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Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman a
M. Mazharul Islam & Charles Saki Bakheit
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Department of Mathematics and Statistics, Sultan Qaboos University, Muscat, Sultanate of Oman Accepted author version posted online: 22 Dec 2014.Published online: 09 Feb 2015.
Click for updates To cite this article: M. Mazharul Islam & Charles Saki Bakheit (2014): Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman, Health Care for Women International, DOI: 10.1080/07399332.2014.990560 To link to this article: http://dx.doi.org/10.1080/07399332.2014.990560
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Health Care for Women International, 0:1–23, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 0739-9332 print / 1096-4665 online DOI: 10.1080/07399332.2014.990560
Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman M. MAZHARUL ISLAM and CHARLES SAKI BAKHEIT
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Department of Mathematics and Statistics, Sultan Qaboos University, Muscat, Sultanate of Oman
To test the hypothesis that advanced maternal age (AMA) of 35 years and above is associated with increased risk of adverse pregnancy outcomes, we performed a population-based retrospective study using data from the 2000 National Health Survey in Oman. The last pregnancy outcomes of mothers aged ≥35 years were compared with adult mothers aged 20–34 years using bivariate and multivariate statistical techniques. Significantly increased risks of spontaneous abortion, gestational diabetes, preeclampsia, prolonged labor, and cesarean section delivery have been observed for advanced maternal age. Our findings may contribute to cross-cultural understanding of the risks associated with AMA and will facilitate evidence-based counseling of older expectant mothers. Over the past several decades, there have been many remarkable changes in reproductive behavior in both developed and developing countries (Frejka, Jones, & Jean-Paul, 2010; Ngowa, Ngassam, Dohbit, Nzedjom, & Kasia, 2013; Nojomi, Haghighi, Bijari, Rezvani, & Tabatabee, 2010; Olusanya & Solanke, 2011; Valadan, Tanha, & Sephi, 2011). Those changes include rising trends in age at first marriage, postponing childbearing until later reproductive years, and increasing proportion of mothers at advanced ages of late thirties and above (Billari, Kohler, Andersoon, & Lundstr¨om, 2007; Prioux, 2005). In the United States, for example, the percentage of first births for women 35–39 years of age increased by 36% and that for women 40–44 years of age increased by 70% between 1991 and 2001 (Cnattingius & Received 30 July 2013; accepted 17 November 2014. Address correspondence to M. Mazharul Islam, Department of Mathematics and Statistics, Sultan Qaboos University, P.O. Box 36, Post Code 123, Al-khoudh, Muscat, Sultanate of Oman. E-mail: [email protected] or [email protected] 1
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Stephannson, 2002; Heffner, 2004). Childbearing at advanced ages have become increasingly common in other industrialized and nonindustrialized countries as well (Lisonkova, Janssen, Sheps, Lee, & Dahlgren, 2010; Ngowa et al., 2010, 2013; Olusanya & Solanke, 2011; Statistics Canada, 2008; Valadan, Tanha, & Sepahi, 2011). This gives rise to many concerns among health care providers and women about the impact of advanced maternal age on maternal morbidity, the increased risk of obstetric complications, and adverse pregnancy outcomes (Mcintyre, Newburn-Cook, O’Brien, & Demianczuk, 2009). It is evident from literature review that most of the studies that have dealt with advanced maternal age are hospital-based studies from developed countries; there is a very limited number of studies from developing countries and there are very few population-based studies (Cnattingius & Stephannson, 2002; Dildy et al., 1996; Gilbert, Nesbitt, & Danielsen, 1999). Population-based studies are likely to produce unbiased and generalized results, while hospital-based studies may suffer from selection bias. We have conducted a retrospective population-based study in the Sultanate of Oman, a newly developed country with a rapidly growing economy, to examine if advanced maternal age (AMA; 35 years and older) is associated with adverse pregnancy outcome. Our results may contribute to cross-cultural understanding of the risks associated with AMA, and the findings may be useful in providing guidance to health care professionals and service providers in Oman and elsewhere, since we believe women at AMAs share common experiences and difficulties across the geographical regions.
BACKGROUND The Sultanate of Oman is a small oil-rich Arabian Gulf country with a population of around 3.6 million (including 1.5 million expatriates) within a total area of 309,500 square kilometers (National Center for Statistical Information [NCSI], 2013). The discovery of oil and gas in the late 1960s and subsequently the booms in oil prices by the middle of the twentieth century has changed the economy and lifestyle of the people of the country. Oman is now a developed country with per capita Gross Domestic Product (GDP) of more than U.S.$20,000. Prior to the commercial exploitation of oil, the economy of Oman consisted of subsistence agriculture and fishing. A social and economic infrastructure was almost nonexistent. Comprehensive modernization began in the early 1970s after the assumption of power in 1970 by the present ruler His Majesty Sultan Qaboos Bin Said. By the late 1980s, Oman had been transformed into a modern state with all modern facilities and infrastructures. The standard of living improved enormously since the mid1980s. The country has a well-organized universal free health care system assuring universal access to health care services. Almost all the health indicators witnessed dramatic
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improvements over the past four decades, and it has been widely recognized and acclaimed by various international organizations, including the World Health Organization (WHO, 2000). Similar to industrialized developed countries, the proportion of women with first birth and higher-order births are increasing in the Sultanate of Oman. With rapid economic development aided by oil and gas export revenue, the country is passing through a rapid socioeconomic, demographic, and health transition. Age at marriage is increasing, and at the same time the fertility rate has declined very rapidly, despite the fact that there is no official population control program in the country with a quantitative target of limiting fertility as adopted by other hig- fertility countries (Islam, Dorvlo, & Al-Qasmi, 2011). The high population growth and large family size observed in the first population and housing census of 1993 in Oman, however, prompted the government to take some policy measures in order to slow down the population growth. Consequently, the Ministry of Health of Oman introduced the “Birth Spacing Programme” in 1994 with two objectives: first to improve the health of Omani women and children by reducing high-risk pregnancies, and, second, to provide women with the means to regulate their fertility safely and effectively with modern contraceptives (Al-Rawahi and Sharts-Hopko, 2002). For effective birth spacing, necessary counseling and free distribution of family planning methods through all kinds of health facilities are provided under the program, which is similar to one of the objectives of the “Family Planning Programme” (FPPs) in other countries. The program was named so in Oman, however, generally to avoid the cultural and religious sensitivity attached to the FPP. About one-fourth of the currently married women are using any family planning methods in Oman (Al-Riyami et al., 2008). The fertility rate in Oman has declined dramatically from 8.6 births per woman in 1988 to 3.3 births per woman in 2008 (Al-Riyami et al., 2008), and thus it still remains as a high fertility country. On the other hand, the proportion of births occurring to women aged 35–49 years has increased from 23.9% in 1988 to 29.8% in 2008, an increase of 25% over the period of 20 years (Figure 1). One of the important characteristics of the age pattern of recent fertility in Oman is that it is broad and flat topped, indicating a continuation of fertility at a higher rate until ages 35–39. The increase in the rate of childbearing in advanced maternal ages is attributed to many voluntary and involuntary factors that include delayed marriage, effective birth control practice, advances in assisted reproductive technology (ART), increasing rates of divorce followed by remarriage, desire for a large family or expected sex composition of children, lack of effective family planning methods, and women’s pursuit of higher education and career advancement (Berkowitz, Skovron, Lapinski, & Berkowitz, 1990; Bianco et al., 1996; Huang, Sauve, Birkett, Fergusson, & Walraven, 2008; Usta & Nassar, 2008). The contribution of these factors to delayed childbearing,
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FIGURE 1 Proportion of total birth and age-specific birth rate per woman in 1988 and 2008, Oman.
