Parental harsh disciplining, like corporal punishment, has consistently been associated with adverse mental health outcomes in children. It remains a challenge to accurately assess the consequences of harsh discipline, as researchers and clinicians generally rely on parent report of young children's problem behaviors. If parents rate their parenting styles and their child's behavior this may bias results. The use of child self-report on problem behaviors is not common but may provide extra information about the relation of harsh parental discipline and problem behavior. We examined the independent contribution of young children's self-report above parental report of emotional and behavioral problems in a study of maternal and paternal harsh discipline in a birth cohort. Maternal and paternal harsh discipline predicted both parent reported behavioral and parent reported emotional problems, but only child reported behavioral problems. Associations were not explained by pre-existing behavioral problems at age 3. Importantly, the association with child reported outcomes was independent from parent reported problem behavior. These results suggest that young children's self-reports of behavioral problems provide unique information on the effects of harsh parental discipline. Inclusion of child self-reports can therefore help estimate the effects of harsh parental discipline more accurately.
Citation: Mackenbach JD, Ringoot AP, van der Ende J, Verhulst FC, Jaddoe VWV, Hofman A, et al. (2014) Exploring the Relation of Harsh Parental Discipline with Child Emotional and Behavioral Problems by Using Multiple Informants. The Generation R Study. PLoS ONE 9(8): e104793. https://doi.org/10.1371/journal.pone.0104793
Editor: Kenji J. Tsuchiya, Hamamatsu University School of Medicine, Japan
Received: February 27, 2014; Accepted: July 12, 2014; Published: August 13, 2014
Copyright: © 2014 Mackenbach et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The first phase of the Generation R Study was made possible by financial support from: Erasmus Medical Center, Rotterdam, Erasmus University Rotterdam, and the Netherlands Organization for Health Research and Development (ZonMw). The present study was supported by an additional grant from the Netherlands Organization for Scientific Research to Henning Tiemeier (NWO ZonMW VIDI; grant no. 017.106.370). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have read the journal's policy and have the following conflicts: Prof. Dr. Frank C. Verhulst is a contributing author of the Achenbach System of Empirically Based Assessments, from which he receives remuneration. Vincent Jaddoe is a PLoS ONE Editorial Board member. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials. The authors have declared that no other potentially competing interests exist.
Parenting practices play a fundamental role in children's emotional and behavioral development. Corporal disciplining practices have consistently been associated with adverse mental health outcomes, such as poor school achievements, behavioral problems, lowered self-esteem and delinquent behaviors –. Milder forms of negative parental disciplining strategies -like harsh discipline- have also been studied repeatedly. Harsh discipline is characterized by parental attempts to control a child using verbal violence (shouting) or physical forms of punishment (pinching or hitting) . These forms of parental disciplining practices have been associated not only with child behavioral problems, in line with a cycle of violence hypothesis , but also with child emotional problems , , , . The effects of these milder forms of harsh disciplining may be less pronounced, yet are important since the prevalence of these forms of parental discipline is high. In a recent study using data from the present cohort we demonstrated that no less than 77% of mothers and 67% of fathers shouted at their child at least once in the last two weeks, in addition the number of parents threatening to slap (20–24%) or angrily pinching the child's arm (15%) was also considerable . Given the high prevalence and the known burden for children it is important to examine the consequences of these milder forms of harsh parental disciplining accurately.
As child behavior problems like aggressive or oppositional behaviors may lead to higher levels of harsh discipline by parents , it is important to study the effects of harsh parental disciplining on child problem behaviors prospectively. A number of longitudinal studies have affirmed that, after controlling for baseline emotional and behavioral problems, children exposed to less extreme forms of parental harsh discipline have an increased risk of behavioral problems and psychiatric disorders later in life , .
Despite a large body of evidence, the existing literature on emotional and behavioral consequences of mild harsh discipline suffers limitations. Most studies relied on parental and often only on maternal report of child behavioral problems , , –. Relying on one informant for both the determinant and the outcome is problematic, as parents who rate their own parenting styles as ‘harsh’ may also perceive their child's behavior differently than parents that do not use harsh disciplining , , , . This problem of shared informant bias can be avoided if the informant reporting on the consequences of harsh discipline differs from the informant reporting on harsh discipline. Including multiple reporters may generate additional evidence regarding the consequences of harsh discipline. It has become widely accepted that young children may be a valuable source of information , as they can provide unique insights into their own behaviors . Indeed, self-report on the consequences of harsh discipline has proven to generate valuable results in adolescents , , . Yet, few studies on the consequences of parental harsh disciplining have used young children's self-reports.
In the present study we examined the consequences of both maternal and paternal harsh discipline on parent reported and young children's self-reported emotional and behavioral problems. Specifically, we investigated whether any effect observed using child report was independent of parent reported problems. We hypothesized that child self-report of problem behavior would strengthen the evidence of an association between harsh discipline and parent reported problem behavior by contributing unique information.
The study was conducted in accordance with the guidelines proposed in the World Medical Association Declaration of Helsinki and has been approved by the Medical Ethical Committee of the Erasmus Medical Center in Rotterdam, the Netherlands (MEC 198.782/2001/31). Full written informed consent for the postnatal phase was obtained from parents for both parental and child data.
Study design and population
This study was embedded in the Generation R Study, a prospective population-based cohort from fetal life onwards. The design and data collection methods have been extensively described elsewhere . Briefly, all pregnant women residing in Rotterdam, with an expected delivery date between April 2002 and January 2006, were eligible for participation in Generation R. For this study, we considered participants with full postnatal written consent (N = 7,295) eligible. A questionnaire including parental disciplining at age three years was returned by 4,733 mothers and constituted the baseline. Of those, 718 children had missing data on child self-reported emotional and behavioral problems (BPI) at age six years, yielding a sample size of 4,015 (follow-up response: 85%) for analyses with maternal harsh discipline and child reported problems. The sample size for analyses with maternal harsh discipline and parent reported problems was n = 3,764. A flow chart is provided in supplementary material (Figure S1).
Information about parental disciplining practices was obtained by postal questionnaires when the children were three years old. We assessed various types of disciplining by ten items that were based on the Parent-Child Conflict Tactics Scale . In a previous study in the same cohort, a harsh discipline scale was confirmed using factor analysis. This resulted in a scale consisting of six items, representing constructs of psychological aggression and (mild) physical assault: “In the past week/month, I angrily pinched my child's arm”, “I shouted, yelled or screamed angrily at my child”, “I scolded at my child”, “I threatened to slap, spank or hit my child but did not actually do it”, “I called my child dumb or lazy or some other name like that” and “I shook my child”. Items were scored on a scale from 0 to 2. In line with this previous study , we calculated separate maternal and paternal harsh discipline scores by summing these six items. This yielded a score ranging from 0 to 12, with higher scores reflecting higher severity of harsh discipline.
Emotional and behavioral problems.
