key: cord-1025281-9ybq873l
authors: Crump, Casey
title: An overview of adult health outcomes after preterm birth
date: 2020-09-09
journal: Early Hum Dev
DOI: 10.1016/j.earlhumdev.2020.105187
sha: 51d43f38ba49a8e9ba5d2a1747ce77b5d3d17dac
doc_id: 1025281
cord_uid: 9ybq873l

Preterm birth (gestational age <37 completed weeks) has increased in prevalence in most countries in the past 20 years and now affects nearly 11% of all births worldwide. Because of treatment advances introduced in the 1970s-1980s, >95% of preterm infants who receive modern neonatal and pediatric care now survive into adulthood. The earliest birth cohorts to benefit from those advances are now in their 4th and 5th decades of life. A growing number of large cohort studies have investigated the long-term health sequelae in adulthood. Evidence has consistently shown that adult survivors of preterm birth have increased risks of chronic disorders involving various organ systems, including cardiovascular, endocrine/metabolic, respiratory, renal, neurodevelopmental, and psychiatric disorders, which either persist from childhood into adulthood or sometimes first manifest in adulthood. These disorders also lead to moderately (30% to 50%) increased mortality risks during early to mid-adulthood among persons born preterm compared with full-term, and even higher risks among those born at the earliest gestational ages. However, the majority of persons born preterm have low absolute risks of these outcomes and good self-reported quality of life in adulthood. Priorities for future research include the assessment of long-term health sequelae of preterm birth in racially and economically diverse populations, additional follow-up of existing cohorts into older adulthood, elucidation of outcomes by preterm birth subtype (e.g., different underlying causes) to improve risk stratification, and identification of protective factors that will support the long-term health trajectory and well-being of preterm-born adults.

Preterm birth (gestational age <37 completed weeks) has increased in prevalence over the past few decades in almost all countries with reliable trend data [1] . In 2014, preterm birth had a worldwide prevalence of 10.6%, affecting nearly 15 million births annually [2] . Because of treatment advances introduced in the 1970s-1980s [3, 4] , survival of preterm infants also has improved dramatically. Over 95% of preterm infants and the majority of those born extremely preterm (<28 weeks) who receive modern neonatal and pediatric care now survive into adulthood (ages 18 years) [5] [6] [7] [8] . As a result, millions of preterm birth survivors are now transitioning to adulthood each year worldwide. A comprehensive understanding of their long-term health sequelae is needed to inform counseling of these patients and their families and to guide their follow-up care across the life course.

In the past 10 years, the number of peer-reviewed articles published annually on adult health outcomes after preterm birth has approximately doubled. In 2015, the U.S. National

Institutes of Health hosted a working group conference on "Adults Born Preterm: Epidemiology and Biological Basis for Adult Outcomes" [5] . Several hundred additional relevant studies have been published since then. The present article will review the current evidence. Much of the evidence to date comes from registry-based studies particularly in Nordic countries, which have the advantages of large national cohorts with nearly complete birth data, several decades of (95% CI, 2.2-4.6) and higher DBP by 2.1 mm Hg (1.3-3.0), with slightly stronger effects among women [17] . A UK study of 7,847 adults aged 44-45 years reported that each additional week of gestation was associated with a lower SBP by 0.53 mm Hg on average (95% CI, 0.32-0. 75) [18].

In a Swedish cohort of 636,552 adults aged 25-37 years, preterm birth was associated with significantly increased prescription of antihypertensive medications [19] .

The largest study of hypertension to date included >4 million persons born as singletons in Sweden during 1973-2014, who were followed up for hypertension identified from nationwide inpatient and outpatient (both specialty and primary care) diagnoses through 2015 (maximum age 43 years) [20] . Adjusted HRs for new-onset hypertension at ages 18-29 years associated with preterm and extremely preterm (22-27 weeks) respectively, compared with full-term birth (39-41 weeks) . These associations affected men and women similarly. Co-sibling analyses suggested that they were largely (60% to 80%) related to shared genetic and/or environmental factors in families [20] . Both spontaneous and medically indicated preterm birth were associated with increased risks of hypertension compared with fullterm birth (adjusted HR, 1.17; 95% CI, 1.08-1.27; P<0.001; and 1.35; 1.23-1.48; P<0.001, respectively) [20] . Figure 2 shows adjusted HRs and 95% CIs for hypertension and other chronic disorders in adulthood associated with preterm birth in the same large Swedish cohort.

persons born in 1924-44 reported no association between preterm birth and IHD risk (adjusted HR, 1.03; 95% CI, 0.89-1.18) [24] . A Swedish study of 1.3 million persons born in 1983-1995 with follow-up to ages 15-27 years reported a non-significant association with IHD risk (adjusted HR comparing 32-36 vs. 37-41 weeks: 1.44; 95% CI, 0.81-2.56) [25] . Another Swedish study of 1.9 million persons (maximum age 38 years) reported a borderline-significant association between preterm birth and IHD risk adjusted for age and sex (HR, 1.36; 95% CI, 1.00-1.85), and no association when further adjusted for other perinatal, familial, and comorbidity factors [26] .