however, often differs between women in developed and developing countries (Olusanya & Solanke, 2011). In developed countries where higher education and career pursuit appear to be more common, AMA women are more likely to be primiparous. In contrast, childbearing at AMA is more common among multiparous women in developing countries as a result of factors such as lack or ineffective family planning methods, favorable cultural disposition toward large family sizes, and poverty (Creanga, Gillespie, Karklins, & Tsui, 2011; Olusanya & Solanke, 2011; Usta & Nassar, 2008). A large number of researchers have reported that increased maternal age (over 35 years) is associated with an increased risk of maternal morbidity, obstetric complications, and adverse pregnancy outcomes (Ataullaha & Freeman-Wang, 2005; Cleary-Goldman et al., 2005; Cnattingius, Forman, Berendes, & Isotalo, 1992; Conde-Agudelo, Belizan, & Diaz-Rossello, 2000; Dildy et al., 1996; Heffner, 2004; Jolly, Sebire, Harris, Robinson, & Regan, 2000; Joseph et al., 2005; Kozinszky et al., 2002; Seoud et al., 2002; Sibai et al., 1997). In contrast, few researchers found no significant association between AMA and adverse obstetric outcomes (Ales, Druzin, & Santibi, 1990; Barkan & Bracken, 1987; Ho, So, & Ma, 1986; Kirz, Dorchester, & Freeman, 1985; Prysak, Lorenz, & Kisly, 1995), although AMA indicated elevated risk of adverse pregnancy outcomes. These contradictory findings may be attributed to a number of methodological differences and limitations of the studies. With the increasing number of women bearing children into their
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mid- to late thirties and beyond, better-designed studies are needed to reach a firm conclusion about the direct and indirect impact of older maternal age on reproductive health of women and the heath of their offspring. As the childbearing in AMA continues to grow, obstetric care providers would benefit from up-to-date outcome data to enhance their preconceptual and antenatal counseling. Given the trend toward delayed child bearing and the increasing availability of assisted reproductive techniques, women aged 35 and over may increasingly seek advice about the risks of pregnancy (Cleary-Goldman et al., 2005). Our objective in this study was to investigate the influence of AMA on adverse obstetric outcomes during pregnancy and delivery. We aimed to test the hypothesis that an AMA of 35 years and above is associated with increased risk of adverse obstetric outcomes for mother and the baby after controlling the effects of potential confounding factors. To the best of our knowledge, no such study has been conducted in Oman. When we consider the growing maternity rate at advanced age in Oman, we see that the findings of the study may have important policy implications for maternity service providers in Oman and elsewhere.
METHODS Study Design and Population The data for this study were obtained from the 2000 Oman National Health Survey (ONHS), a nationally representative survey containing questions on reproductive health and obstetric complications and outcomes. The details of the 2000 ONHS may be seen elsewhere (Al-Riyami, Afifi, Al-Kharusi, & Morsi, 2002). The survey was conducted by the Ministry of Health of Oman in collaboration with the United Nations (UN) organizations such as UNFPA and UNICEF, WHO, and the UN Statistics Division. Ever-married women aged 15–49 years from Omani nationals only were considered as respondents in the survey. Unmarried women were excluded in the survey, because pregnancy or childbearing outside marriage is virtually absent in Oman due to strict adherence to strong religious and cultural beliefs. A nationally representative sample of 2,013 Omani households was selected following a multistage stratified probability sampling design. The sample size was determined by the international experts from UN organizations to provide national estimates as well as to separate estimates for both urban and rural areas. Administratively, Oman is divided into 10 regions, and each region is divided into a number of wiliayats (or districts). The survey covered all the 10 regions of Oman. From each region, wiliayats were chosen following the probability proportional to size (PPS) of the population in each wiliayat. Out of 61 wiliayats in Oman, 16 were selected randomly at the first stage. Each wiliayat was stratified into urban and rural strata.
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In the second stage, enumeration areas (EAs) were chosen from each selected wiliayat, taking one from a rural stratum and one from an urban stratum. Thus, a total of 32 EAs were selected for data collection. The EAs are the census enumeration areas consisting of an average of 100 households used during the 1993 population census in Oman. Before selecting the households from the EAs, a complete updated list of Omani households in each EA with eligible women respondents (i.e., ever-married women ages 15–49 years old) were prepared. The third stage was the selection of households with eligible women respondents in each EA. Households were selected systematically from the EAs. Ultimately, 2,037 eligible women were successfully interviewed from 2,013 selected households. The 2000 ONHS was a household-based community survey, facilitating detailed data collection on socioeconomic and demographic characteristics of households and household members including women with child(en), as well as reproductive health information of eligible women respondents. Data on the general health of the household members and reproductive health characteristics of ever-married women of reproductive age including their nuptiality pattern, pregnancy history, obstetric complications, pregnancy outcomes, and health of offspring including birth weight were collected. To conduct the field data collection work, 25 teams were deployed covering all the 10 regions of Oman. Each team consisted of a female health educator trained to interview the respondents, a nurse to take their physical measurements, a lab technician to obtain the lab samples, a health inspector to transport the lab samples, and a field supervisor (statistician) to supervise and review the questionnaires during the field operation. Eligible women were asked to participate in the survey, which the interviewer completed by means of the household questionnaire, the reproductive health questionnaire, and the questionnaire covering gynecological morbidity symptoms. Each eligible woman was requested to visit the health center within her catchment area for a medical examination (specific health centers were selected for the survey) on the same day as the survey in order to limit the time gap between the home visit and the medical examination. The medical examination included a gynecological examination as well as laboratory tests of blood, urine, vaginal and cervical swabs, and a Pap smear test for sexually transmitted infections, reproductive tract infections, and urinary tract infections. An experienced female physician working in the health center’s gynecology section was chosen to examine the women, and a pathologist supervised the laboratory work. Teams in each region were headed by a research coordinator responsible for communicating with the central research team. Prior to the actual fieldwork, a pretest was designed to test the survey methodology and to determine the general response to the physical examination and specimen collection. Questions related to pregnancy complications and outcomes and health of offspring were mainly administered for last pregnancy that was
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terminated as a live birth or stillbirth or spontaneous abortion before survey date. Women who had twin births and were less than 20 years of age were excluded from this study because of their known elevated risk of obstetric complications and adverse pregnancy outcomes. After all these exclusions, 1,711 women were left for background analysis. For as many as 366 (21%) cases, however, data on obstetric-outcomes-related variables were missing. As this information was collected in the survey retrospectively on the basis of mothers’ self-reporting, they were prone to nonresponses. Thus, there were 1,345 cases for the analysis of obstetric outcomes. In this study, we have considered those women who had a pregnancy that was terminated before survey date as live birth or stillbirth or spontaneous abortion as the unit of analysis rather than births. It is worth mentioning here that delivery in health facilities and at least one antenatal care (ANC) visit to health personnel is almost universal in Oman. ANC is the care received by a pregnant women from health care professionals during pregnancy. According to the 2000 ONHS, 96% of the delivery took place in health facilities, mostly (93%) public health facilities and thus free of cost, and 99.6% of the mothers received at least one ANC visits during their last pregnancy (Al-Riyami et al., 2002). Under such circumstances, mothers’ self-reported obstetric complications were likely to be close to the medically observed obstetric complications, because mothers might have knowledge about their obstetric problems from the pregnancy screening by the medical personnel during ANC visits.
