Assisted reproduction with advancing paternal and maternal age: an Ethics Committee opinion

KEY POINTS

• Risks associated with reproduction at an advanced reproductive age (ARA) fall into three broad categories: risks to offspring associated with the use of gametes from older individuals; increasing health risks of gestating at an older age; and risk from having older parents who may have a limited number of expected healthy life years available for parenting (1). These age-related risks occur on a continuum and can be difficult to quantify. More precise estimates regarding healthy life years can be obtained using actuarial tables.
• Clinics should have written policies regarding inclusion and exclusion criteria as they relate to parental age to ensure consistency in assessments and to reduce the risk of bias. Clinics may base age policy on the predicted number of healthy life years available for parenting, or the risk of parental death before the offspring reach the age of 18.
• Those gestating at an ARA face increased medical risks, and careful counseling is warranted, potentially in conjunction with maternal-fetal medicine specialists.
• Clinics should strongly consider having a policy that declines the transfer of an embryo to the uterus of a person at such age as a program may individually determine a review of the relevant medical literature.
• Prospective patients of ARA should be counseled about the potential negative impact of their age on the success of fertility treatments using autologous gametes and on the increased medical risks to the resultant offspring, including the fact that many of these risks are poorly characterized due to limited data.
• Prospective patients of ARA should be counseled regarding short- and long-term parenting and child-rearing issues specific to their age and health. The age and health of the partner, if present, should also be considered in this discussion.

BACKGROUND

Paternal and maternal ages are increasing across all regions, races, and educational levels in the USA. Within this trend are increases in people having children in their 50s and 60s (2, 3). Although the number of females carrying children in their 50s and 60s and the number of males fathering children in their 70s is low, positive media portrayals of these parents, particularly celebrities, may increase the social acceptability of this choice (3).

Historically, there have always been fathers of advanced reproductive age (ARA). However, it is only recently that advanced paternal age has become a focus of research and clinical consideration. Although females have been routinely advised about the impact of increasing age on fertility and child health, there has been less focus on the impact of ARA in males. It has been speculated that the absence of this type of consistent guidance has erroneously led both males and females to presume that male age is not a concern in reproduction or subsequent child health. This document addresses the ethical, medical, and psychological considerations of both the intended parents and the resulting offspring related to providing fertility care to potential parents at an ARA. It provides guidance to programs for the development of written policies that address thresholds regarding advanced maternal and paternal age. It is important to note that there is no consensus regarding the exact definition of ARA (4). Given the lack of agreement, the number of remaining healthy life years available for child rearing is used to guide the recommendations presented here.

HEALTH OUTCOMES

Medical risks to offspring when the male is of ARA

Advancing paternal age, a continuum beginning in the 4th and 5th decades of life, is associated with an increased risk of 1) stillbirth, 2) pregnancy complications, and 3) accumulation of de novo mutations in sperm leading to monogenic and polygenic disorders in offspring (1, 5, 6). The use of donor sperm, sperm cryopreserved at an earlier age in a male’s life, or embryos created when the male was younger may mitigate these risks (5). Psychological impacts must also be considered and are discussed in a later section (7, 8).

Increasing paternal age is associated with declines in semen volume, sperm motility, and sperm morphology, increases in DNA fragmentation and de novo germline mutations, and may be linked with lower conception rates after intrauterine insemination and in vitro fertilization (IVF) (5, 9, 10). Some studies have found that increasing paternal age is associated with a heightened risk of spontaneous abortion, pre-eclampsia, pre-term birth, low birth weight, and stillbirth, although findings differ (10, 11). Although data suggest that advancing paternal age is not associated with embryo aneuploidy (12), two other studies have found a negative association between advanced paternal age and both pregnancy and live birth rates after IVF (13, 14). Notably, this lower chance of pregnancy with increasing paternal age was also evident among paired recipients using the same oocyte donor, further supporting the impact of paternal age on the likelihood of IVF success (14).

Advanced paternal age has been correlated with autism spectrum disorders, schizophrenia, bipolar disorder, acute lymphatic leukemia, achondroplasia, Apert syndrome, neurofibromatosis, Marfan syndrome, and Klinefelter syndrome in offspring (10, 15, 16). Some data have shown that as men use sperm produced at an older age, their offspring have shorter lifespans and an increased incidence of lower intelligence quotient, learning disabilities, depression, anxiety, eating disorders, and behavioral problems (17–21). This may be due to de novo genetic mutations that accumulate within sperm as men age (5, 22). A next-generation genome sequencing study of parent-offspring trios found that the number of paternal de novo germline mutations in offspring increased by an estimated 4% with each additional year of paternal age at the time of conception (22). Although research regarding the health risks for children born to older fathers is strong and generally consistent, the overall risk per offspring remains low (4). However, it has also been cautioned that although the first-generation offspring in men of ARA may not demonstrate a negative health impact, the accumulation of de novo mutations could accumulate in future generations, such that risks might compound over time (5).