However, previous findings were potentially affected by insufficient follow-up into adulthood or possible survivor bias in the earliest birth cohorts (i.e., the strongest infants who survived may be less susceptible to IHD later in life than more recent survivors). A more recent national cohort study included >2 million persons born as singletons in Sweden during 1973-1994, who were followed up for IHD identified from nationwide inpatient and outpatient diagnoses through 2015 (maximum age 43 years) [27] . Preterm birth was associated with increased risks of IHD in adulthood that were higher after longer follow-up times. The adjusted HRs for IHD associated with preterm birth were 1.32 (95% CI, 0.99-1.76) at ages 18-29 years and 1.53 (1.20-1.94) at ages 30-43 years, compared with full-term birth (39-41 weeks). These risks were even higher among women, likely due to a lower background incidence of IHD in those born at term compared with men. Co-sibling analyses suggested that these associations were not explained by confounding from unmeasured shared genetic or early-life environmental factors in families [27] . This evidence from the largest cohort to date indicates that preterm birth survivors have increased risks of IHD that begin to emerge in early adulthood. These findings also suggest the possibility that known racial/ethnic disparities in preterm birth might contribute significantly to cardiovascular health disparities across the life course [28] . An association between preterm birth and increased risk of stroke in adulthood was reported in some [25] but not all [24, 31] studies, and was limited to those born at the earliest gestational ages.

Preterm birth has consistently been linked with increased risks of both type 1 and type 2 diabetes later in life [21, 22, [32] [33] [34] [35] . A large meta-analysis reported pooled odds ratios of 1.18 (95% CI, 1.11-1.25) for type 1 diabetes (based on 18 studies with 2,176,480 participants, mostly aged <15 years) and 1.51 (1.32-1.72) for type 2 diabetes (based on 5 studies with 31,478 participants, mostly middle-aged adults) [21] . A more recent study with the largest cohort to date yielded very similar risk estimates specifically in adulthood. This study included >4 million persons born as singletons in Sweden during 1973-2014 who were followed up for type 1 and type 2 diabetes identified from nationwide outpatient, inpatient, and pharmacy data through 2015 J o u r n a l P r e -p r o o f Journal Pre-proof (including >2.5 million persons who reached adult ages) [22] . Preterm birth was associated with approximately 1.2-and 1.5-fold risks of new-onset type 1 and type 2 diabetes, respectively, at ages 18-43 years (adjusted HR, type 1: 1.24; 95% CI, 1.13-1.37; type 2: 1.49; 1.31-1.68).

Extremely preterm birth was associated with >2-fold risks of both type 1 and type 2 diabetes in adulthood. The associations between preterm birth and type 2 (but not type 1) diabetes were significantly stronger in women (P<0.01). Co-sibling analyses suggested that the findings for type 2 diabetes were independent of shared familial (genetic and/or environmental) factors, whereas those with type 1 diabetes were partially (~40%) explained by such factors [22] . In addition, both spontaneous and medically indicated preterm birth were associated with increased [22] .

These findings are consistent with those from other smaller studies. A Swedish cohort study of 630,090 adults aged 25-37 years found that those born preterm had modestly (10-25%) increased odds of medication prescription for diabetes that was predominantly type 1 [36] .

Several other studies have reported associations between preterm birth and type 2 diabetes in mid-adulthood. For example, a Finnish cohort study of 12,813 adults aged >40 years reported a 1.6-fold (95% CI, 1.00-2.52) risk among those born at <35 vs. 37-41 weeks [37] . A Swedish cohort study of 6,425 adults aged 37-62 years reported that those born at <33 weeks had a 1.6fold (95% CI, 1.33-2.11) risk of type 2 diabetes based on inpatient diagnoses [38] . A Scottish cohort study of 5,973 adults aged 46-50 years reported that preterm birth was associated with a 2-fold (95% CI, 1.18-3.53) risk of self-reported type 2 diabetes [39] .

J o u r n a l P r e -p r o o f Journal Pre-proof term controls, the mean %FEV 1 was 7.2% (95% CI, 5.6% to 8.7%) lower in persons born preterm without BPD, 16.2% (12.4% to 19.9%) lower in those with BPD who required supplemental oxygen for >28 days, and 18.9% (16.7% to 21.1%) lower in those with BPD who required supplemental oxygen for >36 weeks [40] .

