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Olapeju et al.

BMC Pregnancy and Childbirth (2021) 21:594


https://doi.org/10.1186/s12884-021-04077-w

RESEARCH Open Access

Birth outcomes across the spectrum of


maternal age: dissecting aging effect versus
confounding by social and medical
determinants
Bolanle Olapeju1,2, Xiumei Hong1, Guoying Wang1, Amber Summers2, Irina Burd3, Tina L. Cheng4 and
Xiaobin Wang1,5*

Abstract
Background: Given the trend of increasing maternal age and associated adverse reproductive outcomes in the US,
this study aimed to assess whether this association is due to an independent aging or confounded by
sociodemographic, biomedical, or behavioral determinants in a predominantly Black US population.
Methods: Data was from 8509 women enrolled in the Boston Birth Cohort. Adverse reproductive outcomes
included spontaneous preterm delivery, cesarean delivery, and low birth weight. Covariates included
sociodemographic (parity, race/ethnicity, education, marital status, income, receipt of public assistance, nativity);
biomedical (obesity, hypertensive disorders, diabetes mellitus); and behavioral (consistent intake of multivitamin
supplements, support from father of baby, support from family, major stress in pregnancy, cigarette smoking,
alcohol intake). Analysis included Lowess and marginal probability plots, crude and adjusted sequential logistic
regression models to examine age-outcome associations and to what degree the association can be explained by
the above covariables.
Result: Overall, the study sample had high levels of spontaneous preterm birth (18%), cesarean delivery (33%) and
low birth weight (26%). Unadjusted models showed no significant difference odds of spontaneous preterm birth by
maternal age but higher odds of cesarean section (aOR: 1.77, 95% CI: 1.60, 1.95) and low birth weight (aOR: 1.15,
95% CI: 1.04, 1.28) among women 30 years or older. Adjustment for sociodemographic factors, biomedical
conditions and behavioral factors revealed higher odds of spontaneous preterm birth: (aOR: 1.30, 95% CI: 1.14, 1.49),
cesarean section deliveries (aOR: 1.68, 95% CI: 1.51, 1.87) and low birth weight (aOR: 1.36, 95% CI: 1.21, 1.53). Across
all ages, optimal BMI status and consistent multivitamin supplement intake were protective of spontaneous preterm
birth and low birth weight.

* Correspondence: xwang82@jhu.edu
1
Department of Population, Family and Reproductive Health, Johns Hopkins
University Bloomberg School of Public Health, 615 N. Wolfe Street, E4132,
Baltimore, MD 21205-2179, USA
5
Department of Pediatrics, Johns Hopkins University School of Medicine,
Baltimore, MD, USA
Full list of author information is available at the end of the article

© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
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The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the
data made available in this article, unless otherwise stated in a credit line to the data.
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 2 of 11

Conclusion: In this high-risk minority population, we demonstrated that the association between increasing
maternal age and adverse pregnancy outcomes was due to an independent aging effect and the presence of
confounding by sociodemographic, biomedical, and behavioral factors. Some modifiable risk factors to counteract
aging effect, include optimizing BMI and consistent intake of multivitamin supplement. A fundamental change in
how care is provided to women, particularly low income Black women, is needed with emphasis on the protective
role of optimal nutritional status.
Trial registration: ClinicalTrials.gov Identifier: NCT03228875
Keywords: Age, Cesarean section, High-risk, Low birth weight, Minority, Preterm birth, Race

