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Review Article Association of Food Insecurity with Children’s Behavioral, Emotional, and Academic Outcomes: A Systematic Review Priya Shankar, MPH,* Rainjade Chung, BA,† Deborah A. Frank, MD† ABSTRACT: Objective: Food Insecurity (FI) occurs in 21% of families with children and adolescents in the United States, but the potential developmental and behavioral implications of this prevalent social determinant of health have not been comprehensively elucidated.
This systematic review aims to examine the association between FI and childhood developmental and behavioral outcomes in western industrialized countries.
Method: This review provides a critical summary of 23 peer reviewed articles from developed countries on the associations between FI and adverse childhood developmental behavioral outcomes including early cognitive development, academic performance, inattention, externalizing behaviors, and depression in 4 groups–infants and toddlers, preschoolers, school age, and adolescents.

Various approaches to measuring food insecurity are delineated.
Potential confounding and mediating variables of this association are compared across studies.

Alternate explanatory mechanisms of observed effects and need for further research are discussed.

Results: This review demonstrates that household FI, even at marginal levels, is associated with children’s behavioral, aca- demic, and emotional problems from infancy to adolescence across western industrialized countries - even after controlling for confounders.
Conclusions: While the American Academy of Pediatrics already recommends routine screening for food insecurity during health maintenance visits, the evidence summarized here should encourage developmental behavioral health providers to screen for food insecurity in their practices and in- tervene when possible.

Conversely, children whose families are identified as food insecure in primary care settings warrant enhanced developmental behavioral assessment and possible intervention.
(J Dev Behav Pediatr 38:135–150, 2017) Index terms: food insecurity, child behavior, child development, adolescent mental health, maternal mental health.
The behavioral and developmental sequelae of severe malnutrition in infancy and childhood are well researched.1 Any sustained interruption to a child’s nutrition, if not treated early, can result in persistent deficits not only in physical size, but in cognitive growth and fine and gross motor skills.2 A lack of macronutrients and micro- nutrients for a sustained period of time is associated with learning and behavioral outcomes including impairments in academic performance, linguistic development, social development, and self-regulation, with increased likeli- hood of diagnosis of psychosocial disorders.3 However, the threshold for neurocognitive and de- velopmental correlates of undernutrition in childhood is lower than previously presumed and may occur without visible anthropometric deficits.
Studies have found that in- termittent or modest undernutrition may have long-term implications for a child’s cognitive and school perfor- mance.4,5 Even micronutrient deficiencies during critical periods of brain development in infancy and toddlerhood are linked to persistent adverse outcomes.6,7 For instance, From the *Department of Pediatrics, Boston University School of Medicine, Boston, MA; †Dowling Ground, Boston Medical Center, Boston, MA.

Received April 2016; accepted November 2016.


Disclosure: The authors declare no conflict of interest.

Address for reprints: Deborah A. Frank, Dowling Ground, Boston Medical Center, 771 Albany Street, Boston, MA 02118; e-mail: dafrank@bu.edu.

Copyright 2016 Wolters Kluwer Health, Inc. All rights reserved.
infants with iron deficiency perform more poorly on assessments of attentiveness, memory, academic perfor- mance, and motor development,8–12 with deficits persisting years after the iron deficiency has been treated.11,12 More- over, older iron-deficient children are fatigued, making it more difficult for them to be successful in a classroom.13 Two decades of research also suggests that even care- givers’ reports of difficulty obtaining food of adequate quality and quantity for the household, variously termed as “hunger,” “food insufficiency,” or “food insecurity,” with- out clinically obvious signs or laboratory indicators of child malnutrition, may be associated with a higher incidence of behavioral, emotional, and academic problems for chil- dren.
Food insecurity (FI) fluctuates with economic trends, increasing steeply nationally from 11% to 14.6% in response to the Great Recession in 2008 and remaining at that level until 2010.14,15 As of 2014, the food insecure 14.3% of the national population comprised a total of 49.1 million peo- ple—33.3 million adults and 15.8 million children.17 The 21% prevalence of FI in households with children is higher than the 11.9% prevalence in households without chil- dren.16 Given the high prevalence of FI among families with children, it is important to explore existing evidence of FI’s possible impact on children’s development and be- havior to guide future clinical care, research, and advocacy.
The objective of our systematic review is to assess the current literature that addresses food insecurity from a developmental and behavioral perspective with a focus Vol.

