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Omega-3 fatty acid intake during pregnancy and risk of infant maltreatment: a nationwide birth cohort – the Japan Environment and Children's Study

Published online by Cambridge University Press:  25 June 2021

Kenta Matsumura*
Affiliation:
Toyama Regional Center for Japan Environment and Children's Study, University of Toyama, Toyama, Japan
Kei Hamazaki
Affiliation:
Toyama Regional Center for Japan Environment and Children's Study, University of Toyama, Toyama, Japan Department of Public Health, Faculty of Medicine, University of Toyama, Toyama, Japan Department of Public Health, Graduate School of Medicine, Gunma University, Gunma, Japan
Akiko Tsuchida
Affiliation:
Toyama Regional Center for Japan Environment and Children's Study, University of Toyama, Toyama, Japan Department of Public Health, Faculty of Medicine, University of Toyama, Toyama, Japan
Hidekuni Inadera
Affiliation:
Toyama Regional Center for Japan Environment and Children's Study, University of Toyama, Toyama, Japan Department of Public Health, Faculty of Medicine, University of Toyama, Toyama, Japan
*
Author for correspondence: Kenta Matsumura, E-mail: [email protected]
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Abstract

Background

Intake of omega-3 polyunsaturated fatty acids (PUFAs) has favorable effects, including reducing violent and aggressive behaviors, but its association with infant maltreatment is unknown. We therefore tested the hypothesis that maternal intake of omega-3 PUFAs is associated with a lower risk of infant maltreatment.

Methods

Participants were 92 191 mothers involved in the ongoing Japan Environment and Children's Study. Omega-3 PUFA intake during pregnancy was measured using a food frequency questionnaire. Infant maltreatment was assessed using a self-reported questionnaire administered at 1 and 6 months postpartum.

Results

Analysis using the lowest quintile of intake as a reference revealed that the adjusted odds ratios (ORs) with 95% confidence intervals (CIs) for cases of ‘hitting’ decreased as quintiles increased, with values for the second to fifth quintiles of 0.93 (95% CI 0.77–1.13), 0.79 (95% CI 0.64–0.97), 0.78 (95% CI 0.64–0.96), and 0.72 (95% CI 0.59–0.89), respectively. Adjusted ORs (95% CIs) for ‘shaking very hard’ at 6 months were 0.87 (0.73–1.04), 0.81 (0.67–0.97), 0.73 (0.61–0.89), and 0.78 (0.65–0.94), respectively. Adjusted ORs for ‘leaving alone at home’ for the second to fifth quintiles were 0.92 (0.87–0.98), 0.91 (0.86–0.97), 0.94 (0.88–0.99), and 0.85 (0.80–0.90), respectively.

Conclusions

Higher maternal intake of omega-3 PUFAs during pregnancy was associated with fewer cases of hitting and violent shaking and leaving the child alone at home, implying a lower risk of infant maltreatment. Our results indicate the potential applicability of omega-3 PUFAs in reducing infant maltreatment.

Type
Original Article
Creative Commons
Creative Common License - CCCreative Common License - BY
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Introduction

Child maltreatment is the abuse or neglect of children aged 0–17 years old that leads to potential or actual harm to them (Krug, Dahlberg, Mercy, Zwi, & Lozano, Reference Krug, Dahlberg, Mercy, Zwi and Lozano2002; World Health Organization, 2006). Although the prevalence of child maltreatment shows considerable heterogeneity according to country, type of maltreatment, and children's age (Finkelhor, Turner, Shattuck, & Hamby, Reference Finkelhor, Turner, Shattuck and Hamby2013; Hillis, Mercy, Amobi, & Kress, Reference Hillis, Mercy, Amobi and Kress2016; Moody, Cannings-John, Hood, Kemp, & Robling, Reference Moody, Cannings-John, Hood, Kemp and Robling2018), a 2017 UNICEF report (United Nations Children's Fund, 2017) states that 300 million (3 in 4) young children worldwide are regularly subjected to maltreatment by their caregivers. The most severe consequences of child maltreatment include injury, serious sequelae, and even death (Chevignard & Lind, Reference Chevignard and Lind2014; Palusci & Covington, Reference Palusci and Covington2014). Most such deaths occur in infants (Palusci & Covington, Reference Palusci and Covington2014). The lifetime consequences include depression, smoking, obesity, high-risk sexual behavior, substance use, perpetration, and suicide attempt (Hughes et al., Reference Hughes, Bellis, Hardcastle, Sethi, Butchart, Mikton and Dunne2017; Thepthien & Htike, Reference Thepthien and Htike2020), which in turn can lead to some of the principal causes of death, disease, and disability, including cardiovascular disease, sexually transmitted diseases, cancer, and suicide (World Health Organization, 2006). Therefore, public health measures must address prevention and intervention for child maltreatment.