Background Further research is needed to understand what extent


The mean age of mothers in the US is currently at a record the relationship between maternal age and adverse preg-
high of 29 years, ranging from 27.1 years in American In- nancy outcomes is due to an aging effect or confounded
dian or Alaska Native (AI/AN) women to 31.8 years in by sociodemographic, biomedical, or behavioral factors.
Asian women [1, 2]. The rising age of mothers has been at- The complexity of these factors requires an analysis
tributed to increased birth rates among older women as which is well-designed to interrogate how and to what
provisional birth rates for 2019 show a decline women aged degree each individual component, as well as the com-
15–34 and an increase for women aged 40–44 [3]. While bination thereof, may ultimately contribute to pregnancy
delayed childbearing offers associated societal benefits such outcomes. Such research findings can inform existing
as improved health and education outcomes in children as guidelines and tailor interventions across the female life
well as financially and emotionally empowered women who course, including the preconception, pregnancy, postpar-
are often more prepared for child rearing [4], it is also of tum and interconception periods. In addition, such re-
clinical and public health importance as aging is associated search would also inform whether existing guidelines
with fertility decline, with the fecundity of women decreas- and strategy to address adverse outcomes need to be fur-
ing gradually at age 32 years and more rapidly after age 37 ther stratified by other factors (such as race/ethnicity) in
years [5]. Maternal age also influences the total number of order to mitigate long-lasting unfavorable trends in
births a woman has over a lifetime, impacting the compos- pregnancy outcomes.
ition and growth of the US population [6]. In addition, in- Our study explores the relationship between maternal
creased maternal age is associated with adverse pregnancy age and adverse outcomes- spontaneous preterm birth,
outcomes such as birth defects, preterm birth, cesarean de- cesarean delivery, and low birth weight - among a low-
livery, preeclampsia, postpartum hemorrhage, gestational income minority US population. We explore to what ex-
diabetes among others [7, 8]. tent the relationship between age and adverse outcomes
The mechanisms through which increasing maternal is confounded by sociodemographic, biomedical, and be-
age result in adverse pregnancy outcomes are not yet havioral determinants. Of particular interest is the role
fully understood. In addition to fertility decline, aging also of modifiable risk factors such as pre-pregnancy body
results in a worsened overall health of women [9, 10] in- mass index (BMI) and multivitamin supplement intake
cluding medical conditions such as hypertension, diabetes during pregnancy as confounders. Our study findings
[11] and obesity [12], potentially confounding the relation- aim to inform the design of contextually relevant ap-
ship between maternal age and adverse pregnancy out- proaches and interventions for similar low income mi-
comes. Another major confounder is race/ethnicity as nority US populations.
adverse pregnancy outcomes are more common among
minority populations. Non-Hispanic Black and AI/AN
women are two to three times more likely to die from Methods
pregnancy-related causes than non-Hispanic White Study design
women [13]. This race/ethnic disparity in pregnancy- Study data are from the Boston Birth Cohort (BBC)
related deaths has persisted over time and has recently study, which has been described elsewhere [23]. In sum-
been shown to worsen with the age of the woman mary, participants in the BBC study are women with a
[13]. Other potential confounders identified in the lit- singleton, live infant (without major birth defects) en-
erature include psychosocial factors such as rural resi- rolled from 1998 to date at the Boston Medical Center
dence [14], low maternal socio-economic status [15], (BMC), a large urban hospital serving a predominantly
lower levels of education [14, 16] and inadequate pre- Black, low-income, inner-city patient population. The
natal care [7, 17–22]. BBC oversampled for preterm births and/or low birth
weight in a 1:2 ratio compared with term, normal weight
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 3 of 11

births. Exclusion criteria were deliveries with major birth (none or little, some, excellent, further dichotomized to
defects or congenital chromosomal abnormalities, or due excellent versus not excellent); perceived stress in preg-
to multiple gestation or in-vitro fertilization. Among eli- nancy -(yes versus no); cigarette smoking (never versus
gible mothers approached by the study team, enrollment any), alcohol consumption (never versus any) and con-
rate was about 83%. This cross-sectional study analysis sistent multivitamin supplement (at least three times a
focuses on all women (N = 8509) enrolled in the BBC- a week) throughout pregnancy (yes or no). Women were
reflection of the patient population of the BMC. Data asked how often they took multivitamin or over the
sources include a postpartum questionnaire adminis- counter supplements in each trimester. Options included
tered by trained data collectors within 72 h of birth as none, less than once a week, one to two times a week,
well as participants’ medical records. The study protocol three to five times a week and more than five times a
was approved by the Institutional Review Boards of Bos- week. Multivitamin supplement intake at least three
ton University Medical Center and Johns Hopkins times has been associated with improved pregnancy out-
Bloomberg School of Public Health. comes in this study population as documented previ-
ously [23].
Study variables
The independent variable, maternal age was based on Statistical analysis
age at delivery from medical records categorized into de- All analyses were conducted using STATA version 15
cades as follows: less than 20; 20–29; 30–39; and 40 or (College Station, TX: StataCorp LP). Chi square tests of
more years. Data were extracted from medical records association explored maternal characteristics across the
for the following dependent variables: i) spontaneous different age groups. LOWESS (locally weighted scatter-
preterm delivery, defined as a live birth before 37 com- plot smoothing) plots were used to graph the distribu-
pleted weeks of gestation with a clinical presentation of tion of adverse pregnancy outcomes, obesity, and
uterine contraction or rupture of membranes (yes or multivitamin use in pregnancy by maternal age as well
no); ii) cesarean delivery (yes or no); and iii) low birth as race/ethnicity to highlight any racial differences in the
weight defined as a birthweight less than 2500 g (yes or relationship between these adverse outcomes and age.
no). The relationship between maternal age and adverse out-
Biomedical factors were also extracted from partici- comes were further explored using bivariate and sequen-
pants’ medical records. These included pregestational/ tial multivariable logistic regression models including
gestational diabetes (yes versus no) and hypertensive dis- the groups of sociodemographic, biomedical, and behav-
orders defined as (yes versus no) the presence of any of ioral variables described above. Additional regressions
the following diagnoses: gestational hypertension, pre- were done among the subgroup of Black women only,
eclampsia, eclampsia, or hemolysis, elevated liver en- given their higher risk of these outcomes. Finally, mar-
zymes, and/or low platelets (HELLP) syndrome. In ginal probabilities of all adverse outcomes were plotted
addition, year of delivery (< 2006 (the median) versus by maternal age. Missing data was minimal (< 8%) for all
≥2006) was included as a contextual variable. variables except yearly income (11%) and multivitamin
Maternal self-reported variables assessed from the supplement intake (12%). Initial description of the study
post-partum questionnaire included maternal race cate- population accounted for missing data as a separate cat-
gorized into: Black (Black, African American, Cape Ver- egory while subsequent analyses reclassified missing data
dean or Haitian)) versus non-Black, parity (nulliparous using simple imputation (assigned to the race- and age-
versus multiparous), pre-pregnancy BMI from their specific most frequent category). All P-values in the ana-
weight and height (underweight, normal weight, over- lyses were based on two-sided statistical tests and the
weight and obese), education (<College versus ≥College), Type I error rate was set at 0.05.
marital status (unmarried versus married), year of deliv-
ery, receipt of public assistance including: WIC (Women Results
Infants and Children), Food Stamps, AFDC (Aid to Fam- Table 1 presents the characteristics of the study popula-
ilies with Dependent Children), Housing assistance or tion by maternal age. Overall, women were mostly Black,
Fuel assistance (yes versus no); yearly income (<$30,000 multiparous, had less than a college education, unmar-
(the median), ≥$30,000 and unknown) and nativity (US ried, on public assistance, reported an income of
born versus non-US born). <$30,000. On average, about a fifth (19%) of women
Behavioral factors were also self-reported and in- were obese, 13% had hypertensive disorders of preg-
cluded: perceived support during pregnancy from the nancy while 10% had diabetes mellitus. Less than half of
father of the baby (none or little, some, excellent, further all women reported excellent support from the father of
dichotomized to excellent versus not excellent); per- their baby or from their families while 22% of women
ceived support during pregnancy from family members noted a very stressful pregnancy. Few women reported
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 4 of 11