Children were invited to our research centre in Rotterdam at the age of six years. During this visit, the Berkeley Puppet Interview (BPI) was used to assess emotional and behavioral problems as perceived by the child him/herself as described previously . The BPI is a semi-structured interactive interview technique to obtain self-reports of young children. During the interview, two identical dog hand puppets were introduced to the child and invited the child to engage in a conversation. The puppets made opposing statements about themselves. For example, one puppet said that he was a sad kid, while the other puppet said the he was not a sad kid. Subsequently, the puppets asked children to indicate which statement described themselves best. In this study, we used internalizing (emotional problems) and externalizing (behavioral problems) scales. The Internalizing scale score (20 items) was computed as the sum of the item scores in three scales: Depression, Separation Anxiety and Overanxious. The Externalizing scale score (21 items) was computed as the sum of the item scores in three scales: Oppositional Defiant, Overt Hostility and Conduct Problems. Higher scores on the BPI scales indicate more problems. The psychometric properties of the BPI emotional and behavioral scales in the present study have been described elsewhere , .
Parent-reported child emotional and behavioral problems were assessed with the Dutch version of the Child Behavior Checklist (CBCL/1,5-5), a 99-item questionnaire that was mailed prior to the visit to the research centre . One of the parents, usually the mother, completed the CBCL/1,5-5 just before the visit to the research centre (92% of the questionnaires were completed by the mothers, 8% by other (primary) caregivers). The internalizing (emotional problems) and externalizing (behavioral problems) broadband scales were used in the present study. The Internalizing scale score (36 items) is the sum of the item scores of four scales: Emotionally Reactive, Anxious/Depressed, Somatic Complaints, and Withdrawn. The Externalizing scale score (24 items) is the sum of the item scores of the Attention Problems and Aggressive Behavior scales. Higher scores on the CBCL scales indicated more problems. Good reliability and validity has been reported for the CBCL/1,5-5 .
Assessing child problems at age six years was considered appropriate, as both the BPI and the CBCL are valid tools to assess child emotions and behaviors at this age. , ,  Pre-existing child internalizing and externalizing problems were reported by both mother and father using the CBCL/1,5-5 when children were 3 years old. This provided a three year difference, during transition from preschool to school-age, between determinant and outcome.
Potential confounders were selected based on prior studies , , . Information on gender, date of birth, marital status of the parents, smoking during pregnancy and age of the parents at intake was obtained from midwifery and hospital registries. Information on ethnicity, number of children in the household, educational level of the parents and household income was obtained by questionnaires at age 6 years. The child's ethnicity was classified by the countries of birth of the parents, according to the Dutch standard classification criteria of Statistics Netherlands (2004), and was categorized into Dutch, European and Non-western background (e.g. Turkish, Moroccan, Indonesian, Cape Verdian, Surinamese and Antillean). Educational level of the parents was defined as low (at most lower vocational training), medium low (at most intermediate vocational training), medium high (higher vocational training) and high (university degree). Family household income was divided into two categories: below 2,000 Euros per month which corresponds with below modal income, and 2,000 Euros per month and above. Marital status of parents was defined as either being married/living together or as having no partner.
To assess global parental psychopathology, a selection of 21 items from the Brief Symptom Inventory (BSI)  was administered to both mothers and fathers when the child was three years old.
Family functioning was measured with the 12-item General Functioning scale of the McMasters Family Assessment Device (FAD) . In this validated self-report questionnaire, parents (in 82% of the cases this was the mother) rated family functioning and family stress on a 4-point scale.
We first conducted descriptive analyses of the population. Next, correlational analysis of harsh parenting, emotional (internalizing) and behavioral (externalizing) problems and parental psychopathology was performed.
The relation between harsh discipline at age three years and emotional and behavioral problems at age six years was examined with linear regression analyses. To satisfy the assumption of normality, maternal and paternal harsh discipline scores were square root transformed to achieve a normal distribution. Similarly, BPI and CBCL scale scores were transformed using the natural logarithm and the square root respectively, and z-scores were calculated to be able to compare the emotional and behavioral problems with each other.
We studied the effects of maternal and paternal harsh discipline separately. Similarly, we studied parent and child self-reports of emotional and behavioral problems as separate outcomes.
In model 1, unadjusted linear regression analyses of harsh discipline with child emotional and behavioral problems were performed. In model 2, we adjusted for sociodemographic characteristics (child gender, age and ethnicity, number of children in the household, household income, marital status, smoking during pregnancy, maternal and paternal educational level), maternal and paternal psychopathology score, and family functioning. Covariates were included in the second model if they changed the effect estimates of the unadjusted relation between harsh discipline and emotional and behavioral problems by more than 5%. (However, had we used a 10% change in effect estimates as inclusion criterion -another commonly used criterion - the same confounders would have been selected.) To adjust for pre-existing emotional and behavioral problems, in model 3 we additionally accounted for emotional (if emotional problems were the outcome) or behavioral problems (if behavioral problems were the outcome) assessed at age 3 years. If the association between harsh discipline and problem behavior is independent of baseline problem behavior, this would strengthen the assumption that the temporality of the associations.
Analyses were adjusted for maternal characteristics (maternal education, maternal psychopathology and the maternal report of pre-existing child emotional/externalizing problems) unless paternal harsh discipline was the independent variable; in this case we adjusted for the respective paternal characteristics.
Next, we additionally adjusted the analyses of the child self-report problem behavior (model 3) for parent reported emotional and behavioral problems (model 4). The aim of this analysis was to examine whether harsh discipline could predict child self-reported emotional and behavioral problems, over and above parent report. If the association is independent of parent report, this suggests children can provide unique outcome information in this study of parental harsh discipline.
To test the influence of effect modifiers, we specified interaction terms for harsh discipline with child gender, child ethnicity and a mutual interaction term between maternal harsh discipline and paternal harsh discipline on the risk of emotional and behavioral problems. None of the interaction terms was statistically significant.
Missing values on the covariates were estimated using multiple imputation techniques and were based on available information on determinants, outcome and covariates of this study. The presented results are based on pooled estimates of ten imputed datasets .
Analyses were conducted in the number of children with data available for the outcome of interest (for example parent reported emotional problems). As we did not impute the outcome variables the number of children per analysis differed from 3,047 to 4,015. We repeated all analyses in participants with complete data (N = 3,047). Linear regression analyses were performed using the SPSS version 18.0 (SPSS Inc., Chicago, IL).
Baseline nonresponse and loss-to-follow up analysis
In total, 4,733 mothers completed the questionnaire on harsh discipline at baseline. Mothers (N = 2,562) who did not complete this questionnaire were on average younger (28.6 years versus 31.5 years, F(2, N = 7,295) = 11.8, p<.001), and were more likely to have continued smoking during pregnancy (20.8% versus 12.0%, χ2(2, N = 7,295) = 501.0, p<.001), to have a family income below modal (32.7% versus 15.4%, χ2(1, N = 7,295) = 238.5 p<.001) and to have no partner (21.4% versus 8.2%, χ2(1, N = 7295) = 231.8, p<.001) than mothers who completed the questionnaire.