Various psychopathological, socio-economical, and environmental factors are known to contribute to child maltreatment by mothers (Clement, Berube, & Chamberland, Reference Clement, Berube and Chamberland2016; Palusci, Reference Palusci2011; Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009; Wu et al., Reference Wu, Ma, Carter, Ariet, Feaver, Resnick and Roth2004), but addressing many of these factors through intervention can be difficult. One potentially protective factor that could easily be targeted in intervention, but has currently received little attention, is maternal intake of omega-3 polyunsaturated fatty acid (PUFA). Omega-3 PUFAs are essential fatty acids involved in a wide range of vital activities and include docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA), both of which are found in fish oil. Meta-analyses and literature reviews have shown that omega-3 PUFA intake is effective for reducing violent and aggressive behaviors (Appleton, Rogers, & Ness, Reference Appleton, Rogers and Ness2008; Gajos & Beaver, Reference Gajos and Beaver2016; Hamazaki & Hamazaki, Reference Hamazaki and Hamazaki2008). In addition, animal studies have revealed that omega-3 rich feedings promote nurturing maternal behavior (Asch, Schurdak, & McNamara, Reference Asch, Schurdak and McNamara2019; Harauma, Sagisaka, Horii, Watanabe, & Moriguchi, Reference Harauma, Sagisaka, Horii, Watanabe and Moriguchi2016). For example, homicide mortality rates are inversely related to seafood consumption in a country-specific manner (Hibbeln, Reference Hibbeln2001). Furthermore, interpersonal aggression is suppressed by DHA and EPA supplementation (Hamazaki et al., Reference Hamazaki, Sawazaki, Itomura, Asaoka, Nagao, Nishimura and Kobayashi1996), especially in stressful situations or in individuals under stress (Appleton et al., Reference Appleton, Rogers and Ness2008; Hamazaki & Hamazaki, Reference Hamazaki and Hamazaki2008). Dams fed a diet rich in omega-3 PUFAs show less infanticidal behavior (Harauma et al., Reference Harauma, Sagisaka, Horii, Watanabe and Moriguchi2016). However, to our knowledge, no previous studies have tested these favorable effects of PUFAs in the context of child maltreatment.

In this study, we used data obtained from an ongoing nationwide birth cohort study in Japan to examine the association between maternal intake of omega-3 PUFAs during pregnancy and risk of infant maltreatment. We hypothesized that mothers with a higher intake of omega-3 PUFAs would exhibit less infant maltreatment.

Methods

Study design and population

Participants were members of the Japan Environment and Children's Study (JECS). The JECS is an ongoing, nationwide, government-funded birth cohort study focusing on various environmental factors and child health and development. The design of the JECS has been reported in detail elsewhere (Kawamoto et al., Reference Kawamoto, Nitta, Murata, Toda, Tsukamoto and Hasegawa2014; Michikawa et al., Reference Michikawa, Nitta, Nakayama, Yamazaki, Isobe and Tamura2018). Briefly, expectant mothers were enrolled from 15 regional centers (including both rural and urban locations) in Japan via face-to-face recruitment between January 2011 and March 2014. Follow-up was conducted during the second or third trimester, at childbirth, and at 1 month postpartum during scheduled in-hospital checkups. Subsequent follow-ups were conducted at 6 months postpartum by mail. The present study analyzed the jecs-ta-20190930 dataset, which was released in October 2019. This dataset includes data on 103 060 pregnancies. Of these, 5647 multiple participations and 3561 miscarriages/still births were excluded to derive unique mothers. Among the remaining 93 852 mothers, 1661 were further excluded due to lack of responses or missing data on omega-3 PUFA intake during pregnancy. Finally, a total of 92 191 mother–infant pairs were analyzed (Fig. 1).

Fig. 1. Participant flow chart.