Study Variables There is no precise definition of AMA or delayed maternity. In many studies maternal age 35 and above at the time of pregnancy has been considered as AMA, while others considered maternal age 40 and above as AMA. In this study we have considered maternal age 35 and above at the time of pregnancy as AMA. Thus the study population was categorized into two groups: maternal age 20–34 years (reference group) and maternal age ≥35 years. We refer to mothers aged 20–34 years as “average-aged mothers” and mothers aged ≥ 35 years as “advanced-age mothers” consistently throughout the article. In this study, mother’s self-reported pregnancy complications and adverse pregnancy outcomes were considered as outcome variables, while maternal age and several potential confounding factors were used as explanatory variables. The study variables were selected depending on the availability of information with reasonable frequency. The selected pregnancy complications considered in the study included antepartum hemorrhage, gestational diabetes, preeclampsia, gestational hypertension, and prolonged labor (>24 hours). The adverse pregnancy outcomes included any delivery complications, cesarean sections, spontaneous abortion, stillbirth,
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low birth weight (LBW) and preterm birth. All these variables were considered as binary outcome variables in the analysis. Antepartum hemorrhage was defined as vaginal bleeding during pregnancy regardless of the causes. Gestational hypertension was defined as history of pregnancy-induced hypertension. Gestational diabetes was also defined as history of pregnancy-induced diabetes mellitus. Gestational diabetes is usually diagnosed at the first ANC visit or at the beginning of the pregnancy. It was not possible to make a distinction between chronic and pregnancy-induced hypertension and diabetes, however, due to nonavailability of such information. Any delivery complications were defined as delivery complications from any one of the following complications: breech (i.e., baby’s position was buttock presenting first), episiotomy, antepartum hemorrhage, and vacuum extractor or instrumented delivery. Cesarean section delivery refers to both elective and emergency cesarean delivery. Distinction between elective and emergency caesarian delivery was not possible due to coding both of them under the same category while collecting the data. Spontaneous abortion was defined as fetal loss before 24 weeks of gestation, while stillbirth was defined as a dead fetus (both antepartum and intrapartum) born at 24 completed gestational weeks or later following the definition used in the UK (Royal College of Obstetricians and Gynaecologists [RCOG], 2001). Different durations of gestational age are used in defining spontaneous abortion in different countries and context that range from 16 weeks in Norway, 20 weeks in the United States and Australia, 24 weeks in the UK, to 26 weeks in Italy and Spain (Li, Zeki, Hilder, & Sullivan, 2012; Mohangoo et al., 2013; RCOG, 2001). Following the recommended guideline of the WHO, LBW was defined as the weight at birth of a baby under 2.5 kg, irrespective of gestational duration. LBW of a baby is either the result of a preterm birth (i.e., birth occurring before 37 weeks of gestation) or of restricted fetal growth, called “intrauterine growth retardation.” Preterm births are often termed as premature births. There are sizeable proportions of infants born prematurely, but their weights are normal and, therefore, are not usually consider as a risk group in LBW analysis (Frisbie, Forbes, & Pullum, 1996). Many previous studies as well as the WHO recommended that these two types of births should be treated separately because they are linked to different risks of mortality and morbidity as well as to different etiology, requiring different preventive strategies (Kramer, S´eguin, Lydon, & Goulet, 2000; Tsimbos & Verropoulou, 2011). In this study, we have also considered preterm birth as a separate variable. It is evident from available literature that pregnancy at an advanced age is associated with many demographic, socioeconomic, and health-related confounding factors. In this study, potential confounding factors to the relationship between AMA and obstetric outcomes included parity, level of education, consanguinity, employment status, place of residence, marital status, history of previous pregnancy loss, and ANC visit during last pregnancy.
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Parity usually refers to the total number of live deliveries of the mother and was categorized as primiparae and multiparae. Mothers in their first pregnancy are referred to as primiparae (parity 0) and in their second and higher order pregnancy as multiparae (parity > 1). Maternal education was categorized into less than primary (grade 0–4), primary completed or preparatory (grade 5–9) and secondary and above (grade 10 and above). Consanguinity, that is, marriage between close kin or blood relation, is a unique characteristic among Arab countries including Oman. The inbreeding effects of consanguinity on human reproduction and health of offspring are well documented (Bittles, 1994, 2001; Bittles & Black, 2010; Islam, 2013). Thus, consanguinity could be an important confounder of reproductive outcomes in Oman. In the 2000 ONHS, data on consanguinity was collected by asking evermarried women about their relationship with their husband. The response categories to this question follow: (a) first cousin (father’s or mother’s side), (b) other relation, or (c) no blood relation. Consanguinity level was, therefore, categorized into first-cousin marriage, other degree cousin marriage, and no-relation marriage. Employment status was categorized into work for cash and housewife. ANC visit during last pregnancy variable was categorized into: 24 hours), delivery complications, cesarean section delivery, LBW, and preterm birth. Although, bivariate analysis is a useful first step to understand the association between an outcome variable (say, spontaneous abortion) and an
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explanatory variable (say, maternal age) and how important an explanatory variable, as such, is, however, it fails to provide insight into the relative importance of the explanatory variable in explaining the differences in outcome variable because the explanatory variable may be confounded with other variables (e.g., advanced-age mothers tend to be in higher parity). In this respect, multivariate analysis techniques are used to identify the important factors with independent effects after controlling for the effects of potential confounders. In this study we have employed both univariate and multivariate logistic regression analyses as an analytic technique. Logistic regression was chosen because our outcome variables are categorical (dichotomous) variables. The strength of association between specific outcome variables and the maternal age groups was estimated by odds ratios (ORs) with 95% confidence interval (CI) in logistic regression analysis. We calculated both unadjusted OR and adjusted OR by logistic regression analysis (Hosmer & Lemeshow, 2000). Unadjusted OR and the corresponding 95% CI were obtained by univariable logistic regression without controlling for confounding factors, while adjusted OR and the corresponding 95% CI were obtained by multivariable logistic regression after controlling for potential confounders. Potential confounders were entered in the multivariable logistic regression model based on statistical significance at the bivariate-level analysis. All statistical tests were performed using two-sided tests at the .05 level of significance. For all regression models, the results were expressed as effects (or odds ratios), corresponding two-sided 95% CIs, and associated p values. A p value less than .05 was considered as statistically significant, indicating that a difference in risk exists between the age groups.