At follow-up, when the child was between five and eight years old, 4,015 children (85%) of the 4,733 mothers who returned the questionnaire at age three, completed the Berkeley Puppet Interview. We compared these families with families of children who did not complete the BPI (N = 718). Children without a BPI assessment were more likely to be of non-Dutch origin (38.3% versus 32.2%, χ2(2, N = 4733) = 11.8, p = .003), but did not differ from their peers who completed a BPI assessment in terms of maternal harsh discipline score (2.2 versus 2.2, F = 0.7, p = 0.63), behavioral problems at age three (5.4 versus 5.0, F = 10.2, p = .08), parent reported behavioral problems at age six (7.5 versus 6.9, F = 12.4, p = .13) or family income (14.3% versus 15.6%, below modal, χ2(1, N = 4733) = 0.8, p = .40).
Characteristics of the study sample are presented in Table 1. Children had a mean age of 3.1 years at baseline and a mean age of 6.1 years at follow-up. Sixty-seven percent of the children were of Dutch origin, 8.2% had a European and 24.4% a Non-western background.
Table 2 shows the Pearson correlation coefficients between harsh discipline, the different emotional and behavioral problem scales, and parental psychopathology. Parent reports of emotional and behavioral problems were highly correlated (r at age three = 0.61, p<.001, r at age six = 0.66, p<.001), whereas child reported emotional and behavioral problems were less strongly correlated (r = 0.30, p<.001). Parent and child reports of behavioral problems were more strongly correlated (r = 0.18, p<.001) than emotional problems (r = 0.10, p<.001). Maternal and paternal harsh discipline was correlated to all emotional and behavioral scales, with the exception that there was no correlation between paternal harsh discipline and child reported emotional problems.
Table 3 shows the results of the linear regression analyses with behavioral problems as outcome. First, we assessed the relation between harsh discipline and parent reported behavioral problems (CBCL). Adjustment for sociodemographic covariates and family characteristics attenuated the effect of harsh discipline on behavioral problems. Additional adjustment for baseline behavioral problems at age three further attenuated the effect estimates, but the relation between maternal harsh discipline and parent reported behavioral problems remained (model 3: B = 0.06, 95%CI: 0.02, 0.09). Analyses of the relation between paternal harsh discipline and behavioral problems yielded similar results (model 3: B = 0.08, 95%CI: 0.04, 0.13).
Analyses with child self-reported behavioral problems (BPI) showed that higher levels of maternal harsh discipline were associated with higher levels of child reported behavioral problems. Although effect sizes were somewhat smaller than those for parent reported problems, the overall pattern for child reported behavioral problems across the three models was very similar to the effect observed if based on parent report. Even after adjustment for all covariates, maternal and paternal harsh discipline were associated with a higher score on child self-reported behavioral problems (model 3: B for maternal harsh discipline = 0.07, 95%CI: 0.03, 0.11; B for paternal harsh discipline = 0.07, 95%CI: 0.03, 0.12).
Table 4 shows the relation between harsh discipline and emotional problems. Higher levels of maternal and paternal harsh discipline were associated with more parent reported emotional problems (model 3: B for maternal harsh discipline = 0.06, 95%CI: 0.03, 0.10, model 3; B for paternal harsh discipline = 0.04, 95%CI: 0.00, 0.08). Yet, we found that neither maternal nor paternal harsh discipline was related to emotional problems as reported by the child in model 3 (B for maternal harsh discipline = 0.02, 95%CI: -0.02, 0.06; B for paternal harsh discipline = 0.01, 95%CI: -0.03, 0.006).
To test whether the association of harsh discipline with child self-reported behavioral problems was independent of parent report, we additionally adjusted this relation for parent reports of behavioral problems. Both maternal and paternal harsh discipline predicted child reported behavioral problems, independently of parent reported behavioral problems (B for maternal harsh discipline = 0.06, 95%CI: 0.02, 0.10, R2 = 0.06; B for paternal harsh discipline = 0.06, 95%CI: 0.02, 0.11, R2 = 0.06).
The above analyses were conducted in the number of children with data available for one or more of the outcome measures to reduce selection bias. Next, we repeated all analyses in those participants with complete data to allow for optimal comparison between analyses. Results were essentially unchanged.
Parental harsh discipline -whether used by father or mother- increases the risk of behavioral problems in young children. In the present study, mild forms of harsh parental discipline were negatively associated with parent and child reported behavioral problems. By adjusting for pre-existing problems, we showed that this reflects an increase in problems across a three-year period. Most importantly, we demonstrated that children provide independent information when assessing the effects of parental harsh discipline on behavioral problems, whereas the results for child and parent-reported emotional problems were less consistent.
Studies have repeatedly associated harsh disciplining practices based on parent reports of child emotional and behavioral problems (i.e. , ). However, in the present study the effects of harsh discipline on behavioral problems were not restricted to harsh discipline by the father, as proposed by Avakame  and reported by Chang et al. . Rather, maternal harsh discipline had effects very comparable to harsh discipline of the father. Possibly, the disciplining tactics we studied were mild and verbally oriented (e.g. screaming and threatening) and may thus not discriminate well between maternal and paternal disciplining tactics. Clear differences between mothers and fathers may be detected only if more extreme forms of harsh disciplining are studied. Alternatively, the presence of any harsh behavior in a family is more important than the gender of the disciplining parent. Indeed, partners are often similar in antisocial behavior , i.e., mothers who tend to discipline their children harshly more often have partners who also practice this parenting discipline.
Our findings based on child self-reported behavioral problems were not only consistent with those from parent reported behavioral problems, but effects observed using child reports were independent of the parental report. Increased explained variance underpinned this finding. This supports our hypothesis and suggests that children provide unique information on the behavioral consequences of harsh parenting. This observation is clinically relevant since parents using harsh disciplining strategies may interpret their children's behavior differently than other parents , , , . These biased reports may come about for a number of reasons. For example, parents may report higher levels of child problems in their own defense due to emotional overinvolvement. Alternatively, highly critical parenting may cause some parents to have a low tolerance for otherwise normal child problems due to stress. Lastly, from the perspective of authoritarian parenting, certain parents tend to notice only the most extreme behaviors. 
Concluding, if all information (on outcome and determinant) is obtained from one informant, reporter bias may occur . The results from this study indicate young children may be considered as one of the sources of information in a multi-informant approach on the consequences of harsh parenting. Child self-reports not only confirmed the parental reports but suggest that scientists may underestimate the effect of harsh parenting as the child provided independent information on the possible behavioral consequences of harsh parenting.