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on data from relatively wealthy industrialized western countries: United States of America, United Kingdom, Canada, and Australia.
We critically review and summa- rize the association of food insecurity and analogous measures with cognition, behavior, emotional regula- tion, and academic achievement, controlling for socio- economic status and other variables, among infants, preschoolers, school-aged children, and adolescents.
Food insecurity is defined as “limited or uncertain availability of nutritionally adequate and safe foods or lim- ited or uncertain ability to acquire food in socially accept- able ways.”16 In contrast to malnutrition, which is defined and diagnosed based on anthropometric or laboratory data, FI is assessed by structured questionnaires.
Alaimo et al.8 argued that “questionnaire-based measures of food in- sufficiency, FI, or hunger are more appropriate than an- thropometric measures for recognizing a relationship between current resource-constrained food deprivation and negative outcomes because they capture the phenomena of interest directly rather than through an indirect indicator,” such as height which may indicate past rather than current nutritional deprivation and may be influenced by genetics.
The science of assessing resource-constrained food deprivation by questionnaire evolved from the twentieth to the twenty-first century.
FI was initially measured us- ing the Community Childhood Hunger Identification Project (C-CHIP) scale in the early 1990s as part of a project to measure hunger nationwide in families with children, and also by the Cornell Radimer scale, a ques- that tionnaire developed from in-depth interviews addressed the quantitative, qualitative, psychological, and social components of FI.17 In 1999, the United States Department of Agriculture (USDA) developed a new measure drawing on the C-CHIP and Radimer scales while reframing the construct of “hunger” as “food in- security,” given that hunger was interpreted as a re- flection of an individual’s physiological perception of lack of food and not that of an entire household.
In re- search and epidemiological studies, FI has since been measured using the validated USDA Food Security Survey Module, an 18-item questionnaire considered the gold standard in identifying household and child FI.

In households with children, the module is administered to the primary caregiver and consists of 10 household- specific questions and 8 child-specific questions (Fig.

1).

With the USDA module, families are categorized as having high, marginal, low (LFS), or very low food se- curity (VLFS).
In households with children, marginally food secure families express anxiety about sufficiency of food and answer affirmatively to 1 to 2 of the 18 ques- tions.

Families that have LFS (formerly termed food in- security without hunger) change the quality, variety, and desirability of food with little or no changes in quantity of food, as reflected by affirmative answers to 3 to 7 questions on the USDA food security module.
Finally, families with VLFS (formerly termed food insecurity with hunger) report changing their eating patterns, cutting back or skipping meals entirely, with greater than 8 or more affirmative responses to questions on the USDA food security questionnaire.

Child food insecurity has Figure 1.


Comparison of the United States Department of Agriculture (USDA) Food Security Survey and Community Childhood Hunger Identification Project (C-CHIP) questionnaire used to identify food insecure households and children.

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been defined as 2 out of 8 affirmative answers on the child-focused questions.

In our review, many of the studies grouped VLFS and LFS together and categorized them as food insecure because the number of families with children who reported VLFS is relatively small.

In addition, some of the studies reviewed in this article use condensed versions of the USDA module or the C-CHIP scale or study-specific questions as a means of identifying FI.
For ease of synthesis, these related but not identical measures will be referred to throughout this systematic review as FI; issues of level of exposure according to a given measure will be specified when relevant.

Fig- ure 1 compares the categories of FI identified using the USDA 18-item scale with the earlier C-CHIP measure.
Figure 2 summarizes abbreviated or idiosyncratic food insecurity study-specific questionnaires and scales which have been used in a the developmental-behavioral research summarized here.

small proportion of METHODS We searched 4 databases: PubMed, Agricola, PsycInfo, and Web of Science.

