Paternal characteristics associated with maternal periconceptional use of folic acid supplementation

Paternal characteristics associated with maternal periconceptional use of folic acid supplementation Background: Maternal predictors of folic acid (FA) supplementation use to reduce offspring risk of neural tube defects are well known, while paternal determinants for maternal FA use are less known. Such knowledge is important to increase women’s compliance to recommended periconceptional FA use. Methods: In a nation-wide study of 683,785 births registered in the Medical Birth Registry of Norway during 1999–2010, the associations between paternal characteristics (age, education, occupation, country of origin) and maternal FA use were estimated by relative risks (RR) with 95% confidence intervals (CI), using log- binomial regression. Results: Maternal FA use before and during pregnancy (adequate FA use) was found in 16% of the births. The association between paternal age and adequate FA use was inversely U-shaped; adjusted RRs for adequate FA use were 0.35 (95% CI 0.28–0.43) and 0.72 (95% CI 0.71–0.74) for paternal age < 20 and ≥ 40 years, respectively, comparing age 30–34 years. Compulsory education (1–9 years) among fathers was compared to tertiary education; the RR was 0.69 (95% CI 0.68–0.71) for adequate FA use. The lower risk of adequate FA use for paternal compulsory education was present in all categories of maternal education. Occupation classes other than “Higher professionals” were associated with decreased risk of adequate FA use, compared with the reference “Lower professionals”.RRfor adequate FA use was 0.58 (95% CI 0.56–0.60) comparing fathers from “Low/middle-income countries” with fathers born in Norway. Conclusion: Adequate FA use in the periconceptional period was lower when fathers were younger or older than 30–34 years, had shorter education, had manual or self-employed occupations, or originated from low/ middle-income countries. Partners may contribute to increase women’suse of periconceptional FA supplementation. Keywords: Pregnancy, Supplement use, Folic acid, Norway Background [6]. Start of FA supplementation prior to conceiving is Folate is necessary in foetal development, and folic acid important in order to reduce the risk of NTDs because (FA) supplementation is widely acknowledged to reduce the neural tube closes between 21 and 28 days after the risk of neural tube defects (NTDs) [1–5]. FA is the conception [7]. synthetic form of the B-vitamin folate, which is essential Randomized clinical trials and non-randomized in the synthesis of DNA, methylation, and DNA repair intervention trials have demonstrated that periconcep- tional FA use reduces the risk of NTDs [1–3]. Recent * Correspondence: jan.mortensen@uib.no studies have reported that FA is associated with protec- Department of Global Public Health and Primary Care, University of Bergen, tion against other neurodevelopmental disorders and Kalfarveien 31, N-5018 Bergen, Norway some severe pregnancy complications [8–10]. The pro- Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway tective effect of FA on NTDs has led health authorities Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 2 of 8 in several countries, including Norway, to recommend MBRN is a population-based registry containing women to take FA supplements before pregnancy and in information on all births in Norway since 1967 [28]. The early pregnancy [11–13]. registry holds demographic information on the mother Many countries in Europe, including Norway, have and the father, the mother’s health before and during performed information campaigns to increase the use of pregnancy, including chronic diseases, information on in periconceptional FA supplementation among women vitro fertilization (IVF), complications during pregnancy planning pregnancy [14–16]. Presently there is no and delivery as well as information on the infant, includ- mandatory folic acid food fortification in Norway [17]. ing birth defects and other perinatal problems. Midwives Official Norwegian guidelines from 1998, states that all and physicians attending the deliveries register the data. women planning their pregnancy should use 0.4 mg FA Since 1967, there has been mandatory reporting of all daily from 1 month before pregnancy and throughout live and stillbirths from the 16 gestational week to the first 2–3 months of pregnancy to reduce the risk of MBRN. NTDs [12]. However, the proportion of preconception NR contains demographic information on all residents FA supplementation use in Norway is still too low [18] in Norway since 1960, including the date of birth, and by 2015 it was 33% [19]. country of origin, and the dates of immigration, emigra- Previous studies have identified maternal factors tion, or death [30]. NR assigns a unique personal identi- associated with inadequate FA in the periconceptional fication number to all individuals born or immigrated to period, such as low maternal age, shorter education, Norway, enabling accurate record linkages. single parenthood, unplanned pregnancy, lower parity, NAV was established in 2006 after governmental smoking, alcohol use, less physical activity, or originating reorganization of the Directorate of Labour in Norway from a foreign country [15, 16, 20–24]. (founded in 1945), and has registered information on Since couples tend to exhibit concordant health occupation, health status, and social benefits of all indi- behaviour’s for dietary intake, smoking, alcohol viduals with residence in Norway since 1992. The consumption, physical activity, and body mass index Norwegian occupational code system is based on the (BMI) [25–27], a woman’s partner may contribute to her International Standard Classification of Occupations use of periconceptional FA supplements. In fact, in an (ISCO), revised version from 1988 [31]. early report from the Norwegian Mother and Child Since 1970, NUDB holds information on all individ- Cohort Study (MoBa), 2000–2003, counting 22,500 uals’ education history from primary school up to women, FA supplements were used more frequently doctoral studies in one database [32]. The classification among women with partners with a higher education is based on the Norwegian Standard Classification of [22]. However, the study did not assess other paternal Education. factors or combined paternal and maternal factors as to identify women with inadequate FA use. Maternal FA supplement use Taking advantage of the Medical Birth Registry of We constructed a binary variable for intake of FA sup- Norway that to our knowledge is the only national regis- plement use (0.4 mg/day) (regardless of concomitant try with information on periconceptional use of FA sup- multivitamin use) registered in the MBRN since Decem- plements [28], we updated parent information with data ber 1998 onwards; adequate FA use (recommended FA from national registries to investigate whether paternal supplementation before and during pregnancy), and in- factors (age, education, occupation, country of origin) adequate FA use (FA supplementation only before preg- was associated with mothers’ intake of recommended FA nancy, or only during pregnancy, or no record of FA in pregnancy. use). MBRN also registers multivitamin use, but our investi- gation focused on periconceptional FA use as such in- Methods take was according to official guidelines. Data-sources Maternal FA use before and/or during pregnancy was Paternal characteristics collected from the Medical Birth Registry of Norway We used the following paternal variables in our (MBRN) [28]. Paternal and maternal demographic data analyses of adequate FA supplementation; paternal came from the National Registry (NR). Information on age (< 20, 20–24, 25–29, 30–34, 35–39, 40+ years); paternal and maternal occupation originated from the education (Compulsory (1–9 years), Intermediate (10– Norwegian Labour and Welfare Administration (NAV), 12 years), Tertiary (13–19 years)); occupation accord- and we retrieved paternal and maternal educational data ing to the class scheme of Erikson, Goldthorpe, and from the Norwegian National Education Database Portocarero (I Higher professionals, II Lower profes- (NUDB) [29]. sionals, IIIa Higher routine, IIIb Lower routine, IV Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 3 of 8 Other self-employed workers, V Technicians, VI overall difference between the categories of paternal Skilled, VII Semiskilled and unskilled, VIIb Agricul- characteristics were calculated using likelihood ratio tural, Unclassified) (EGP) [33]; and country of origin tests. We evaluated and tested the potential effect modi- according to the classification by World Health fication of the association between paternal education Organization, Health statistics and information sys- and maternal FA use by stratification and likelihood ra- tems, Estimates for 2000–2012 (Norway, High income tio test. countries, Low/middle-income countries) [34]. Covariates Results We used directed acyclic graphs (DAGs) and Our study included 683,785 births during 1999–2010. subject-matter knowledge to select a minimally sufficient Table 1 presents the characteristics of the parents. The adjustment set of variables that identify the uncon- median ages of the fathers and mothers at childbirth founded association of paternal characteristics on ad- were 33 and 30 years, respectively. For about 41% of the equate maternal FA supplementation use [35–37]. births, the mothers were primiparous, and about 2% of The potential confounders of the paternal characteris- the births were conceived after in vitro fertilization tics and maternal FA use relationship included year of (IVF). The majority of the births were of childbirth (continuous), paternal age (< 20, 20–24, 25– Norwegian-born parents (84% of the fathers and 83% of 29, 30–34, 35–39, 40+ years), education (Compulsory, the mothers). For about 34% of the births, the fathers Intermediate, Tertiary), or country of origin (Norway, had tertiary education, and for about 19% of the births, High-income countries, Low/middle-income countries). the fathers had compulsory education only. The paternal Furthermore, we included maternal age (< 20, 20–24, educational level