Maternal and paternal harsh discipline were associated with emotional problems as reported by the primary caregiver but not with emotional problems reported by the child. This was in contrast to rather similar effect sizes observed for the association of harsh parenting with child and parent reported behavioral problems. A relation between harsh discipline and emotional problems in children was hypothesized as children can develop a negative view of the self and feel worthless as a result of a harsh parental discipline style . On the other hand, emotional problems are determined more by genetic variations and less by role modeling than behavioral problems , . However, some methodological explanations for the discrepancy in the analyses using between parent and child reports of emotional problems must be discussed. First, parents distinguish less between emotional and behavioral problems than children. The correlations between parent reported emotional and behavioral problems are higher than those of child reported emotional and behavioral problems (.66 vs .30 in this study). The effect of harsh discipline on parent reported emotional problems may partly reflect the association between harsh discipline and behavioral problems. Second, children may be less accurate reporters of emotional problems  as these are less concrete aspects of behavior . Third, children's ideas about the self do not necessarily match with objectively observable constructs. The concordance between self-perceptions and observable behavior may grow stronger when children age . Therefore, we recommended studying the children's perspective on the consequences of harsh discipline over a longer period of time. Finally, these inconsistent results support findings from previous studies suggesting that all informants' reports are imperfect measures of child behavior . Therefore, combining information from multiple sources is considered most optimal .
Strengths and limitations
Some methodological considerations need to be taken into account. Strengths of this study are the large number of population-based participants. In addition, we obtained both parent and child reports of emotional and behavioral problems at age six, and reports of both maternal and paternal harsh discipline were available. Adjusting for baseline problems (pre-existing child problems at age three) allowed us to analyse changes in emotional and behavioral problems in a relatively short period of time.
One of the limitations of our study is that, although we included large numbers of participants, non-response analysis showed some selective attrition. This resulted in an under-representation of children from families with a lower income and mothers without a partner, while families from a low socioeconomic background are at increased risk for both parental harsh discipline  and child behavioral problems . However, although prevalence rates have an impact on statistical power, these changes do not necessarily alter the relationship between determinant and outcome .
A second limitation is that we had to rely on parent reports only of baseline child problems. Adjusting child self-reported problems for baseline parent reported child problems is not the optimal adjustment to rule out reverse causality. However, it is not feasible to conduct interviews in three-year old children about their behavior because the BPI and other child self-report instruments only yield reliable estimates in children from older ages . Although the primary caregiver was asked to fill out the questionnaire assessing child behavior at age six, mostly mothers completed the questionnaire. Therefore, parent reported child emotional and behavioral problems mostly reflected the mothers' views of child problem behavior.
“Third, when parents report on their own harsh disciplining, social desirability may lead to a response bias. Even though, in this study only mild forms of harsh discipline were investigated - as three items on the physical assault scale were excluded from the questionnaire  - parental underreporting of any verbal or psychological tactics may have been the case. Yet, misclassification in the group of parents that did report harsh disciplining is less likely: if parents reported harsh disciplining tactics, this has most probably been the case. Taken together, these response patterns may have resulted in an underestimation of the effect.”
Fourth, emotional and behavioral problems were assessed differently between children and parents as items in the CBCL-questionnaire differ from items in the BPI interview. However, both measures are accepted ways of assessing child emotional and behavioral problems. , 
Our study confirmed that even mild forms of harsh parental discipline have substantial effects on the behavioral development of a child. Importantly, this study showed that young children can provide independent, valuable information on behavioral problems as a result of harsh disciplining styles. Although information from young children should be treated with some caution, the possibility to obtain information from very young children provides opportunities for instances when parents are unavailable or unwilling to serve as informants on emotional or behavioral consequences of their parenting behavior. In general, child self-report could be used in addition to caregiver report when assessing problem behavior, because both the perspective of the child and the parent is important.
The current findings have implications for programs that aim to identify and provide support for children at risk of, or experiencing, harsh discipline. Health care workers should be well aware of the effects of even mild harsh discipline on behavioral problems in children.
The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the Erasmus University Rotterdam, School of Law and Faculty of Social Sciences, the Municipal Health Service Rotterdam area, Rotterdam, the Rotterdam Homecare Foundation, Rotterdam, and the Stichting Trombosedienst & Artsenlaboratorium Rijnmond (STAR), Rotterdam. We gratefully acknowledge the contribution of general practitioners, hospitals, midwives and pharmacies in Rotterdam. The current study was made possible in close collaboration with the department of child and adolescent psychiatry of Riagg Rijnmond.
Conceived and designed the experiments: JDM AR HT. Performed the experiments: AR JDM PWJ. Analyzed the data: JDM AR JvdE. Contributed reagents/materials/analysis tools: FV AH VWVJ HWT. Wrote the paper: JDM AR JvdE FV VWVJ AH PWJ HWT.
- 1. Teicher MH, Samson JA, Polcari A, McGreenery CE (2006) Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. Am J Psychiatry 163: 993–1000.
- 2. Larzelere RE (2000) Child outcomes of nonabusive and customary physical punishment by parents: an updated literature review. Clin Child Fam Psychol 3: 199–221.
- 3. Sidebotham P, Golding J (2001) Child maltreatment in the “children of the nineties” a longitudinal study of parental risk factors. Child Abus Negl 25: 1177–1200.
- 4. Berger LM (2005) Income, family characteristics, and physical violence toward children. Child Abus Negl 29: 107–133.
- 5. Chang L, Schwartz D, Dodge KA, McBride-Chang C (2003) Harsh parenting in relation to child emotion regulation and aggression. J Fam Psychol 17: 598–606.
- 6. Avakame EF (1998) Intergenerational transmission of violence, self-control, and conjugal violence: a comparative analysis of physical violence and psychological aggression. Violence Vict 13: 301–316.
- 7. Taylor CA, Manganello JA, Lee SJ, Rice JC (2010) Mothers' spanking of 3-year-old children and subsequent risk of children's aggressive behavior. Pediatrics 125: e1057–65.
- 8. Vostanis P, Graves A, Meltzer H, Goodman R, Jenkins R, et al. (2006) Relationship between parental psychopathology, parenting strategies and child mental health—findings from the GB national study. Soc Psychiatry Psychiatr Epidemiol 41: 509–14.
- 9. Jansen PW, Raat H, Mackenbach JP, Hofman A, Jaddoe VWV, et al. (2012) Early Determinants of Maternal and Paternal Harsh Discipline: The Generation R Study. Fam Relat 61: 253–270.
- 10. Anderson KE, Lytton H, Romney DM (1986) Mothers' interactions with normal and conduct-disordered boys: Who affects Whom? Dev Psychol 22: 604–609.
- 11. Lansford JE, Dodge KA, Malone PS, Oburu P, Palme K, et al. (2005) Physical Discipline and Children's Adjustment: Cultural Normativeness as a Moderator. Child Dev 76: 1234–1246.