RESULTS Characteristics of Mothers A total of 1,711 mothers aged 20 and above (with an average age of 32 years) at the time of their last deliveries occurred before survey data were considered in this study. Among these mothers, 1,328 were average-aged mothers of age 20-34 years at the time of delivery and the rest 383 were aged ≥35 years (i.e., AMAs) at the time of delivery. Thus the study population consisted of 77.6% average-aged mothers and the remaining 22.4% were advanced-age mothers. The distributions of average-aged and advanced-age mothers by selected demographic, socioeconomic, and health characteristics are presented in Table 1. There were some similarities and differences in background characteristics of the two groups of mothers. As expected, the mean ages were significantly different between the two age groups (p < .001). The mean ages of the average-aged and advanced-age group were 29.6 years and 41.1 years, respectively. Parity was significantly associated
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TABLE 1 Background Characteristics of Mothers Grouped According to Age at Delivery, Oman 2000 Maternal age at delivery
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Characteristic Mean age (SD) Parity Primiparae 1–4 >4 Maternal education Less than primary (0–4 years) Primary/preparatory (5–9 years) Secondary + (10+ years) Consanguinity First cousin marriage Other cousin marriage No relation Employment status Work for cash House wife Place of residence Urban Rural Marital status Currently married Widowed/divorced/ separated Previous history of pregnancy loss Yes No ANC visit during last pregnancy < 4 visits ≥4 visits Mean ANC visits Total
20–34 years n (%)
≥35 years n (%)
Total n (%)
p value for χ 2 test
29.6 ( ± 5.95%) 41.1 ( ± 3.68%)
32.2 ( ± 5.44%)
4), with an average parity of 4.9 children. As a result, in many cases, physicians might have adopted cesarean delivery to avoid any risk of adverse pregnancy outcomes. This may explain the higher rate of cesarean delivery among advanced-age mothers than average-aged mothers (15.6% vs. 10.7%, OR = 1.57, p = .021). The overall cesarean delivery in Oman is on the rise. It has increased from 6.6% in 1995 (Sulaiman, Al-Ghassany, & Farid, 2000) to 11.55% in 2000 (Al-Riyami et al., 2002) and further increased to 16.45% in 2010 (Ministry of Health, 2012). With rising age at childbearing, more women will choose to have children in their late thirties and above, and because advanced-age mothers are at greater risk for certain complications during pregnancy that may require cesarean delivery, cesarean births are likely to continue to increase. This rising trend in cesarean delivery needs special attention in health care planning. In many recent studies, researchers demonstrated that cesarean section rates above a certain limit have not shown additional benefit for the mother or the baby, and some researchers have even shown that high CS rates could be linked to negative consequences in maternal and child health (Barros et al., 2005; Beliz´an, Althabe, & Cafferata, 2007; Hall & Bewley, 1999; Villar et al., 2006). In 1985, the WHO cautioned about the excessive use of CS for childbirth, stating a CS rate higher than 10–15% as unjustified, for whatever reason, in any region or country (WHO, 1985).
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Some of the limitations of the study are worth mentioning here. As the study was a retrospective study, it was prone to missing data, and the analysis was done ignoring the missing cases. This might have introduced some sort of selection bias, because the individuals for whom information was missing may have different characteristics than those for whom information was available. Our data lack information on some other relevant confounding factors in the evaluation of the risk, namely, the mother’s socioeconomic status, health, nutrition, her reproductive history and preexisting chronic conditions prior to the recorded delivery, and management of the pregnancy. The small number of cases in some obstetric outcomes for advanced-age mothers, particularly in the case of stillbirths (only seven cases) and preterm births (only five cases), may also be responsible for inconsistent results in our study. To determine the independent effects of maternal age on adverse obstetric outcomes, future studies should control relevant age-dependent confounders, namely, parity, socioeconomic status, lifestyle factors such as smoking, maternal education, maternal health history such as preexisting chronic conditions (hypertension and diabetes), pregnancy complications, history of infertility, how the pregnancy was conceived (naturally versus assisted reproduction), and the reasons for delaying childbearing (NewburnCook & Onyskiw, 2005). Care should also be taken about appropriate sample size. In conclusion, we found increased risks of some adverse obstetric outcomes among advanced-age women of age 35 and above. Our data indicate higher risk of gestational diabetes, preeclampsia, gestational hypertension, spontaneous abortion, prolonged labor, cesarean section delivery, and overall higher risk of any delivery complications among advanced-age mothers in Oman. These findings have implications for maternity service providers, particularly as trends of AMA continue in Oman. The recent social trend toward delayed childbearing will thus have an increasing impact on the demand for health care services and population health. There is a need to offer older women special counseling both before and after conception so that they become informed about the increased risks involved.
ACKNOWLEDGMENTS The authors thank the Ministry of Health of Oman, especially the Director of Planning and Research, for providing the raw data file of the 2000 National Health Survey of Oman. The views expressed herein are solely those of the authors and do not necessarily reflect the views of any institution. Additional thanks go to the two anonymous reviewers for their valuable and helpful comments and suggestions on an earlier version of the manuscript that improved the quality of the article enormously.
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Lehmann, D. K., & Chism, J. (1987). Pregnancy outcome in medically complicated and uncomplicated patients aged 40 years and older. American Journal of Obstetrics and Gynecology, 157, 738–742. Li, Z., Zeki, R., Hilder, L., & Sullivan, E. A. (2012). Australia’s mothers and babies 2010 (Perinatal statistics series no. 27, Cat. no. PER 57). Canberra, Australia: Australian Institute of Health and Welfare National Perinatal Statistics Unit, Australian Government. Lin, H. C., Sheen, T. C., Tang, C. H., & Kao, S. (2004). Association between maternal age and the likelihood of a cesarean section: A population-based multivariate logistic regression analysis. Acta Obstetrica et Gynecologica Scandinavica, 83, 1178–1183. Lisonkova, S., Janssen, P. A., Sheps, S. B., Lee, S. K., & Dahlgren, L. (2010). The effect of maternal age on averse birth outcomes: Does parity matter? Journal of Obstetrics and Gynaecology Canada, 32, 541–548. Mcintyre, S. H., Newburn-Cook, C. V., O’Brien, B., & Demianczuk, N. N. (2009). Effect of older maternal age on the risk of spontaneous preterm labor: A population-based study. Health Care for Women International, 30, 670–689. Ministry of Health (MoH). (2012). Annual health report 2010. Muscat, Oman: Author. Mohangoo, A. D., Blondel, B., Gissler, M., Velebil, P., Macfarlane, A., Zeitlin, J., & Euro-Peristat Scientific Committee. (2013). International comparisons of fetal and neonatal mortality rates in high-income countries: Should exclusion thresholds be based on birth weight or gestational age?. PLoS ONE, 8(5), e64869. doi:10.1371/journal.pone.0064869 National Centre for Statistical Information (NCSI). (2013). Statistical year book 2012. Muscat, Oman: Ministry of National Economy. Newburn-Cook, C. V., & Onyskiw, J. E. (2005). Is older maternal age a risk factor for preterm birth and fetal growth restriction? A systematic review. Health Care for Women International, 26, 852–875. Ngowa, J.D.K., Ngassam, A. N., Dohbit, J. S., Nzedjom, C., & Kasia, J. M. (2013). Pregnancy outcome at advanced maternal age in a group of African women in two teaching Hospitals in Yaounde, Cameroon. Pan African Medical Journal, 14, 134–139. Nojomi, M., Haghighi, L., Bijari, B., Rezvani, L., & Tabatabaee, S. K. (2010). Delayed childbearing: Pregnancy and maternal outcomes. Iranian Journal of Reproductive Medicine, 8, 80–85. Olusanya, B. O., & Solanke, O. A. (2011). Perinatal correlates of delayed childbearing in a developing country. Archives of Gynecology and Obstetrics, 285, 951–957. Peipert, J. F., & Bracken, M. B. (1993). Maternal age: An independent risk factor for cesarean delivery. Obstetrics & Gynaecology, 81, 200–205. Prioux, F. (2005). Late fertility in Europe: Some comparative and historical data. Revue d’Epid´emiologie et de Sant´e Publique, 53, 2S3–2S11. Prysak, M., Lorenz, R. P., & Kisly, A. (1995). Pregnancy outcome in nulliparous women 35 years and older. Obstetrics & Gynaecology, 85, 65–70 Rajab, A, & Patton, M. A. (2000). A study of consanguinity in the Sultanate of Oman. Annals of Human Biology, 27, 321–326.