varied by his country of origin. Fathers 25–29, 30–34, 35–39, 40+ years), maternal education originating from low/middle-income countries generally (Compulsory, Intermediate, Tertiary), and maternal had lower educational level compared to fathers origin- country of origin (Norway, High-income countries, Low/ ating from Norway and other high-income countries middle-income countries) as possible confounders of the (not shown). Occupation classified as “Lower profes- associations between paternal age, education, or country sionals,” accounted for 22% of all the births. For about of origin, and maternal adequate FA use. 14% of the births, the women smoked daily at the start Maternal smoking was not included in the final of pregnancy, about 3% smoked intermittently, and 67% models because smoking was not considered a con- did not smoke. Nearly 17% of the smoking data were founder of the association of paternal characteristics on missing. maternal FA supplementation use [38]. For about 16% of all births in the study population, the mothers were assigned to the category adequate FA Study population supplementation users. However, during 1999 through During 1999–2010, 716,021 births were registered in 2010, the proportion of adequate FA supplementation MBRN. We excluded births (induced abortions) without use increased from 4% at the start of the study period information on FA or multivitamin supplementation use (1999) to 26% in 2010. (2519) and births without maternal identification num- Table 2 presents crude and adjusted RRs for ad- ber (4091). For multiple births, we included data for the equate maternal periconceptional FA use by paternal first birth and excluded 12,927 next born individuals. variables (determinants). Adjusted analyses showed an Among the remaining 696,484 births, we excluded inverse “U-shaped” relationship between paternal age 12,699 births without paternal identification number, and adequate maternal FA supplement use where the leaving 683,785 live births and stillbirths for analyses. smallest RRs were found for paternal age below 20 years (RR 0.35 (95% CI 0.28–0.43)), 20–24 years Statistical analysis (RR 0.68 (95% CI 0.66–0.71)), and 40 years and above Associations between paternal characteristics (age, edu- (RR 0.72 (95% CI 0.71–0.74)) compared to paternal cation, occupation, country of origin) and maternal FA age 30–34 years. Paternal compulsory education was use were estimated as relative risks (RRs) with 95% con- associated with reduced risk of adequate FA use (RR fidence intervals (CIs) by log-binomial regression, using 0.69 (95% CI 0.68–0.71)) compared to paternal ter- the log-link function in Stata version 15 [39]. The 95% tiary education. All paternal occupation classes were CIs were based on robust variance estimation with the associated with reduced risk of adequate FA use ex- sandwich estimator to correct for the intra-individual cept for “I Higher professionals”,whencomparedto correlation in women with more than one pregnancy “II Lower professionals”, in particular “VII Semiskilled during the study period [40]. Births with missing data on and unskilled” (RR 0.75 (95% CI 0.73–0.76)), and covariates were excluded from the analyses. P-values for “VIIb Agricultural” (RR 0.73 (95% CI 0.69–0.78)). Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 4 of 8 Table 1 Paternal and maternal characteristics in 683,785 births Table 1 Paternal and maternal characteristics in 683,785 births in Norway, 1999–2010 in Norway, 1999–2010 (Continued) Births Maternal chronic disease Fathers % Mothers % No 623,817 91.2 Number of births 683,785 100.0 683,785 100.0 Yes 59,968 8.8 Age Maternal smoking before pregnancy < 20 4401 0.6 15,464 2.3 Non-smoker 456,797 66.8 20–24 48,448 7.1 100,016 14.6 Intermittent 18,518 2.7 25–29 162,671 23.8 223,480 32.7 Daily 93,662 13.7 30–34 235,401 34.4 228,203 33.4 Missing data 114,808 16.8 35–39 151,540 22.2 99,727 14.6 Maternal folic acid use in pregnancy 40+ 81,324 11.9 16,895 2.5 No use 371,820 54.4 Education Only before 8930 1.3 Compulsory education (1–9 years) 130,953 19.2 125,479 18.4 Only during 192,169 28.1 Intermediate (10–12 years) 302,384 44.2 230,320 33.7 Before and during 110,866 16.2 Categorized according to the class scheme of Erikson, Goldthorpe and Tertiary education (13–19 years) 229,818 33.6 298,036 43.6 Portocarero (EGP) [33] Missing data 20,630 3.0 29,950 4.4 Categorized according to the classification by World Health Organization, Health statistics and information systems, Estimates for 2000–2012 [34] Occupational class Asthma, hypertension, kidney disease, chronic urinary infection, rheumatoid I Higher professionals 86,635 12.7 50,650 7.4 arthritis, heart disease, epilepsy, diabetes mellitus (type I or II), and thyroid disease II Lower professionals 152,781 22.3 122,804 18.0 IIIa Higher routine 77,540 11.3 197,174 28.8 Mothers whose children’s father originated from low/ middle-income countries had also a reduced risk of ad- IIIb Lower routine 40,070 5.9 114,795 16.8 equate FA use (RR 0.58 (95% CI 0.56–0.60)) compared IV Other self-employed workers 358 0.1 119 0.0 to fathers originating from Norway. V Technicians 5550 0.8 1492 0.2 Table 3 presents crude and adjusted RRs with 95% CIs VI Skilled 108,755 15.9 15,961 2.3 of adequate FA use by maternal and paternal education. VII Semiskilled and unskilled 111,584 16.3 73,994 10.8 Adjusted analyses showed that adequate FA use was less VIIb Agricultural 7663 1.1 2720 0.4 likely in births were fathers had compulsory education, regardless of maternal education. The association of pa- Unclassified 52,824 7.7 51,264 7.5 ternal compulsory education and recommended FA use Missing data 40,025 5.9 52,812 7.7 was weakened by increasing level of maternal education. Country of origin However, even when the mother had tertiary education, Norway 574,602 84.0 567,241 83.0 the association of compulsory paternal education on ad- High income countries 33,487 4.9 30,920 4.5 equate maternal FA use was significant (RR 0.75 (95% CI Low/middle-income countries 75,497 11.0 85,597 12.5 0.73–0.77)), compared to fathers with tertiary education. Missing data 199 0.0 27 0.0 Discussion Marital status The present population-based study (683,785 births Unmarried 37,057 5.4 during 1999–2010) showed that recommended maternal Married/Partnership 634,283 92.8 FA use was low among fathers who were young or older Divorced 3417 0.5 at their children’s birth, had achieved shorter education, Missing data 9028 1.3 held a manually or self-employed occupation, or originated from low/middle-income countries. Even In vitro fertilization (IVF) among mothers who had achieved higher education, rec- No 669,024 97.8 ommended periconceptional maternal FA use was low Yes 14,761 2.2 among less educated fathers. Birth order Several studies have investigated the association be- 1 280,178 41.0 tween maternal socio-demographic, reproductive, and 2 244,532 35.8 medical characteristics and adherence to recommended intake of periconceptional FA. A common feature among ≥3 159,075 23.3 mothers is that young age, low educational level, low Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 5 of 8 Table 2 Relative risks (RRs) with 95% confidence intervals (95% CIs) of adequate maternal periconceptional folic acid supplement use (before and during pregnancy) by paternal characteristics, in 683,785 births, Norway, 1999–2010 ab Folic acid supplementation Unadjusted Adjusted for paternal factors Further adjusted for maternal ac use factors Characteristics Yes No RR* 95% CI RR* 95% CI RR* 95% CI Paternal age (years) < 20 86 4315 0.11 0.09–0.13 0.10 0.08–0.13 0.35 0.28–0.43 20–24 3325 45,123 0.37 0.36–0.39 0.37 0.36–0.38 0.68 0.66–0.71 25–29 22,886 139,785 0.76 0.75–0.78 0.77 0.76–0.79 0.94 0.93–0.96 30–34 43,348 192,053 1.00 Reference 1.00 Reference 1.00 Reference 35–39 28,488 123,052 1.02 1.01–1.03 0.97 0.96–0.99 0.90 0.89–0.91 40+ 12,733 68,591 0.85 0.83–0.87 0.80 0.78–0.81 0.72 0.71–0.74 Paternal education Compulsory (1–10 years) 11,694 119,259 0.40 0.39–0.40 0.52 0.51–0.53 0.69 0.68–0.71 Intermediate (11–13 years) 45,411 256,973 0.67 0.66–0.67 0.75 0.74–0.76 0.87 0.85–0.88 Tertiary (14–20 years) 51,894 177,924 1.00 Reference 1.00 Reference 1.00 Reference Missing data 1867 18,763 Paternal occupational class I Higher professionals 19,957 66,678 1.05 1.04–1.07 1.05 1.03–1.06 II Lower professionals 33,366 119,415 1.00 Reference 1.00 Reference IIIa Higher routine 12,292 65,248 0.73 0.71–0.74 0.89 0.88–0.91 IIIb Lower routine 5352 34,718 0.61 0.59–0.63 0.85 0.83–0.87 IV Other self-employed workers 60 298 0.77 0.61–0.97 0.83 0.65–1.05 V Technicians 836 4714 0.69 0.65–0.74 0.89 0.84–0.95 VI Skilled 15,174 93,581 0.64 0.63–0.65 0.84 0.83–0.86 VII Semiskilled and unskilled 11,643 99,941 0.48 0.47–0.49 0.75 0.73–0.76 VIIb Agricultural 908 6755 0.54 0.51–0.58 0.73 0.69–0.78 Unclassified 7575 45,249 0.66 0.64–0.67 0.96 0.94–0.99 Missing data 3703 36,322 Paternal country of origin Norway 99,339 475,263 1.00 Reference 1.00 Reference 1.00 Reference High income countries 6535 26,952 1.13 1.10–1.16 1.06 1.04–1.09 1.06 1.03–1.08 Low-middle-income countries 4975 70,522 0.38 0.37–0.39 0.35 0.34–0.36 0.58 0.56–0.60 Missing data 17 182 All RRs for adequate folic acid supplementation adjusted for year of childbirth (continuous) RRs by paternal age, no other adjustment for paternal factors; RRs by paternal education adjusted for paternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+), paternal country of origin (Norway, high-income countries, low/middle-income countries); RRs by paternal occupation adjusted for paternal age, fathers country of origin, fathers education (compulsory, intermediate, tertiary); and RR by paternal origin of country, no other adjustment for paternal factors RRs by paternal age, further adjusted for maternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+); RRs by paternal education, further adjusted for maternal education (compulsory, intermediate, tertiary); RRs by paternal occupation, no further adjustment for maternal factors; RRs by paternal country of origin adjusted for maternal country of origin (Norway, High-income countries, Low/middle-income countries) Categorized according to the class scheme of Erikson, Goldthorpe