We also conducted a hand search by reading through citations of articles that were found.

For all of these databases, we searched using the key- words academic achievement and child mental health.
Our search in PubMed also used the following keywords: food insecurity, development, behavior, child, adoles- cent, and mental health.

Our Web of Science search in- cluded the following keywords: hunger, scholastic achievement, child behavior, and nutrition.

Our PsycInfo search used the keywords food insecurity and child be- havior, and our Agricola search included food security and child behavior.
We selected articles published in English from 1985 to 2016 in developed countries (United States of America, United Kingdom, Canada, and Australia) and excluded articles which addressed correlates of FI other than child development and behavior, including, but not limited to, obesity, chronic conditions such as asthma, and other health outcomes.

Studies that did not use explicit metrics to measure FI were not reviewed.
We also excluded studies with a sample size of less than 100 because of concern they might lack adequate statistical power to detect clinically meaningful effects.

RESULTS As shown in Figure 3 and Tables 1–4, our systematic review assessed 23 articles.

The articles were abstracted by one of the 2 authors, P.S.

or R.C., whose findings were then reviewed by the senior author.

Disagreements were resolved by re-review and consensus.
Some studies assessed multiple age groups: 3 studies analyzed infants and toddlers,5,29,30 4 assessed preschoolers,31–34 14 looked at school-aged children,8,31,33,35,37–43,51,52,56 and 6 assessed adolescents.8,44–46,51,62 8 used the entire 18-item USDA Food Security Scale,29,30,32,39,42,43,51,61 7 used modifications or abridged versions of the 18-item USDA Food Security Scale,5,31,34,37,38,46,52 2 used “food insufficiency” as the predictor,8,44 3 used the C-CHIP scales,33,36,40 and 3 used idiosyncratic food insecurity measures.35,41,45 Of note, all “n” values in tables represent the final analytic sample size.
See Tables 1–4 for analysis of articles describing findings in infants and toddlers, preschoolers, school-aged children, and adolescents.

The Early Childhood Longitudinal Study—Kindergarten—will be referenced as ECLS-K in Tables 1–4.

In addition, as shown in Figure 4, a range of disparate instruments were used to measure childhood outcomes.

As the tables summarize, these articles demonstrated a number of associations between household FI and children’s cognitive, emotional, and behavioral out- comes.
The studies differ not only in the measure of food insecurity used, but in sample size and selection, the statistical methods used, the outcome measures, and the range of potential covariates evaluated.

(List of covariates for each article can be obtained from the authors by request.)

Each table is alphabetized by first author within age group, with a parallel construction of columns for Figure 2.
Summary of abbreviated or idiosyncratic food insecurity study specific questionnaires and scales in developmental-behavioral research.

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Figure 3.

Flow chart for identifying eligible articles for systematic review.
these domains to facilitate readers’ rapid comparative assessment of the findings.

underweight were excluded, LFS was still associated with increased developmental risk for young children.

Infants and Toddlers Table 1 shows that the impact of FI can be identified in infants and toddlers.

Rose-Jacobs et al.
Rose-Jacobs et al.

found that caretakers of 4 to 36 months old children from food in- secure households reported a 3-fold increase in child- ren’s developmental risk as identified using the Parents’ Evaluation of Developmental screening in- strument.18 In this study, when families with very low food security (VLFS) (“hunger”) and children who were Status Zaslow et al.
assessed children at ages 9 to 24 months using the Bayley Short Form Research Edition (BSF-R) mental and motor subscale assessment and parent-toddler Attachment Sort (TAS)-45.19 The authors found that in- creasing levels of FI at 9 months of age were associated with insecure child attachment and lower mental pro- ficiency at 24 months of age, an association mediated en- tirely other confounders.20 Hernandez and Jacknowitz5 found that 24- month-old toddlers with food insecure mothers scored 1.5 through maternal depression and Figure 4.
Instruments used to measure childhood and adolescent outcomes.