Table 1 Characteristics of the study population by maternal age groups (N = 8509)


Maternal < 20 years 20–29 years 30–39 years 40+ years Total P-
Characteristics valuea
N % N % N % N % N %
Total 907 100 4305 100 2960 100 337 100 8509 100
Sociodemographic
Race/ethnicity < 0.001
Blackb 488 53.8 2073 48.2 1613 54.5 219 65.0 4393 51.6
Non-Black 419 46.2 2232 51.8 1347 45.5 118 35.0 4116 48.4
Parity < 0.001
Nulliparous 760 83.8 2103 48.9 751 25.4 49 14.5 3663 43.0
Multiparous 147 16.2 2202 51.1 2209 74.6 288 85.5 4846 57.0
Education (n = 8349) < 0.001
< College 813 91.3 2733 64.9 1658 56.9 219 66.0 5423 65.0
≥ College 77 8.7 1479 35.1 1257 43.1 113 34.0 2926 35.0
Marital Status (n = 8340) < 0.001
Not married 842 94.8 2984 70.8 1473 50.7 170 51.5 5469 65.6
Married 46 5.2 1232 29.2 1433 49.3 160 48.5 2871 34.4
c
Public assistance (n = 8378) 0.580
No 157 17.5 813 19.2 572 19.6 63 18.9 1605 19.2
Yes 738 82.5 3423 80.8 2341 80.4 271 81.1 6773 80.8
Yearly Income in US$ (n = 7616) < 0.001
≥ $30,000 18 2.3 470 12.1 547 20.7 59 19.2 1094 14.4
< $30,000 321 40.1 1861 48.1 1167 44.2 138 44.8 3487 45.8
Don’t know 461 57.6 1538 39.8 925 35.1 111 36.0 3035 39.9
Place of birth (n = 8310) < 0.001
Not US born 309 34.7 2400 57.0 2096 72.8 270 81.3 5075 61.1
US born 581 65.3 1809 43.0 783 27.2 62 18.7 3235 38.9
Biomedical
Body Mass Index (n = 7930) < 0.001
< 19 97 11.3 324 8.1 109 3.9 6 1.9 536 6.8
19–24 467 54.4 1899 47.5 1147 41.5 118 37.9 3631 45.8
25–29 197 22.9 1003 25.1 853 30.9 103 33.1 2156 27.2
≥ 30 98 11.4 770 19.3 655 23.7 84 27.0 1607 20.3
Hypertensive disorders of pregnancy (n = 8498) < 0.001
No 810 89.3 3830 89.1 2519 85.2 272 80.7 7431 87.4
Yes 97 10.7 467 10.9 438 14.8 65 19.3 1067 12.6
Pregestational/gestational diabetes (n = 8500) < 0.001
No 876 96.7 3957 92.1 2524 85.3 260 77.2 7617 89.6
Yes 30 3.3 340 7.9 436 14.7 77 22.8 883 10.4
Behavioral
Father of baby support (n = 7829) < 0.001
None/Little 201 24.3 634 16.1 383 14.0 55 17.6 1273 16.3
Some 278 33.6 1474 37.3 993 36.3 126 40.4 2871 36.7
Excellent 349 42.1 1842 46.6 1363 49.8 131 42.0 3685 47.1
Family support (n = 7917) 0.014
None/Little 47 5.6 301 7.5 215 7.7 30 9.3 593 7.5
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 5 of 11