and Portocarero (EGP) [33] Categorized according to the classification by World Health Organization, Health statistics and information systems, Estimates for 2000–2012 [34] *p-value for difference between categories of paternal characteristics was < 0.001 using likelihood ratio test socioeconomic status, unplanned pregnancy, higher par- In Denmark, a cross-sectional study consisting of ity, smoking, single marital status, and non-western 22,000 pregnant women (primiparious and multipar- birthplace is the most important determinants for inad- ous) showed that only 14% of the women used FA as equate FA supplementation use [20–23]. Furthermore, recommended and compliance was positively associ- maternal chronic diseases and IVF were positively asso- ated with being primiparous, older than 25 years and ciated with adequate periconceptional FA supplementa- non-smoker [21]. Similarly, for about 16% of the tion use [22, 38]. births in our study, the mothers had followed the Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 6 of 8 Table 3 Relative risks (RRs) with 95% confidence intervals (95% CI) of adequate maternal periconceptional folic acid supplement use (before and during pregnancy) by combining maternal and paternal education in 683,785 pregnancies, Norway, 1999–2010 Adequate folic acid use Unadjusted Adjusted Maternal education Paternal education Yes No RR* 95% CI RR* 95% CI Compulsory education Compulsory education 2557 48,326 0.46 0.43–0.50 0.53 0.50–0.57 Intermediate education 4758 52,693 0.77 0.72–0.81 0.76 0.72–0.81 Tertiary education 1292 10,651 1.00 Reference 1.00 Reference Missing information 208 4994 Intermediate education Compulsory education 5079 43,708 0.60 0.57–0.62 0.66 0.64–0.68 Intermediate education 18,055 116,378 0.77 0.75–0.79 0.81 0.79–0.83 Tertiary education 7477 35,269 1.00 Reference 1.00 Reference Missing information 426 3928 Tertiary education Compulsory education 3805 17,985 0.70 0.67–0.72 0.75 0.73–0.77 Intermediate education 22,150 80,373 0.86 0.85–0.87 0.88 0.87–0.89 Tertiary education 42,541 126,896 1.00 Reference 1.00 Reference Missing information 747 3539 Missing data (maternal education) 28,179 1771 Adjusted for paternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+), year of childbirth (1999–2010 (continuous)), paternal country of origin (Norway, high income countries, low/middle income countries), stratified by maternal education *p values for interaction between maternal and paternal education were calculated by likelihood-ratio tests (unadjusted p value < 0.001; adjusted p value < 0.001) national guidelines of FA use in the study period and other European countries (Netherlands, Belgium, (1999–2010). Ireland and the United Kingdom) [23, 43–46]. These In Norway, a publication from the Norwegian Mother studies show that supplement use is less common and Child Cohort Study (MoBa), comprising 27% of the among most ethnic minority groups than among the births registered in MBRN during 2000–2003, showed comparison groups. We have similar findings in our similar results to ours [22]. They found a positive associ- study, showing a lower risk of adequate maternal FA use ation between paternal education and recommended among fathers originating from low/middle-income periconceptional FA use. In pregnancies with fathers countries. having university or college education the adjusted rela- The strengths of our study included use of compre- tive risk (RR) of periconceptional maternal FA use was hensive data from population-based registries in Norway 1.4 (95% CI 1.1–1.8) compared to pregnancies with fa- that assures generalizability of our results, and registra- thers with primary education. However, the association tion of individual-level information on periconceptional was weaker than for maternal education. When paternal FA intake for all births in Norway since 1999 (except for tertiary education was compared to paternal compulsory terminated pregnancies). education (reference) in our analyses, we found a similar Our study had some limitations. Maternal FA intake result for adjusted RR of 1.45 (95% CI 1.42–1.48). could have been misclassified; in the beginning of the Couples who live together share the same environ- study period, FA users were underreported to the MBRN ment, social network, financial resources, and to some [47]. Our results may therefore be somewhat weaker extent, the same health risk; beneficial or negative to than the true associations. Furthermore, we could not health outcomes depending on the health behaviour of adjust for pregnancy planning, maternal physical activity the spouses [25, 27]. Furthermore, a Dutch study of or maternal use of alcohol [16, 18, 20–24], as these po- 40,000 individuals aged 25–74 years showed that women tential confounders/covariates were not available in our seems more affected by their partner’s educational level dataset. However, a recent longitudinal study during than men are with regard to healthy behaviour [41]. 2014 on men’s pregnancy planning comprising about In accordance with our findings, a cross-sectional 800 participants in Sweden, showed that 81% of the household survey conducted in Pakistan (comprising pregnancies were planned and the level of paternal edu- 6266 women), showed that maternal intake of iron and cation was positively associated with pregnancy planning FA supplements was positively associated with the edu- [48]. Moreover, data from 22,500 mothers in the MoBa cational status of the mothers’ husband [42]. study with deliveries recorded in 2000–2003 showed that The association of ethnic background and maternal 78% of the mothers had planned their pregnancy [22]. periconceptional FA use have been studied in Norway However, MoBA is not entirely representative of the Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 7 of 8 total pregnant population in Norway, since the partici- Funding The Norwegian Cancer Society, Western Norway Regional Health Authority, pants are somewhat better educated, slightly older at de- project number 911629 to Dr. Nina Øyen, and the University of Bergen livery, and with a lower percentage of smokers than the supported this study. The study sponsors had no role in the design, analysis, overall pregnant population. interpretation of data, or writing of this manuscript. Information about fathers was not available in 12,699 Availability of data and materials births (2% of all births in the study population) and were Principal investigator, prof. Nina Øyen, sought and obtained all permissions excluded from the study population. They represent to access data from the Medical Birth Registry of Norway (MBRN), the National Registry (NR), the Norwegian Labour and Welfare Administration, births with fathers unreported by the pregnant woman and the Norwegian National Education Database (NUDB). The datasets or fathers without identification number from the NR. analysed during the current study are not freely available due to national Among the excluded births (missing father information), regulations. 10% of the mothers had adequate periconceptional FA Authors’ contributions supplementation (16% in the study population) with an JHM conceived the study, performed all analyses, and led the writing. NØ RR of 0.63 (95% CI 0.60–0.66) for adequate maternal FA and TB conceived the study and participated in manuscript preparation and writing. RMN participated in the analyses and writing. TF participated in the use comparing births with unregisterd fathers with statistical analyses. ST participated in manuscript preparation. All authors births having registered fathers. helped to conceptualize ideas, interpret findings, and review drafts of the Adjusting for maternal confounders (maternal age, manuscript. All authors read and approved the final manuscript. No conflicts of interest are declared. education, or country of origin) in our analysis reduced the strength of the associations between paternal deter- Ethics approval and consent to participate minants (age, education or country of origin) and ad- The study was approved by the Regional Committee for Medical and Health Research Ethics of Western Norway (REK ref. number 2010/3310). equate maternal periconceptional FA use. This suggest that paternal factors are important, but targeting mater- Competing interests nal demographic and socioeconomic conditions and The authors declare that they have no competing interests. other factors related to low use is still important. How- ever, our findings have implications for public health Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in practice. Recent research on men’s birth intentions has published maps and institutional affiliations. shown that 63% of pregnancies were intended (wanted) by the father [49]. Further, our study demonstrates the Author details Department of Global Public Health and Primary Care, University of Bergen, importance of the partner’s impact on maternal repro- Kalfarveien 31, N-5018 Bergen, Norway. Department of Obstetrics and ductive health and family planning through shared 3 Gynecology, Haukeland University Hospital, Bergen, Norway. Center for decision-making. Medical Genetics and Molecular Medicine, Haukeland University Hospital, Bergen, Norway. Department of Health and Social Sciences, Western Norway University of Applied Sciences, Bergen, Norway. Cancer Registry of Conclusions Norway, Oslo, Norway. In conclusion, our study supports the importance of fa- Received: 4 February 2017 Accepted: 15 May 2018 ther’s prenatal role in their children’s health. In order to improve maternal periconceptional FA supplementation References use, information and knowledge about the importance of 1. MRC. Prevention of neural tube defects: results of the Medical Research FA’s preventive potential needs to be directed to both Council vitamin study. MRC vitamin study research group. Lancet. 1991; men and women. Furthermore, our findings show that 338(8760):131–7. 