121.Hahn KA, Wesselink AK, Wise LA, Mikkelsen EM, Cueto HT, Tucker KL, Vinceti M, Rothman KJ, Sorensen HT, Hatch EE. Iron consumption is not consistently associated with fecundability among North American and Danish pregnancy planners. J Nutr. 2019;149(9):1585–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
123.Mills JL, Buck Louis GM, Kannan K, Weck J, Wan Y, Maisog J, Giannakou A, Wu Q, Sundaram R. Delayed conception in women with low-urinary iodine concentrations: a population-based prospective cohort study. Hum Reprod. 2018;33(3):426–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
128.Grieger JA, Grzeskowiak LE, Wilson RL, Bianco-Miotto T, Leemaqz SY, Jankovic-Karasoulos T, Perkins AV, Norman RJ, Dekker GA, Roberts CT. Maternal selenium, copper and zinc concentrations in early pregnancy, and the association with fertility. Nutrients. 2019;11(7):1609. [DOI] [PMC free article] [PubMed] [Google Scholar]
132.Harding KB, Peña-Rosas JP, Webster AC, Yap CM, Payne BA, Ota E, De-Regil LM. Iodine supplementation for women during the preconception, pregnancy and postpartum period. Cochrane Database Syst Rev. [Internet] 2017; [cited 2020 Dec 31]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6464647/. [DOI] [PMC free article] [PubMed] [Google Scholar]
135.Unfer V, Casini ML, Costabile L, Mignosa M, Gerli S, Di Renzo GC. High dose of phytoestrogens can reverse the antiestrogenic effects of clomiphene citrate on the endometrium in patients undergoing intrauterine insemination: a randomized trial. J Soc Gynecol Investig. 2004;11(5):323–8. [DOI] [PubMed] [Google Scholar]
136.Vanegas JC, Afeiche MC, Gaskins AJ, Mínguez-Alarcón L, Williams PL, Wright DL, Toth TL, Hauser R, Chavarro JE. Soy food intake and treatment outcomes of women undergoing assisted reproductive technology. Fertil Steril. 2015;103(3):749–755.e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
137.Unfer V, Casini ML, Gerli S, Costabile L, Mignosa M, Di Renzo GC. Phytoestrogens may improve the pregnancy rate in in vitro fertilization-embryo transfer cycles: a prospective, controlled, randomized trial. Fertil Steril. 2004;82(6):1509–13. [DOI] [PubMed] [Google Scholar]
138.Jacobsen BK, Jaceldo-Siegl K, Knutsen SF, Fan J, Oda K, Fraser GE. Soy isoflavone intake and the likelihood of ever becoming a mother: the Adventist Health Study-2. Int J Womens Health. 2014;6:377–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
139.Mumford SL, Sundaram R, Schisterman EF, Sweeney AM, Barr DB, Rybak ME, Maisog JM, Parker DL, Pfeiffer CM, Louis GMB. Higher urinary lignan concentrations in women but not men are positively associated with shorter time to pregnancy. J Nutr. 2014;144(3):352–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
140.Wesselink AK, Hatch EE, Mikkelsen EM, Trolle E, Willis SK, McCann SE, Valsta L, Lundqvist A, Tucker KL, Rothman KJet al. Dietary phytoestrogen intakes of adult women are not strongly related to fecundability in 2 preconception cohort studies. J Nutr. 2020;150(5):1240–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
142.Eisenbrand G; Senate Commission on Food Safety (SKLM) of the German Research Foundation (DFG) . Isoflavones as phytoestrogens in food supplements and dietary foods for special medical purposes. Opinion of the Senate Commission on Food Safety (SKLM) of the German Research Foundation (DFG) (shortened version). Mol Nutr Food Res. 2007;51(10):1305–12. [DOI] [PubMed] [Google Scholar]
158.Mier-Cabrera J, Aburto-Soto T, Burrola-Méndez S, Jiménez-Zamudio L, Tolentino MC, Casanueva E, Hernández-Guerrero C. Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet. Reprod Biol Endocrinol. 2009;7(1):54. [DOI] [PMC free article] [PubMed] [Google Scholar]
159.Mier-Cabrera J, Genera-García M, De la Jara-Díaz J, Perichart-Perera O, Vadillo-Ortega F, Hernández-Guerrero C. Effect of vitamins C and E supplementation on peripheral oxidative stress markers and pregnancy rate in women with endometriosis. Int J Gynecol Obstet. 2008;100(3):252–6. [DOI] [PubMed] [Google Scholar]
