiences \nQuestionnaire (SPEQ) [73]) a psychological questionnaire \n(Rosenberg’s Self Esteem Questionnaire [ 74–77]) and a \ngeneric questionnaire (SF-36 Short Form Survey from the \nRAND Medical Outcomes Study (SF-36) [65– 67]). All the \nHrQoL instruments used are described in Table  4, a more \ndetailed summary of the six questionnaires used in the stud-\nies included in the meta-analysis can be found as Online \nResource ESM_5.\nSynthesis of results and risk of bias (results \nof meta‑analysis)\nSix studies were included in the meta-analysis [41– 45, 54] \n(Fig.  2) with 645 POI participants and 492 normal-ovarian \ncontrols. Where data on average age was available the POI \ngroup had a pooled mean age of 33.3 ± 5.47; and the control \ngroup a pooled mean age of 32.87 ± 5.61.\nAt the overall HrQoL level (Fig.  2a) four studies [42, 44, \n45, 54] had lower level of HrQoL recorded in the POI group \n(pooled SMD = − 0.73, 95% CI − 0.94, − 0.51; I2 = 54%) as \ncompared to a normal ovarian control group. The pooled \nTable 2  (continued)\nAuthor, year [ref], \ncountry\nTitle Type of study Objective of the study Questionnaire Sample size/observation \ngroup (age range) and \npopulation\nControl group(size) and \npopulation\nNOS\nSchmidt et al. 2011 [49], \nUSA\nDepression in Women \nwith Spontaneous 46, \nXX Primary Ovarian \nInsufficiency\nCross-sectional study To characterize the prev-\nalence of psychiatric \ndisorders and the onset \ntiming of clinically \nsignificant depression \nrelative to POI and \nthe onset of menstrual \nirregularity in women \nwith POI\n[DSM-IV] (SCID) N = 174\n31.6 ± 5.3 years\nHospital-based\nTurner syndrome \nN = 100\nno description of age \nrange\nHospital-based\n3 Low\na English translations of the Chinese abstracts are included as Online Resources ESM_4\n\n27Quality of Life Research (2020) 29:19–36 \n1 3\nTable 3  Studies included in the systematic review not included in the meta-analysis due to insufficient data and no control group\nAuthor/year, country Title Type of study Objective of the study Questionnaire Sample size/Observation \ngroup (age range) and \npopulation\nControl group(size) and \npopulation\nAllshouse et al. 2014 [47], \nUSA + International\nEvidence for prolonged and \nunique amenorrhea-related \nsymptoms in women with \nPOF/POI\nCross-sectional study Aims to describe POF/POI \nsymptoms experienced by \nwomen from members of a \nPOF/POI-specific support \ngroup\n1. Menopause-specific QoL\n+ 10 symptoms\n2. CAMS-R\nN = 160\n39.3 ± 7.3 years\nPopulation-based\nNo control group\nSinger et al. 2011 [50], UK The silent grief: psychosocial \naspects of premature ovar-\nian failure\nCross-sectional study To investigate experiences \nof diagnosis, perception of \ncause, treatment, concerns, \na self-esteem, sexual func-\ntioning and HrQoL\n1. Rosenberg’s Self Esteem\n2. SF 36; 3. YMA; 4. SPEQ\nN = 136\n38.7 ± 7.03 years\nHospital-based\nNo control group\nVentura et al. 2007 [52], USA Functional well-being is posi-\ntively correlated with spir-\nitual well-being in women \nwho have spontaneous \npremature ovarian failure\nCross-sectional study To examine the relation-\nship between spiritual \nwell-being and functional \nwell-being in women who \nhave spontaneous POF\n1. FANLTC\n2. FACIT-Sp-12\nN = 137\n32 years\nHospital-based\nNo control group\nSterling et al. 2009 [36], USA A study of the relational \naspects of spiritual well-\nbeing and functional \nwell-being in women with \nspontaneous 46, XX POI\nCross-sectional study To analyze the relational \naspects of spirituality and \nfunctional well-being in \nwomen with spontaneous \n46, XX sPOI\n1. FACIT-Sp-Ex\n2. FANLTC\nN = 140\nNo description of age range\nSource unreported\nNo