2. Czeizel AE, Dudas I. Prevention of the first occurrence of neural-tube defects women having partners originating from low/middle-in- by periconceptional vitamin supplementation. N Engl J Med. 1992;327(26): come countries, partners at age < 30 and > 34 years, hav- 1832–5. ing compulsory education only, and having occupations 3. Berry RJ, Li Z, Erickson JD, Li S, Moore CA, Wang H, Mulinare J, Zhao P, Wong LY, Gindler J, et al. Prevention of neural-tube defects with folic acid other than “higher professional”, compared to “lower in China. China-U.S. collaborative project for neural tube defect prevention. professionals”, are particularly susceptible to low peri- N Engl J Med. 1999;341(20):1485–90. conceptional FA use. Therefore, campaigns for improved 4. Scientific Advisory Committee on Nutrition. Folate and Disease Prevention. TSO (The Stationery Office), vol. 2006. London: Scientific Advisory FA supplementation use should focus particularly on Committee on Nutrition. these groups. 5. De-Regil LM, Pena-Rosas JP, Fernandez-Gaxiola AC, Rayco-Solon P. Effects and safety of periconceptional oral folate supplementation for preventing Abbreviations birth defects. Cochrane Database Syst Rev. 2015;12:CD007950. BMI: Body mass index; DAGs: Directed acyclic graphs; IVF: In vitro fertilization; 6. Wagner C. Biochemical role of folate in cellular metabolism (reprinted from MBRN: Medical Birth Registry of Norway; MoBa: Norwegian Mother and Child folate and health disease, pgs 23-42, 1995). Clin Res Regul Aff. 2001;18(3): Cohort Study; NAV: Norwegian Labour and Welfare Administration; 161–80. NTDs: Neural tube defects; NUDB: Norwegian National Education Database 7. Sadler TWTW, Langman J. Langman's medical embryology, 11th ed. / T.W. Sadler; original illustrations by Jill Leland; computer illustrations by Susan L. Acknowledgements Sadler-Redmond; scanning electron micrographs by Kathy Tosney; The Norwegian Cancer Society, Western Norway Regional Health Authority, ultrasound images by Nancy Chescheir and Hytham Imseis. United States: and the University of Bergen are acknowledged. Philadelphia: Wolters Kluwer Lippincott Williams & Wilkins; 2010. Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 8 of 8 8. Suren P, Roth C, Bresnahan M, Haugen M, Hornig M, Hirtz D, Lie KK, Lipkin 28. Irgens LM. The medical birth registry of Norway. Epidemiological research WI, Magnus P, Reichborn-Kjennerud T, et al. Association between maternal and surveillance throughout 30 years. Acta Obstet Gynecol Scand. 2000; use of folic acid supplements and risk of autism spectrum disorders in 79(6):435–9. children. JAMA. 2013;309(6):570–7. 29. Kinge JM, Steingrimsdottir OA, Moe JO, Skirbekk V, Naess O, Strand BH. 9. Roth C, Magnus P, Schjolberg S, Stoltenberg C, Suren P, McKeague IW, Educational differences in life expectancy over five decades among the Davey Smith G, Reichborn-Kjennerud T, Susser E. Folic acid supplements in oldest old in Norway. Age Ageing. 2015; pregnancy and severe language delay in children. JAMA. 2011;306(14): 30. Hammer H. The central population registry in medical research. Tidsskr Nor 1566–73. Laegeforening. 2002;122(26):2550. 31. STYRK-08: [Standard Classification of Occupations (STYRK-08)] Standard for 10. Nilsen RM, Vollset SE, Rasmussen SA, Ueland PM, Daltveit AK. Folic acid and yrkesklassifisering (STYRK-08). In: Notater. Oslo–Kongsvinger: Statistics multivitamin supplement use and risk of placental abruption: a population- Norway; 2011. ISSN 1891-5906. https://www.ssb.no/en/. based registry study. Am J Epidemiol. 2008;167(7):867–74. 32. Vangen T: Nasjonal utdanningsdatabase NUDB. 2007. 11. Centers for disease control. Recommendations for the use of folic acid to 33. Erikson R, Goldthorpe JH. The constant flux: a study of class mobility in reduce the number of cases of spina bifida and other neural tube defects. industrial societies: Oxford University Press, USA; 1992. MMWR. 1992;41(RR-14):1–7. 34. Global Health Estimates 2015: Disease burden by Cause, Age, Sex, by 12. National Council on Nutrition and Physical Activity. Recommendations and Country and by Region, 2000-2015. Geneva: World Health Organization; means to increase folate intake among women in fertile age [Anbefalinger og virkemidler for økt folatinntak blant kvinner i fertil alder]. Report no 1/ 35. Shrier I, Platt RW. Reducing bias through directed acyclic graphs. BMC Med 1998. Oslo: National Council on Nutrition and Physical Activity [Statens Res Methodol. 2008;8(1):70. Ernæringsråd]; 1998. 36. Textor J, Hardt J, Knuppel S. DAGitty: a graphical tool for analyzing causal 13. Nordic Nutrition Recommendations 2012. In: Integrating nutrition and diagrams. Epidemiology. 2011;22(5):745. physical activity. Edited by 2014 NCoM. 5th ed. Copenhagen; 2014. http:// 37. Pearl J. An introduction to causal inference. Int J Biostat. 2010;6(2):Article 7. dx.doi.org/10.6027/Nord2014-002. 38. Nilsen RM, Leoncini E, Gastaldi P, Allegri V, Agostino R, Faravelli F, Ferrazzoli 14. Lumley J, Watson L, Watson M, Bower C. Periconceptional supplementation F, Finale E, Ghirri P, Scarano G, et al. Prevalence and determinants of with folate and/or multivitamins for preventing neural tube defects. preconception folic acid use: an Italian multicenter survey. Ital J Pediatr. Cochrane Database Syst Rev. 2001;(3):CD001056. https://doi.org/10.1002/ 2016;42(1):1–10. 14651858.CD001056. 39. StataCorp. Stata Statistical Software: Release 15. College Station. TX: 15. Daltveit AK, Vollset SE, Lande B, Oien H. Changes in knowledge and StataCorp LLC; 2017. attitudes of folate, and use of dietary supplements among women of 40. Cameron AC, Miller DL. A Practitioner's guide to cluster-robust inference. J reproductive age in Norway 1998-2000. Scand J Public Health. 2004;32(4): Hum Resour. 2015;50(2):317–73. 264–71. 41. Monden CW, van Lenthe F, de Graaf ND, Kraaykamp G. Partner's and own 16. Bower C, Miller M, Payne J, Serna P. Promotion of folate for the prevention education: does who you live with matter for self-assessed health, smoking of neural tube defects: who benefits? Paediatr Perinat Epidemiol. 2005;19(6): and excessive alcohol consumption? Soc Sci Med. 2003;57(10):1901–12. 435–44. 42. Nisar YB, Dibley MJ, Mir AM. Factors associated with non-use of antenatal 17. Ministry of Health and Care Services. [National action plan for a better diet iron and folic acid supplements among Pakistani women: a cross sectional (2017–2021)] Nasjonal handlingsplan for bedre kosthold (2017–2021). In: household survey. BMC Pregnancy Childbirth. 2014;14:305. Edited by omsorgsdepartementet MoHaCSH-o: Departementenes 43. Kinnunen TI, Sletner L, Sommer C, Post MC, Jenum AK. Ethnic differences in sikkerhets- og serviceorganisasjon; 2017. p. 57. folic acid supplement use in a population-based cohort of pregnant 18. Nilsen RM, Mastroiacovo P, Gunnes N, Alsaker ER, Bjorke-Monsen AL, Eussen women in Norway. BMC Pregnancy Childbirth. 2017;17(1):143. SJ, Haugen M, Johannessen A, Meltzer HM, Stoltenberg C, et al. Folic acid 44. Baraka MA, Steurbaut S, Leemans L, Foulon W, Laubach M, Coomans D, supplementation and interpregnancy interval. Paediatr Perinat Epidemiol. Jansen E, Dupont AG. Determinants of folic acid use in a multi-ethnic 2014;28(3):270–4. population of pregnant women: a cross-sectional study. J Perinat Med. 19. Medical birth registry and abortion registry - statistical database 2011;39(6):685–92. [Medisinsk fødselsregister og abortregisteret - statistikkbanker] [http:// 45. McGuire M, Cleary B, Sahm L, Murphy DJ. Prevalence and predictors of statistikk.fhi.no/mfr/]. Accessed 23 May 2018. periconceptional folic acid uptake–prospective cohort study in an Irish 20. Cueto HT, Riis AH, Hatch EE, Wise LA, Rothman KJ, Mikkelsen EM. Predictors urban obstetric population. Hum Reprod. 2010;25(2):535–43. of preconceptional folic acid or multivitamin supplement use: a cross- 46. Brough L, Rees GA, Crawford MA, Dorman EK. Social and ethnic differences sectional study of Danish pregnancy planners. Clin Epidemiol. 2012;4:259–65. in folic acid use preconception and during early pregnancy in the UK: effect 21. Knudsen VK, Orozova-Bekkevold I, Rasmussen LB, Mikkelsen TB, Michaelsen on maternal folate status. J Hum Nutr Diet. 2009;22(2):100–7. KF, Olsen SF. Low compliance with recommendations on folic acid use in 47. Nilsen RM, Vollset SE, Gjessing HK, Skjaerven R, Melve KK, Schreuder P, relation to pregnancy: is there a need for fortification? Public Health Nutr. Alsaker ER, Haug K, Daltveit AK, Magnus P. Self-selection and bias in a large 2004;7(7):843–50. prospective pregnancy cohort in Norway. Paediatr Perinat Epidemiol. 2009; 22. Nilsen RM, Vollset SE, Gjessing HK, Magnus P, Meltzer HM, Haugen M, 23(6):597–608. Ueland PM. Patterns and predictors of folic acid supplement use among 48. Bodin M, Kall L, Tyden T, Stern J, Drevin J, Larsson M. Exploring men's pregnant women: the Norwegian mother and child cohort study. Am J Clin pregnancy-planning behaviour and fertility knowledge:a survey among Nutr. 2006;84(5):1134–41. fathers in Sweden. Ups J Med Sci. 2017;122(2):127–35. 23. Timmermans S, Jaddoe VW, Mackenbach JP, Hofman A, Steegers- 49. Lindberg LD, Kost K. Exploring U.S. men's birth intentions. Matern Child Theunissen RP, Steegers EA. Determinants of folic acid use in early Health J. 2014;18(3):625–33. pregnancy in a multi-ethnic urban population in the Netherlands: the generation R study. Prev Med. 2008;47(4):427–32. 24. Braekke K, Staff AC. Periconceptional use of folic acid supplements in Oslo. Acta Obstet Gynecol Scand. 2003;82(7):620–7. 25. Jackson SE, Steptoe A, Wardle J. The influence of partner's behavior on health behavior change: the English longitudinal study of ageing. JAMA Intern Med. 2015;175(3):385–92. 26. Desrosiers A, Thompson A, Divney A, Magriples U, Kershaw T. Romantic partner influences on prenatal and postnatal substance use in young couples. J Public Health (Oxf). 2016;38(2):300–7. 27. Cornelius T, Desrosiers A, Kershaw T. Spread of health behaviors in young couples: how relationship power shapes relational influence. Soc Sci Med. 2016;165:46–55. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Pregnancy and Childbirth Springer Journals

Paternal characteristics associated with maternal periconceptional use of folic acid supplementation

Free
8 pages

Loading next page...
 
/lp/springer_journal/paternal-characteristics-associated-with-maternal-periconceptional-use-BOG1HEKXOu
Publisher
Springer Journals
Copyright
Copyright © 2018 by The Author(s).