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The JECS protocol was reviewed and approved by the Ministry of the Environment's Institutional Review Board on Epidemiological Studies (100910001) and the ethics committees of all participating institutions. Written informed consent was obtained from all participants. This specific study was also approved by the Ethics Committee of University of Toyama (R2020163).

Measures

Exposure

Omega-3 PUFA intake during pregnancy (i.e. from the time of learning of pregnancy to the second or third trimester) was measured using a food frequency questionnaire (FFQ). The FFQ is a semi-quantitative instrument that assesses the average consumption of 171 food and beverage items, including 21 items related to fish or shellfish. The FFQ has been validated for use in large-scale Japanese epidemiologic studies (Sasaki, Kobayashi, & Tsugane, Reference Sasaki, Kobayashi and Tsugane2003; Yokoyama et al., Reference Yokoyama, Takachi, Ishihara, Ishii, Sasazuki, Sawada and Tsugane2016). To calculate the energy-adjusted intake using the residual model (Willett, Howe, & Kushi, Reference Willett, Howe and Kushi1997), we performed log-transformation of omega-3 PUFAs. Because 345 participants reported a value of 0 g/day for omega-3 PUFA intake, we replaced this value with 0.001 g/day, which is one-tenth of the lowest omega-3 PUFA intake of all participants (excluding 0 g/day). Energy-adjusted omega-3 PUFA intake was categorized into quintiles (Hamazaki et al., Reference Hamazaki, Matsumura, Tsuchida, Kasamatsu, Tanaka and Ito2020) and then used as an exposure variable.

Outcome

Infant maltreatment was assessed via a self-reported questionnaire administered at 1 and 6 months postpartum. Because there is no clear gold standard as to what constitutes maltreatment (Moody et al., Reference Moody, Cannings-John, Hood, Kemp and Robling2018), we carefully selected items involved in maltreatment by referring to the original definition (World Health Organization, 2006) and the definitions used in earlier surveys (Hussey, Chang, & Kotch, Reference Hussey, Chang and Kotch2006; Straus, Hamby, Finkelhor, Moore, & Runyan, Reference Straus, Hamby, Finkelhor, Moore and Runyan1998) while also taking into consideration the sensitive nature of the subject matter. Items regarding maltreatment used in this study were as follows:

Physical abuse

  • Hitting the baby (at 1 month postpartum)

  • Shaking the baby very hard when he/she cries (at 1 month postpartum)

  • Shook the child very hard in the past month (at 6 months postpartum)

Neglect

  • Leaving the baby alone at home (at 1 month postpartum)

Mothers were instructed to indicate the frequency of these behaviors on a four-point Likert scale. Following the original definition of maltreatment (i.e. any behavior resulting in potential harm to the child; Krug et al., Reference Krug, Dahlberg, Mercy, Zwi and Lozano2002; World Health Organization, 2006), answers to the aforementioned items other than ‘never’ were considered to indicate a case of maltreatment and were used as an outcome variable in this study.

Potential confounders

Based on existing evidence, we selected potential confounders as variables likely to affect both the prevalence of maltreatment (Fujiwara, Yamaoka, & Morisaki, Reference Fujiwara, Yamaoka and Morisaki2016; Palusci, Reference Palusci2011; Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009; Wu et al., Reference Wu, Ma, Carter, Ariet, Feaver, Resnick and Roth2004) and the intake amount or physiological (functional) effectiveness of omega-3 PUFAs (de Groot, Emmett, & Meyer, Reference de Groot, Emmett and Meyer2019; Itomura et al., Reference Itomura, Fujioka, Hamazaki, Kobayashi, Nagasawa, Sawazaki and Hamazaki2008; Lin, Huang, & Su, Reference Lin, Huang and Su2010; Mozaffarian, Bryson, Lemaitre, Burke, & Siscovick, Reference Mozaffarian, Bryson, Lemaitre, Burke and Siscovick2005; Schiepers, de Groot, Jolles, & van Boxtel, Reference Schiepers, de Groot, Jolles and van Boxtel2010; Thesing, Bot, Milaneschi, Giltay, & Penninx, Reference Thesing, Bot, Milaneschi, Giltay and Penninx2018). These variables included maternal age, pre-pregnancy body mass index, highest education level, full-time work, annual household income, smoking status, alcohol intake, parity, marital status, living with mother's parents, living with partner's parents, stressful events, intimate partner violence, negative attitude toward pregnancy, history of depression, anxiety disorder, dysautonomia, or schizophrenia, and psychological distress measured using the Japanese version (Furukawa et al., Reference Furukawa, Kawakami, Saitoh, Ono, Nakane, Nakamura and Kikkawa2008; Sakurai, Nishi, Kondo, Yanagida, & Kawakami, Reference Sakurai, Nishi, Kondo, Yanagida and Kawakami2011) of the Kessler Psychological Distress Scale (K6: Kessler et al., Reference Kessler, Andrews, Colpe, Hiripi, Mroczek, Normand and Zaslavsky2002). All the variables were categorized according to standard medical practice and common practice in Japan (Hamazaki et al., Reference Hamazaki, Takamori, Tsuchida, Kigawa, Tanaka and Ito2018; Matsumura, Hamazaki, Tsuchida, Kasamatsu, & Inadera, Reference Matsumura, Hamazaki, Tsuchida, Kasamatsu and Inadera2019). The categorizations are shown in Table 1.