control group Abstract only\nIslam et al. 2011 [37], UK The impact of premature \novarian failure on quality \nof life: results from the UK \n1958 Birth Cohort\nCross-sectional study To assess the prevalence and \nquality-of-life impact of \npremature ovarian failure \nin a large population based \nsample\nSF-36 N = 370\nNo description of age range\nPopulation-based\nNo control group Abstract only\nNicopoullos et al. 2009 [38], \nUK\nEffect of age and aetiology of \npremature ovarian failure on \nsymptoms at presentation \ndata from the west London \nPOF database\nCross-sectional study To assess the effect of age at \ndiagnosis and aetiology on \npresentation\nSymptom questionnaire(no \ndetails)\nN = 239\nNo description of age range\nHospital-based\nNo control group Abstract only\nCovington et al. 2009 [39], \nUSA\nPerceived mastery and emo-\ntional well-being in women \nwith 46, XX primary ovar-\nian insufficiency\nCross-sectional study To compare mastery in \nwomen with 46, XX sPOI \nto controls and assess asso-\nciated affective symptoms\n1. Pearlin Mastery Scale\n2. CES-D;\n3. STAI;\n4. PANAS\nN = 100\nNo description of age range\nSource unreported\nControl women N = 60\nno description of age range\nSource unreported Abstract \nonly\nVanderhoof et al. 2009 [40], \nUSA\nSpirituality and emotional \nwell-being in women with \nspontaneous 46, XX pri-\nmary ovarian insufficiency \n(SPOI)\nCross-sectional study To compare spirituality and \nreligiousness of women \nwith sPOI to controls, and \nassess the association with \naffective symptoms\n1 Spirituality and Religion\n2. CES-D; 3. STAI; 4. \nPANAS\nN = 100\nNo description of age range\nSource unreported\nControl women N = 60\nno description of age range\nSource unreported Abstract \nonly\n\n28 Quality of Life Research (2020) 29:19–36\n1 3\nTable 4  Questionnaires used in the studies included in the systematic review\nFocus of scale Instrument Instrument description Study Study origin\nGeneric HrQoL World Health Organization Quality of Life (WHO-\nQoL-BREF) [62–64]a\nLast 4 weeks/5 point Likert. 4 domains: Social, Emo-\ntional, Physical, Environmental (28 items)\nBenetti-Pinto 2011 [43]\nYela 2018 [54]\nSão Paulo, Brazil\nSão Paulo, Brazil\nSF-36 RAND Medical Outcomes Study [65–67]\na Last 4 weeks/5 point Likert. 8 domains: Physical, \nRole limitations, Bodily pain, Social, General men-\ntal health, Role limitations/emotional, Vitality, Gen \nhealth. (36 items)\nSinger 2011 [50]\nIslam 2011 [37]\nJi 2013 [44]\nb\nLondon, UK\nLondon, UK\nGuangZhou, China\nFunctional well-being Functional Assessment of Non-Life-Threatening Con-\nditions (FANLTC) [78]\nLast 7 days/5 point Likert 4 domains: Physical, Social/\nFamily, Emotional, Functional (25 items)\nVentura 2007 [52]\nSterling 2009 [36]\nNICH, USA\nNIH, USA\nPsychological aspects of HrQoL The Cognitive and Affective Mindfulness Scale V \nRevised (CAMS-R) [79]\nNo time scale/4 point Likert. 1 domain: Mindfulness \n(10 items)\nAllshouse 2014 [47] Colorado, USA\nThe Pearlin Mastery Scale (PM) [80, 81] No time scale/7 point Likert. 1 domain: Mastery (7 \nitems)\nCovington 2009 [39] Arizona, USA\nEpidemiologic Studies Depression Scale (CES-D) \n[82–84]\nLast 7 days/4 point Likert 1 domain: Depression (20 \nitems)\nCovington 2009 [39]\nVanderhoof 2009 [40]\nDavis 2010 [51]\nNIH, USA\nNIH, USA\nNIH, USA\nState-Trait Anxiety Inventory (STAI) [85–88] At the moment/4 point Likert. 2 domains: State and \nTrait Anxiety (40 items)\nPang 2006 [46]\nCovington2009 [39]\nVanderhoof2009 [40]\nDavis 2010 [51]\nGuangZhou, China\nNIH, USA\nNIH, USA\nNIH, USA\nPositive and Negative Affect Schedule (PANAS) [ \n[89–91]\nTime scale appropriate to the study/5 point Likert. 