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ORIGINAL RESEARCH |
From the Department of Maternal and Child Health, University of Alabama at Birmingham, Birmingham, Alabama.
Address reprint requests to: Hamisu M. Salihu, MD, PhD, Department of Maternal and Child Health, School of Public Health, University of Alabama at Birmingham, 320 Ryals Building, 1665 University Boulevard, Birmingham, Alabama 35294-0022; E-mail: hsalihu{at}uab.edu.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: This was a retrospective study on all deliveries in the United States from 1997 to 1999. Four maternal age groups of 20–29 (young), 30–39 (mature), 40–49 (very mature), and 50 or more years (older) were constructed to assess risk gradients for fetal morbidity and mortality.
RESULTS: A total of 539 deliveries among older mothers (aged 50 and above) were documented (four per 100,000). Among singleton gestations, the risks for low birth weight, preterm, and very preterm were tripled among older mothers, whereas the occurrence of very low birth weight, small size for gestational age, and fetal mortality were approximately doubled compared with those for young mothers. Older mothers also had greater risks for fetal morbidity and mortality than their immediate younger counterparts (40–49 year olds) except for very low birth weight. Among multiple gestations, the differences in risk between older and young mothers were lower than those noted among singletons. Still, compared with young mothers, older mothers had significantly higher risks of low birth weight, very low birth weight, very preterm, and small size for gestational age. Older mothers also had higher risk estimates for multiples than 40–49-year-old gravidas in terms of all fetal morbidity and mortality indices.
CONCLUSION: Pregnancy beyond age 50 was associated with increased risks for the fetus. Our findings suggest that this age group is a distinct obstetric high-risk entity that requires special counseling before and after conception.
"Her name was Margaret Krasiowa. She was born in Konin, Poland, in the year 1655, and died in 1763 at the age of 108 completed years. At age 94, she married her third husband, who was then 105 years old. During the 14 years they lived together, she bore him two boys and a girl."1 That scenario, if true, represents probably the most fascinating documented case of childbearing at older maternal age. Before the time of Margaret Krasiowa and even in our contemporary world, childbearing beyond the maternal age of 50 years has been a source of curiosity frequently punctuated with disbelief because of its rarity. However, recent advances in assisted reproduction technology, including oocyte donation, make it possible for postmenopausal women to conceive.2–4 Although extremely rare, women can naturally continue bearing children even beyond the age of 50 years.5 It remains unclear, however, what the potential fetal risks are when a woman in her 50s becomes pregnant. More precise knowledge of these risks is important because increasingly more women are delaying childbearing in our society while progress continues to be made in the area of assisted reproduction technology. Published studies on pregnant women aged 50 years and older are limited to case reports or observations on a handful of women from a particular health care facility.2–6 Although important, these few case reports and case series cannot provide precise estimates of risk because the small number of cases observed (the largest had 55 cases of clinical pregnancies)3 precluded controlling for confounding factors, in addition to making these limited findings on highly selected cases nongeneralizable.
Previously, the reported age of women was truncated and documented as 49 on US public-access national natality files if they were 50 years old or older. The decision of the National Center for Health Statistics in 1997 to start recording on vital record files the actual age of pregnant women aged 50–54 years provided a unique opportunity to examine the magnitude of fetal morbidity and mortality in this age group of mothers. Our aim was to determine whether these older mothers constitute a specific and unique risk group distinct, in terms of magnitude of risks, from their younger counterparts. As delayed childbearing continues to increase in our society, this information could provide useful as well as more precise estimates that could be used by health providers in counseling older women about the risks of pregnancy at that age.
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MATERIALS AND METHODS |
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Maternal age in years was grouped into the following four maternal age cohorts: 20–29, 30–39, 40–49, and 50 and above. For the purpose of this study, we sometimes used the following terms to describe the four maternal age cohorts: 20–29 as young, 30–39 as mature mothers, 40–49 as very mature, and 50 and above as older mothers.