Table 1. Participant characteristics according to quintile for energy-adjusted omega-3 polyunsaturated fatty acid (PUFA) intake during pregnancy

Values show the imputed data for the 92191 mothers.

Statistical analysis

To calculate the crude and adjusted odds ratios (ORs) and their 95% CIs for each outcome, marginal structural models were fitted to a pseudo-population created using the inverse probability of treatment weighting such that no association existed between the potential confounders and the exposure variable; in other words, all backdoor paths were blocked (Cole & Hernán, Reference Cole and Hernán2008; Hernán & Robins, Reference Hernán and Robins2020; Sato & Matsuyama, Reference Sato and Matsuyama2003). The exposure variable was the quintile of omega-3 PUFA intake, and the first quintile was used as the reference. Outcome variables were each of the cases of infant maltreatment.

Loss to follow-up (1.44% at 1 month and 5.91% at 6 months) was treated using the inverse probability of censoring weighting (Hernán & Robins, Reference Hernán and Robins2020). Missing data were treated using multiple imputation (⩽1% for all variables excluding 2.47% for parity and 7.24% for annual household income). We created 10 imputed datasets using chained equations (van Buuren, Reference van Buuren2007), and the results were combined using standard rules (Rubin, Reference Rubin2004). All analyses were performed using SAS software (version 9.4; SAS Institute Inc.) or R 4.0.0.

Sensitivity analysis

To assess the robustness of the results, ORs were calculated using multivariable logistic regression analysis. In addition, the analysis was repeated using energy-adjusted fish intake in place of omega-3 PUFA intake. To evaluate unmeasured confounding, the E-value (Ding & VanderWeele, Reference Ding and VanderWeele2016; VanderWeele & Ding, Reference VanderWeele and Ding2017), which is the minimum association required to completely cancel out the observed association, was calculated.

Additional analysis

To assess the assumption of positivity, the weights used for creating the pseudo-population where no association existed between the covariates and exposure as well as loss to follow-up as missing at random were summarized. Generalized variance inflation factors were calculated to assess multicollinearity.

Results

A total of 92 191 mothers were analyzed; of these, 73.7% were less than 35 years of age, 74.0% had a pre-pregnancy body mass index of 18.5–25, and 43.4% were primiparous. Median omega-3 PUFA values, adjusted for total energy intake, for each quintile were 0.96, 1.30, 1.55, 1.82, and 2.31 g/day, respectively. Table 1 shows the participant characteristics according to omega-3 PUFA intake. Omega-3 PUFA intake was associated with almost all the potential confounders. In contrast, no apparent association was observed between omega-3 PUFA intake and the potential confounders in a pseudo-population created using the inverse probability of treatment weighting (all p values >0.870; online Supplementary eTable 1). Compared with mothers who were included in the analysis (n = 92 191), those who were excluded (n = 1661), due to lack of responses or missing data on omega-3 PUFA intake during pregnancy, tended, in descending order, to be younger (Cramer's V = 0.025), to be unmarried (Cramer's V = 0.021), and to have psychological distress (Cramer's V = 0.019).