1 \ndomain: Positive/negative affect (40 items)\nDavis 2010 [51]\nCovington2009 [39]\nVanderhoof 2009 [40]\nNIH, USA\nNIH, USA\nNIH, USA\nType A behavior pattern TABP/TCBP [57–59]\na Current time/dichotomous. 3 domains: Time urgency, \nHostility, Competitive drive (60 items)\nPang 2007 [51]\nPang 2006 [46]\nGuangZhou, China\nGuangZhou, China\nRosenberg’s Self Esteem Questionnaire [74–77] Current time/4 point Likert. 1 domain: Self worth (10 \nitmes)\nSinger 2011 [50]\nOrshan 2009 [53]\nLondon, UK\nNICH, USA\nPurpose in Life subscale from the Positive Mental \nWell-Being Inventory [92, 93]\nCurrent time/7 point Unmarked Semantic Differential \nScale. 1 domain: Meaning and purpose (20 items)\nDavis 2010 [51] NIH, USA\nFunctional Assessment of Chronic Illness Therapy—\nSpiritual Well-Being Scale (FACIT-Sp-12) [94]\nLast 7 days/5 point Likert. 3 domains: Spiritual well-\nbeing (peace, meaning, faith) (12 items)\nVentura 2007 [52] NICH, USA\nFunctional Assessment of Chronic Illness Therapy—\nSpiritual Well-Being Scale Expanded (FACIT-Sp-\nEx) [94]\nLast 7 days/5 point Likert. 3 domains: Spiritual well-\nbeing (peace, meaning, faith) (23 items)\nSterling 2009 [36] NIH, USA\nBrief Multidimensional Measure of Religiousness/\nSpirituality [95, 96]\nCurrent time/6-point scale. 9 domains: Daily spiritual \nexperiences, Meaning, Values/Beliefs, Forgiveness, \nReligious practice, Spiritual coping, Religious sup-\nport, Religious History, Commitment (40 items)\nVanderhoof 2009 [40] NIH, USA\nLife events Life events scale(LES) [97] No time limit/. 1 domain: Life events (48 items) Pang 2006 [46] GuangZhou, China\n\n29Quality of Life Research (2020) 29:19–36 \n1 3\na Six questionnaires included in the meta-analysis are further summarized in Table S5\nb Ji gives a measure of overall HrQoL derived from the SF-36 but does not explain how this is calculated\nc Singer refers to the measure as the Sexual Personal Experiences Questionnaire but gives a reference to the Dennerstein Short Personal Experiences Questionnaire\nTable 4  (continued)\nFocus of scale Instrument Instrument description Study Study origin\nSexual function Female Sexual Function Index (FSFI) [70–72]a Last 4 weeks/5 point Likert. 6 domains: Desire, \nArousal, Lubrication, Orgasm, Satisfaction, Pain (19 \nitems)\nYela 2018 [54] São Paulo, Brazil\nDerogatis Interview for Sexual Function (DISF-SR—\nFemale Version) [60, 61]a\nCurrent time/9 and 5 point scales. 4 domains: Sexual \ncognition and fantasy; Sexual arousal; Sexual \nbehaviour and experience; orgasm; Sexual drive and \nrelationship (25 items)\nKalantaridou 2008 [42] NIH, USA\nShort Personal Experiences Questionnaire (SPEQ) \n[73]\nCurrent time/8 domains: Desire, Arousal, Orgasm, \nEnjoyment, Satisfied by frequency, Frequency of \nintercourse, Frequency of fantasies, Dyspareunia (9 \nitems)\nSinger 2011 [50]\nb London, UK\nDisease or symptom-specific Fertility Quality of Life Questionnaire(FertiQoL) [68, \n69]a\nCurrent time/5 point Likert. 4 domains: Emotional, \nMind–body, Relational; Social. (36 items)\nYang 2017 [45] Henan, China\nMenopause-specific Quality of Life questionnaire [28, \n29, 98]\n4 Weeks/7 point Likert 5 domains: Physical; Vasomo-\ntor; Psychosocial; Sexual; working life (30 items)\nAllshouse 2014 [47] Colorado, USA\nGreene Climacteric Scale (GCS) [99–101] Symptoms checklist (21) Gibson-Helm 2014 [48] Monash, Australia\nPOI specific Young Menopause Assessment (YMA) [50] 3 Domains: Description of POF; Treatment; informa-\ntion and support (3 items 6) (Designed for this study \nreferred to as developed in a pilot study—unpub-\nlished)\nSinger 2011 [50]\nc London, UK\nPerceived social support Personal Resource Questionnaire 1985, part 2 \n(PRQ85) [102]\nCurrent time/7-point scale. 