160.Hernández Guerrero CA, Bujalil Montenegro L, de la Jara Díaz J, Mier Cabrera J, Bouchán Valencia P. Endometriosis and deficient intake of antioxidants molecules related to peripheral and peritoneal oxidative stress. Ginecol Obstet Mex. 2006;74:20–8. [PubMed] [Google Scholar]
164.Zheng X, Lin D, Zhang Y, Lin Y, Song J, Li S, Sun Y. Inositol supplement improves clinical pregnancy rate in infertile women undergoing ovulation induction for ICSI or IVF-ET. Medicine (Baltimore). 2017;96(49):e8842. [DOI] [PMC free article] [PubMed] [Google Scholar]
165.Pundir J, Psaroudakis D, Savnur P, Bhide P, Sabatini L, Teede H, Coomarasamy A, Thangaratinam S. Inositol treatment of anovulation in women with polycystic ovary syndrome: a meta-analysis of randomised trials. BJOG. 2018;125(3):299–308. [DOI] [PubMed] [Google Scholar]
167.Genazzani AD, Lanzoni C, Ricchieri F, Santagni S, Rattighieri E, Chierchia E, Monteleone P, Jasonni VM. Acetyl-L-carnitine (ALC) administration positively affects reproductive axis in hypogonadotropic women with functional hypothalamic amenorrhea. J Endocrinol Invest. 2011;34(4):287–91. [DOI] [PubMed] [Google Scholar]
168.Samimi M, Jamilian M, Ebrahimi FA, Rahimi M, Tajbakhsh B, Asemi Z. Oral carnitine supplementation reduces body weight and insulin resistance in women with polycystic ovary syndrome: a randomized, double-blind, placebo-controlled trial. Clin Endocrinol (Oxf). 2016;84(6):851–7. [DOI] [PubMed] [Google Scholar]
176.Lyngsø J, Ramlau-Hansen CH, Bay B, Ingerslev HJ, Hulman A, Kesmodel US. Association between coffee or caffeine consumption and fecundity and fertility: a systematic review and dose-response meta-analysis. Clin Epidemiol. 2017;9:699–719. [DOI] [PMC free article] [PubMed] [Google Scholar]
Eliran178.James JE. Maternal caffeine consumption and pregnancy outcomes: a narrative review with implications for advice to mothers and mothers-to-be. BMJ Evidence-Based Medicine. [Internet] 2020; [cited 2021 Apr 10]. Available from: https://ebm.bmj.com/content/early/2020/09/01/bmjebm-2020-111432, [DOI] [PMC free article] [PubMed] [Google Scholar]
181.Fan D, Liu L, Xia Q, Wang W, Wu S, Tian G, Liu Y, Ni J, Wu S, Guo Xet al. Female alcohol consumption and fecundability: a systematic review and dose-response meta-analysis. Sci Rep. 2017;7(1):13815. [DOI] [PMC free article] [PubMed] [Google Scholar]
Many recent societal trends have led to the need for fertility education, including the age at which individuals become parents, the development of new reproductive technologies, and family diversity. Fertility awareness has emerged as a concept very recently and is increasingly gaining recognition. However, fertility education is often neglected as there is no consensus on the appropriate content, target populations, or on who should provide it. This article attempts to provide an overview of the use of interventions to improve fertility education. We emphasize the importance of delivering evidence-based information on fertility and reproductive health through various methods while providing guidelines for their standardization and systematization. Recommendations are provided to aid the development and implementation of fertility education tools, including: the establishment of a comprehensive understanding of the target populations; the incorporation of theories of behavioural change; the inclusion of the users’ perspectives and the use of participatory research; and the use of specific guidelines for increasing engagement. By following these recommendations, it is expected that fertility education resources can contribute to improving fertility literacy, empowering individuals and couples to make informed reproductive decisions, and ultimately reducing the incidence of infertility and need for fertility treatment.