Prevalence of ‘hitting the baby’, ‘shaking the baby very hard when he/she cries’, ‘shook the child very hard in the past month’, and ‘leaving the baby alone at home’ was 1.00, 17.79, 1.33, and 15.65%, respectively. Table 2 shows the prevalence, numbers, and crude and adjusted ORs (95% CIs) for the cases of each item according to the quintile of omega-3 PUFA intake, with the first quintile as the reference. Adjusted ORs (95% CIs) for the second through fifth quintiles were as follows: for ‘hitting the baby’, 0.93 (0.77–1.13), 0.79 (0.64–0.97), 0.78 (0.64–0.96), and 0.72 (0.59–0.89); for ‘shaking the baby very hard when he/she cries’, 0.98 (0.93–1.03), 0.94 (0.90–0.997), 0.93 (0.88–0.98), and 0.88 (0.83–0.93); for ‘shook the child very hard in the past month’, 0.87 (0.73–1.04), 0.81 (0.67–0.97), 0.73 (0.61–0.89), and 0.78 (0.65–0.94); and for ‘leaving the baby alone at home’, 0.92 (0.87–0.98), 0.91 (0.86–0.97), 0.94 (0.88–0.99), and 0.85 (0.80–0.90), respectively. A linear trend was observed for all outcomes.

Table 2. Odds ratios (95% CIs) for cases of infant maltreatment according to quintile for energy-adjusted omega-3 polyunsaturated fatty acid (PUFA) intake during pregnancy

a Adjusted for maternal age, pre-pregnancy body mass index, highest education level, full-time work, annual household income, smoking status, alcohol intake, parity, marital status, living with mother's parents, living with partner's parents, stressful events, intimate partner violence, negative attitude toward pregnancy, history of depression, anxiety disorder, dysautonomia, or schizophrenia, and psychological distress.

No meaningful differences were observed in the results derived using multivariable logistic regression models and those derived from the main analysis (online Supplementary eTable 2). Online Supplementary eTable 3 shows the results for fish intake. A weak but similar tendency was observed relative to that for omega-3 PUFA intake. The E-values corresponding to the fifth quintile for ‘hitting the baby’ (OR 0.72) and the fourth quintile for ‘shook the child very hard’ (OR 0.73) were 2.11 and 2.07, respectively. These values suggest that relatively strong unmeasured potential confounders would be necessary to cancel out the observed association.

The mean value (SD) of standardized treatment weights for the omega-3 PUFA model was 1.000 (0.114). The mean values (SDs) of censoring weights at 1 and 6 months were 1.015 (0.011) and 1.063 (0.050), respectively. Online Supplementary eTable 4 shows the details and weights for the fish model. The findings suggest that a positivity violation was unlikely to occur. Multicollinearity was not detected among the covariates; that is, all generalized variance inflation factors were below 1.34.

Discussion

Our analyses revealed that even when controlling for up to 16 carefully selected potential confounders, omega-3 PUFA intake during pregnancy was associated with fewer cases of hitting the baby, shaking the baby very hard at 1 and 6 months, and leaving the baby alone at home. These relationships were more salient for omega-3 PUFA intake than for fish intake. Importantly, clear dose-response relationships were observed in most cases. These findings support our hypothesis that mothers with a higher intake of omega-3 PUFAs during pregnancy exhibit less infant maltreatment.

Our findings on infant abuse are consistent with those of a meta-analysis (Gajos & Beaver, Reference Gajos and Beaver2016) of 40 studies, including both randomized controlled trials and cohort studies, that examined 73 effect sizes and concluded that omega-3 PUFA intake reduces violent and aggressive behaviors. Hitting and/or shaking babies constitutes physical abuse among the types of infant maltreatment. The association was stronger for omega-3 PUFA intake than for fish consumption, which might be due to the fact that not all species of fish contain high levels of omega-3 PUFAs. In addition, our findings showed a relatively stronger association and clearer dose-dependent response, which was likely due to our participants being perinatal mothers who recently experienced pregnancy, delivery, and nurturing, which may be regarded as a series of stressful events (Holmes & Rahe, Reference Holmes and Rahe1967), despite the desire of these women to have a baby. Previous studies have pointed out that the effects of omega-3 PUFAs may be augmented in stressful and/or vulnerable situations (Appleton et al., Reference Appleton, Rogers and Ness2008; Hamazaki & Hamazaki, Reference Hamazaki and Hamazaki2008). To our knowledge, this is the first study to suggest that the suppressing effect of omega-3 PUFAs on violent and aggressive behaviors might also be applicable to child abuse.