- 12. Prinzie P, Onghena P, Hellinckx W (2006) A cohort-sequential multivariate latent growth curve analysis of normative CBCL aggressive and delinquent problem behavior: Associations with harsh discipline and gender. Int J Behav Dev 30: 444–459.
- 13. McLeod JD, Kruttschnitt C, Dornfeld M (1994) Does parenting explain the effects of structural conditions on children's antisocial behavior? A comparison of Blacks and Whites. Soc Forces 73: 575–604.
- 14. Fox RA, Platz DL, Bentley KS (1994) Maternal factors related to parenting practices, developmental expectations, and perceptions of child behavior problems. J Genet Psychol Res Theory Hum Dev 156: 431–441.
- 15. Reid JB, Kavanagh K, Baldwin DV (1987) Abusive parents' perceptions of child problem behaviors: An example of parental bias. J Abnorm Child Psychol 15: 457–466.
- 16. Kraemer HC, Measelle JR, Ablow JC, Essex MJ, Thomas Boyce, et al. (2003) A new approach to integrating data from multiple informants in psychiatric assessment and research: mixing and matching contexts and perspectives. Am J Psychiatry 160: 1566–1577.
- 17. Arsenault L, Moffitt TE, Caspi A, Taylor A, Rijsdijk FV, et al. (2003) Strong genetic effects on cross-situational antisocial behaviour among 5-year-old children according to mothers, teachers, examiner-observers, and twins' self-reports. J Child Psychol Psychiatry 44: 832–848.
- 18. Bolger KE, Patterson CJ (2001) Pathways from child maltreatment to internalizing problems: perceptions of control as mediators and moderators. Dev Psychopathol 13: 913–40.
- 19. Lansford JE, Deater-Deckard K, Dodge KA, Bates JE, Pettit GS (2004) Ethnic differences in the link between physical discipline and later adolescent externalizing behaviors. J Child Psychol Psychiatry 45: 801–812.
Citation: Tromp I, Kiefte-de Jong J, Raat H, Jaddoe V, Franco O, Hofman A, et al. (2017) Breastfeeding and the risk of respiratory tract infections after infancy: The Generation R Study. PLoS ONE 12(2): e0172763. https://doi.org/10.1371/journal.pone.0172763
Editor: Stephania A. Cormier, University of Tennessee Health Science Center, UNITED STATES
Received: March 14, 2016; Accepted: February 9, 2017; Published: February 23, 2017
Copyright: © 2017 Tromp et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: This phase of the Generation R Study was supported by the Erasmus Medical Center, the Erasmus University Rotterdam, the Netherlands Organization for Health Research and Development (Zon Mw) and Europe Container terminals B.V. The funders had no role in the design of the study, the data collection and analyses, the interpretation of data, or the preparation of, review of, and decision to submit the manuscript.
Competing interests: I have read the journal's policy and the authors of this manuscript have the following competing interests: J.C. Kiefte-de Jong and O.H. Franco work at ErasmusAGE, a center for aging research across the life course funded by Nestlé Nutrition (Nestec Ltd.); Metagenics Inc.; and AXA. The other authors have indicated they have no potential conflicts of interest to disclose. This does not alter our adherence to PLOS ONE policies on sharing data and materials.
Infectious diseases, including respiratory tract infections, are a leading cause of morbidity and hospitalization in infants and children.[1, 2] There is much epidemiological evidence for the benefits of breastfeeding against a wide range of infections and illnesses.[3, 4] Breast milk contains various antimicrobial substances, anti-inflammatory components and factors that promote immune development.[4, 5] It enhances the immature immune system of the infant and strengthens defense mechanisms against infectious and other agents during the breastfeeding period.[4–7] Exclusive breastfeeding for the first 6 months of life with breastfeeding along with complementary feeding thereafter is recommended by the World Health Organization (WHO). The benefits have been found to be dose-dependent and related to the duration of breastfeeding.[3, 4] The protection of exclusive and prolonged breastfeeding against respiratory tract infections in the first year of life has often been suggested and also found in The Generation R Study.[3, 4, 9, 10] But, not all studies found breastfeeding exclusivity and duration to reduce the occurrence of respiratory tract infections.[11, 12] It is suggested that the influences of breast milk on the infant’s immune system may persist beyond the breastfeeding period, as it not only provides passive immunity but also maturation of the immune system in the long run.[13, 14] Since breastfeeding might protect against diseases in adulthood such as type 1 diabetes and inflammatory bowel disease [3, 4, 15] a prolonged protection against respiratory tract infections after the first year of life seems plausible. However, only few studies have examined the effect of breastfeeding on respiratory tract infections after infancy and reported inconsistent results.[16–21]
The aim of this study was to examine the association between breastfeeding and lower and upper respiratory tract infections after infancy up to 4 years of age.
Subjects and methods
Participants and study design
This study was embedded in the Generation R study, a population-based prospective cohort study from fetal life until young adulthood and has been described in detail previously. In total, 9778 mothers with a delivery date from April 2002 through January 2006 enrolled in the study. Consent for postnatal follow-up was provided by 7893 participants (S1 Fig). The study was approved by the medical ethical review board of the Erasmus Medical Center, Rotterdam, the Netherlands.
Respiratory tract infections
Data on respiratory tract infections was obtained by postal parent-reported questionnaires at the age of 2, 3 and 4 years. Parents were asked whether their child had suffered from a respiratory tract infection in the previous year and had visited a doctor for the infectious disease. Information on upper respiratory tract infections was obtained by asking parents whether their child had suffered from a serious cold, ear infection or throat infection. Information on lower respiratory tract infections was obtained by asking parents whether their child had pneumonia or bronchitis. Upper and lower respiratory tract infections were defined as present or absent in the second, third and fourth year of life. Questionnaire response rates were 76%, 69% and 73% at the age of 2, 3 and 4 years respectively. No information was available for the number of episodes or severity of these infections.
Data on breastfeeding were collected by a combination of delivery reports and postnatal postal questionnaires at the age of 2, 6 and 12 months. By questionnaire the mothers were asked whether they had ever breastfed their child and at which age (in months) the child had stopped receiving breast milk. The duration of breastfeeding was categorized as (I) never breastfed, (II) breastfed for less than 3 months, (III) breastfed for 3–6 months, and (IV) breastfed for 6 months and longer. The majority of infants had stopped receiving breast milk before the age of 12 months, only 3 infants thereafter. An approximation of breastfeeding exclusivity was defined on the basis of parent reports of the child’s age at which solid foods were first introduced, including the introduction of formula feeding. Predominant breastfeeding was defined as receiving breastfeeding without any other infant formula, milk or solid foods. Breastfeeding dose was categorized as (I) never breastfed, (II) partially breastfed until 4 months, and (III) predominantly breastfed until 4 months. Partial breastfeeding was defined as receiving both breast milk and infant formula and/or solid foods. Questionnaire response rates were 82%, 73% and 72% at the age 2, 6 and 12 months respectively.