5 domains: Valued \nindividual; part of a group; intimacy; nurturance; \ninfo emotional and material help + description and \nsatisfaction with resources (25 items)\nOrshan 2009 [53] NICH, USA\n\n30 Quality of Life Research (2020) 29:19–36\n1 3\nFig. 2  a Patients with POI compared with normal ovarian reference \npopulations: overall health related quality-of-life (HrQoL). b Patients \nwith POI compared with normal ovarian reference populations: phys-\nical functioning. c Patients with POI compared with normal ovarian \nreference populations: mental health. d Patients with POI compared \nwith normal ovarian reference populations: social functioning\n\n31Quality of Life Research (2020) 29:19–36 \n1 3\nheterogeneity can be considered moderate. To address the \nheterogeneity, a subgroup analysis (2 studies included) was \nperformed to separately examine the measures of sexual \nfunctioning (Fig.  2a3) (SMD = − 0.78, 95% CI − 1.00, \n− 0.55; I\n2 = 0%) the effect size was medium to large and \nthere was no indication of heterogeneity. The largest effect \nsize (large) was found for ‘overall HrQoL’ as measured by \nthe SF-36 (− 0.93, 95% CI − 1.22, − 0.64).\nIn regard to the physical functioning aspects of HrQoL \n(Fig.  2b), this was measured by four studies using nine \ndifferent indicators. The results again showed moderate \npooled effect size and moderate heterogeneity (pooled \nSMD = − 0.54, 95% CI − 0.69, − 0.39; I\n2 = 55%) as com-\npared to a normal ovarian control group. The sexual function \n(2 studies included) measures explained the heterogeneity \nwhere these alone demonstrated substantial heterogeneity \n(I\n2 = 64%) but with a medium effect size (SMD = 0–0.52, \n95% CI − 0.70, − 0.34; I2 = 64%). The largest effect size \n(moderate) was found for ‘Lubrication’ as measured by the \nFSFI (− 0.74, 95% CI − 1.06, − 0.42).\nIn the mental health area (Fig.  2c1, 2), the studies agreed \nthat there was a lower level of mental health in the POI group \nthan was found in the controls however the pooled effect size \nwas small [1. SMD = − 0.43, 95% CI − 0.54, − 0.32; I\n2 = 0% \n(higher score = better Fig. 2c1); 2. SMD = 0.72, 95% CI 0.50, \n0.95; I2 = 0% (lower score = better Fig.  2c2)]. The largest \neffect size (moderate) was found for ‘Optimism’ as measured \nby the TABP/TABC (− 0.64, 95% CI − 0.95, − 0.32).\nThe social functioning domain (Fig. 2d) was addressed by \nfive of the six studies, the pooled effect size was small with \nno heterogeneity (pooled SMD  = −  0.27, 95% CI −  0.38, \n−  0.15; I\n2 = 0%). The largest effect size (moderate) was \nfound for ‘Drive and relationship’ in the DISF (− 0.48, 95% \nCI − 0.78, − 0.17).\nJi [44] has calculated a total QoL score for the SF-36. \nThere is not information on how this was calculated. For \ndiscussion on this issue see by Lins and Martins Carvalho \n(2016) https ://doi.org/10.1177/20503 12116 67172 5.\nDiscussion\nNineteen studies reported the empirical measurement of \nHrQoL among patients with POI. Reports of the impact of \nPOI on different aspects of HrQoL differed between stud -\nies. However, impaired physical, psychological and gen-\neral health was reported across all areas of HrQoL. There \nwere no articles prior to 2006 and studies used a variety \nof HrQoL instruments both generic and condition specific \nalthough only one measure was specially designed for POI \n[50]. Although subjective experiences of patients with POI \nhave received more attention from the medical profession in \nthe past decade, relevant and valid evaluation instruments \nhave not been developed, and long-term follow-up studies \nof HrQoL have not been carried out.