The present findings on neglect are also consistent with evidence from animal studies demonstrating that dams deficient in omega-3 PUFAs exhibit reduced maternal nurturing behavior, such as less licking and grooming and poorer nesting behaviors (Asch et al., Reference Asch, Schurdak and McNamara2019; Harauma et al., Reference Harauma, Sagisaka, Horii, Watanabe and Moriguchi2016). Notably, approximately 40% of dams with deficits in omega-3 PUFAs attacked or neglected pups on the day of delivery, with some pups from omega-3 PUFA-deficient dams dying (Harauma et al., Reference Harauma, Sagisaka, Horii, Watanabe and Moriguchi2016). In humans, it is known that more infants die of neglect than of physical abuse (Ministry of Health, Labour and Welfare, 2020; Palusci & Covington, Reference Palusci and Covington2014), suggesting that maternal nurturing behavior plays a pivotal role in the survival of offspring. To our knowledge, this is also the first study to suggest that the beneficial effects of omega-3 PUFAs might also be applicable to human neglecting behavior.

Although the precise mechanisms underlying the impact of omega-3 PUFA intake on infant maltreatment remain unclear, several possible pathways exist. The first is via stress reduction. Omega-3 PUFAs modulate a wide range of neural substrates that contribute to emotional regulation, such as noradrenaline, dopamine, serotonin, and endocannabinoid systems (Freeman et al., Reference Freeman, Hibbeln, Wisner, Davis, Mischoulon, Peet and Stoll2006; Lafourcade et al., Reference Lafourcade, Larrieu, Mato, Duffaud, Sepers, Matias and Manzoni2011). In addition, omega-3 PUFAs reduce stressor-evoked augmentation of autonomic activity (Ginty & Conklin, Reference Ginty and Conklin2012; Hamazaki et al., Reference Hamazaki, Itomura, Huan, Nishizawa, Sawazaki, Tanouchi and Yazawa2005; Matsumura et al., Reference Matsumura, Noguchi, Nishi, Hamazaki, Hamazaki and Matsuoka2017) as a whole-body preparation for fight-or-flight stress responses. Thus, intake of omega-3 PUFAs may reduce infant maltreatment by reducing the mother's behavioral stress response toward the baby, hitting and shaking as a fight response, and escaping from the baby (leaving the baby alone at home) as a flight response.

The second pathway is via a reduction in depression. Omega-3 PUFAs are known to exert antidepressant effects (Freeman et al., Reference Freeman, Hibbeln, Wisner, Davis, Mischoulon, Peet and Stoll2006; Lin & Su, Reference Lin and Su2007), including in mothers with postpartum depression (Urech et al., Reference Urech, Eussen, Alder, Stahl, Boehm, Bitzer and Hoesli2020; Zhang et al., Reference Zhang, Zou, Li, Wang, Sun, Shi and Li2020). Because postpartum depression is a risk factor for infant maltreatment (Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009), intake of omega-3 PUFAs may reduce infant maltreatment via a reduction in postpartum depression.

The third pathway is via behavioral changes in infants. Omega-3 PUFA supplementation in children is effective for reducing externalizing behaviors such as aggression, non-compliance, and hyperactivity (Portnoy, Raine, Liu, & Hibbeln, Reference Portnoy, Raine, Liu and Hibbeln2018). Given that maternal concentrations of essential fatty acids, including omega-3 PUFAs, are correlated with those in newborn babies (Al, Hornstra, van der Schouw, Bulstra-Ramakers, & Huisjes, Reference Al, Hornstra, van der Schouw, Bulstra-Ramakers and Huisjes1990), omega-3 PUFAs in infants that were transferred from mothers may play a role in reducing fretful behavior in infants. Triggers of physical abuse-related deaths include crying and disobedience (Palusci & Covington, Reference Palusci and Covington2014), which might be reduced by the intake of omega-3 PUFAs.