Table 1 Characteristics of the study population by maternal age groups (N = 8509) (Continued)
Maternal < 20 years 20–29 years 30–39 years 40+ years Total P-
Characteristics valuea
N % N % N % N % N %
Total 907 100 4305 100 2960 100 337 100 8509 100
Some 368 44.2 1786 44.8 1225 44.1 167 51.9 3546 44.8
Excellent 418 50.2 1900 47.7 1335 48.1 125 38.8 3778 47.7
Major stressful events in pregnancy 0.030
No 663 75.8 3136 75.5 2262 79.1 256 79.3 6317 76.9
Yes 212 24.2 1017 24.5 598 20.9 67 20.7 1894 23.1
Smoking cigarettes (n = 8441) < 0.001
Never 717 79.3 3321 77.8 2478 84.4 289 87.0 6805 80.6
Ever 187 20.7 949 22.2 457 15.6 43 13.0 1636 19.4
Drinking alcohol (n = 8201) 0.606
Never 798 91.3 3747 90.6 2630 91.5 290 90.6 7465 91.0
Ever 76 8.7 387 9.4 243 8.5 30 9.4 736 9.0
Multivitamin supplement intake at least 3 times a week throughout pregnancy (n = 7496) < 0.001
No 273 34.3 1050 27.7 587 22.4 71 24.5 1981 26.4
Yes 524 65.7 2742 72.3 2030 77.6 219 75.5 5515 73.6
a
p-value from chi square tests of association; b Maternal self-report as Black, African American, Haitian or Cape Verdian;c receipt of public assistance including:
WIC (Women Infants and Children), Food Stamps, AFDC (Aid to Families with Dependent Children), Housing assistance or Fuel assistance

ever smoking cigarettes (19%), drinking alcohol (9%) or increased linearly with age. Across all ages, low birth
inconsistent vitamin supplement intake (23%). Of note, weight rates were higher among Blacks.
most maternal characteristics varied by age groups ex- In Fig. 2, the distribution of some major risk factors of
cept drinking of alcohol and receipt of public assistance. adverse outcomes as well as nutritional status by mater-
Adverse pregnancy outcomes among this population nal age and race shows that the rates of hypertensive dis-
highlighted in Table 2 included spontaneous preterm orders and BMI increased with maternal age and was
birth (18%), cesarean delivery (33%) and low birth weight higher among Blacks. Consistent multivitamin supple-
(26%). Spontaneous preterm delivery rates did not differ ment intake in pregnancy also increased with age, but
significantly across maternal age groups. Figure 1 high- was lower in Blacks .
lights the distribution of adverse outcomes by maternal Table 3 highlights the crude and adjusted odds of ad-
age and race. The relationship between both spontan- verse outcomes across age groups (reference: 20–29 year
eous preterm deliveries and low birth weight with age olds), controlling for sociodemographic factors (maternal
was sinusoidal with rates being highest among women race, parity, education, marital status, receipt of public
less than 20 or more than 40 while cesarean deliveries assistance, yearly income, nativity), biomedical condi-
tions (obesity, hypertensive disorders and diabetes

Table 2 Adverse outcomes in study population by maternal age groups (N = 8509)


Adverse < 20 years 20–29 years 30–39 years 40+ years Total P-
Pregnancy valuea
N % N % N % N % N %
Outcomes
Total 907 100 4305 100 2960 100 337 100 8509 100
Spontaneous preterm delivery 0.546
No 736 81.1 3561 82.7 2417 81.7 275 81.6 6989 82.1
Yes 171 18.9 744 17.3 543 18.3 62 18.4 1520 17.9
Cesarean delivery (n = 8420) < 0.001
No 725 80.8 3045 71.6 1731 58.9 158 47.2 5659 67.2
Yes 172 19.2 1206 28.4 1206 41.1 177 52.8 2761 32.8
Low birth weight 0.037
No 659 72.7 3240 75.3 2147 72.5 242 71.8 6288 73.9
Yes 248 27.3 1065 24.7 813 27.5 95 28.2 2221 26.1
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 6 of 11

Fig. 1 Lowess smoothing plots showing prevalence of adverse outcomes (spontaneous preterm birth, cesarean delivery, and low birth weight)
by maternal age in total sample and stratified by racial groups

Fig. 2 Lowess smoothing plots showing selected covariables (hypertensive disorders, BMI, and consistent multivitamin intake) by maternal age in
total sample and stratified by racial groups
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 7 of 11

Table 3 Crude and sequentially adjusted associations of maternal age with adverse pregnancy outcomes in all women (N = 8509)
and among black women only (N = 4393)
Maternal Age All Women Black Women Only
a
Crude OR Adjusted OR Crude OR Adjusted ORa
Spontaneous Preterm Birth
20–29 years (ref) 1.00 1.00 1.00 1.00
< 20 years 1.11 (0.92–1.34) 0.93 (0.76–1.13) 1.12 (0.87–1.45) 0.88 (0.67–1.16)
30–39 years 1.08 (0.95–1.21) 1.30 (1.14–1.49) 1.11 (0.94–1.32) 1.42 (1.18–1.71)
40+ years 1.08 (0.81–1.44) 1.39 (1.03–1.88) 1.02 (0.70–1.47) 1.37 (0.93–2.02)
Cesarean Section
20–29 years (ref) 1.00 1.00 1.00 1.00
< 20 years 0.60 (0.50–0.72) 0.62 (0.51–0.74) 0.59 (0.46–0.75) 0.61 (0.47–0.79)
30–39 years 1.77 (1.60–1.95) 1.68 (1.51–1.87) 1.68 (1.47–1.93) 1.64 (1.41–1.92)
40+ years 2.84 (2.27–3.56) 2.58 (2.03–3.27) 2.52 (1.90–3.34) 2.42 (1.79–3.28)
Low Birth Weight
20–29 years (ref) 1.00 1.00 1.00 1.00
< 20 years 1.14 (0.97–1.35) 0.92 (0.77–1.10) 1.17 (0.94–1.46) 0.91 (0.72–1.16)
30–39 years 1.15 (1.04–1.28) 1.36 (1.21–1.53) 1.19 (1.03–1.37) 1.58 (1.34–1.87)
40+ years 1.19 (0.93–1.53) 1.42 (1.09–1.85) 1.20 (0.88–1.62) 1.66 (1.19–2.32)
a
Covariates include: sociodemographic factors (maternal race, parity, education, marital status, receipt of public assistance, yearly income, nativity), biomedical
conditions (obesity, hypertensive disorders and diabetes mellitus) and behavioral factors (including positive factors such as consistent intake of multivitamin
supplements, support from father of baby, support from family, and negative factors such as major stress in pregnancy, cigarette smoking and alcohol intake)