Subject
Medicine & Public Health; Reproductive Medicine; Maternal and Child Health; Gynecology
eISSN
1471-2393
D.O.I.
10.1186/s12884-018-1830-1
Publisher site
See Article on Publisher Site

Abstract

Background: Maternal predictors of folic acid (FA) supplementation use to reduce offspring risk of neural tube defects are well known, while paternal determinants for maternal FA use are less known. Such knowledge is important to increase women’s compliance to recommended periconceptional FA use. Methods: In a nation-wide study of 683,785 births registered in the Medical Birth Registry of Norway during 1999–2010, the associations between paternal characteristics (age, education, occupation, country of origin) and maternal FA use were estimated by relative risks (RR) with 95% confidence intervals (CI), using log- binomial regression. Results: Maternal FA use before and during pregnancy (adequate FA use) was found in 16% of the births. The association between paternal age and adequate FA use was inversely U-shaped; adjusted RRs for adequate FA use were 0.35 (95% CI 0.28–0.43) and 0.72 (95% CI 0.71–0.74) for paternal age < 20 and ≥ 40 years, respectively, comparing age 30–34 years. Compulsory education (1–9 years) among fathers was compared to tertiary education; the RR was 0.69 (95% CI 0.68–0.71) for adequate FA use. The lower risk of adequate FA use for paternal compulsory education was present in all categories of maternal education. Occupation classes other than “Higher professionals” were associated with decreased risk of adequate FA use, compared with the reference “Lower professionals”.RRfor adequate FA use was 0.58 (95% CI 0.56–0.60) comparing fathers from “Low/middle-income countries” with fathers born in Norway. Conclusion: Adequate FA use in the periconceptional period was lower when fathers were younger or older than 30–34 years, had shorter education, had manual or self-employed occupations, or originated from low/ middle-income countries. Partners may contribute to increase women’suse of periconceptional FA supplementation. Keywords: Pregnancy, Supplement use, Folic acid, Norway Background [6]. Start of FA supplementation prior to conceiving is Folate is necessary in foetal development, and folic acid important in order to reduce the risk of NTDs because (FA) supplementation is widely acknowledged to reduce the neural tube closes between 21 and 28 days after the risk of neural tube defects (NTDs) [1–5]. FA is the conception [7]. synthetic form of the B-vitamin folate, which is essential Randomized clinical trials and non-randomized in the synthesis of DNA, methylation, and DNA repair intervention trials have demonstrated that periconcep- tional FA use reduces the risk of NTDs [1–3]. Recent * Correspondence: jan.mortensen@uib.no studies have reported that FA is associated with protec- Department of Global Public Health and Primary Care, University of Bergen, tion against other neurodevelopmental disorders and Kalfarveien 31, N-5018 Bergen, Norway some severe pregnancy complications [8–10]. The pro- Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway tective effect of FA on NTDs has led health authorities Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 2 of 8 in several countries, including Norway, to recommend MBRN is a population-based registry containing women to take FA supplements before pregnancy and in information on all births in Norway since 1967 [28]. The early pregnancy [11–13]. registry holds demographic information on the mother Many countries in Europe, including Norway, have and the father, the mother’s health before and during performed information campaigns to increase the use of pregnancy, including chronic diseases, information on in periconceptional FA supplementation among women vitro fertilization (IVF), complications during pregnancy planning pregnancy [14–16]. Presently there is no and delivery as well as information on the infant, includ- mandatory folic acid food fortification in Norway [17]. ing birth defects and other perinatal problems. Midwives Official Norwegian guidelines from 1998, states that all and physicians attending the deliveries register the data. women planning their pregnancy should use 0.4 mg FA Since 1967, there has been mandatory reporting of all daily from 1 month before pregnancy and throughout live and stillbirths from the 16 gestational week to the first 2–3 months of pregnancy to reduce the risk of MBRN. NTDs [12]. However, the proportion of preconception NR contains demographic information on all residents FA supplementation use in Norway is still too low [18] in Norway since 1960, including the date of birth, and by 2015 it was 33% [19]. country of origin, and the dates of immigration, emigra- Previous studies have identified maternal factors tion, or death [30]. NR assigns a unique personal identi- associated with inadequate FA in the periconceptional fication number to all individuals born or immigrated to period, such as low maternal age, shorter education, Norway, enabling accurate record linkages. single parenthood, unplanned pregnancy, lower parity, NAV was established in 2006 after governmental smoking, alcohol use, less physical activity, or originating reorganization of the Directorate of Labour in Norway from a foreign country [15, 16, 20–24]. (founded in 1945), and has registered information on Since couples tend to exhibit concordant health occupation, health status, and social benefits of all indi- behaviour’s for dietary intake, smoking, alcohol viduals with residence in Norway since 1992. The consumption, physical activity, and body mass index Norwegian occupational code system is based on the (BMI) [25–27], a woman’s partner may contribute to her International Standard Classification of Occupations use of periconceptional FA supplements. In fact, in an (ISCO), revised version from 1988 [31]. early report from the Norwegian Mother and Child Since 1970, NUDB holds information on all individ- Cohort Study (MoBa), 2000–2003, counting 22,500 uals’ education history from primary school up to women, FA supplements were used more frequently doctoral studies in one database [32]. The classification among women with partners with a higher education is based on the Norwegian Standard Classification of [22]. However, the study did not assess other paternal Education. factors or combined paternal and maternal factors as to identify women with inadequate FA use. Maternal FA supplement use Taking advantage of the Medical Birth Registry of We constructed a binary variable for intake of FA sup- Norway that to our knowledge is the only national regis- plement use (0.4 mg/day) (regardless of concomitant try with information on periconceptional use of FA sup- multivitamin use) registered in the MBRN since Decem- plements [28], we updated parent information with data ber 1998 onwards; adequate FA use (recommended FA from national registries to investigate whether paternal supplementation before and during pregnancy), and in- factors (age, education, occupation, country of origin) adequate FA use (FA supplementation only before preg- was associated with mothers’ intake of recommended FA nancy, or only during pregnancy, or no record of FA in pregnancy. use). MBRN also registers multivitamin use, but our investi- gation focused on periconceptional FA use as such in- Methods take was according to official guidelines. Data-sources Maternal FA use before and/or during pregnancy was Paternal characteristics collected from the Medical Birth Registry of Norway We used the following paternal variables in our (MBRN) [28]. Paternal and maternal demographic data analyses of adequate FA supplementation; paternal came from the National Registry (NR). Information on age (< 20, 20–24, 25–29, 30–34, 35–39, 40+ years); paternal and maternal occupation originated from the education (Compulsory (1–9 years), Intermediate (10– Norwegian Labour and Welfare Administration (NAV), 12 years), Tertiary (13–19 years)); occupation accord- and we retrieved paternal and maternal educational data ing to the class scheme of Erikson, Goldthorpe, and from the Norwegian National Education Database Portocarero (I Higher professionals, II Lower profes- (NUDB) [29]. sionals, IIIa Higher routine, IIIb Lower routine, IV Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 3 of 8 Other self-employed workers, V Technicians, VI overall difference between the categories of paternal Skilled, VII Semiskilled and unskilled, VIIb Agricul- characteristics were calculated using likelihood ratio tural, Unclassified) (EGP) [33]; and country of origin tests. We evaluated and tested the potential effect modi- according to the classification by World Health fication of the association between paternal education Organization, Health statistics and information sys- and maternal FA use by stratification and likelihood ra- tems, Estimates for 2000–2012 (Norway, High income tio test. countries, Low/middle-income countries) [34]. Covariates Results We used directed acyclic graphs (DAGs) and Our study included 683,785 births during 1999–2010. subject-matter knowledge to select a minimally sufficient Table 1 presents the characteristics of the parents. The adjustment set of variables that identify the uncon- median ages of the fathers and mothers at childbirth founded association of paternal characteristics on ad- were 33 and 30 years, respectively. For about 41% of the equate maternal FA supplementation use [35–37]. births, the mothers were primiparous, and about 2% of The potential confounders of the paternal characteris- the births were conceived after in vitro fertilization tics and maternal FA use relationship included year of (IVF). The majority of the births were of childbirth (continuous), paternal age (< 20, 20–24, 25– Norwegian-born parents (84% of the fathers and 83% of 29, 30–34, 35–39, 40+ years), education (Compulsory, the mothers). For about 34% of the births, the fathers Intermediate, Tertiary), or country of origin (Norway, had tertiary education, and for about 19% of the births, High-income countries, Low/middle-income countries). the fathers had compulsory education only. The paternal