Medical risks to offspring when the female is of ARA

Advanced maternal age is a risk factor for female infertility, pregnancy loss, fetal anomalies, stillbirth, and obstetric complications (1, 23–25). Oocyte donation circumvents the age-related decline in implantation and birth rates and largely restores pregnancy potential beyond menopause. Reliance on a gestational carrier to carry the pregnancy can circumvent the risks associated with carrying a pregnancy at an advanced maternal reproductive age. The combined use of both donor oocytes and a gestational carrier eliminates pregnancy-related health impacts on the mother and both gestational and genetic risks to the offspring. As in males of ARA, the psychological impacts on children must also be considered and are discussed in a later section (7).

In pregnancies resulting from IVF, it is well established that medical and obstetric complications, particularly hypertensive disorders, gestational diabetes, and intrauterine growth restriction, are significantly increased in those who carry a pregnancy over the age of 45 years (23–26). These risks are significantly higher in those individuals who are ≥ 50 years of age when compared with those aged 45–49 (27). It has been suggested that pregnancy beyond age 50 may be associated with a distinct risk pattern that differs from that observed for mature (30-39 years of age) and very mature mothers (40-49 years of age) (28).

Similar to data discussed regarding advanced paternal age, one study found that children born to older females have shorter life spans (29). Other studies of pediatric health have been reassuring, including one that examined hospitalizations of offspring up to age 18 years of age in a population-based cohort, which found no increase in the incidence of cardiovascular, endocrine, neurological, hematological, respiratory, or gastrointestinal morbidities for children born to females at 40–50 years of age as compared with children born to women at 35–39 years of age (30).

In one series of 177 live births achieved with donated oocytes, pregnancy-induced hypertension was noted in 16.7% of women aged 45–49 years vs. 33.3% of women aged 50 or older (27). In this same study, gestational diabetes was noted in 14.7% of the 45–49 year old group and 29.6% of the ≥ 50 year old group, and birth rates before 37 weeks’ gestation were 18.7% in the 45–49 age group vs. 37% for the ≥ 50 year old group (27). A similar study comparing outcomes of women aged 50–54 to women ≥ 55 years of age demonstrated that risks were even higher in the older age group (25). For example, the risk of pregnancy-induced hypertension was 26% in the 50–54 age group but increased to 60% in patients over 55 years of age. Further, a study comparing singleton pregnancy outcome data for 252,299 women aged 40–49 years to 341 women ≥ 50, found that fetal mortality rates were 1.18% (adjusted odds ratio of 1.94; confidence interval, 1.67–2.26) vs. 2.35% (adjusted odds ratio, 2.20; confidence interval, 1.01–4.75), respectively (28). These risks and the limitations of these data should be clearly communicated to individuals and couples of ARA considering reproduction. It is recommended that clinics strongly consider having a policy that declines the transfer of an embryo to the uterus of a person at such age as a program may individually determine after a review of the relevant medical literature.

Risks to children born to parents of ARA psychological considerations

Children born to individuals of advanced age, regardless of the age of the gametes contributing to their conception and the age of the individual carrying the pregnancy, are more likely to experience health decline of their parent or parents relative to peers born to younger parents (7). Declining parental health can lead children to have heightened fears of parental death and experience the emotional struggles associated with observing parental decline, illness, and pain (31, 32). Children may also take on caregiving roles for their parent at a younger age than many of their peers, placing them at increased risk for depression, anxiety, eating disorders, substance abuse, and behavioral problems. They may have difficulty emancipating from the home due to a commitment to care for the parent(s) and may consequently delay advanced education, dating, and marriage (31).

Children born to parents of ARA are also more likely to experience the death of a parent while they are still minors (Table 1) (3). As an example, fathers who are 50 years old when their child is born have a 21.7% chance of dying by the time the child is 18 years old. Fathers who are 60 when their child is born have a 39% chance of dying before the child reaches the age of 18. Mothers who are 50 years old when their child is born have a 13.8% chance of dying by the time the child is 18 years old. Mothers who are 60 when their child is born have a 27.5% chance of dying before the child reaches the age of 18. This contrasts with a 3.5% national average baseline risk of parental death by the time a child is 18 years old for all births in the United States (33–37). Children whose parents die while they are minors face an increased risk of all-cause mortality that persists into early adulthood, irrespective of the child’s sex and age at bereavement and after accounting for the effects of specific baseline characteristics like socioeconomic status and birth characteristics. This risk differs between paternal death (mortality rate ratio, 1.54 [1.45–1.63]) and maternal death (mortality rate ratio, 1.67 [1.54–1.82]) (38). Psychological risks for children experiencing parental death include higher rates of depression, anxiety, post-traumatic stress disorder, alcohol/drug problems, social withdrawal, and lowered self-esteem (39).