mellitus) and behavioral factors (including positive fac- Supplemental Table 2. Of note, Blacks had higher odds
tors such as consistent intake of multivitamin supple- of low birth weight. While smoking and sub-optimal
ments, support from father of baby, support from family, BMI worsened all outcomes, nulliparity was protective
and negative factors such as major stress in pregnancy, of all outcomes. Consistent multivitamin supplement in-
cigarette smoking and alcohol intake). take, higher education and being married reduced spon-
Unadjusted models show no significant difference in taneous preterm birth and low birth weight but US
spontaneous preterm birth odds by maternal age. How- nativity worsened all three outcomes.
ever, adjusted odds were higher among women 30–39 Figure 3 highlights the marginal probabilities of ad-
year old (aOR: 1.30, 95% CI: 1.14, 1.49) and 40 years and verse outcomes by maternal age after accounting for
older (aOR: 1.39, 95% CI: (1.03–1.88). Both crude and sociodemographic, biomedical, and behavioral factors.
adjusted odds of cesarean section was significantly lower The marginal probability of spontaneous preterm birth
among women less than 20 years old (aOR: 0.62, 95% CI: increases gradually with maternal age from less than 20
0.51, 0.74) but higher odds among women 30–39 (aOR: years to 30–39 years with a very slight increase at 40
1.68, 95% CI: 1.51, 1.87) and 40 years and older (aOR: years or older. For cesarean section, the marginal prob-
2.58, 95% CI: 2.03, 3.27). Similarly, both crude and ad- ability increases linearly with maternal age from whereas
justed odds of low birth weight was significantly higher for low birth weight, the marginal probability increases
among 30–39 (aOR: 1.36, 95% CI: 1.21, 1.53) and 40 linearly for with maternal age up to 30–39 years old but
years and older (aOR: 1.42, 95% CI: 1.09, 1.85). The does not change among women 40 years or older. The
trends in crude and adjusted odds of adverse outcomes observed trends are unchanged for the sub-group of
persisted among a sub-sample of Black women only. Of Black women only.
note, the adjusted odds of spontaneous preterm birth
(aOR: 1.42, 95% CI: 1.18, 1.71) and low birth weight Discussion
(aOR: 1.58, 95% CI: 1.34, 1.87) were higher among 30– This study aimed to explore the relationship between
39 year old Black women compared to the full sample. maternal age and adverse outcomes- spontaneous pre-
The changes in the odds ratios of adverse outcomes term birth, cesarean delivery, and low birth weight -
with sequential adjustments for sociodemographic, bio- among a low-income minority US population. Our study
medical and behavioral factors are presented in Supple- shows that after accounting for race and other psycho-
ment Table 1 while further analysis on the influence of social risk factors, adverse pregnancy outcomes were
these factors on adverse outcomes is presented in higher among older mothers, particularly those 30 years
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 8 of 11

Fig. 3 Marginal Probabilities of Adverse Outcomes after Adjusting for Sociodemographic, Biomedical, and Behavioral Factors by Maternal Age
Overall and among Black Women only