Furthermore, we included maternal age (< 20, 20–24, educational level varied by his country of origin. Fathers 25–29, 30–34, 35–39, 40+ years), maternal education originating from low/middle-income countries generally (Compulsory, Intermediate, Tertiary), and maternal had lower educational level compared to fathers origin- country of origin (Norway, High-income countries, Low/ ating from Norway and other high-income countries middle-income countries) as possible confounders of the (not shown). Occupation classified as “Lower profes- associations between paternal age, education, or country sionals,” accounted for 22% of all the births. For about of origin, and maternal adequate FA use. 14% of the births, the women smoked daily at the start Maternal smoking was not included in the final of pregnancy, about 3% smoked intermittently, and 67% models because smoking was not considered a con- did not smoke. Nearly 17% of the smoking data were founder of the association of paternal characteristics on missing. maternal FA supplementation use [38]. For about 16% of all births in the study population, the mothers were assigned to the category adequate FA Study population supplementation users. However, during 1999 through During 1999–2010, 716,021 births were registered in 2010, the proportion of adequate FA supplementation MBRN. We excluded births (induced abortions) without use increased from 4% at the start of the study period information on FA or multivitamin supplementation use (1999) to 26% in 2010. (2519) and births without maternal identification num- Table 2 presents crude and adjusted RRs for ad- ber (4091). For multiple births, we included data for the equate maternal periconceptional FA use by paternal first birth and excluded 12,927 next born individuals. variables (determinants). Adjusted analyses showed an Among the remaining 696,484 births, we excluded inverse “U-shaped” relationship between paternal age 12,699 births without paternal identification number, and adequate maternal FA supplement use where the leaving 683,785 live births and stillbirths for analyses. smallest RRs were found for paternal age below 20 years (RR 0.35 (95% CI 0.28–0.43)), 20–24 years Statistical analysis (RR 0.68 (95% CI 0.66–0.71)), and 40 years and above Associations between paternal characteristics (age, edu- (RR 0.72 (95% CI 0.71–0.74)) compared to paternal cation, occupation, country of origin) and maternal FA age 30–34 years. Paternal compulsory education was use were estimated as relative risks (RRs) with 95% con- associated with reduced risk of adequate FA use (RR fidence intervals (CIs) by log-binomial regression, using 0.69 (95% CI 0.68–0.71)) compared to paternal ter- the log-link function in Stata version 15 [39]. The 95% tiary education. All paternal occupation classes were CIs were based on robust variance estimation with the associated with reduced risk of adequate FA use ex- sandwich estimator to correct for the intra-individual cept for “I Higher professionals”,whencomparedto correlation in women with more than one pregnancy “II Lower professionals”, in particular “VII Semiskilled during the study period [40]. Births with missing data on and unskilled” (RR 0.75 (95% CI 0.73–0.76)), and covariates were excluded from the analyses. P-values for “VIIb Agricultural” (RR 0.73 (95% CI 0.69–0.78)). Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 4 of 8 Table 1 Paternal and maternal characteristics in 683,785 births Table 1 Paternal and maternal characteristics in 683,785 births in Norway, 1999–2010 in Norway, 1999–2010 (Continued) Births Maternal chronic disease Fathers % Mothers % No 623,817 91.2 Number of births 683,785 100.0 683,785 100.0 Yes 59,968 8.8 Age Maternal smoking before pregnancy < 20 4401 0.6 15,464 2.3 Non-smoker 456,797 66.8 20–24 48,448 7.1 100,016 14.6 Intermittent 18,518 2.7 25–29 162,671 23.8 223,480 32.7 Daily 93,662 13.7 30–34 235,401 34.4 228,203 33.4 Missing data 114,808 16.8 35–39 151,540 22.2 99,727 14.6 Maternal folic acid use in pregnancy 40+ 81,324 11.9 16,895 2.5 No use 371,820 54.4 Education Only before 8930 1.3 Compulsory education (1–9 years) 130,953 19.2 125,479 18.4 Only during 192,169 28.1 Intermediate (10–12 years) 302,384 44.2 230,320 33.7 Before and during 110,866 16.2 Categorized according to the class scheme of Erikson, Goldthorpe and Tertiary education (13–19 years) 229,818 33.6 298,036 43.6 Portocarero (EGP) [33] Missing data 20,630 3.0 29,950 4.4 Categorized according to the classification by World Health Organization, Health statistics and information systems, Estimates for 2000–2012 [34] Occupational class Asthma, hypertension, kidney disease, chronic urinary infection, rheumatoid I Higher professionals 86,635 12.7 50,650 7.4 arthritis, heart disease, epilepsy, diabetes mellitus (type I or II), and thyroid disease II Lower professionals 152,781 22.3 122,804 18.0 IIIa Higher routine 77,540 11.3 197,174 28.8 Mothers whose children’s father originated from low/ middle-income countries had also a reduced risk of ad- IIIb Lower routine 40,070 5.9 114,795 16.8 equate FA use (RR 0.58 (95% CI 0.56–0.60)) compared IV Other self-employed workers 358 0.1 119 0.0 to fathers originating from Norway. V Technicians 5550 0.8 1492 0.2 Table 3 presents crude and adjusted RRs with 95% CIs VI Skilled 108,755 15.9 15,961 2.3 of adequate FA use by maternal and paternal education. VII Semiskilled and unskilled 111,584 16.3 73,994 10.8 Adjusted analyses showed that adequate FA use was less VIIb Agricultural 7663 1.1 2720 0.4 likely in births were fathers had compulsory education, regardless of maternal education. The association of pa- Unclassified 52,824 7.7 51,264 7.5 ternal compulsory education and recommended FA use Missing data 40,025 5.9 52,812 7.7 was weakened by increasing level of maternal education. Country of origin However, even when the mother had tertiary education, Norway 574,602 84.0 567,241 83.0 the association of compulsory paternal education on ad- High income countries 33,487 4.9 30,920 4.5 equate maternal FA use was significant (RR 0.75 (95% CI Low/middle-income countries 75,497 11.0 85,597 12.5 0.73–0.77)), compared to fathers with tertiary education. Missing data 199 0.0 27 0.0 Discussion Marital status The present population-based study (683,785 births Unmarried 37,057 5.4 during 1999–2010) showed that recommended maternal Married/Partnership 634,283 92.8 FA use was low among fathers who were young or older Divorced 3417 0.5 at their children’s birth, had achieved shorter education, Missing data 9028 1.3 held a manually or self-employed occupation, or originated from low/middle-income countries. Even In vitro fertilization (IVF) among mothers who had achieved higher education, rec- No 669,024 97.8 ommended periconceptional maternal FA use was low Yes 14,761 2.2 among less educated fathers. Birth order Several studies have investigated the association be- 1 280,178 41.0 tween maternal socio-demographic, reproductive, and 2 244,532 35.8 medical characteristics and adherence to recommended intake of periconceptional FA. A common feature among ≥3 159,075 23.3 mothers is that young age, low educational level, low Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 5 of 8 Table 2 Relative risks (RRs) with 95% confidence intervals (95% CIs) of adequate maternal periconceptional folic acid supplement use (before and during pregnancy) by paternal characteristics, in 683,785 births, Norway, 1999–2010 ab Folic acid supplementation Unadjusted Adjusted for paternal factors Further adjusted for maternal ac use factors Characteristics Yes No RR* 95% CI RR* 95% CI RR* 95% CI Paternal age (years) < 20 86 4315 0.11 0.09–0.13 0.10 0.08–0.13 0.35 0.28–0.43 20–24 3325 45,123 0.37 0.36–0.39 0.37 0.36–0.38 0.68 0.66–0.71 25–29 22,886 139,785 0.76 0.75–0.78 0.77 0.76–0.79 0.94 0.93–0.96 30–34 43,348 192,053 1.00 Reference 1.00 Reference 1.00 Reference 35–39 28,488 123,052 1.02 1.01–1.03 0.97 0.96–0.99 0.90 0.89–0.91 40+ 12,733 68,591 0.85 0.83–0.87 0.80 0.78–0.81 0.72 0.71–0.74 Paternal education Compulsory (1–10 years) 11,694 119,259 0.40 0.39–0.40 0.52 0.51–0.53 0.69 0.68–0.71 Intermediate (11–13 years) 45,411 256,973 0.67 0.66–0.67 0.75 0.74–0.76 0.87 0.85–0.88 Tertiary (14–20 years) 51,894 177,924 1.00 Reference 1.00 Reference 1.00 Reference Missing data 1867 18,763 Paternal occupational class I Higher professionals 19,957 66,678 1.05 1.04–1.07 1.05 1.03–1.06 II Lower professionals 33,366 119,415 1.00 Reference 1.00 Reference IIIa Higher routine 12,292 65,248 0.73 0.71–0.74 0.89 0.88–0.91 IIIb Lower routine 5352 34,718 0.61 0.59–0.63 0.85 0.83–0.87 IV Other self-employed workers 60 298 0.77 0.61–0.97 0.83 0.65–1.05 V Technicians 836 4714 0.69 0.65–0.74 0.89 0.84–0.95 VI Skilled 15,174 93,581 0.64 0.63–0.65 0.84 0.83–0.86 VII Semiskilled and unskilled 11,643 99,941 0.48 0.47–0.49 0.75 0.73–0.76 VIIb Agricultural 908 6755 0.54 0.51–0.58 0.73 0.69–0.78 Unclassified 7575 45,249 0.66 0.64–0.67 0.96 0.94–0.99 Missing data 3703 36,322 Paternal country of origin Norway 99,339 475,263 1.00 Reference 1.00 Reference 1.00 Reference High income countries 6535 26,952 1.13 1.10–1.16 1.06 1.04–1.09 1.06 1.03–1.08 Low-middle-income countries 4975 70,522 0.38 0.37–0.39 0.35 0.34–0.36 0.58 0.56–0.60 Missing data 17 182 All RRs for adequate folic acid supplementation adjusted for year of childbirth (continuous) RRs by paternal age, no other adjustment for paternal factors; RRs by paternal education adjusted for paternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+), paternal country of origin (Norway, high-income countries, low/middle-income countries); RRs by paternal occupation adjusted for paternal age, fathers country of origin, fathers education (compulsory, intermediate, tertiary); and RR by paternal origin of country, no other adjustment for paternal factors RRs by paternal age, further adjusted for maternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+); RRs by paternal education, further adjusted for maternal education (compulsory, intermediate, tertiary); RRs by paternal occupation, no further adjustment for maternal factors; RRs by paternal country of origin adjusted for maternal