Profound sociodemographic changes occurred within the last few decades: gender roles are more fluid, families are more diverse and smaller, and parents are older than previously. Developments in ART have accompanied these changes with increasing possibilities of parenting a child (Inhorn and Birenbaum-Carmeli, 2008), and legislation across different countries is adjusting to these changes. The number of fertility treatment cycles undertaken increases every year around the world (Wyns et al., 2022). While medically assisted reproduction (MAR) accommodates new ways of forming families, the leading cause behind the rise in infertility is the increasing age of parenthood in high income countries (Kuhnt and Passet-Wittig, 2022). The chance of conception is largely (female) age dependent (Raymer et al., 2020), but many individuals and couples feel shocked by a diagnosis of age-related infertility and regret not having been educated about this earlier on (Lee, 2019).
The World Health Organization (WHO) recently recognized the need for fertility education. The term ‘fertility awareness’ was included in the latest revision of the International Glossary on Infertility and Fertility Care and defined as ‘the understanding of reproduction, fecundity, fecundability, and related individual risk factors (e.g. advanced age, sexual health factors such as sexually transmitted infections (STIs), and lifestyle factors such as smoking, obesity) and non-individual risk factors (e.g. environmental and workplace factors); including the awareness of societal and cultural factors affecting options to meet reproductive family planning, as well as family building needs’ (Zegers-Hochschild et al., 2017). The need to improve fertility awareness was demonstrated in a systematic review, which revealed that fertility knowledge is in general low to moderate and that neither age nor child wish predict higher levels of fertility awareness (Pedro et al., 2018). There is also strong evidence that individuals overestimate the probability of pregnancy (Ekelin et al., 2012), the age at which fertility declines (Delbaere et al., 2020), and the success rates of treatments (Conceição et al., 2017).
Although fertility awareness is essential for making informed reproductive decisions, fertility education is still omitted in reproductive health guidelines (Bakkensen and Goldman, 2021; Practice Committee of the American Society for Reproductive Medicine and Practice Committee of the Society for Reproductive Endocrinology and Infertility, 2022). Furthermore, school sex education programmes focus on how to reduce the risk of STIs and unintended pregnancy (Haberland and Rogow, 2015), but fertility education remains ignored (Harper et al., 2021). Similarly, family planning is mainly directed at contraception and reducing fertility (Cleland et al., 2006; Frayne, 2017), but few preconception health programmes exist (Berglund and Lindmark, 2016). While the need for fertility education and infertility prevention has been emphasized (Bakkensen and Goldman, 2021; Harper et al., 2021), we have yet to implement it.
The International Reproductive Health Education Collaboration (IRHEC), formerly known as the International Fertility Education Initiative (IFEI), adopted as one of its missions to improvereproductive health literacy. Educational resources that effectively increase fertility health literacy or awareness are pivotal to enable informed reproductive decisions, and prevent and manage subfertility and infertility. Still, there is no consensus on the contents of such resources, who they should target or who should provide them (Berglund and Lindmark, 2016; Ojukwu et al., 2016).
Since health education can have many definitions (Liu et al., 2020), it is essential to start by defining fertility education. Adopting the widely accepted WHO definition of health education (World Health Organization, 2020), fertility education is hereby defined as the use of communication strategies and materials to inform and influence decisions and actions to improve fertility literacy or awareness. Fertility education should lead to greater fertility awareness and enable competences to be gradually built into everyday activities, social interactions and across generations (Nutbeam and Muscat, 2021) to inform and facilitate reproductive decision-making. This includes fertility education tools or resources to deliver evidence-based information on fertility and reproductive health effectively. Methods to convey such information may involve traditional forms of communication (e.g. doctor–patient communication in a family planning consultation; lectures in school; brochures at a primary health care centre) and/or digital forms of communication (e.g. website, fertility patient app, video, social media account). The more accessible, understandable, and of practical value for the intended target population, the more effective these tools will be (World Health Organization, 2020).