In a systematic review of 14 studies that included young adults, all studies found that survivors of BPD who were born either preterm or with very low birthweight had reduced pulmonary function, increased respiratory symptoms, and/or radiologic abnormalities that persisted into adulthood [41] . A Finnish study with 719 participants reported that early preterm (<34 weeks) but not late preterm (34-36 weeks) birth in the presurfactant era was associated with substantially reduced expiratory airflow in young adulthood (mean age 23 years), even after excluding those with BPD [42] . An Australian study with 294 participants found that extremely preterm birth in the postsurfactant era also was linked with substantially reduced expiratory airflow at age 25 years, which was more severe in those with BPD [43] . A meta-analysis of 11 studies reported that persons born very preterm or with very low birthweight (mostly in the presurfactant era) had substantially reduced expiratory airflow at a mean age of 23 years [44] .

Preterm birth survivors, either with or without BPD, have increased frequency of respiratory symptoms commonly reported as asthma and increased bronchodilator use early in life [45] . These outcomes may persist into adulthood, although previous findings are inconsistent [42, [46] [47] [48] . A Swedish national cohort study of 622,616 persons born in 1973-1979 found that extremely preterm birth was associated with more than a 2-fold risk of asthma medication prescription at ages 25-35 years compared with term birth [49] . Other smaller studies J o u r n a l P r e -p r o o f Journal Pre-proof of young adults in Norway (ages 20-24 years) [50] and the UK (ages 18-25 years) [51] reported non-significant associations between preterm birth and asthma symptoms or diagnosis. A survey of 5,192 Finnish adults aged 31 years reported no association between preterm birth and asthma [52] . A retrospective cohort study of 149,398 Swedish males aged 17-20 years also did not confirm an association between preterm birth and physician-diagnosed asthma [53] . Preterm birth and BPD combined with harmful environmental exposures may potentially lead to higher risks of chronic obstructive pulmonary disease (COPD) later in adulthood [54] , but large cohort studies with longer follow-up times are needed for more definitive assessment.

Because of pulmonary and immune system immaturity, preterm children are more susceptible to respiratory viral infections and their complications [55, 56] , which may contribute to persistently reduced lung function later in life [57] . However, risks of respiratory infections and their complications have rarely been explored in adult survivors of preterm birth. A Swedish cohort analysis of 674,820 persons born in 1973-1979 found that preterm birth was associated with increased mortality attributed to infections (which were predominantly respiratory) at ages 29-36 years [58] . New population-based studies will be needed to assess the risks of complications and mortality associated with the novel virus SARS-CoV-2 in pretermborn children and adults.

A Swedish cohort study of >4 million persons examined whether preterm birth is associated with increased risk of sleep-disordered breathing (SDB), as identified from J o u r n a l P r e -p r o o f Journal Pre-proof nationwide outpatient and inpatient diagnoses [59] . After adjusting for other perinatal and maternal factors, preterm birth was associated with approximately 1. weeks) was associated with 2-fold risks of SDB in adulthood. These associations were found in both males and females, although preterm birth accounted for more SDB cases in males (additive interaction, P=0.003). Co-sibling analyses suggested that these findings were largely independent of unmeasured shared genetic or environmental factors in families. This evidence from a large national cohort suggests that preterm birth is an independent risk factor for SDB in early to mid-adulthood [59] . SDB symptomatology has rarely been explored in adult survivors of preterm birth.

However, a Finnish case-control study reported a >2-fold odds of chronic snoring among 158 young adults (ages 18-27 years) born preterm with very low birthweight (<1500 g) compared with 167 term controls (adjusted odds ratio, 2.21; 95% CI, 1.07-4.54) [60] .

Preterm birth interrupts fetal nephrogenesis, resulting in a lower nephron endowment [61, 62] and heightened susceptibility to chronic kidney disease (CKD) later in life. A recent national cohort study examined the risk of CKD identified from outpatient and inpatient diagnoses in >4 million persons born as singletons in Sweden during 1973-2014 who were followed up through 2015 [63] . After adjusting for other perinatal and maternal factors, persons born preterm or extremely preterm had nearly 2-fold and 3-fold risks of CKD, respectively, from birth to age 43 years. These associations were strongest in childhood, then weakened but remained substantially Co-sibling analyses suggested that these findings were not due to shared genetic or environmental factors in families, but rather to direct effects of preterm birth [63] .

Other studies have linked low birthweight (<2500 g) with higher risk of CKD in adulthood, without specifically examining gestational age at birth. A meta-analysis of 18 such studies reported a pooled odds ratio of 1.7 (95% CI, 1.4-2.1) [64] . The largest of those was a Norwegian cohort study of 2.2 million births, which reported that small for gestational age was associated with an increased risk of end-stage renal disease (ESRD) at ages up to 38 years (HR, 1.5; 95% CI, 1.2-1.9) [65] . In an overlapping Norwegian cohort of 1.8 million births, low birthweight was associated with an increased risk of ESRD at ages up to 42 years (adjusted HRs 1.6 to 1.8), which appeared to be unrelated to shared familial factors, and preterm birth was associated with a non-significantly increased risk of ESRD (adjusted HR, 1.3; 95% CI, 0.8-2.0) [66] .