We considered the following covariates: maternal race or ethnicity, marital status, education, prenatal care utilization, smoking and drinking alcohol during pregnancy, and year of birth. Parity refers to the total number of live deliveries the mother had and was classified into primipara (
1), multipara (2–4), grand multipara (5–9), and great grand multipara (
10). Adequacy of prenatal care was determined using the R-GINDEX algorithm8,9 and was categorized into adequate and less than adequate prenatal care utilization. The R-GINDEX assesses the adequacy of care based on three variables (trimester prenatal care began, number of visits, and the gestational age of the infant at birth). In this study, inadequate prenatal care utilization refers to women who had missing prenatal care information, had prenatal care but the level was considered suboptimal, or mothers who had no prenatal care at all. The accuracy of all these aforementioned variables on the birth certificate has been validated in previous studies.10,11
For this study, the main birth outcomes of interest were fetal mortality rate (intrauterine fetal demise at 20 weeks’ gestation or later), low and very low birth weight (<2500 and <1500 g, respectively), preterm and very preterm delivery (<37 and <33 weeks’ gestation, respectively), and small size for gestational age (<10th percentile of birth weight for gestational age). For perimenopausal and menopausal women, gestational age was based on clinical estimation. We also examined the following maternal complications and compared the rates of their occurrence across the four maternal age categories: anemia, cardiac disease, diabetes, chronic hypertension, preeclampsia, eclampsia, abruptio placentae, and placenta previa. Because multiple births constituted 37% of the individual fetuses among women 50 years and older, we applied growth curve references constructed for singletons, twins, and triplets as appropriate.12,13 For quadruplets and higher-order fetuses, we used the growth curves for triplets.
We calculated relative risks for those outcomes across the four maternal age strata using maternal age 20–29 years as the reference. Crude odds ratios for each outcome measure were generated using 2 x 2 contingency tables, whereas adjusted odds ratios were obtained from a multivariable logistic model that controlled for the effects of parity, marital status, educational level, smoking, drinking, level of prenatal care utilization, and year of birth. We used the -2 log likelihood ratio tests to determine model fit.14 We created interaction terms for a combination of risk factors and added them to the adjusted model. Interaction terms did not improve the model fit and were excluded from the final model.
In our analysis, both singleton and multifetal gestations were considered. Outcome observations made on multiple gestations are a good example of clustered data. The siblings within a plurality (twin, triplet, etc.) set are exposed to similar prevailing conditions in the womb and are presumably equally affected by the same attributes that characterize the mother (eg, advanced maternal age, adequacy of prenatal care, maternal hypertension, and smoking or drinking during pregnancy). It is therefore logical to expect conditions leading to the morbidity or intrauterine death of a plurality set member to have affected the other womb mates as well, even though unexplained factors determining vulnerability and extent of morbidity caused may vary. Observations or outcome measures on members of the same plurality set will tend to correlate, and it is important to take into account this lack of independence of observations to avoid spurious results. Siblings of mothers who had at least two documented pregnancies in our data could also have observations that were correlated. We therefore, attempted to identify members of the same plurality set and siblings of the same mother.
Although plurality within multiples could be determined, matched siblings were not identifiable in the data set. We developed an algorithm consisting of maternal and infant characteristics to identify matched siblings. Infants and fetuses were considered to be matched siblings if the values for the following variables matched: month of birth, state and county of birth, maternal age, maternal race, level of maternal education, place of birth of the mother, number of prenatal visits, month in which prenatal care visits began, and gestational age. We used approximately a similar algorithm to identify mothers with more than one pregnancy during the period of study. This algorithm has been validated previously and found by us and other investigators to be more than 90% accurate.15,16 We then applied the generalized estimating equation framework to generate random effect estimates that captured sibling correlations using the PROC GENMOD in SAS (8.2; SAS Institute, Cary, NC). However, for the analysis of singletons, both the crude and adjusted estimates did not differ from the results of the conventional logistic model. Hence, we report the results obtained from the conventional logistic model constructed for outcome estimation on singletons. For multiples, we report the results generated from the generalized estimating equation because of the observed differences between the results from the two models.
We tested for dose-response relationships between the burden of fetal morbidity and mortality and maternal age using 
2 tests for linear trend.14 All tests of the hypothesis were two-tailed with a type 1 error rate fixed at 5%. This study was approved by the Institutional Review Board of the University of Alabama at Birmingham (protocol approval number X-030530015).
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RESULTS |
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and compared with the other age groups. Older mothers belonged to three broad racial groups. The overwhelming majority of them were white, with Asian or Pacific Islanders (main component of the group denoted as other) and black women constituting the rest. Whereas the proportion of blacks among pregnant mothers declined with advancing age that of Asian and Pacific Islanders increased. Primiparity showed a roughly U-shaped pattern, being most frequent in the 20–29 age group, with a trough at the 40–49 age category, and another modest increase at 50 years and older. Great grand multiparity was most frequent among older mothers, twice the frequency in the 40–49 year old group. The majority of women aged at least 50 years were married, had received at least 12 years of education, but surprisingly, only about half of them could be described as having utilized prenatal care services adequately. For cases where information was available, smoking and alcohol ingestion during pregnancy were relatively rare habits among older pregnant women in comparison with younger mothers. Multiple gestations, on the other hand, were most frequent among 50-year-old mothers, comprising about one third of all deliveries in that age group. This rate for multiple pregnancy was seven times that of 40 year olds.