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Rajab, A., Vaishnav, A., Freeman, N. V., & Patton, M. A. (1998). Neural tube defects and congenital hydrocephalus in the Sultanate of Oman. Journal of Tropical Pediatrics, 44, 300–303. Royal College of Obstetricians and Gynaecologists (RCOG). (April 2001). Further issues relating to late abortion, fetal viability and registration of births and deaths. London, UK: Author. Seoud, M., Nassar, A. H., Usta, I. M., Melhem, Z., Kazma, A., & Khalil, A. M. (2002). Impact of advanced maternal age on pregnancy outcome. American Journal of Perinatology, 19, 1–7. Sibai, B., Ewell, M., Levine, R., Klebanoff, M., Esterlitz, J., Catalano, P., Goldenberg, R., & Joffe, G. (1997). Risk factors associated with pre-eclampsia in healthy nulliparous women. American Journal of Obstetrics and Gynecology, 177, 1003–1010. Statistics Canada. (2008). CANSIM Table Number 1024508—Live births, by age and parity of mother, Canada, annual. Ottawa, Canada: Author. Sulaiman, A.J.M., Al-Ghassany, A., & Farid, S. (2000). Oman Child Health survey 1988–89. Muscat, Oman: Ministry of Health. Tsimbos, C., & Verropoulou, G. (2011). Demographic and socioeconomic determinants of low birth weight and preterm births among natives and immigrants in Greece: An analysis using nationwide vital registration micro-data. Journal of Biosocial Science, 43, 271–283. Usta, I. M., & Nassar, A. H. (2008). Advanced maternal age, Part I: Obstetric complications. American Journal of Perinatology, 25, 521–534. Valadan, M., Tanha, F. D., & Sepahi, A. (2011). Pregnancy outcomes in women of advanced age. Journal of Family and Reproductive Health, 5, 57–61. Villar, J., Valladares, E., Wojdyla, D., Zavaleta, N., Shah, A., Campod´onico L., . . . Acosta, A. (2006). Caesarean delivery rates and pregnancy outcomes: The 2005 WHO global survey on maternal and perinatal health in Latin America. Lancet, 367, 1819–1829. World Health Organization (WHO). (1985). Appropriate technology for birth. Lancet, 2 (8452), 436–437. World Health Organization (WHO). (2000). The World Health Report 2000: Health systems—Improving performance. Geneva, Switzerland: Author. Yasin, S. Y., & Beydoun, S. N. (1988). Pregnancy outcome at greater than or equal to 20 weeks’ gestation in women in their 40s: A case-control study. The Journal of Reproductive Medicine, 33, 209–213.
Health Care for Women International Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uhcw20
Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman a
M. Mazharul Islam & Charles Saki Bakheit
a
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Department of Mathematics and Statistics, Sultan Qaboos University, Muscat, Sultanate of Oman Accepted author version posted online: 22 Dec 2014.Published online: 09 Feb 2015.
Click for updates To cite this article: M. Mazharul Islam & Charles Saki Bakheit (2014): Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman, Health Care for Women International, DOI: 10.1080/07399332.2014.990560 To link to this article: http://dx.doi.org/10.1080/07399332.2014.990560
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Health Care for Women International, 0:1–23, 2015 Copyright © Taylor & Francis Group, LLC ISSN: 0739-9332 print / 1096-4665 online DOI: 10.1080/07399332.2014.990560
Advanced Maternal Age and Risks for Adverse Pregnancy Outcomes: A Population-Based Study in Oman M. MAZHARUL ISLAM and CHARLES SAKI BAKHEIT
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Department of Mathematics and Statistics, Sultan Qaboos University, Muscat, Sultanate of Oman
To test the hypothesis that advanced maternal age (AMA) of 35 years and above is associated with increased risk of adverse pregnancy outcomes, we performed a population-based retrospective study using data from the 2000 National Health Survey in Oman. The last pregnancy outcomes of mothers aged ≥35 years were compared with adult mothers aged 20–34 years using bivariate and multivariate statistical techniques. Significantly increased risks of spontaneous abortion, gestational diabetes, preeclampsia, prolonged labor, and cesarean section delivery have been observed for advanced maternal age. Our findings may contribute to cross-cultural understanding of the risks associated with AMA and will facilitate evidence-based counseling of older expectant mothers. Over the past several decades, there have been many remarkable changes in reproductive behavior in both developed and developing countries (Frejka, Jones, & Jean-Paul, 2010; Ngowa, Ngassam, Dohbit, Nzedjom, & Kasia, 2013; Nojomi, Haghighi, Bijari, Rezvani, & Tabatabee, 2010; Olusanya & Solanke, 2011; Valadan, Tanha, & Sephi, 2011). Those changes include rising trends in age at first marriage, postponing childbearing until later reproductive years, and increasing proportion of mothers at advanced ages of late thirties and above (Billari, Kohler, Andersoon, & Lundstr¨om, 2007; Prioux, 2005). In the United States, for example, the percentage of first births for women 35–39 years of age increased by 36% and that for women 40–44 years of age increased by 70% between 1991 and 2001 (Cnattingius & Received 30 July 2013; accepted 17 November 2014. Address correspondence to M. Mazharul Islam, Department of Mathematics and Statistics, Sultan Qaboos University, P.O. Box 36, Post Code 123, Al-khoudh, Muscat, Sultanate of Oman. E-mail: [email protected] or [email protected] 1
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Stephannson, 2002; Heffner, 2004). Childbearing at advanced ages have become increasingly common in other industrialized and nonindustrialized countries as well (Lisonkova, Janssen, Sheps, Lee, & Dahlgren, 2010; Ngowa et al., 2010, 2013; Olusanya & Solanke, 2011; Statistics Canada, 2008; Valadan, Tanha, & Sepahi, 2011). This gives rise to many concerns among health care providers and women about the impact of advanced maternal age on maternal morbidity, the increased risk of obstetric complications, and adverse pregnancy outcomes (Mcintyre, Newburn-Cook, O’Brien, & Demianczuk, 2009). It is evident from literature review that most of the studies that have dealt with advanced maternal age are hospital-based studies from developed countries; there is a very limited number of studies from developing countries and there are very few population-based studies (Cnattingius & Stephannson, 2002; Dildy et al., 1996; Gilbert, Nesbitt, & Danielsen, 1999). Population-based studies are likely to produce unbiased and generalized results, while hospital-based studies may suffer from selection bias. We have conducted a retrospective population-based study in the Sultanate of Oman, a newly developed country with a rapidly growing economy, to examine if advanced maternal age (AMA; 35 years and older) is associated with adverse pregnancy outcome. Our results may contribute to cross-cultural understanding of the risks associated with AMA, and the findings may be useful in providing guidance to health care professionals and service providers in Oman and elsewhere, since we believe women at AMAs share common experiences and difficulties across the geographical regions.