country of origin (Norway, High-income countries, Low/middle-income countries) Categorized according to the class scheme of Erikson, Goldthorpe and Portocarero (EGP) [33] Categorized according to the classification by World Health Organization, Health statistics and information systems, Estimates for 2000–2012 [34] *p-value for difference between categories of paternal characteristics was < 0.001 using likelihood ratio test socioeconomic status, unplanned pregnancy, higher par- In Denmark, a cross-sectional study consisting of ity, smoking, single marital status, and non-western 22,000 pregnant women (primiparious and multipar- birthplace is the most important determinants for inad- ous) showed that only 14% of the women used FA as equate FA supplementation use [20–23]. Furthermore, recommended and compliance was positively associ- maternal chronic diseases and IVF were positively asso- ated with being primiparous, older than 25 years and ciated with adequate periconceptional FA supplementa- non-smoker [21]. Similarly, for about 16% of the tion use [22, 38]. births in our study, the mothers had followed the Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 6 of 8 Table 3 Relative risks (RRs) with 95% confidence intervals (95% CI) of adequate maternal periconceptional folic acid supplement use (before and during pregnancy) by combining maternal and paternal education in 683,785 pregnancies, Norway, 1999–2010 Adequate folic acid use Unadjusted Adjusted Maternal education Paternal education Yes No RR* 95% CI RR* 95% CI Compulsory education Compulsory education 2557 48,326 0.46 0.43–0.50 0.53 0.50–0.57 Intermediate education 4758 52,693 0.77 0.72–0.81 0.76 0.72–0.81 Tertiary education 1292 10,651 1.00 Reference 1.00 Reference Missing information 208 4994 Intermediate education Compulsory education 5079 43,708 0.60 0.57–0.62 0.66 0.64–0.68 Intermediate education 18,055 116,378 0.77 0.75–0.79 0.81 0.79–0.83 Tertiary education 7477 35,269 1.00 Reference 1.00 Reference Missing information 426 3928 Tertiary education Compulsory education 3805 17,985 0.70 0.67–0.72 0.75 0.73–0.77 Intermediate education 22,150 80,373 0.86 0.85–0.87 0.88 0.87–0.89 Tertiary education 42,541 126,896 1.00 Reference 1.00 Reference Missing information 747 3539 Missing data (maternal education) 28,179 1771 Adjusted for paternal age (< 20, 20–24, 25–29, 30–34, 35–39, 40+), year of childbirth (1999–2010 (continuous)), paternal country of origin (Norway, high income countries, low/middle income countries), stratified by maternal education *p values for interaction between maternal and paternal education were calculated by likelihood-ratio tests (unadjusted p value < 0.001; adjusted p value < 0.001) national guidelines of FA use in the study period and other European countries (Netherlands, Belgium, (1999–2010). Ireland and the United Kingdom) [23, 43–46]. These In Norway, a publication from the Norwegian Mother studies show that supplement use is less common and Child Cohort Study (MoBa), comprising 27% of the among most ethnic minority groups than among the births registered in MBRN during 2000–2003, showed comparison groups. We have similar findings in our similar results to ours [22]. They found a positive associ- study, showing a lower risk of adequate maternal FA use ation between paternal education and recommended among fathers originating from low/middle-income periconceptional FA use. In pregnancies with fathers countries. having university or college education the adjusted rela- The strengths of our study included use of compre- tive risk (RR) of periconceptional maternal FA use was hensive data from population-based registries in Norway 1.4 (95% CI 1.1–1.8) compared to pregnancies with fa- that assures generalizability of our results, and registra- thers with primary education. However, the association tion of individual-level information on periconceptional was weaker than for maternal education. When paternal FA intake for all births in Norway since 1999 (except for tertiary education was compared to paternal compulsory terminated pregnancies). education (reference) in our analyses, we found a similar Our study had some limitations. Maternal FA intake result for adjusted RR of 1.45 (95% CI 1.42–1.48). could have been misclassified; in the beginning of the Couples who live together share the same environ- study period, FA users were underreported to the MBRN ment, social network, financial resources, and to some [47]. Our results may therefore be somewhat weaker extent, the same health risk; beneficial or negative to than the true associations. Furthermore, we could not health outcomes depending on the health behaviour of adjust for pregnancy planning, maternal physical activity the spouses [25, 27]. Furthermore, a Dutch study of or maternal use of alcohol [16, 18, 20–24], as these po- 40,000 individuals aged 25–74 years showed that women tential confounders/covariates were not available in our seems more affected by their partner’s educational level dataset. However, a recent longitudinal study during than men are with regard to healthy behaviour [41]. 2014 on men’s pregnancy planning comprising about In accordance with our findings, a cross-sectional 800 participants in Sweden, showed that 81% of the household survey conducted in Pakistan (comprising pregnancies were planned and the level of paternal edu- 6266 women), showed that maternal intake of iron and cation was positively associated with pregnancy planning FA supplements was positively associated with the edu- [48]. Moreover, data from 22,500 mothers in the MoBa cational status of the mothers’ husband [42]. study with deliveries recorded in 2000–2003 showed that The association of ethnic background and maternal 78% of the mothers had planned their pregnancy [22]. periconceptional FA use have been studied in Norway However, MoBA is not entirely representative of the Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 7 of 8 total pregnant population in Norway, since the partici- Funding The Norwegian Cancer Society, Western Norway Regional Health Authority, pants are somewhat better educated, slightly older at de- project number 911629 to Dr. Nina Øyen, and the University of Bergen livery, and with a lower percentage of smokers than the supported this study. The study sponsors had no role in the design, analysis, overall pregnant population. interpretation of data, or writing of this manuscript. Information about fathers was not available in 12,699 Availability of data and materials births (2% of all births in the study population) and were Principal investigator, prof. Nina Øyen, sought and obtained all permissions excluded from the study population. They represent to access data from the Medical Birth Registry of Norway (MBRN), the National Registry (NR), the Norwegian Labour and Welfare Administration, births with fathers unreported by the pregnant woman and the Norwegian National Education Database (NUDB). The datasets or fathers without identification number from the NR. analysed during the current study are not freely available due to national Among the excluded births (missing father information), regulations. 10% of the mothers had adequate periconceptional FA Authors’ contributions supplementation (16% in the study population) with an JHM conceived the study, performed all analyses, and led the writing. NØ RR of 0.63 (95% CI 0.60–0.66) for adequate maternal FA and TB conceived the study and participated in manuscript preparation and writing. RMN participated in the analyses and writing. TF participated in the use comparing births with unregisterd fathers with statistical analyses. ST participated in manuscript preparation. All authors births having registered fathers. helped to conceptualize ideas, interpret findings, and review drafts of the Adjusting for maternal confounders (maternal age, manuscript. All authors read and approved the final manuscript. No conflicts of interest are declared. education, or country of origin) in our analysis reduced the strength of the associations between paternal deter- Ethics approval and consent to participate minants (age, education or country of origin) and ad- The study was approved by the Regional Committee for Medical and Health Research Ethics of Western Norway (REK ref. number 2010/3310). equate maternal periconceptional FA use. This suggest that paternal factors are important, but targeting mater- Competing interests nal demographic and socioeconomic conditions and The authors declare that they have no competing interests. other factors related to low use is still important. How- ever, our findings have implications for public health Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in practice. Recent research on men’s birth intentions has published maps and institutional affiliations. shown that 63% of pregnancies were intended (wanted) by the father [49]. Further, our study demonstrates the Author details Department of Global Public Health and Primary Care, University of Bergen, importance of the partner’s impact on maternal repro- Kalfarveien 31, N-5018 Bergen, Norway. Department of Obstetrics and ductive health and family planning through shared 3 Gynecology, Haukeland University Hospital, Bergen, Norway. Center for decision-making. Medical Genetics and Molecular Medicine, Haukeland University Hospital, Bergen, Norway. Department of Health and Social Sciences, Western Norway University of Applied Sciences, Bergen, Norway. Cancer Registry of Conclusions Norway, Oslo, Norway. In conclusion, our study supports the importance of fa- Received: 4 February 2017 Accepted: 15 May 2018 ther’s prenatal role in their children’s health. In order to improve maternal periconceptional FA supplementation References use, information and knowledge about the importance of 1. MRC. Prevention of neural tube defects: results of the Medical Research FA’s preventive potential needs to be directed to both Council vitamin study. MRC vitamin study research group. Lancet. 1991; men and women. Furthermore, our findings show that 338(8760):131–7. 