Information on potential confounders, including mode of delivery, gender and gestational age, were obtained from obstetric records assessed in mid-wife practices and hospital registries. Additional information was obtained by a combination of prenatal and postnatal questionnaires completed by both parents. The questionnaires included information on maternal age, maternal educational level, maternal marital status, maternal ethnicity, household income per month, maternal BMI before pregnancy, any maternal smoking during pregnancy, any maternal alcohol use during pregnancy, parity and parental history of asthma or atopy. Ethnicity of the mother was defined as follows: if both parents were born in The Netherlands, the ethnicity of the mother was defined as Dutch; if one of the parents was born in another country than The Netherlands, that country applied; if parents were born in different countries other than The Netherlands, the country of the mother applied. Ethnicity of the mother was categorized into Western (Dutch, European, American-Western, Asian-Western) and non-Western (American non-Western, Asian non Western, African, Turkish, Cape Verdean, Moroccan, Dutch Antillean, Surinamese, Oceania, and Indonesian). Maternal educational level was defined as follows; low: no education, primary school or less than 3 years of secondary school, mid: more than 3 years of secondary school, higher vocational training or bachelor's degree, and high: academic education. Household income per month was categorized into two income-groups using the approximate monthly general labour income during the inclusion period of this study as cut off point (≤ € 2200 and > € 2200). Postnatal questionnaire completed by the mother at the child’s age of 6 months included information on smoke exposure of the child inside and outside the home. Environmental smoking was defined as maternal smoking, smoking of mother or anybody else at home in the presence of the child and smoking in any other places in the presence of the child at the age of 6 months. Postnatal questionnaires completed by the mother at age 12 months included information on vitamin D supplementation in the previous 6 months and questionnaires at age 12 and 24 months included information on day-care attendance.
Population for analyses
Children whose parents did not provide informed consent for the use of postnatal questionnaire data (n = 1885) and children without information on respiratory tract infections at ages 2 to 4 years (n = 2015) were excluded from the analysis. To prevent clustering, only one child per family within the Generation R cohort was included by random selection (n = 556 excluded). To reduce attrition bias, variables with missing values were multiple imputed (20 imputations) based on the correlation between the variable with missing values with other maternal and child characteristics (S1 Table). Consequently data of 5322 children were available after multiple imputation for statistical analyses (S1 Fig).
First, independent Student’s t test and chi-square test were performed to test for differences in characteristics between the 4 groups of breastfeeding duration. Second, logistic regression analyses by using generalized estimating equations (GEE) were performed. Regression analysis by GEE assesses the association between two variables by correction for the within subject's dependence as a result of the repeated observations on lower and upper respiratory tract infections (age 2, 3 and 4 years) since repeated measurements within one individual are frequently correlated. An unstructured working correlation structure was used in the GEE analyses as adjustment for the dependency between the repeated measurements, since the within-subject correlation coefficient for lower and upper respiratory tract infections between the three time points were different (r = 0.13–0.32). Logistic regression analysis with GEE was performed with lower respiratory tract infections and upper respiratory tract infections as dependent variables and breastfeeding as independent variable. All analyses were adjusted for the age (time) at which observations of illness were assessed to account for potential confounding by age as well as clustering of repeated measurement. The selection of potential confounders was performed by the alteration in odds ratio (OR) and kept in the multivariable model in case of an alteration of ≥ 10% in OR. The pooled results of the 20 imputed datasets were reported in this paper as odds ratio’s (OR’s) and 95% confidence intervals (95% CIs). A P-value < 0 .05 was considered as statistically significant. The statistical analyses were carried out by using SPSS 22.0 for Windows (SPSS Inc, Chicago, IL).
Maternal and child characteristics are presented in Table 1 and S1 Table. Out of 5322 children, 14% had suffered from at least one episode of lower respiratory tract infection in the second year of life, 8% in the third year and 6% in the fourth year of life (Table 2). At least one episode of upper respiratory tract infection was reported for 44% of children in the second year of life, 36% in the third year and 31% in the fourth year of life (Table 2).
Duration of breastfeeding and respiratory tract infections
Compared to children who were never breastfed, breastfeeding for 6 months or longer was significantly associated with a decreased risk of lower respiratory tract infections after infancy up to 4 years of age (aOR: 0.71; 95% CI: 0.51–0.98) (Table 3) (S2 Table). Similar ORs for lower respiratory tract infections were found with breastfeeding for less than 3 months and breastfeeding for 3–6 months but this was not statistically significant (aOR: 0.75; 95% CI: 0.56–1.00 and aOR: 0.78; 95% CI: 0.53–1.13) (Table 3) (S2 Table). Although in the same direction, weaker ORs were found for upper respiratory tract infections and breastfeeding for less than 3 months, 3–6 months or 6 months and longer after adjustment for confounding variables (aOR: 0.86; 95% CI: 0.70–1.04 for less than 3 months, aOR: 0.91; 95% CI: 0.73–1.12 for 3–6 months and aOR: 0.85; 95% CI: 0.69–1.05 for 6 months and longer) (Table 3) (S2 Table). The effects of the duration of breastfeeding on respiratory tract infections did not differ between the ages of 2, 3 and 4 years (pinteraction >0.23 for lower and upper respiratory tract infections).
Dose of breastfeeding and respiratory tract infections
Partial breastfeeding until 4 months was significantly associated with a decreased risk of lower respiratory tract infections after infancy up to age 4 years (OR: 0.76; 95% CI: 0.59–0.99). However, the association did not remain significant after adjustment for confounders (aOR: 0.78; 95% CI: 0.59–1.02) (Table 4) (S3 Table). The same trend was found for predominant breastfeeding but not statistically significant (Table 4). Before multiple imputation, predominant breastfeeding was associated with lower respiratory tract infections (S3 Table). Although partial breastfeeding until 4 months and predominant breastfeeding until 4 months was not significantly associated with upper respiratory tract infections, the effect estimates were found to be in the same direction (aOR: 0.89; 95% CI: 0.72–1.10 and aOR: 0.93; 95% CI: 0.72–1.20) (Table 4) (S3 Table). The effects of breastfeeding dose on respiratory tract infections did not differ between the ages of 2, 3 and 4 years (pinteraction >0.59 for upper and lower respiratory tract infections).
In this population-based prospective birth cohort study we found children who were breastfed for 6 months or longer to have a reduced risk of lower respiratory tract infections after infancy. For breastfeeding for less than 3 months and 3–6 months similar direction of the effect estimates were found. Also, similar direction of the effect estimates were found for the association between the duration and dose of breastfeeding and upper respiratory tract infections but not significant.