BACKGROUND The Sultanate of Oman is a small oil-rich Arabian Gulf country with a population of around 3.6 million (including 1.5 million expatriates) within a total area of 309,500 square kilometers (National Center for Statistical Information [NCSI], 2013). The discovery of oil and gas in the late 1960s and subsequently the booms in oil prices by the middle of the twentieth century has changed the economy and lifestyle of the people of the country. Oman is now a developed country with per capita Gross Domestic Product (GDP) of more than U.S.$20,000. Prior to the commercial exploitation of oil, the economy of Oman consisted of subsistence agriculture and fishing. A social and economic infrastructure was almost nonexistent. Comprehensive modernization began in the early 1970s after the assumption of power in 1970 by the present ruler His Majesty Sultan Qaboos Bin Said. By the late 1980s, Oman had been transformed into a modern state with all modern facilities and infrastructures. The standard of living improved enormously since the mid1980s. The country has a well-organized universal free health care system assuring universal access to health care services. Almost all the health indicators witnessed dramatic
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improvements over the past four decades, and it has been widely recognized and acclaimed by various international organizations, including the World Health Organization (WHO, 2000). Similar to industrialized developed countries, the proportion of women with first birth and higher-order births are increasing in the Sultanate of Oman. With rapid economic development aided by oil and gas export revenue, the country is passing through a rapid socioeconomic, demographic, and health transition. Age at marriage is increasing, and at the same time the fertility rate has declined very rapidly, despite the fact that there is no official population control program in the country with a quantitative target of limiting fertility as adopted by other hig- fertility countries (Islam, Dorvlo, & Al-Qasmi, 2011). The high population growth and large family size observed in the first population and housing census of 1993 in Oman, however, prompted the government to take some policy measures in order to slow down the population growth. Consequently, the Ministry of Health of Oman introduced the “Birth Spacing Programme” in 1994 with two objectives: first to improve the health of Omani women and children by reducing high-risk pregnancies, and, second, to provide women with the means to regulate their fertility safely and effectively with modern contraceptives (Al-Rawahi and Sharts-Hopko, 2002). For effective birth spacing, necessary counseling and free distribution of family planning methods through all kinds of health facilities are provided under the program, which is similar to one of the objectives of the “Family Planning Programme” (FPPs) in other countries. The program was named so in Oman, however, generally to avoid the cultural and religious sensitivity attached to the FPP. About one-fourth of the currently married women are using any family planning methods in Oman (Al-Riyami et al., 2008). The fertility rate in Oman has declined dramatically from 8.6 births per woman in 1988 to 3.3 births per woman in 2008 (Al-Riyami et al., 2008), and thus it still remains as a high fertility country. On the other hand, the proportion of births occurring to women aged 35–49 years has increased from 23.9% in 1988 to 29.8% in 2008, an increase of 25% over the period of 20 years (Figure 1). One of the important characteristics of the age pattern of recent fertility in Oman is that it is broad and flat topped, indicating a continuation of fertility at a higher rate until ages 35–39. The increase in the rate of childbearing in advanced maternal ages is attributed to many voluntary and involuntary factors that include delayed marriage, effective birth control practice, advances in assisted reproductive technology (ART), increasing rates of divorce followed by remarriage, desire for a large family or expected sex composition of children, lack of effective family planning methods, and women’s pursuit of higher education and career advancement (Berkowitz, Skovron, Lapinski, & Berkowitz, 1990; Bianco et al., 1996; Huang, Sauve, Birkett, Fergusson, & Walraven, 2008; Usta & Nassar, 2008). The contribution of these factors to delayed childbearing,
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FIGURE 1 Proportion of total birth and age-specific birth rate per woman in 1988 and 2008, Oman.
however, often differs between women in developed and developing countries (Olusanya & Solanke, 2011). In developed countries where higher education and career pursuit appear to be more common, AMA women are more likely to be primiparous. In contrast, childbearing at AMA is more common among multiparous women in developing countries as a result of factors such as lack or ineffective family planning methods, favorable cultural disposition toward large family sizes, and poverty (Creanga, Gillespie, Karklins, & Tsui, 2011; Olusanya & Solanke, 2011; Usta & Nassar, 2008). A large number of researchers have reported that increased maternal age (over 35 years) is associated with an increased risk of maternal morbidity, obstetric complications, and adverse pregnancy outcomes (Ataullaha & Freeman-Wang, 2005; Cleary-Goldman et al., 2005; Cnattingius, Forman, Berendes, & Isotalo, 1992; Conde-Agudelo, Belizan, & Diaz-Rossello, 2000; Dildy et al., 1996; Heffner, 2004; Jolly, Sebire, Harris, Robinson, & Regan, 2000; Joseph et al., 2005; Kozinszky et al., 2002; Seoud et al., 2002; Sibai et al., 1997). In contrast, few researchers found no significant association between AMA and adverse obstetric outcomes (Ales, Druzin, & Santibi, 1990; Barkan & Bracken, 1987; Ho, So, & Ma, 1986; Kirz, Dorchester, & Freeman, 1985; Prysak, Lorenz, & Kisly, 1995), although AMA indicated elevated risk of adverse pregnancy outcomes. These contradictory findings may be attributed to a number of methodological differences and limitations of the studies. With the increasing number of women bearing children into their
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mid- to late thirties and beyond, better-designed studies are needed to reach a firm conclusion about the direct and indirect impact of older maternal age on reproductive health of women and the heath of their offspring. As the childbearing in AMA continues to grow, obstetric care providers would benefit from up-to-date outcome data to enhance their preconceptual and antenatal counseling. Given the trend toward delayed child bearing and the increasing availability of assisted reproductive techniques, women aged 35 and over may increasingly seek advice about the risks of pregnancy (Cleary-Goldman et al., 2005). Our objective in this study was to investigate the influence of AMA on adverse obstetric outcomes during pregnancy and delivery. We aimed to test the hypothesis that an AMA of 35 years and above is associated with increased risk of adverse obstetric outcomes for mother and the baby after controlling the effects of potential confounding factors. To the best of our knowledge, no such study has been conducted in Oman. When we consider the growing maternity rate at advanced age in Oman, we see that the findings of the study may have important policy implications for maternity service providers in Oman and elsewhere.
METHODS Study Design and Population The data for this study were obtained from the 2000 Oman National Health Survey (ONHS), a nationally representative survey containing questions on reproductive health and obstetric complications and outcomes. The details of the 2000 ONHS may be seen elsewhere (Al-Riyami, Afifi, Al-Kharusi, & Morsi, 2002). The survey was conducted by the Ministry of Health of Oman in collaboration with the United Nations (UN) organizations such as UNFPA and UNICEF, WHO, and the UN Statistics Division. Ever-married women aged 15–49 years from Omani nationals only were considered as respondents in the survey. Unmarried women were excluded in the survey, because pregnancy or childbearing outside marriage is virtually absent in Oman due to strict adherence to strong religious and cultural beliefs. A nationally representative sample of 2,013 Omani households was selected following a multistage stratified probability sampling design. The sample size was determined by the international experts from UN organizations to provide national estimates as well as to separate estimates for both urban and rural areas. Administratively, Oman is divided into 10 regions, and each region is divided into a number of wiliayats (or districts). The survey covered all the 10 regions of Oman. From each region, wiliayats were chosen following the probability proportional to size (PPS) of the population in each wiliayat. Out of 61 wiliayats in Oman, 16 were selected randomly at the first stage. Each wiliayat was stratified into urban and rural strata.