or older. In addition, adverse outcomes were higher This study reaffirms maternal age and race disparities
among Black women across the age spectrum. However, in low birth weight demonstrated in the literature [26].
the relationship between maternal age and adverse out- Racial disparities are typically explored without taking
comes varied depending on the sociodemographic, bio- age groups into account, despite age being an important
medical, and behavioral factors accounted for. biologic factor for several outcomes. In contrast, this
The increased risk of adverse outcomes with age study explores disparities across the entire spectrum of
may be due to an inherent increased risk in pregnan- reproductive age among a predominantly urban, low in-
cies in mothers at the extreme ages. Research sug- come (on public assistance) population. However, poor
gests that adolescent pregnancy is associated with outcomes may be due to a constellation of causes be-
immature pelvises and an increased risk of longer yond race/ethnicity, including health providers’ implicit/
labor and cesarean delivery indicated for failure to explicit bias, segregation, poverty, poorly-funded schools,
progress or descent [24]. However this study found etc., which disproportionately affect communities of
adolescents at lower risk of cesarean delivery as well color and manifest as low health literacy, poor access to
as hypertensive disorders. Aging typically results in a high-quality care, lack of social support. To mitigate
deterioration of most physiological functions [25], and these disparities, a fundamental change in how care is
chronological age is used as a marker for (though not provided to women, particularly low income Black
equivalent to) biological or reproductive age. In- women, may be needed. Women’s health care should
creased cerebrovascular, cardiac, and respiratory mor- seek to mitigate sociodemographic, biomedical and be-
bidity in older mothers is partly attributed to havioral risk factors as well as employ a life course per-
physiological changes associated with aging, such as spective in order to combat the observed persistent
muscle atrophy, reduced cardiac reserve, atheroscler- health disparities across the age spectrum. Our study
osis, and reduced lung function. Due to the added highlighted potentially modifiable factors influencing ad-
physiological burden of pregnancy, declining organ verse pregnancy outcomes. Such factors include optimal
function may be more apparent in older women. BMI, multivitamin supplement intake, level of education,
Given the trend of increasing maternal age in the US, social support, stress during pregnancy, and cigarette
pregnancy complications are likely to persist or even smoking. These findings underscore the importance of
rise, unless relevant public health and social interven- optimal nutritional status and social support in promot-
tions are instituted to optimize pregnancy outcomes ing healthy behavior across all age groups. The study
among the growing population of older mothers. suggests that maternal age, particularly adolescence (less
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 9 of 11

than 20) and advanced maternal age (40 years or more) National and state level health insurance policy changes
may be a social and public health issue given the influ- are critical and are urgently needed to ensure expanded
ence of maternal age on individual health as well as access to health care particularly among low or middle
population level outcomes [20, 27]. income minority young women.
The study also observed that US nativity worsened the This study has a number of strengths. First, with a ma-
risk of adverse outcomes while nulliparity was protect- jority low income (on public assistance), racial minority,
ive. Our findings and other recent publication from the urban population, the BBC is representative of a high
BBC [28, 29] corroborate the healthy migrant theory risk yet understudied population. Thus, study findings
[30] which has been documented among South America are generalizable to similar low income, minority, urban
and Asia born US migrants [31]. However, given this US populations. The study employed a rich dataset in-
study does not disaggregate women by race and nativity, cluding sociodemographic, biomedical, and behavioral
the degree to which this would apply to Black migrants variables. In addition, the study explored associations
specifically and warrants further investigation. The pro- with biological age groups- and did not include multiple
tective effect of nulliparity on adverse pregnancy has gestations, major chromosomal abnormalities, congenital
been well-documented and may be partly explained by malformations, and IVF which typically occur more in
its association with younger maternal age [32]. older women.
Study findings can inform tailored interventions in However, the study acknowledges the following limita-
order to mitigate adverse health outcomes particularly tions. First, the data is cross sectional and cannot infer
among high risk groups such as Blacks or advanced ma- causality. Second, a number of outcomes including age,
ternal age pregnancies. Given the role of BMI and con- race and consistent multivitamin supplement were self-
sistent vitamin intake on adverse outcomes, targeted reported and this may potentially lead to misclassifica-
interventions should start as early as possible and aim to tion. Of note, all adverse pregnancy outcomes and BMI
improve nutritional status and may include promoting status were objectively assessed using clinical data. The
micronutrient supplementation/fortification, an individ- study does not explore other aspects of nutritional status
ualized approach for food/nutrient provision, nutrition such as diet and physical activity. In view of these, our
education, nutrition counselling and co-ordination of findings warrant additional studies. In addition, due to
nutrition care across all ages with emphasis among Black the low prevalence of some racial groups such as Asians
mothers and those at the extreme ages, as well as those and AI/AN, this study was unable to fully explore some
with a sub-optimal nutritional status, or low levels of so- racial, ethnic or nativity differences that may explain
cial support [33]. some of the study findings.
Given the role of BMI on adverse outcomes, efforts to In summary, our study found that in this predomin-
integrate individualized nutrition care into clinical guide- antly urban, low-income, predominantly Black US popu-
lines for preconception and prenatal care should be lation, adverse pregnancy outcomes differed significantly
thoroughly explored. A study demonstrated that an inte- by maternal age. However, this relationship was complex
grated WIC and obstetrical service model employing en- and was in part attributable to confounding by sociode-
hanced nutrition services and education is feasible and mographic, biomedical, and behavioral factors. Add-
can limit postpartum weight retention in women with itional research and structural and policy interventions
obesity [34]. Study findings reinforce the need for holis- should take these factors into account.
tic interventions that take women’s context into account,
employing the social ecological model which considers Supplementary Information
the complex interplay between individual, interpersonal, The online version contains supplementary material available at https://doi.
org/10.1186/s12884-021-04077-w.
community, and societal factors influencing health.
School based interventions [35] may prove beneficial for
Additional file 1 : Supplement Table 1. Crude and Sequentially
younger women while workplace interventions for older Adjusted Associations of Maternal Age with Adverse Pregnancy
women [36]. Community level interventions should Outcomes (N=8509). Supplement Table 2. Maternal age, race,
strive to create social support for pregnant women such nutritional status, and other characteristics associated with adverse
outcomes (N=8509).
as the use of in-person or virtual support groups where
mothers with similar contexts can engage. Structural,
Acknowledgements
and policy interventions are needed to improve availabil- Not applicable.
ity of healthy food options particularly among low in-
come populations that often live in food deserts. Authors’ contributions
Furthermore, all women should have access to quality XW, BO and IB conceptualized the study. XH and GW performed the data
cleaning and management. BO and XW analyzed and interpreted the data.
preconception, prenatal and postnatal health care, re- All authors participated in the revision of the manuscript and reviewed and
gardless of their age, race, or socioeconomic status. approved the final manuscript.
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 10 of 11