There are many identified risk factors for child maltreatment. However, many risk factors are hard to address in intervention, such as unplanned pregnancy, unemployment, psychopathology, drug abuse, and lower age (Clement et al., Reference Clement, Berube and Chamberland2016; Palusci, Reference Palusci2011; Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009; Wu et al., Reference Wu, Ma, Carter, Ariet, Feaver, Resnick and Roth2004). It would be easier to increase omega-3 PUFA intake, however. Conveniently, omega-3 PUFAs seem to effectively reduce anger/hyper-reactivity, depression, and stress in mothers, which a meta-analysis identified as strong risk factors (Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009). Moreover, pregnant women are usually deficient in omega-3 PUFAs (Hornstra, Al, van Houwelingen, & Foreman-van Drongelen, Reference Hornstra, Al, van Houwelingen and Foreman-van Drongelen1995; Markhus et al., Reference Markhus, Rasinger, Malde, Froyland, Skotheim, Braarud and Graff2015) and are therefore recommended to increase their intake during pregnancy (Coletta, Bell, & Roman, Reference Coletta, Bell and Roman2010). This means that it is not necessary to establish completely new systems for recommending increased omega-3 PUFA intake, but rather to emphasize the importance of omega-3 PUFA intake in ongoing nutritional guidance for pregnant women. One efficient method for ensuring sufficient intake of omega-3 PUFAs includes eating blue-backed omega-3 PUFA-rich fish, such as sardines, saury, and horse mackerel. Conveniently, blue-backed fishes are small and are not at the top of the food chain, so biological concentrations of toxic chemicals such as mercury and/or PCBs are rare. Flaxseed oil is rich in the omega-3 PUFA α-linolenic acid; however, α-linolenic acid needs to be converted into EPA and subsequently DHA before use, and so is less widely recommended. It usually takes 6–8 weeks before the effects of omega-3 PUFA supplementation manifest (Gajos & Beaver, Reference Gajos and Beaver2016; Zhang et al., Reference Zhang, Zou, Li, Wang, Sun, Shi and Li2020), and therefore commencing this dietary practice as early as possible is recommended. Other recommended fishes may be found elsewhere in the literature (Coletta et al., Reference Coletta, Bell and Roman2010; Mozaffarian & Rimm, Reference Mozaffarian and Rimm2006) and in local guidelines.

This study has several strengths. First, our sample size was large, including over 90 000 mothers, which resulted in successful detection of differences in physical abuse with a low prevalence of approximately 1%. Second, the participants were enrolled from multiple regions throughout Japan from 2011 to 2014 and are therefore reflective of the entire nation. Third, the dropout rate was relatively low (approximately 5.9% at 6 months postpartum), suggesting the existence of low selection bias due to dropout. Fourth, statistical models used in the study were conditioned on a wide range of potential confounders, thereby possibly yielding estimates close to the true effects. Fifth, missing value rates for maltreatment items excluding dropout were low (maximum of 0.70%) compared with those for other sensitive items related to income (7.24%), demonstrating that participants answered these items without being too defensive or having a psychological set. Finally, our findings may be generalizable to other populations given that the assumed mechanisms are biological.

This study has several limitations. First, we examined infant maltreatment only in mothers. Mothers are the leading offenders of infant maltreatment deaths in Japan (Ministry of Health, Labour and Welfare, 2020), but further research examining this association in fathers and non-parent caregivers is needed (Stith et al., Reference Stith, Liu, Davies, Boykin, Alder, Harris and Dees2009). Second, infant maltreatment was measured using a self-reported questionnaire. Although a gold standard measure for infant maltreatment is lacking (Moody et al., Reference Moody, Cannings-John, Hood, Kemp and Robling2018), further studies using objective markers such as maladaptive responses in the hypothalamic-pituitary-adrenal axis and DNA methylation in children (McGowan et al., Reference McGowan, Sasaki, D'Alessio, Dymov, Labonte, Szyf and Meaney2009; Weaver et al., Reference Weaver, Cervoni, Champagne, D'Alessio, Sharma, Seckl and Meaney2004) would be beneficial. Third, we did not measure sexual abuse, partly because we were unable to determine a hypothetical link between omega-3 PUFA intake and sexual abuse. Although infant death due to sexual abuse is rare yet not non-existent (Palusci & Covington, Reference Palusci and Covington2014), further studies pursuing this issue are necessary. Fourth, we measured child maltreatment only until 6 months postpartum. Continuous follow-up assessment is necessary for at least a decade to cover the entire period in which potential maltreatment of children could occur. Fifth, we included various potential confounders in the model but cannot rule out the possible existence of unmeasured potential confounders. Thus, randomized controlled trials are warranted to establish a standard prevention strategy against maltreatment. Finally, we measured omega-3 PUFA intake using an FFQ only. The FFQ has been validated for use in large-scale Japanese epidemiologic studies (Sasaki et al., Reference Sasaki, Kobayashi and Tsugane2003; Yokoyama et al., Reference Yokoyama, Takachi, Ishihara, Ishii, Sasazuki, Sawada and Tsugane2016), but it has not been validated for use with pregnant women. In general, the FFQ is less accurate than the food weighing method. Therefore, further research measuring omega-3 PUFA intake using the food weighing method and/or by directly measuring the composition of erythrocyte PUFAs should be conducted.