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In the second stage, enumeration areas (EAs) were chosen from each selected wiliayat, taking one from a rural stratum and one from an urban stratum. Thus, a total of 32 EAs were selected for data collection. The EAs are the census enumeration areas consisting of an average of 100 households used during the 1993 population census in Oman. Before selecting the households from the EAs, a complete updated list of Omani households in each EA with eligible women respondents (i.e., ever-married women ages 15–49 years old) were prepared. The third stage was the selection of households with eligible women respondents in each EA. Households were selected systematically from the EAs. Ultimately, 2,037 eligible women were successfully interviewed from 2,013 selected households. The 2000 ONHS was a household-based community survey, facilitating detailed data collection on socioeconomic and demographic characteristics of households and household members including women with child(en), as well as reproductive health information of eligible women respondents. Data on the general health of the household members and reproductive health characteristics of ever-married women of reproductive age including their nuptiality pattern, pregnancy history, obstetric complications, pregnancy outcomes, and health of offspring including birth weight were collected. To conduct the field data collection work, 25 teams were deployed covering all the 10 regions of Oman. Each team consisted of a female health educator trained to interview the respondents, a nurse to take their physical measurements, a lab technician to obtain the lab samples, a health inspector to transport the lab samples, and a field supervisor (statistician) to supervise and review the questionnaires during the field operation. Eligible women were asked to participate in the survey, which the interviewer completed by means of the household questionnaire, the reproductive health questionnaire, and the questionnaire covering gynecological morbidity symptoms. Each eligible woman was requested to visit the health center within her catchment area for a medical examination (specific health centers were selected for the survey) on the same day as the survey in order to limit the time gap between the home visit and the medical examination. The medical examination included a gynecological examination as well as laboratory tests of blood, urine, vaginal and cervical swabs, and a Pap smear test for sexually transmitted infections, reproductive tract infections, and urinary tract infections. An experienced female physician working in the health center’s gynecology section was chosen to examine the women, and a pathologist supervised the laboratory work. Teams in each region were headed by a research coordinator responsible for communicating with the central research team. Prior to the actual fieldwork, a pretest was designed to test the survey methodology and to determine the general response to the physical examination and specimen collection. Questions related to pregnancy complications and outcomes and health of offspring were mainly administered for last pregnancy that was
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terminated as a live birth or stillbirth or spontaneous abortion before survey date. Women who had twin births and were less than 20 years of age were excluded from this study because of their known elevated risk of obstetric complications and adverse pregnancy outcomes. After all these exclusions, 1,711 women were left for background analysis. For as many as 366 (21%) cases, however, data on obstetric-outcomes-related variables were missing. As this information was collected in the survey retrospectively on the basis of mothers’ self-reporting, they were prone to nonresponses. Thus, there were 1,345 cases for the analysis of obstetric outcomes. In this study, we have considered those women who had a pregnancy that was terminated before survey date as live birth or stillbirth or spontaneous abortion as the unit of analysis rather than births. It is worth mentioning here that delivery in health facilities and at least one antenatal care (ANC) visit to health personnel is almost universal in Oman. ANC is the care received by a pregnant women from health care professionals during pregnancy. According to the 2000 ONHS, 96% of the delivery took place in health facilities, mostly (93%) public health facilities and thus free of cost, and 99.6% of the mothers received at least one ANC visits during their last pregnancy (Al-Riyami et al., 2002). Under such circumstances, mothers’ self-reported obstetric complications were likely to be close to the medically observed obstetric complications, because mothers might have knowledge about their obstetric problems from the pregnancy screening by the medical personnel during ANC visits.
Study Variables There is no precise definition of AMA or delayed maternity. In many studies maternal age 35 and above at the time of pregnancy has been considered as AMA, while others considered maternal age 40 and above as AMA. In this study we have considered maternal age 35 and above at the time of pregnancy as AMA. Thus the study population was categorized into two groups: maternal age 20–34 years (reference group) and maternal age ≥35 years. We refer to mothers aged 20–34 years as “average-aged mothers” and mothers aged ≥ 35 years as “advanced-age mothers” consistently throughout the article. In this study, mother’s self-reported pregnancy complications and adverse pregnancy outcomes were considered as outcome variables, while maternal age and several potential confounding factors were used as explanatory variables. The study variables were selected depending on the availability of information with reasonable frequency. The selected pregnancy complications considered in the study included antepartum hemorrhage, gestational diabetes, preeclampsia, gestational hypertension, and prolonged labor (>24 hours). The adverse pregnancy outcomes included any delivery complications, cesarean sections, spontaneous abortion, stillbirth,
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low birth weight (LBW) and preterm birth. All these variables were considered as binary outcome variables in the analysis. Antepartum hemorrhage was defined as vaginal bleeding during pregnancy regardless of the causes. Gestational hypertension was defined as history of pregnancy-induced hypertension. Gestational diabetes was also defined as history of pregnancy-induced diabetes mellitus. Gestational diabetes is usually diagnosed at the first ANC visit or at the beginning of the pregnancy. It was not possible to make a distinction between chronic and pregnancy-induced hypertension and diabetes, however, due to nonavailability of such information. Any delivery complications were defined as delivery complications from any one of the following complications: breech (i.e., baby’s position was buttock presenting first), episiotomy, antepartum hemorrhage, and vacuum extractor or instrumented delivery. Cesarean section delivery refers to both elective and emergency cesarean delivery. Distinction between elective and emergency caesarian delivery was not possible due to coding both of them under the same category while collecting the data. Spontaneous abortion was defined as fetal loss before 24 weeks of gestation, while stillbirth was defined as a dead fetus (both antepartum and intrapartum) born at 24 completed gestational weeks or later following the definition used in the UK (Royal College of Obstetricians and Gynaecologists [RCOG], 2001). Different durations of gestational age are used in defining spontaneous abortion in different countries and context that range from 16 weeks in Norway, 20 weeks in the United States and Australia, 24 weeks in the UK, to 26 weeks in Italy and Spain (Li, Zeki, Hilder, & Sullivan, 2012; Mohangoo et al., 2013; RCOG, 2001). Following the recommended guideline of the WHO, LBW was defined as the weight at birth of a baby under 2.5 kg, irrespective of gestational duration. LBW of a baby is either the result of a preterm birth (i.e., birth occurring before 37 weeks of gestation) or of restricted fetal growth, called “intrauterine growth retardation.” Preterm births are often termed as premature births. There are sizeable proportions of infants born prematurely, but their weights are normal and, therefore, are not usually consider as a risk group in LBW analysis (Frisbie, Forbes, & Pullum, 1996). Many previous studies as well as the WHO recommended that these two types of births should be treated separately because they are linked to different risks of mortality and morbidity as well as to different etiology, requiring different preventive strategies (Kramer, S´eguin, Lydon, & Goulet, 2000; Tsimbos & Verropoulou, 2011). In this study, we have also considered preterm birth as a separate variable. It is evident from available literature that pregnancy at an advanced age is associated with many demographic, socioeconomic, and health-related confounding factors. In this study, potential confounding factors to the relationship between AMA and obstetric outcomes included parity, level of education, consanguinity, employment status, place of residence, marital status, history of previous pregnancy loss, and ANC visit during last pregnancy.