\nThe six controlled studies included in the meta-analysis \ndemonstrated that overall HrQoL in patients with POI/POF \nis lower than individuals with normal ovarian functioning \nwith low to medium pooled effect sizes [41– 45, 54]. The \nmoderate heterogeneity in the general measure of HrQoL \nappears to be due to the different concept being measured \nunder the term HrQoL. It may also come from the different \nFig. 2  (continued)\n\n32 Quality of Life Research (2020) 29:19–36\n1 3\nsocioeconomic groups being included in the various studies. \nInformation on socioeconomic status was sparsely reported \nand it was not possible for us to make an assessment of the \ninfluence of this moderator.\nThe finding that studies concerning HrQoL in relation \nto POI were not found prior to 2006 may be related to fact \nthat the definition of POI had not been standardized. Recent \nguidelines from the European Society of Human Reproduc-\ntion and Embryology, published in 2015 [2 ], coincide with \nthe beginning of investigations into HrQoL in POI. However, \nsome variation in diagnostic criteria is evident. Some studies \nused broader age intervals, and the levels of Follicle-Stimu-\nlating Hormone (FSH), which is a very important indicator \nof POI diagnosis [2 ], were vague. This may lead to hetero-\ngeneity of the results.\nThe factors measured in the six studies in the meta-anal-\nysis varied and included: fertility, sexual function, anxiety, \ndepression, menopausal symptoms. Although all the meas-\nurements were cross-sectional, the concepts measures could \nall be considered to have long-term effects and would vary \naccording to, for example, diagnostic age, marriage con-\ndition or education. In one study [45], an association was \ninvestigated between personal character traits and the impact \nof POI this highlighted the patient’s response to the stress of \na POI diagnosis and of living with the condition.\nGeographical diversity is apparent from our review. It is \nnoted that studies were found in five countries and included \none multi-national study [47]. Studies taking a cross-cultural \nperspective were not conducted. This highlights the possibil-\nity of cultural bias in the results [103]. The sparsity of these \nstudies may be due to the lack of a single agreed and vali-\ndated condition specific instrument translated into multiple \nlanguage. In addition, despite substantial clinical studies on \nthe use of traditional medicine with this condition, there is \na lack of controlled studies that can be used as evidence of \ntreatment effects.\nThe large number of instruments used (23) in 19 stud -\nies with a very low repetition rate, indicates that there is \nno common view concerning instruments. In some studies, \nthe generic instruments were used to address a comprehen-\nsive array of domains of QoL, however, this focus may have \nlimited the sensitivity to detect subtle aspects of POI. It is \ninteresting to speculate on what we did not find, which was \nthe patient perspective. The instrument designed for POI \nby Singer [50] for their study was based on ‘clinical expe-\nrience’ and covered the areas of ‘About your POF/young \nmenopause’, ‘Treatment’, and ‘Information and Support’. \nFor many patients, there are concerns about the implica-\ntions of the treatment and of possible long-term side effects \nwhich might be more meaningful to the patient [104, 105] \nand yet these aspects were not investigated. Some studies \nchoose questionnaires that are specific for similar conditions \nsuch as menopause or infertility, however, even though the \nsymptoms may be similar, the patients’ experiences and \nrequirements may not be the same [47, 48, 54]. It also must \nbe considered that these questionnaires may not be sensi-\ntive to all patients with POI. Although the majority of the \nquestionnaires used to measure HrQoL in these studies had \ngood psychometric properties, none of them had evidence to \nconfirm the sensitivity and specificity of the instruments in \nrelation to POI. There were ten studies [36, 39, 40, 46, 47, \n50–54] that used a combination of questionnaires to capture \nmore comprehensive information. However, mood, symp-\ntom, and fertility questions specific for women with POI \nwere lacking [47, 50].