Digital fertility literacy solutions are of particular interest because they can enable a more active role from the user or patient (Conard, 2019). Digital health literacy is the most significant social determinant of health (Sieck et al., 2021), but most digital health tools are not evidence-based (Jandoo, 2020). More than ever, patients bring their own information to consultations with their doctor, primarily from the Internet (Tan and Goonawardene, 2017). Guiding people to reliable sources of information may reduce the potential damage of inaccurate information, decrease shame in requesting information (Parikh et al., 1996), and lead to better decision-making skills (Conard, 2019).
This article attempts to describe the process of developing fertility education tools, thereby contributing to the effort in standardising and systematizing best-practice guidelines in this field. Recently many noteworthy resources have been developed (for a detailed list, see www.eshre.eu/IRHEC) based on the fact that infertility may be preventable if potentially modifiable factors, such as lifestyle, are considered. However, estimates show that research results can take up to 17 years until effective implementation by health professionals (Morris et al., 2011). Practice guidelines can bridge this gap (Car et al., 2019) and, for that reason, their publication and implementation are increasing (Rod and Høybye, 2015). It is important to notice that fertility education resources, like any other health education tools, are developed to provide information that enables individuals to make positive behaviour changes that improve reproductive outcomes (Kumar and Preetha, 2012). Conversely, strategies to improve fertility knowledge at a population level usually involve cross-sectoral or cross-government approaches and aim to change policies and patterns of consumption (Kumar and Preetha, 2012) and are out of the scope of this article. We believe that the following recommendations can increase the feasibility and efficacy of implementation of resources designed to increase fertility awareness and/or prevent infertility.
Fertility education aims include increasing knowledge about fertility for children and adolescents; promoting informed reproductive decisions for adults (including if and when to have children and whether to undergo fertility preservation); and facilitating decision-making about fertility treatments if facing infertility or if in a same-sex relationship or considering single parenthood. Thus, the goal of fertility education varies depending on stage of reproductive life, and a framework can be adapted accordingly (Fig. 1).
While it was first considered that fertility education interventions should target women intending to have children, we now know that such interventions can induce anxiety (Maeda et al., 2018) as they intensify the societal pressure on women to have children. Based on research that shows that men want children as much as women do and that their understanding of fertility is low (Hammarberg, 2017), contemporary approaches to fertility education also target men. Additionally, fertility education needs to consider those who do not wish to have children to ensure they can avoid unplanned pregnancy. Regardless of the target population, the focus of fertility care interventions should always be on empowering people to make informed decisions, assisting ‘individuals and couples to realize their desires associated with reproduction and/or to build a family’ (Zegers-Hochschild et al., 2017).
Health and education professionals are also important targets for fertility education. These are indirect recipients and are not depicted in Fig. 1 because interventions must first consider who the patients or users are. They include primary health providers, family planning nurses, gynaecologists and urologists, counsellors, and teachers. Interventions for professionals should focus on developing training-specific skills or increasing knowledge regarding communication in a particular age-range or problem.
Understanding the population goes beyond knowing what education people need at the different reproductive life stages and involves a deep understanding of the context in which the intervention will occur. Context is a core element to consider when developing any complex intervention (Skivington et al., 2021). Within fertility education, approaches need to be adapted to the context of the target population. For example, a fertility education intervention to increase literacy in reproductive rights needs to consider the legislation in the country or region where it takes place. Likewise, interventions to support medical help-seeking for people with fertility difficulties must consider the options that realistically are available to them.
The type of the educational tool will, of course, depend on population and context. While online training may be suitable for educating specialised nurses on how to talk about fertility education with young adults, a social media resource may be effective in improving adolescents’ fertility knowledge directly.
Theories provide a valuable framework for understanding the complex factors that might influence and/or change individuals’ knowledge, attitudes, or behaviours regarding fertility. Only by testing the directional relationships between concepts, i.e. establishing a hypothesis, will a researcher or practitioner know if an intervention is effective in changing what it was intended to change (Moullin et al., 2020). Moreover, theory-driven interventions are known to be more effective than interventions lacking a theoretical basis (Davis et al., 2015), and there is evidence that suboptimal use of frameworks in both research and practice leads to wasted resources, errors in implementation methods and data analyses, and erroneous conclusions (Moullin et al., 2020).