Preterm birth is the most commonly reported cause of cerebral palsy and has been associated with other lifelong neurodevelopmental disorders. A meta-analysis of 26 studies reported a nearly 15% prevalence of cerebral palsy in those born extremely preterm (<28 weeks) [67] . Preterm birth survivors also have increased risks of cognitive impairment [68, 69] . Those born very preterm (<32 weeks) or with very low birthweight (<1500 g) have been reported to have lower head circumference at birth (mean difference, 7.5 cm) and lower IQ at age 26 years J o u r n a l P r e -p r o o f Journal Pre-proof have sufficient rigor reported no differences, whereas 4 studies reported lower quality of life in those born very preterm or with very low birthweight, and 3 were inconclusive [90] .

A recent national cohort study examined the prevalence of survival without any major comorbidities in 2.5 million persons born during 1973-1998 in Sweden who were followed up to ages 18-43 years [8] . Major comorbidities were assessed using the Adolescent and Young Adult Health Outcomes and Patient Experience (AYA HOPE) Comorbidity Index, comprised of 43 chronic disorders that commonly manifest in adolescence or young adulthood [8, 91] . The majority (54.6%) of persons born preterm and 22.3% of those born extremely preterm (22) (23) (24) (25) (26) (27) weeks) were still alive without any major comorbidities at ages 18-43 years, compared with 63.0% of those born full-term (P<0.001 for each comparison) [8] . These findings were similar among men and women, and appeared independent of birth year and other perinatal or maternal factors. When comorbidities were alternatively assessed using the Charlson Comorbidity Index [92] , 73.1% of those born preterm and 32.5% of those born extremely preterm survived into adulthood without any major comorbidities, compared with 81.8% of those born full-term, which also were significant differences (P<0.001 for each). Co-sibling analyses suggested that these differences were not explained by unmeasured shared genetic or environmental factors in families. The relatively high prevalence (>50%) of survival without major comorbidities among preterm-born adults reflects both the treatment advances that have occurred in the past 50 years and the resilience of preterm survivors in maintaining good health. However, those born at the earliest gestational ages face significantly greater long-term health and social challenges [8] . Figure 3 shows the prevalence of survival into adulthood without any major comorbidities (based on the AYA HOPE Index) by gestational age at birth and birth decade in this large cohort [8] .

J o u r n a l P r e -p r o o f

The present overview reveals several priorities for future research. First, most evidence on adult outcomes after preterm birth has originated from cohorts in a few high-income populations, especially in Nordic countries [93] . However, those populations have a lower prevalence of preterm birth [2] as well as other sociodemographic and health care differences compared with the US and many other countries. New studies will be needed in other populations when feasible, including in low-and middle-income countries, to explore the longterm sequelae of preterm birth and potential heterogeneity in racial/ethnic subgroups. Second, additional follow-up of existing cohorts will be needed to assess outcomes in later adulthood as such data become available. Increased risks of IHD associated with preterm birth were only recently identified after follow-up times were extended into mid-adulthood [27] , and other important associations may potentially emerge with follow-up to older ages. Third, most large cohort studies have lacked highly detailed or complete information on underlying causes of preterm birth. Studies with additional data on preterm birth subtypes that include follow-up into adulthood are a high priority to further elucidate mechanisms and improve long-term risk stratification. Lastly, studies with access to data on lifestyle factors later in life (e.g., physical activity, diet, obesity, alcohol or other substance use, social networks) are needed to assess their potential modifying effects on long-term outcomes in preterm-born adults. Such studies may help further identify protective factors that enhance resilience and well-being across the life course.

J o u r n a l P r e -p r o o f Journal Pre-proof A rapidly growing body of research indicates that preterm birth is associated with higher risks of cardiovascular, endocrine/metabolic, respiratory, renal, neurodevelopmental, and psychiatric disorders in early to mid-adulthood. These associations also lead to moderately increased mortality risks among men and women who were born preterm [6, 7, 9] . However, despite these increased risks, the majority of persons born preterm survive into adulthood without major comorbidities [8] and report a good health-related quality of life [90] .

Preterm birth should be recognized as a chronic condition that requires long-term followup to facilitate preventive actions and timely detection and treatment of adverse sequelae across the life course [4, 6] . Gestational age and other birth history should be routinely included in history-taking and medical records for patients of all ages [94] [95] [96] . Such information can provide additional valuable context for understanding patients' health and help trigger counseling and anticipatory screening in those born preterm [94] . High priorities for future research include the assessment of long-term sequelae of preterm birth in racially and economically diverse populations, further risk stratification by preterm birth subtype, and identification of protective factors that will support the long-term health trajectory of preterm birth survivors. 

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