Recommended medical screening and psychological counseling

Women of ARA who plan to gestate should undergo comprehensive medical testing focused on ascertaining cardiovascular and metabolic fitness and a careful medical evaluation. Additionally, providers should incorporate potential implications of advancing male and female age in patient counseling and informed consent discussions. A psychosocial consultation may be a helpful component of this patient counseling, particularly regarding the presence of additional supporting individuals that may help raise and support a child to adulthood and how children may be impacted by the health decline or death of their parents.

ETHICS

Requests for infertility treatment from prospective fathers and mothers of advancing ages present questions about reproductive rights, the welfare of offspring, justice, and nondiscrimination. Fertility clinics should consider both the reproductive interests of the prospective parent(s) and the welfare of resultant children when prospective parents of ARA request assistance in family building.

There may be benefits to children born to individuals of ARA, such as potential increased financial stability and emotional maturity in their parents. However, some studies suggest that these benefits may not be as robust or lasting as previously presumed (40, 41). Children born to parents of ARA may also face serious health, psychological, and social risks stemming from the ages of their parents.

The principle of justice obliges us to distribute benefits, risks, costs, and resources equitably. Historically, women have been counseled that having children later in life increases risks of infertility and potential negative health consequences for the child. Further, maternal age restrictions in fertility care have been carefully discussed in the ethics literature and commonly limit women’s access to reproductive care. Men have not received this same counsel, nor have they been as likely to face age restrictions in reproductive care. It has been asserted that this imbalance across men and women may convey the message that fathers and mothers are not equally responsible for or invested in the health and care of their children (42).

Differential access to reproductive care based on age has been raised as a concern regarding justice. It has been suggested that establishing an age limit in assisted reproductive care is ageist in that it suggests that an individual’s ability to parent is lessened with increasing age (43). Examples of grandparents providing supportive and effective parenting challenge this presumed age-related concern. Further, the health-promoting effects of grandparent involvement in a child’s life are supported in the literature (44). A grandparent providing parenting to an existing child, in the context of the parent not fulfilling this role, is a benefit to the child. This differs considerably, however, from a prospective parent of ARA initiating a pregnancy at an age point when the resulting child would be at increased risk of experiencing early parental health decline and death.

ARGUMENTS AGAINST SETTING MALE AND/OR FEMALE AGE LIMITS IN ART

Arguments against setting a male age limit in assisted reproduction are based on historical and societal precedent, reproductive freedom, and medical efficacy and safety. Historically, men have not faced external, age-based limitations to their reproductive choices. Implementing a male age-based policy in assisted reproduction would be a substantial departure from the degree of reproductive freedom that men have long held. Another argument against setting a male age limit is the fact that most children born to fathers of ARA will not experience any medical health conditions related to their father’s age. Further arguments point to the fact that assisted reproduction is offered to prospective single parents, and research suggests that the resulting children are healthy and developing well without indication of a negative impact of having one parent (45).

Arguments against setting a female age limit in assisted reproduction are based on medical efficacy and safety, societal practices, gender equality, and reproductive freedom. Live birth rates per embryo transfer in women undergoing oocyte or embryo donation are generally above 50% (46). Further, although maternal and offspring health risks are elevated when the person carrying the pregnancy is of ARA, most women and children will enjoy a reasonably good immediate health outcome (46). Regarding societal norms, as noted earlier, individuals of ARA have been capable of meeting the needs of children, suggesting that age alone may not be a reason to question a positive parenting impact. Also, men of ARA are often able to naturally father children and historically have not been restricted from assisted reproductive care when seeking fertility services. A gender equity perspective would suggest that women should enjoy the same level of reproductive opportunity. Finally, the tenet of reproductive freedom asserts the rights of individuals to make reproductive choices regardless of age or life expectancy. Given the possibility that late-life parenting may satisfy the desire of a woman or couple to have a child, it can be argued that it is unreasonable to deny women assisted reproduction care based solely on maternal age.