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presents a comparison of maternal age by maternal complications. Cardiac disease, diabetes, chronic hypertension, placenta previa, and abruptio placentae showed a positive association with maternal age in a dose-dependent fashion. For these risk factors, with the exception of abruptio placentae (for which there was no difference between 50 year olds and the immediate younger age group [40–49 year olds]), the rates for 50 year olds were typically higher than those for the 40–49 age category. Anemia showed a consistently negative relationship with age, whereas for preeclampsia and eclampsia, the maternal age-specific risk distribution was nonlinear, with a J-shaped and U-shaped pattern, respectively.
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and 2 and Tables 3 and 4). Of the 198 multiples among older mothers, 165 (83.3%) were twins, 29 were triplets (14.7%), and four were quadruplets (2.0%). Since only viable fetuses (20 weeks of gestation) were considered in the analysis, the number for twins and triplets may not be exact multiples of 2 and 3 respectively. Among very mature mothers, the corresponding rates were 90.6% twins, 8.9% triplets, and 0.5% quadruplets and higher-order multiples; for mature mothers, the plurality distribution was 90.9% twins, 8.3% triplets, and 0.8% quadruplets and higher-order multiples; and among young mothers, twins constituted 95.7% of multiples, triplets 3.9%, and quadruplets and higher-order multiples 0.4%.
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and 2 show the crude rates for fetal morbidity and mortality across the maternal age categories for singletons and multiples, respectively, and adjusted estimates are shown in Tables 3 and 4. Compared with the referent group (20–29 year olds), singleton infants of older mothers had higher risks for all morbidity and mortality indices. These increased levels of risk were significantly elevated except for very low birth weight, where the confidence limits contained unity. The risks for low birth weight, preterm, and very preterm were about three times as likely among infants of older mothers, whereas the occurrence of very low birth weight, small size for gestational age, and fetal mortality was about twice as likely. Compared with their immediate younger counterparts (40–49 year olds), older mothers still had increased risks of fetal morbidity and mortality except for very low birth weight, for which the estimates were slightly higher among very mature mothers.
Among multiples (Table 4), the fetal morbidity and mortality differences between older mothers and the referent category were much lower than the corresponding values for singletons. Nevertheless, significantly higher risk levels were noted for low birth weight, very low birth weight, very preterm, and small size for gestational age among infants of older mothers. For all the fetal morbidity and mortality indices, older mothers had higher risk estimates than 40–49-year-old gravidas. The difference in risk between the two maternal age categories was highest for low birth weight (relative risk difference = 65%) and lowest for preterm delivery (relative risk difference = 24%). When we compared mature and very mature gravidas with the referent category, the only significant finding was with respect to low birth weight. Multiples of mature and very mature mothers were less likely to be of low birth weight than those born to young mothers. Otherwise, the risk estimates for the other morbidity indices and fetal mortality were comparable for young, mature, and very mature mothers.
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DISCUSSION |
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The risks for adverse pregnancy-associated conditions generally increased from one advanced maternal age category to the next higher one. The definition of advanced maternal age varies from study to study, with most of the earlier reports fixing the cutoff point at 35 years17,29–33 and the more recent ones around 40 years.19–28 This is probably a reflection of improvement in birth outcomes over the years as a result of enhanced understanding of the risks associated with these pregnancies.