Various studies, including a previous study within our cohort, found exclusive breastfeeding for 6 months to be protective for the development of respiratory tract infections in infancy, thereby supporting the recommendation of the WHO.[10, 19, 30] Our study found breastfeeding for 6 months or longer to be associated with a reduced risk for lower respiratory tract infections after infancy till the age of 4 years. Contrary to our findings, a prospective longitudinal study found that breastfeeding duration, including breastfeeding longer than 6 months, was not associated with pneumonia or lung infection in 6 year old children. However, the association was only examined in children who initiated breastfeeding whereas we also included children who were never breastfed. In agreement with our findings on breastfeeding dose, Li et al  did not find breastfeeding exclusivity to be associated with lower respiratory tract infections. As for upper respiratory tract infections, we did not observe a significant association among children who were breastfed (duration and dose) compared to those who were never breastfed. Similarly, Chantry et al  found full breastfeeding for less than 6 months not to be associated with an increased risk of recurrent upper respiratory tract infections and recurrent otitis media in children 6–72 months of age. Li et al  also found no association between breastfeeding, including duration and exclusivity, and colds or upper respiratory tract infections among 6 year old children. The possibility that the protective effect of breastfeeding might wear off after breastfeeding cessation has previously been suggested.[31–33] Other studies that did find breastfeeding to be associated with a reduced risk of upper respiratory tract infections after infancy mainly focused on otitis media and mostly before the age of 3 years.[20, 34, 35] Some studies examined the effect of breastfeeding on respiratory tract infections in general. A Japanese study reported breastfeeding duration for 6–7 months to be borderline significantly associated with a reduced risk of hospitalization for respiratory tract infections between the age of 18–30 months. Respiratory tract infections for which hospitalization is needed are often more serious and mainly infections of the lower respiratory tract [2, 36] which might explain the discrepancy between these latter results and those from our study. Conversely, another study did not find a protective effect of breastfeeding for all acute respiratory illness in children 1–6 years  which might be due to an overrepresentation of upper respiratory tract infections since these symptoms are more common in childhood. The WHO definition of exclusive breastfeeding allows for ORS, drops and syrups but no other food or drink, not even water. Therefore, this study examined the effect of predominant breastfeeding defined as no infant formula, milk or solid foods. This study cannot examine the effect of predominant breastfeeding per month neither for the duration of 6 months or longer due to small group size. The majority of mothers in the Netherlands do not continue breastfeeding after the age of 4 months. Thus, our study precludes conclusions on the effect of exclusive breastfeeding for 6 months as defined by the WHO. In line with our findings, a birth cohort study from Hong Kong did not find exclusive and partial breastfeeding for 3 months to be associated with a reduced risk for hospital admissions for respiratory tract infections after the age of 6 months up to age 8 years. However, Yamakawa et al. did find exclusive breastfeeding at 6–7 months of age to be significantly associated with hospitalization for respiratory tract infections between the age of 18–42 months. Also, Li et al. reported exclusive breastfeeding for 6 months and longer, compared to breastfeeding between 0 to 4 months, to be significantly associated with a reduced odds for ear, throat, and sinus infection at age 6 years.
We performed multiple imputation to account for bias associated with missing data. Children with and without questionnaire data differed in socioeconomic background, ethnicity, and a selection towards a relative more healthy study population seems to be present. However, this would only affect the interpretation of our results if the association between breastfeeding and respiratory infections was different for children without questionnaire data compared with those with questionnaire data, which is unlikely. For the analyses on breastfeeding duration ≥6 months and lower respiratory tract infections, results were comparable in the original data (aOR: 0.56; 95% CI: 0.32–0.99) and after the multiple imputation procedure (aOR: 0.71; 95% CI: 0.51–0.98). However, for the analyses on predominant breastfeeding and lower respiratory tract infections the estimate in the original data analysis (aOR: 0.53; 95% CI: 0.30–0.93) slightly weakened after the imputation procedure (aOR: 0.72; 95% CI: 0.48–1.09). This would suggest that the missing data was not completely random and affected the uncertainty of the effect estimates for predominant breastfeeding.
An important strength of this study is the large study population drawn from the general population. On the basis of previous findings in our cohort, respiratory illnesses are socially patterned and related to several mother and child characteristics. Our study design provided information on multiple potential confounders and allowed for follow-up into childhood. However, due to the observational nature of our study, residual confounding cannot be fully excluded. In addition, the prospective design made it possible to obtain information on breastfeeding at multiple time points during infancy therefore limiting recall bias. Whereas other studies examined the effect of respiratory tract infections in general, or focused on specific infections,[20, 21, 34, 35] we examined the effect of breastfeeding on the development of lower and upper respiratory tract infections separately.
A weakness may be that the diagnosis of respiratory tract infection was obtained by parent-reported questionnaires at yearly intervals. The questions used to obtain information on respiratory infections were comparable to other studies. Parents were asked whether their child had suffered from a respiratory tract infection and whether they had visited a doctor for this infection since physician diagnosis is more accurate. However, this could have led to misclassification of the outcome as parents may not be able to distinguish between lower and upper respiratory tract infections and children who had not visited a doctor may even so have suffered from a respiratory tract infection. However, since the outcome was measured after the breastfeeding period we do not expect such misclassification to be differential and to have influenced the effect of the duration or dose of breastfeeding. Also, our study did not have information on the number of episodes of infection. Li et al. found a relation between two or more visits to the physician and breastfeeding duration and exclusivity.
Several long-term effects of breastfeeding on the offspring have been reported.[3–5, 15] Different mechanisms for the stimulation of the immune response by breastfeeding have been suggested, among others transfer of anti-idiotypic antibodies and lymphocytes.[6, 13] However, the mechanism by which breastfeeding might add to a long-term protection remain unclear.
In conclusion, this study showed that breastfeeding duration for 6 months or longer is associated with a reduced risk of lower respiratory tract infections in pre-school children. These findings are compatible with the hypothesis that the protective effect of the duration of breastfeeding for respiratory tract infections persist after infancy therefore supporting current WHO recommendations for breastfeeding for at least 6 months also in industrialized countries.
The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the School of Law and Faculty of Social Sciences of the Erasmus University Rotterdam, the Municipal Health Service–Rotterdam Metropolitan Area, the Rotterdam Homecare Foundation, and the Stichting Trombosedienst & Artsenlaboratorium Rijnmond. We acknowledge the contributions of children and parents, general practitioners, hospitals and midwives in Rotterdam.
- Conceptualization: VJ AH HM.
- Formal analysis: IT JKJ.
- Funding acquisition: VJ AH HM OF HR JJ.
- Investigation: IT JKJ HM.
- Methodology: IT JKJ HM.
- Project administration: VJ.
- Resources: VJ AH HR OF JJ HM.
- Supervision: JKJ HM.
- Writing – original draft: IT JKJ.
- Writing – review & editing: HR VJ OF AH JJ HM.