Funding 11. Campbell KH, Savitz D, Werner EF, Pettker CM, Goffman D, Chazotte C, et al.
Sources of Financial Support: Maternal morbidity and risk of death at delivery hospitalization. Obstet
The Boston Birth Cohort (the parent study) was supported in part by the Gynecol. 2013;122(3):627–33.
March of Dimes PERI grants (20-FY02–56, #21-FY07–605); the National 12. Hinkle SN, Sharma AJ, Kim SY, Park S, Dalenius K, Brindley PL, et al.
Institutes of Health (NIH) grants (R21ES011666, 2R01HD041702, Prepregnancy obesity trends among low-income women, United States,
R21HD066471, R01HD086013, R01HD098232, R01 ES031272, R01ES031521); 1999–2008. Matern Child Health J. 2012;16(7):1339–48.
and the Health Resources and Services Administration (HRSA) of the U.S. 13. Petersen EE, Davis NL, Goodman D, Cox S, Syverson C, Seed K, et al. Racial/
Department of Health and Human Services (HHS) (UJ2MC31074). This ethnic disparities in pregnancy-related deaths—United States, 2007–2016.
information or content and conclusions are those of the authors and should Morb Mortal Wkly Rep. 2019;68(35):762.
not be construed as the official position or policy of, nor should any 14. Amjad S, MacDonald I, Chambers T, Osornio-Vargas A, Chandra S,
endorsements be inferred by any funding agencies. Voaklander D, et al. Social determinants of health and adverse maternal and
birth outcomes in adolescent pregnancies: a systematic review and meta-
Availability of data and materials analysis. Paediatr Perinat Epidemiol. 2019;33(1):88–99.
The datasets used and/or analyzed during the current study are available 15. Margerison-Zilko CE, Li Y, Luo Z. Economic conditions during pregnancy
from the corresponding author on reasonable request. and adverse birth outcomes among singleton live births in the United
States, 1990-2013. Am J Epidemiol. 2017;186(10):1131–9.
Declarations 16. Biney AAE, Nyarko P. Is a woman's first pregnancy outcome related to her
years of schooling? An assessment of women's adolescent pregnancy
Ethics approval and consent to participate outcomes and subsequent educational attainment in Ghana. Reprod Health.
All research was performed in accordance with the Declaration of Helsinki 2017;14(1):123.
and other relevant guidelines and regulations. The study protocol was 17. Kassa GM, Arowojolu AO, Odukogbe AA, Yalew AW. Adverse neonatal
approved by the Institutional Review Boards of Boston University Medical outcomes of adolescent pregnancy in Northwest Ethiopia. PLoS One. 2019;
Center (#H23525) and Johns Hopkins Bloomberg School of Public Health 14(6):e0218259.
(#00003960). Informed consent for study participation was obtained from all 18. Leftwich HK, Alves MV. Adolescent Pregnancy. Pediatr Clin N Am. 2017;64(2):
subjects. 381–8.
19. Narukhutrpichai P, Khrutmuang D, Chattrapiban T. The obstetrics and
Consent for publication neonatal outcomes of teenage pregnancy in Naresuan University Hospital. J
Not applicable. Med Assoc Thail. 2016;99(4):361–7.
20. Lemoine M-E, Ravitsky V. Sleepwalking into infertility: the need for a public
Competing interests health approach toward advanced maternal age. Am J Bioeth. 2015;15(11):
The authors declare that they have no competing interests 37–48.
21. Malabarey OT, Balayla J, Klam SL, Shrim A, Abenhaim HA. Pregnancies in
Author details young adolescent mothers: a population-based study on 37 million births. J
1
Department of Population, Family and Reproductive Health, Johns Hopkins Pediatr Adolesc Gynecol. 2012;25(2):98–102.
University Bloomberg School of Public Health, 615 N. Wolfe Street, E4132, 22. Geronimus AT. Damned if you do: culture, identity, privilege, and teenage
Baltimore, MD 21205-2179, USA. 2Center for Communication Programs, Johns childbearing in the United States. Soc Sci Med. 2003;57(5):881–93.
Hopkins Bloomberg School of Public Health, Baltimore, MD, USA. 3Integrated 23. Olapeju B, Saifuddin A, Wang G, Ji Y, Hong X, Raghavan R, et al. Maternal
Research Center for Fetal Medicine, Department of Gynecology and postpartum plasma folate status and preterm birth in a high-risk US
Obstetrics, Johns Hopkins University School of Medicine, Baltimore, MD, USA. population. Public Health Nutr. 2018;22:1281–91.
4 24. Ganchimeg T, Ota E, Morisaki N, Laopaiboon M, Lumbiganon P, Zhang J,