Among singleton births in this study, we found the risks for adverse fetal outcomes to be considerably elevated among older mothers. The risks for low birth weight, preterm and very preterm births, small size for gestational age, and fetal mortality were significantly elevated in comparison with those of young mothers, even after adjusting for the confounding effects of parity, marital status, education, smoking and drinking, and year of birth. In addition, we noted that there was a positive correlation between maternal age and fetal outcomes in a dose-dependent pattern, an observation that further buttresses the argument that fetal outcomes are significantly influenced by advancing maternal age, as also reported in previous studies using large sample sizes.17,22,27
Among multiple births and in comparison with young mothers, the relative risks for fetal outcomes were still higher among older mothers, although the magnitude of these differences was less marked than those observed among singletons. Conversely, we noted that among multiples of mature and very mature mothers, the risks for fetal morbidity and mortality were either lower than (as was the case for low birth weight) or comparable to those of young mothers. One possible explanation for this contrasting result is that the proportion of higher-order multiples (triplets and above) was greater among older mothers than in the other younger maternal age categories. Because higher-order multiples have higher morbidity and mortality risks,34 their preponderance among older mothers could explain the excess fetal morbidity and mortality in that group. Using the same reasoning, one would expect excess levels of morbidity and mortality among mature and very mature mothers in comparison to the referent category (20–29 year old). However, the fact that similar or even better results (in the case of low birth weight) were detected among mature and very mature mothers goes counter to the hypothesis of the preponderance of higher-order multiples with advancing age as an explanation.
Previous investigators have reported increased adverse birth outcomes with increasing maternal age (at least 35 years) among singletons. However, among twins they observed no difference, and with triplets, older maternal age was protective.35 This concurs with our findings across the maternal age groups, with the exception of multiples in the 50 and older age category. Although we found lower relative risks among multiples of mature and very mature mothers, these estimates were not statistically significant, probably because most of the multiples in our study were twins, a subgroup that had been shown not to be affected by maternal age on birth outcomes.35 Also, the fact that 50-year-old mothers showed consistently higher risks for fetal morbidity and mortality not only among singletons but also multiples (the findings among multiples being a deviation from an expected trend), suggests that this advanced maternal age category is a distinct obstetric entity in terms of fetal birth outcomes.
Another possible factor that could have influenced our result is the effect of assisted reproduction technology in the United States. Although the absence of information on assisted reproduction technology in our data set limits our ability to investigate its role in fetal birth outcomes, it is still possible to reasonably discuss its likely impact in this study. A recent report36 provided insight as to the proportion of multiple births (twins and triplets) that can be accounted for by assisted reproduction technology in the United States. For young, mature, very mature, and older mothers, the proportions of multiple births associated with assisted reproduction technology were 4.3%, 18.3%, 40%, and 65%, respectively. This also means that the effect of assisted reproduction technology will be related to maternal age, becoming most pronounced among 50-year-old gravidas. Studies have found that pregnancies resulting from assisted reproduction technology have less favorable outcomes compared with naturally conceived gestations.37,38 Hence, this could have contributed to the higher fetal morbidity and mortality indices among older mothers compared with 20–29 year olds. By contrast, the expected negative contribution of assisted reproduction technology procedures among mature and very mature mothers seemed to have been obscured, probably by the effects of other favorable factors (eg, higher socioeconomic status, intense prenatal care, etc).
A possible source of bias in this study is the use of 20 weeks’ gestation as the cutoff point for fetal mortality. Because of variations across the states regarding the definition of fetal death, underreporting might have occurred, as recently reported.39 One plausible assumption is that such underreporting is random with respect to maternal age, in which case our reported relative risks would represent underestimates. Conversely, if underreporting of fetal deaths is influenced more by maternal age (ie, more likely among older than younger mothers) than by state-specific definitions, then we probably overestimated our relative risks for fetal mortality among the higher age categories. However, from the documentation of the National Center for Health Statistics, it appears that state-specific definitions regarding reports of fetal deaths are more important in affecting fetal mortality estimates than maternal age.40 Hence, our results concerning fetal mortality are more likely to be conservative estimates.
In conclusion, we found increased risks for fetal morbidity and mortality among 50-year-old mothers for both singleton and multiple gestations. Among mature and very mature mothers, the risks were elevated for singletons only, whereas for multiples these risks were either lower than or comparable to those of younger mothers. These findings suggest that pregnancy beyond age 50 may represent a distinct obstetric entity with a risk pattern that differs from that observed for mature and very mature mothers. Consequently, there is a need to offer older women special counseling both before and after conception so that they become informed of the increased risks involved.
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Footnotes |
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Received March 3, 2003. Received in revised form June 9, 2003. Accepted June 19, 2003.
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REFERENCES |
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18. Cunningham FG, Leveno KJ. Childbearing among older women-the message is cautiously optimistic. N Engl J Med 1995;333:1002–4.
19. Seoud MAF, Nassar AH, Usta IM, Melhem Z, Kazma A, Khalil AM. Impact of advanced maternal age on pregnancy outcome. Am J Perinatol 2002;19:1–7.[Medline]
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