2. Czeizel AE, Dudas I. Prevention of the first occurrence of neural-tube defects women having partners originating from low/middle-in- by periconceptional vitamin supplementation. N Engl J Med. 1992;327(26): come countries, partners at age < 30 and > 34 years, hav- 1832–5. ing compulsory education only, and having occupations 3. Berry RJ, Li Z, Erickson JD, Li S, Moore CA, Wang H, Mulinare J, Zhao P, Wong LY, Gindler J, et al. Prevention of neural-tube defects with folic acid other than “higher professional”, compared to “lower in China. China-U.S. collaborative project for neural tube defect prevention. professionals”, are particularly susceptible to low peri- N Engl J Med. 1999;341(20):1485–90. conceptional FA use. Therefore, campaigns for improved 4. Scientific Advisory Committee on Nutrition. Folate and Disease Prevention. TSO (The Stationery Office), vol. 2006. London: Scientific Advisory FA supplementation use should focus particularly on Committee on Nutrition. these groups. 5. De-Regil LM, Pena-Rosas JP, Fernandez-Gaxiola AC, Rayco-Solon P. Effects and safety of periconceptional oral folate supplementation for preventing Abbreviations birth defects. Cochrane Database Syst Rev. 2015;12:CD007950. BMI: Body mass index; DAGs: Directed acyclic graphs; IVF: In vitro fertilization; 6. Wagner C. Biochemical role of folate in cellular metabolism (reprinted from MBRN: Medical Birth Registry of Norway; MoBa: Norwegian Mother and Child folate and health disease, pgs 23-42, 1995). Clin Res Regul Aff. 2001;18(3): Cohort Study; NAV: Norwegian Labour and Welfare Administration; 161–80. NTDs: Neural tube defects; NUDB: Norwegian National Education Database 7. Sadler TWTW, Langman J. Langman's medical embryology, 11th ed. / T.W. Sadler; original illustrations by Jill Leland; computer illustrations by Susan L. Acknowledgements Sadler-Redmond; scanning electron micrographs by Kathy Tosney; The Norwegian Cancer Society, Western Norway Regional Health Authority, ultrasound images by Nancy Chescheir and Hytham Imseis. United States: and the University of Bergen are acknowledged. Philadelphia: Wolters Kluwer Lippincott Williams & Wilkins; 2010. Mortensen et al. BMC Pregnancy and Childbirth (2018) 18:188 Page 8 of 8 8. Suren P, Roth C, Bresnahan M, Haugen M, Hornig M, Hirtz D, Lie KK, Lipkin 28. Irgens LM. The medical birth registry of Norway. Epidemiological research WI, Magnus P, Reichborn-Kjennerud T, et al. Association between maternal and surveillance throughout 30 years. Acta Obstet Gynecol Scand. 2000; use of folic acid supplements and risk of autism spectrum disorders in 79(6):435–9. children. JAMA. 2013;309(6):570–7. 29. Kinge JM, Steingrimsdottir OA, Moe JO, Skirbekk V, Naess O, Strand BH. 9. Roth C, Magnus P, Schjolberg S, Stoltenberg C, Suren P, McKeague IW, Educational differences in life expectancy over five decades among the Davey Smith G, Reichborn-Kjennerud T, Susser E. Folic acid supplements in oldest old in Norway. Age Ageing. 2015; pregnancy and severe language delay in children. JAMA. 2011;306(14): 30. Hammer H. The central population registry in medical research. Tidsskr Nor 1566–73. Laegeforening. 2002;122(26):2550. 31. STYRK-08: [Standard Classification of Occupations (STYRK-08)] Standard for 10. Nilsen RM, Vollset SE, Rasmussen SA, Ueland PM, Daltveit AK. Folic acid and yrkesklassifisering (STYRK-08). In: Notater. Oslo–Kongsvinger: Statistics multivitamin supplement use and risk of placental abruption: a population- Norway; 2011. ISSN 1891-5906. https://www.ssb.no/en/. based registry study. Am J Epidemiol. 2008;167(7):867–74. 32. Vangen T: Nasjonal utdanningsdatabase NUDB. 2007. 11. Centers for disease control. Recommendations for the use of folic acid to 33. Erikson R, Goldthorpe JH. The constant flux: a study of class mobility in reduce the number of cases of spina bifida and other neural tube defects. industrial societies: Oxford University Press, USA; 1992. MMWR. 1992;41(RR-14):1–7. 34. Global Health Estimates 2015: Disease burden by Cause, Age, Sex, by 12. National Council on Nutrition and Physical Activity. Recommendations and Country and by Region, 2000-2015. Geneva: World Health Organization; means to increase folate intake among women in fertile age [Anbefalinger og virkemidler for økt folatinntak blant kvinner i fertil alder]. Report no 1/ 35. Shrier I, Platt RW. Reducing bias through directed acyclic graphs. BMC Med 1998. Oslo: National Council on Nutrition and Physical Activity [Statens Res Methodol. 2008;8(1):70. Ernæringsråd]; 1998. 36. Textor J, Hardt J, Knuppel S. DAGitty: a graphical tool for analyzing causal 13. Nordic Nutrition Recommendations 2012. In: Integrating nutrition and diagrams. Epidemiology. 2011;22(5):745. physical activity. Edited by 2014 NCoM. 5th ed. Copenhagen; 2014. http:// 37. Pearl J. An introduction to causal inference. Int J Biostat. 2010;6(2):Article 7. dx.doi.org/10.6027/Nord2014-002. 38. Nilsen RM, Leoncini E, Gastaldi P, Allegri V, Agostino R, Faravelli F, Ferrazzoli 14. Lumley J, Watson L, Watson M, Bower C. Periconceptional supplementation F, Finale E, Ghirri P, Scarano G, et al. Prevalence and determinants of with folate and/or multivitamins for preventing neural tube defects. preconception folic acid use: an Italian multicenter survey. Ital J Pediatr. Cochrane Database Syst Rev. 2001;(3):CD001056. https://doi.org/10.1002/ 2016;42(1):1–10. 14651858.CD001056. 39. StataCorp. Stata Statistical Software: Release 15. College Station. TX: 15. Daltveit AK, Vollset SE, Lande B, Oien H. Changes in knowledge and StataCorp LLC; 2017. attitudes of folate, and use of dietary supplements among women of 40. Cameron AC, Miller DL. A Practitioner's guide to cluster-robust inference. J reproductive age in Norway 1998-2000. Scand J Public Health. 2004;32(4): Hum Resour. 2015;50(2):317–73. 264–71. 41. Monden CW, van Lenthe F, de Graaf ND, Kraaykamp G. Partner's and own 16. Bower C, Miller M, Payne J, Serna P. Promotion of folate for the prevention education: does who you live with matter for self-assessed health, smoking of neural tube defects: who benefits? Paediatr Perinat Epidemiol. 2005;19(6): and excessive alcohol consumption? Soc Sci Med. 2003;57(10):1901–12. 435–44. 42. Nisar YB, Dibley MJ, Mir AM. Factors associated with non-use of antenatal 17. Ministry of Health and Care Services. [National action plan for a better diet iron and folic acid supplements among Pakistani women: a cross sectional (2017–2021)] Nasjonal handlingsplan for bedre kosthold (2017–2021). In: household survey. BMC Pregnancy Childbirth. 2014;14:305. Edited by omsorgsdepartementet MoHaCSH-o: Departementenes 43. Kinnunen TI, Sletner L, Sommer C, Post MC, Jenum AK. Ethnic differences in sikkerhets- og serviceorganisasjon; 2017. p. 57. folic acid supplement use in a population-based cohort of pregnant 18. Nilsen RM, Mastroiacovo P, Gunnes N, Alsaker ER, Bjorke-Monsen AL, Eussen women in Norway. BMC Pregnancy Childbirth. 2017;17(1):143. SJ, Haugen M, Johannessen A, Meltzer HM, Stoltenberg C, et al. Folic acid 44. Baraka MA, Steurbaut S, Leemans L, Foulon W, Laubach M, Coomans D, supplementation and interpregnancy interval. Paediatr Perinat Epidemiol. Jansen E, Dupont AG. Determinants of folic acid use in a multi-ethnic 2014;28(3):270–4. population of pregnant women: a cross-sectional study. J Perinat Med. 19. Medical birth registry and abortion registry - statistical database 2011;39(6):685–92. [Medisinsk fødselsregister og abortregisteret - statistikkbanker] [http:// 45. McGuire M, Cleary B, Sahm L, Murphy DJ. Prevalence and predictors of statistikk.fhi.no/mfr/]. Accessed 23 May 2018. periconceptional folic acid uptake–prospective cohort study in an Irish 20. Cueto HT, Riis AH, Hatch EE, Wise LA, Rothman KJ, Mikkelsen EM. Predictors urban obstetric population. Hum Reprod. 2010;25(2):535–43. of preconceptional folic acid or multivitamin supplement use: a cross- 46. Brough L, Rees GA, Crawford MA, Dorman EK. Social and ethnic differences sectional study of Danish pregnancy planners. Clin Epidemiol. 2012;4:259–65. in folic acid use preconception and during early pregnancy in the UK: effect 21. Knudsen VK, Orozova-Bekkevold I, Rasmussen LB, Mikkelsen TB, Michaelsen on maternal folate status. J Hum Nutr Diet. 2009;22(2):100–7. KF, Olsen SF. Low compliance with recommendations on folic acid use in 47. Nilsen RM, Vollset SE, Gjessing HK, Skjaerven R, Melve KK, Schreuder P, relation to pregnancy: is there a need for fortification? Public Health Nutr. Alsaker ER, Haug K, Daltveit AK, Magnus P. Self-selection and bias in a large 2004;7(7):843–50. prospective pregnancy cohort in Norway. Paediatr Perinat Epidemiol. 2009; 22. Nilsen RM, Vollset SE, Gjessing HK, Magnus P, Meltzer HM, Haugen M, 23(6):597–608. Ueland PM. Patterns and predictors of folic acid supplement use among 48. Bodin M, Kall L, Tyden T, Stern J, Drevin J, Larsson M. Exploring men's pregnant women: the Norwegian mother and child cohort study. Am J Clin pregnancy-planning behaviour and fertility knowledge:a survey among Nutr. 2006;84(5):1134–41. fathers in Sweden. Ups J Med Sci. 2017;122(2):127–35. 23. Timmermans S, Jaddoe VW, Mackenbach JP, Hofman A, Steegers- 49. Lindberg LD, Kost K. Exploring U.S. men's birth intentions. Matern Child Theunissen RP, Steegers EA. Determinants of folic acid use in early Health J. 2014;18(3):625–33. pregnancy in a multi-ethnic urban population in the Netherlands: the generation R study. Prev Med. 2008;47(4):427–32. 24. Braekke K, Staff AC. Periconceptional use of folic acid supplements in Oslo. Acta Obstet Gynecol Scand. 2003;82(7):620–7. 25. Jackson SE, Steptoe A, Wardle J. The influence of partner's behavior on health behavior change: the English longitudinal study of ageing. JAMA Intern Med. 2015;175(3):385–92. 26. Desrosiers A, Thompson A, Divney A, Magriples U, Kershaw T. Romantic partner influences on prenatal and postnatal substance use in young couples. J Public Health (Oxf). 2016;38(2):300–7. 27. Cornelius T, Desrosiers A, Kershaw T. Spread of health behaviors in young couples: how relationship power shapes relational influence. Soc Sci Med. 2016;165:46–55.

Journal

BMC Pregnancy and ChildbirthSpringer Journals

Published: May 30, 2018

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off