Department of Pediatrics, Cincinnati Children’s Hospital Medical Center,
University of Cincinnati, Cincinnati, OH, USA. 5Department of Pediatrics, et al. Pregnancy and childbirth outcomes among adolescent mothers: a
Johns Hopkins University School of Medicine, Baltimore, MD, USA. World Health Organization multicountry study. BJOG Int J Obstet Gynaecol.
2014;121:40–8.
Received: 28 March 2021 Accepted: 9 August 2021 25. Cohen W. Does maternal age affect pregnancy outcome? BJOG Int J Obstet
Gynaecol. 2014;121(3):252–4.
26. Berger BO, Wolfson C, Reid LD, Strobino DM. Adverse birth outcomes
References among women of advanced maternal age with and without health
1. Martin JA, Hamilton BE, Osterman MJ, Driscoll AK. Births: final data for 2018; conditions in Maryland. Womens Health Issues. 2021;31(1):40–8.
2019. 27. Melnikas AJ, Romero D. Ideal age at first birth and associated factors among
2. Mathews T, Hamilton BE. Mean age of mother, 1970–2000. Natl Vital Stat young adults in greater new York City: findings from the social position and
Rep. 2002;51(1):1–13. family formation study. J Fam Issues. 2020;41(3):288–311.
3. Martin JA, Hamilton BE, Osterman MJ. Births: Provisional data for 2019. USA: 28. Boakye E, Sharma G, Ogunwole SM, Zakaria S, Vaught AJ, Kwapong YA, et al.
Services USDoHaH, Prevention CfDCa, Statistics NCfH, System NVS; 2020. Relationship of preeclampsia with maternal place of birth and duration of
4. Duncan GJ, Lee KT, Rosales-Rueda M, Kalil A. Maternal age and child residence among non-Hispanic black women in the United States.
development. Demography. 2018;55(6):2229–55. Circulation. 2021;14(2):e007546.
5. Medicine PCotASfR. Female age-related fertility decline. Committee opinion 29. Olapeju B, Ahmed S, Hong X, Wang G, Summers A, Cheng TL, et al.
no. 589. Obstet Gynecol. 2014;123(3):719–21. Maternal hypertensive disorders in pregnancy and postpartum plasma B
6. Mathews TJ, Hamilton BE. Mean age of mothers is on the rise: United vitamin and Homocysteine profiles in a high-risk multiethnic US Population.
States, 2000-2014. USA: NCHS data brief. 2016(232):1–8. J Womens Health. 2020;29(12):1520–9.
7. Lean SC, Derricott H, Jones RL, Heazell AE. Advanced maternal age and 30. Wingate MS, Alexander GR. The healthy migrant theory: variations in
adverse pregnancy outcomes: a systematic review and meta-analysis. PLoS pregnancy outcomes among US-born migrants. Soc Sci Med. 2006;62(2):
One. 2017;12(10):e0186287. 491–8.
8. Lisonkova S, Potts J, Muraca GM, Razaz N, Sabr Y, Chan W-S, et al. Maternal 31. Alexander GR, Mor JM, Kogan MD, Leland NL, Kieffer E. Pregnancy
age and severe maternal morbidity: a population-based retrospective outcomes of US-born and foreign-born Japanese Americans. Am J Public
cohort study. PLoS Med. 2017;14(5):e1002307. Health. 1996;86(6):820–4.
9. Callaghan WM, Creanga AA, Kuklina EV. Severe maternal morbidity among 32. Chan BC-P, Lao TT-H. Effect of parity and advanced maternal age on
delivery and postpartum hospitalizations in the United States. Obstet obstetric outcome. Int J Gynecol Obstet. 2008;102(3):237–41.
Gynecol. 2012;120(5):1029–36. 33. Salam RA, Hooda M, Das JK, Arshad A, Lassi ZS, Middleton P, et al.
10. Azeez O, Kulkarni A, Kuklina EV, Kim SY, Cox S. Peer reviewed: hypertension Interventions to improve adolescent nutrition: a systematic review and
and diabetes in non-pregnant women of reproductive age in the United meta-analysis. J Adolesc Health. 2016;59(4):S29–39.
States. Prev Chronic Dis. 2019;16. https://doi.org/10.5888/pcd16.190105.
Olapeju et al. BMC Pregnancy and Childbirth (2021) 21:594 Page 11 of 11

34. Gross SM, Augustyn M, Henderson JL, Baig K, Williams CA, Ajao B, et al.
Integrating obstetrical care and WIC nutritional services to address maternal
obesity and postpartum weight retention. Matern Child Health J. 2018;22(6):
794–802.
35. O'dea J. School-based interventions to prevent eating problems: first do no
harm. Eat Disord. 2000;8(2):123–30.
36. Reed JL, Prince SA, Elliott CG, Mullen K-A, Tulloch HE, Hiremath S, et al.
Impact of workplace physical activity interventions on physical activity and
cardiometabolic health among working-age women: a systematic review
and meta-analysis. Circulation. 2017;10(2):e003516.

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