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Parity usually refers to the total number of live deliveries of the mother and was categorized as primiparae and multiparae. Mothers in their first pregnancy are referred to as primiparae (parity 0) and in their second and higher order pregnancy as multiparae (parity > 1). Maternal education was categorized into less than primary (grade 0–4), primary completed or preparatory (grade 5–9) and secondary and above (grade 10 and above). Consanguinity, that is, marriage between close kin or blood relation, is a unique characteristic among Arab countries including Oman. The inbreeding effects of consanguinity on human reproduction and health of offspring are well documented (Bittles, 1994, 2001; Bittles & Black, 2010; Islam, 2013). Thus, consanguinity could be an important confounder of reproductive outcomes in Oman. In the 2000 ONHS, data on consanguinity was collected by asking evermarried women about their relationship with their husband. The response categories to this question follow: (a) first cousin (father’s or mother’s side), (b) other relation, or (c) no blood relation. Consanguinity level was, therefore, categorized into first-cousin marriage, other degree cousin marriage, and no-relation marriage. Employment status was categorized into work for cash and housewife. ANC visit during last pregnancy variable was categorized into: 24 hours), delivery complications, cesarean section delivery, LBW, and preterm birth. Although, bivariate analysis is a useful first step to understand the association between an outcome variable (say, spontaneous abortion) and an
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explanatory variable (say, maternal age) and how important an explanatory variable, as such, is, however, it fails to provide insight into the relative importance of the explanatory variable in explaining the differences in outcome variable because the explanatory variable may be confounded with other variables (e.g., advanced-age mothers tend to be in higher parity). In this respect, multivariate analysis techniques are used to identify the important factors with independent effects after controlling for the effects of potential confounders. In this study we have employed both univariate and multivariate logistic regression analyses as an analytic technique. Logistic regression was chosen because our outcome variables are categorical (dichotomous) variables. The strength of association between specific outcome variables and the maternal age groups was estimated by odds ratios (ORs) with 95% confidence interval (CI) in logistic regression analysis. We calculated both unadjusted OR and adjusted OR by logistic regression analysis (Hosmer & Lemeshow, 2000). Unadjusted OR and the corresponding 95% CI were obtained by univariable logistic regression without controlling for confounding factors, while adjusted OR and the corresponding 95% CI were obtained by multivariable logistic regression after controlling for potential confounders. Potential confounders were entered in the multivariable logistic regression model based on statistical significance at the bivariate-level analysis. All statistical tests were performed using two-sided tests at the .05 level of significance. For all regression models, the results were expressed as effects (or odds ratios), corresponding two-sided 95% CIs, and associated p values. A p value less than .05 was considered as statistically significant, indicating that a difference in risk exists between the age groups.
RESULTS Characteristics of Mothers A total of 1,711 mothers aged 20 and above (with an average age of 32 years) at the time of their last deliveries occurred before survey data were considered in this study. Among these mothers, 1,328 were average-aged mothers of age 20-34 years at the time of delivery and the rest 383 were aged ≥35 years (i.e., AMAs) at the time of delivery. Thus the study population consisted of 77.6% average-aged mothers and the remaining 22.4% were advanced-age mothers. The distributions of average-aged and advanced-age mothers by selected demographic, socioeconomic, and health characteristics are presented in Table 1. There were some similarities and differences in background characteristics of the two groups of mothers. As expected, the mean ages were significantly different between the two age groups (p < .001). The mean ages of the average-aged and advanced-age group were 29.6 years and 41.1 years, respectively. Parity was significantly associated
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TABLE 1 Background Characteristics of Mothers Grouped According to Age at Delivery, Oman 2000 Maternal age at delivery
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Characteristic Mean age (SD) Parity Primiparae 1–4 >4 Maternal education Less than primary (0–4 years) Primary/preparatory (5–9 years) Secondary + (10+ years) Consanguinity First cousin marriage Other cousin marriage No relation Employment status Work for cash House wife Place of residence Urban Rural Marital status Currently married Widowed/divorced/ separated Previous history of pregnancy loss Yes No ANC visit during last pregnancy < 4 visits ≥4 visits Mean ANC visits Total
20–34 years n (%)
≥35 years n (%)
Total n (%)
p value for χ 2 test
29.6 ( ± 5.95%) 41.1 ( ± 3.68%)
32.2 ( ± 5.44%)
4), with an average parity of 4.9 children. As a result, in many cases, physicians might have adopted cesarean delivery to avoid any risk of adverse pregnancy outcomes. This may explain the higher rate of cesarean delivery among advanced-age mothers than average-aged mothers (15.6% vs. 10.7%, OR = 1.57, p = .021). The overall cesarean delivery in Oman is on the rise. It has increased from 6.6% in 1995 (Sulaiman, Al-Ghassany, & Farid, 2000) to 11.55% in 2000 (Al-Riyami et al., 2002) and further increased to 16.45% in 2010 (Ministry of Health, 2012). With rising age at childbearing, more women will choose to have children in their late thirties and above, and because advanced-age mothers are at greater risk for certain complications during pregnancy that may require cesarean delivery, cesarean births are likely to continue to increase. This rising trend in cesarean delivery needs special attention in health care planning. In many recent studies, researchers demonstrated that cesarean section rates above a certain limit have not shown additional benefit for the mother or the baby, and some researchers have even shown that high CS rates could be linked to negative consequences in maternal and child health (Barros et al., 2005; Beliz´an, Althabe, & Cafferata, 2007; Hall & Bewley, 1999; Villar et al., 2006). In 1985, the WHO cautioned about the excessive use of CS for childbirth, stating a CS rate higher than 10–15% as unjustified, for whatever reason, in any region or country (WHO, 1985).
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Some of the limitations of the study are worth mentioning here. As the study was a retrospective study, it was prone to missing data, and the analysis was done ignoring the missing cases. This might have introduced some sort of selection bias, because the individuals for whom information was missing may have different characteristics than those for whom information was available. Our data lack information on some other relevant confounding factors in the evaluation of the risk, namely, the mother’s socioeconomic status, health, nutrition, her reproductive history and preexisting chronic conditions prior to the recorded delivery, and management of the pregnancy. The small number of cases in some obstetric outcomes for advanced-age mothers, particularly in the case of stillbirths (only seven cases) and preterm births (only five cases), may also be responsible for inconsistent results in our study. To determine the independent effects of maternal age on adverse obstetric outcomes, future studies should control relevant age-dependent confounders, namely, parity, socioeconomic status, lifestyle factors such as smoking, maternal education, maternal health history such as preexisting chronic conditions (hypertension and diabetes), pregnancy complications, history of infertility, how the pregnancy was conceived (naturally versus assisted reproduction), and the reasons for delaying childbearing (NewburnCook & Onyskiw, 2005). Care should also be taken about appropriate sample size. In conclusion, we found increased risks of some adverse obstetric outcomes among advanced-age women of age 35 and above. Our data indicate higher risk of gestational diabetes, preeclampsia, gestational hypertension, spontaneous abortion, prolonged labor, cesarean section delivery, and overall higher risk of any delivery complications among advanced-age mothers in Oman. These findings have implications for maternity service providers, particularly as trends of AMA continue in Oman. The recent social trend toward delayed childbearing will thus have an increasing impact on the demand for health care services and population health. There is a need to offer older women special counseling both before and after conception so that they become informed about the increased risks involved.
ACKNOWLEDGMENTS The authors thank the Ministry of Health of Oman, especially the Director of Planning and Research, for providing the raw data file of the 2000 National Health Survey of Oman. The views expressed herein are solely those of the authors and do not necessarily reflect the views of any institution. Additional thanks go to the two anonymous reviewers for their valuable and helpful comments and suggestions on an earlier version of the manuscript that improved the quality of the article enormously.
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