\nStrengths and limitations\nSome limitations of the study need to be taken into consid-\neration. It is possible that some studies have been missed \ndue to the use of different terms for POI or in languages \nthat were not included in the databases we examined. There \nwere some studies that were only published as Abstracts and \nalthough we tried to contact these researchers we were una-\nble to obtain more information. Our study has the strength \nof including both European and Asian databases. Those \ndatabases that were searched are those that have the highest \nlikelihood of finding studies of HrQoL and POI.\nConclusion and future recommendations\nThis literature review and meta-analysis gives new informa-\ntion on HrQoL in patients with POI. In this review, the mag-\nnitude of the subjective effects is found to vary with effect \nsizes between low and medium. The largest effect sizes were \nfound in the area of sexual function and general HrQoL. \nCross-cultural approaches and international collaboration \nwere found in only one study. Additional studies are recom-\nmended to make a stratified comparison of patients, larger \nsample sizes to identify real changes in outcomes and long-\nterm follow-ups need to be done in order to have sufficient \ninformation for evidence based clinical practice decisions. \nFuture research should focus on developing condition spe-\ncific and sensitive assessments of the effect of POI based on \nthe patient perspective. This can be achieved through focus \ngroups with the aim of achieving a broader understanding \nof the outcome domains that are relevant to this population.\nFunding This study was funded by National Key R&D Projects: Inter-\nnational Cooperation Research on Evaluation of the Effect of Acupunc-\nture on Superiority Diseases (Grant Number 2017YFC1703600) and \nNational 13th Five-Year Plan: Evaluation of the Effect of Acupuncture \non Ovarian Function (Grant Number 2017YFC1703603).\n\n33Quality of Life Research (2020) 29:19–36 \n1 3\nCompliance with ethical standards \nEthical approval We will report this review in accordance with the \nPreferred Reporting Items for Systematic Review and Meta-Analysis \nstatement. A submission to the ethics committee of the Clinical Basic \nMedicine Institute, China Academy of Chinese Medical Sciences con-\nsidered that an ethics review was not required (ref 2019/1).\nOpen Access This article is distributed under the terms of the Crea-\ntive Commons Attribution 4.0 International License (http://creat iveco \nmmons .org/licen ses/by/4.0/), which permits unrestricted use, distribu-\ntion, and reproduction in any medium, provided you give appropriate \ncredit to the original author(s) and the source, provide a link to the \nCreative Commons license, and indicate if changes were made.\nReferences\n 1. Torrealday, S., Kodaman, P., & Pal, L. (2017). Premature ovarian \ninsufficiency—An update on recent advances in understanding \nand management. F1000research, 6, 2069.\n 2. Webber, L., Davies, M., Anderson, R., Bartlett, J., Braat, D., \nCartwright, B., et al. (2016). ESHRE Guideline: Management of \nwomen with premature ovarian insufficiency. 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