ARGUMENTS IN FAVOR OF SETTING A MALE AND/OR FEMALE AGE LIMIT IN ART

Arguments in favor of setting male and/or female age limits in ART are based on the concern for risk of harm for the resulting offspring, medical risks for the gestating person, and the importance of gender-neutral policies. Additionally, the right to reproduce is considered a negative, rather than a positive right. This distinction can be understood as the right of individuals to not face interference in their reproductive decisions, but does not imply an obligation of others to assist them in building a family. As such, physicians may decline to provide reproductive care to individuals due to concerns of elevated risk to either the intended parents or the potential offspring. Such refusals to offer care should be provided in an unbiased and non-discriminatory manner. Although the choice to parent a child at an ARA may have benefits, including potentially increased financial resources and emotional maturity, it also may carry potential negative risks to the offspring. These include increased pregnancy-related risks when the gestating person is of ARA, increased risk of health issues from the use of gametes from ARA individuals, and the psychological and health risks of caring for or losing a parent at a young age. Reproductive rights must be balanced with the well-being of the resultant child (47, 48).

Maternal age-based restrictions in ART have generally been accepted by society, ethicists, and clinicians. The fact that age restrictions are deemed acceptable, even when the heightened maternal pregnancy risks are avoided with the use of a gestational carrier, implies that age restrictions reflect risks and societal attitudes beyond the narrow time window of pregnancy. A major risk beyond obstetric outcome is the loss of a mother before reaching adulthood.

CONCLUSION

The central concern in this ethical discourse is whether the interests of intended parents of ARA and their resultant children are well served by facilitating ART and third-party reproduction in those of ARA. There has been a call for the American Society for Reproductive Medicine Ethics Committee to guide the provision of reproductive services to individuals of ARA. This document endeavors to present data and ethical considerations to assist clinics and clinicians as they develop their own policies regarding providing care to individuals of ARA. 

Reproductive health providers should counsel patients about the potential impact of increasing paternal and maternal age on reproductive outcomes and offspring wellbeing. Defining the age point at which to routinely provide this counsel should be set by individual programs, and may change over time given that societal health determinants and life expectancy estimates are dynamic.

As the maternal and obstetric risks of pregnancy increase with advancing age, it is recommended that clinics strongly consider having a policy that declines the transfer of an embryo to the uterus of a person at such age as a program may individually determine after a review of the relevant medical literature. Programs that have established an age limit for women irrespective of whether they carry a pregnancy may elect to use a similar age limit for men. When there are two intended parents, the age of each of the parents as well as their combined age may influence decisions regarding the provision of fertility treatment.

As the number of children born to parents of ARA increases, and as data continues to be collected, the impact on these children will become clearer. Ongoing research into the health and well-being of both parents as well as of children born to individuals of ARA will help inform future considerations surrounding the role of age limits in assisted reproduction.

Acknowledgments

This report was developed under the direction of the Ethics Committee of the American Society for Reproductive Medicine as a service to its members and other practicing clinicians. Although this document reflects appropriate management of a problem encountered in the practice of reproductive medicine, it is not intended to be the only approved standard of practice or to dictate an exclusive course of treatment. Other plans of management may be appropriate, taking into account the needs of the individual patient, available resources, and institutional or clinical practice limitations. The Ethics Committee and the Board of Directors of the American Society for Reproductive Medicine have approved this report.

This document was reviewed by ASRM members and their input was considered in the preparation of the final document. The following members of the ASRM Ethics Committee participated in the development of this document: Sigal Klipstein, M.D.; Sina Abhari, M.D.; Aishwarya Arjunan, M.S., M.P.H., C.G.C.; Paula Amato, M.D.; Tolulope Bakare, M.D.; Kim Bergman, Ph.D.; Michelle Beyefsky, M.D.; Zeki Beyhan, Ph.D.; Katherine Cameron, M.D.; Susan Crockin, J.D.; Ruth Farrell, M.D.; Elizabeth Ginsburg, M.D.; Insoo Hyun, Ph.D.; Mandy Katz-Jaffe, Ph.D.; Jennifer Kawwass, M.D.; Jeanne O’Brien, M.D.; Torie Comeaux Plowden, M.D.; Robert Rebar, M.D.; Chevis N Shannon, Dr.P.H., M.P.H., M.B.A.; Sean Tipton, M.A.; Julianne Zweifel, Ph.D. The Ethics Committee acknowledges the special contribution of Julianne Zweifel, Ph.D.; Elizabeth Ginsburg, M.D.; and Jennifer Kawwass, M.D. in the preparation of this document. All Committee members disclosed commercial and financial relationships with manufacturers or distributors of goods or services used to treat patients. Members of the Committee who were found to have conflicts of interest based on the relationships disclosed did not participate in the discussion or development of this document.

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