- 1. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875): 1405–16. pmid:23582727
- 2. Hasegawa K, Tsugawa Y, Cohen A, Camargo CA Jr. Infectious Disease-related Emergency Department Visits Among Children in the United States. Pediatr Infect Dis J. 2015;34(7): 681–5. pmid:25860534
- 3. Hörnell A, Lagström H, Lande B, Thorsdottir I. Breastfeeding, introduction of other foods and effects on health: a systematic literature review for the 5th Nordic Nutrition Recommendations. Food Nutr Res. 2013;12;57.
- 4. ESPGHAN Committee on Nutrition, Agostoni C, Braegger C, Decsi T, Kolacek S, Koletzko B, et al. Breast-feeding: A commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr. 2009;49(1): 112–25. pmid:19502997
- 5. Hanson LA. Session 1: Feeding and infant development breast-feeding and immune function. Proc Nutr Soc. 2007;66(3): 384–96. pmid:17637091
- 6. Hanson LA, Korotkova M, Lundin S, Håversen L, Silfverdal SA, Mattsby-Baltzer I, et al. The transfer of immunity from mother to child. Ann N Y Acad Sci. 2003;987: 199–206. pmid:12727640
- 7. Jansen MA, van den Heuvel D, van Zelm MC, Jaddoe VW, Hofman A, de Jongste JC, et al. Decreased Memory B Cells and Increased CD8 Memory T Cells in Blood of Breastfed Children: The Generation R Study. PLoS One. 2015;18;10(5): e0126019. pmid:25993335
- 8. World Health Organization. The optimal duration of exclusive breastfeeding: report of the expert consultation. Geneva: World Health Organization; March 28–30, 2001. Available: http://www.who.int/nutrition/publications/optimal_duration_of_exc_bfeeding_report_eng.pdf. Accessed February 20 2016.
- 9. Duijts L, Ramadhani MK, Moll HA. Breastfeeding protects against infectious diseases during infancy in industrialized countries. A systematic review. Matern Child Nutr. 2009;5(3): 199–210. pmid:19531047
- 10. Duijts L, Jaddoe VW, Hofman A, Moll HA. Prolonged and exclusive breastfeeding reduces the risk of infectious diseases in infancy. Pediatrics. 2010; 126(1): e18–25. pmid:20566605
- 11. Rebhan B, Kohlhuber M, Schwegler U, Fromme H, Abou-Dakn M, Koletzko BV. Breastfeeding duration and exclusivity associated with infants' health and growth: data from a prospective cohort study in Bavaria, Germany. Acta Paediatr. 2009;98(6): 974–80. pmid:19484835
- 12. Kramer MS, Chalmers B, Hodnett ED, Sevkovskaya Z, Dzikovich I, Shapiro S, et al. Promotion of Breastfeeding Intervention Trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA. 2001;285(4): 413–20. pmid:11242425
- 13. Hanson LA. Breastfeeding provides passive and likely long-lasting active immunity. Ann Allergy Asthma Immunol. 1998;81(6): 523–33; quiz 533–4, 537. pmid:9892025
- 14. Hanson LA. The mother-offspring dyad and the immune system. Acta Paediatr. 2000;89(3): 252–8. pmid:10772267
- 15. Schack-Nielsen L, Michaelsen KF. Breast feeding and future health. Curr Opin Clin Nutr Metab Care. 2006;9(3): 289–96. pmid:16607131
- 16. Tarrant M, Kwok MK, Lam TH, et al. Schooling CM. Breast-feeding and childhood hospitalizations for infections. Epidemiology. 2010;21(6): 847–54.
- 17. Li R, Dee D, Li CM, Hoffman HJ, Grummer-Strawn LM. Breastfeeding and risk of infections at 6 years. Pediatrics. 2014;134 Suppl 1: S13–20.
- 18. Prietsch SO, Fischer GB, César JA, Lempek BS, Barbosa LV, Zogbi L, et al. Acute lower respiratory illness in under-five children in Rio Grande, Rio Grande do Sul State, Brazil: prevalence and risk factors. Cad Saude Publica. 2008;24(6): 1429–38. pmid:18545768
- 19. Chantry CJ, Howard CR, Auinger P. Full breastfeeding duration and associated decrease in respiratory tract infection in US children. Pediatrics. 2006;117(2): 425–32. pmid:16452362
- 20. Hatakka K, Piirainen L, Pohjavuori S, Poussa T, Savilahti E, Korpela R. Factors associated with acute respiratory illness in day care children. Scand J Infect Dis. 2010;42(9): 704–11. pmid:20465487
- 21. Yamakawa M, Yorifuji T, Kato T, Inoue S, Tokinobu A, Tsuda T, et al. Long-Term Effects of Breastfeeding on Children's Hospitalization for Respiratory Tract Infections and Diarrhea in Early Childhood in Japan. Matern Child Health J. 2015;19(9): 1956–65. pmid:25656723
- 22. Jaddoe VW, van Duijn CM, Franco OH, van der Heijden AJ, van Iizendoorn MH, de Jongste JC, et al. The Generation R Study: design and cohort update 2012. Eur J Epidemiol. 2012;27(9): 739–56. pmid:23086283
- 23. Indicators for Assessing Breast-Feeding Practices. Geneva, Switzerland: World Health Organization. WHO Document WHO/CDD/SER 1991; 91:14.
- 24. Swertz O, Duimelaar P, Thijssen J. Migrants in the Netherlands 2004. Voorburg/Heerlen: Statistics Netherlands, 2004.
- 25. Statistics, Netherlands. Dutch Standard Classification of Education 2003. Voorburg/Heerlen: Statistics Netherlands, 2004.
- 26. Statistics, Netherlands. Welfare in the Netherlands. Income, welfare and spending of households and individuals. Den Haag/Heerlen: Statistics Netherlands, 2012.
- 27. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ. 2009;338: b2393. pmid:19564179
- 28. Twisk JW. Longitudinal data analysis. A comparison between generalized estimating equations and random coefficient analysis. Eur J Epidemiol. 2004;19(8): 769–76. pmid:15469034
- 29. Mickey RM, Greenland S. The impact of confounder selection criteria on effect estimation. Am J Epidemiol. 1989;129(1): 125–37. pmid:2910056
- 30. Ladomenou F, Moschandreas J, Kafatos A, Tselentis Y, Galanakis E. Protective effect of exclusive breastfeeding against infections during infancy: a prospective study. Arch Dis Child. 2010;95(12): 1004–8. pmid:20876557
- 31. Fisk CM, Crozier SR, Inskip HM, Godfrey KM, Cooper C, Roberts GC, et al. Breastfeeding and reported morbidity during infancy: findings from the Southampton Women's Survey. Matern Child Nutr. 2011;7(1): 61–70. pmid:21143586
- 32. Quigley MA, Kelly YJ, Sacker A. Breastfeeding and hospitalization for diarrheal and respiratory infection in the United Kingdom Millennium Cohort Study. Pediatrics. 2007;119(4): e837–42. pmid:17403827