Conclusions

This study demonstrated that higher maternal intake of omega-3 PUFAs was associated with fewer cases of hitting, hard shaking, and leaving babies alone at home, suggesting a lower risk of infant maltreatment. Our results indicate the potential applicability of omega-3 PUFAs in reducing infant maltreatment.

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S0033291721002427.

Acknowledgements

We are grateful to all of the JECS participants and all of the individuals involved in the data collection.

Author contributions

Conceptualization, K.M.; methodology, K.M.; formal analysis, K.M.; data curation, The JECS Group; writing – original draft preparation, K.M.; writing – review and editing, K.H., A.T., H.I., and The JECS Group; funding acquisition, The JECS Group. All authors have read and agreed to the published version of the manuscript.

Financial support

JECS is funded by the Ministry of the Environment, Japan. The funding source played no role in the study's design; in the collection, analysis, or interpretation of data; in the writing of the report; or in the decision to submit this paper for publication. The findings and conclusions of this article are solely the responsibility of the authors, and do not represent the official views of the above government.

Conflict of interest

K.H. received a research grant from the First Bank of Toyama Scholarship Foundation, speaking honoraria from the DHA & EPA Association, Niigata Medical Association, Toyama Medical Association, and Toyama Occupational Health Promotion Center, and a supervision fee from Otsuka Pharmaceutical Factory. The remaining authors declare no conflicts of interest.

Ethical standards

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The JECS protocol was reviewed and approved by the Ministry of the Environment's Institutional Review Board on Epidemiological Studies (100910001) and the ethics committees of all participating institutions. Written informed consent was obtained from all participants. This specific study was also approved by the Ethics Committee of University of Toyama (R2020163).

Appendix

Members of the JECS Group as of 2021: Michihiro Kamijima (Principal Investigator, Nagoya City University, Nagoya, Japan), Shin Yamazaki (National Institute for Environmental Studies, Tsukuba, Japan), Yukihiro Ohya (National Center for Child Health and Development, Tokyo, Japan), Reiko Kishi (Hokkaido University, Sapporo, Japan), Nobuo Yaegashi (Tohoku University, Sendai, Japan), Koichi Hashimoto (Fukushima Medical University, Fukushima, Japan), Chisato Mori (Chiba University, Chiba, Japan), Shuichi Ito (Yokohama City University, Yokohama, Japan), Zentaro Yamagata (University of Yamanashi, Chuo, Japan), Hidekuni Inadera (University of Toyama, Toyama, Japan), Takeo Nakayama (Kyoto University, Kyoto, Japan), Hiroyasu Iso (Osaka University, Suita, Japan), Masayuki Shima (Hyogo College of Medicine, Nishinomiya, Japan), Youichi Kurozawa (Tottori University, Yonago, Japan), Narufumi Suganuma (Kochi University, Nankoku, Japan), Koichi Kusuhara (University of Occupational and Environmental Health, Kitakyushu, Japan), and Takahiko Katoh (Kumamoto University, Kumamoto, Japan).

Footnotes

*

The study group members are listed in the Appendix.

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Figure 0

Fig. 1. Participant flow chart.

Figure 1

Table 1. Participant characteristics according to quintile for energy-adjusted omega-3 polyunsaturated fatty acid (PUFA) intake during pregnancy

Figure 2

Table 2. Odds ratios (95% CIs) for cases of infant maltreatment according to quintile for energy-adjusted omega-3 polyunsaturated fatty acid (PUFA) intake during pregnancy

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