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Informants Outcome Results Limitations Table 1.
Infants and Toddlers Longitudinal/ Cross-sectional Longitudinal N 5 7900 Author Hernandez et al.5 Study Population, Age Early Childhood Longitudinal Survey-Birth Cohort (ECLS-B) FI: parents Cognitive Ability: Bayley Short Form Research (BSF-R) Edition mental and motor subscales19 Rose- Cross-sectional 2010 Low-income FI: parents Child Jacobs et al.29 households, children 4–36 mo Zaslow et al.30 Longitudinal 10,688 parents and 10,211 children at 9 mo; 9835 parents and 9218 children at 24 mo ECLS-B FI: parents Developmental Risk PEDS screening instrument18 Cognitive ability: BSF-R Edition mental subscales19 Child Attachment: Toddler Attachment Sort (TAS-45) Toddlers living with temporarily Oversampling of Asian and Native food insecure adult experienced small but immediate negative effects on development.
Toddlers scored 1.5 points Y on cognitive assessments at 24 mo if living with food insecure adults.

Underweight children 3x more likely to have developmental risk; food insecure children more likely to be at developmental risk even when underweight and children with VLFS removed from analysis.
American children, twins, low and very low birth weight children; substantial loss to follow-up; Variables do not indicate timing, intensity, and duration of FI; informant unclear English, Spanish, Somali only; multisite, not national; shared- method variance Greater FI at 9 mo predicted Single method rather than multiple insecure child attachment and less advanced mental proficiency at 24 mo.
measures for each domain of child development; child attachment measure not gold standard; concurrent FI and parental characteristics not measured at 24 mo; shared-method variance for FI and attachment V o l .

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points lower on cognitive assessments.

In addition, this study showed that 24 month olds residing with temporarily food insecure adults, compared with never food insecure adults, experienced small but immediate negative effects on their cognitive development and health status.
Preschoolers In the preschool years, several studies identify a re- lationship between FI and adverse behavioral outcomes and mental health symptoms (Table 2).

Slack et al.

used parents’ responses to the Social Skills Rating System Parent Form28 and found that “food hardship” was as- sociated with both externalizing and internalizing prob- lems among children aged 3 to 5 years.31 Kimbro et al.
found that there were consistently adverse impacts of transitions to FI on teachers’ reports of children’s ex- ternalizing behaviors, self-control, and interpersonal skills.21 In contrast to Zaslow’s findings, 2 other studies identified adverse behavioral/emotional correlates of FI among children during the preschool years, even after control for sociodemographic variables and mothers’ mental health.

Weinreb et al.
Weinreb et al.

reported severe “hunger” was associated with higher levels of children’s in- ternalizing behavior problems.22 Whitaker et al.
found that preschoolers from food insecure households had increased risk of aggressive behavior, anxious/depressed mood, and attention-deficit/hyperactivity.23 School Age An association was also seen between FI and behav- ioral/emotional symptoms among school-aged children (Table 3).24,25,34 Children aged 6 to 13 years in food in- secure households were more likely to miss school and activities and display atypical or borderline emotional symptoms, even if the exposure to FI was intermittent.26 Belsky et al.
also showed an association between FI and childhood anxiety and depression.27 FI also affected other noncognitive skill development, including interpersonal to learning.39 relations, self-control, and approaches Kleinman et al.
found that problems such as aggression and anxiety were more prevalent among children with “hunger.”40 Importantly, Kleinman et al.40 also found a dose-response relationship using C-CHIP scales in which “hungry” children younger than 12 years old were more likely to report previous mental health counseling, com- pared with those “at risk for hunger.” In a study based in Quebec, Canada, Melchior et al.35 also found that food insecure children had higher rates of hyperactivity and inattention.
This finding was corroborated in the United States by Murphy et al., who found higher rates of hy- peractivity, absenteeism, and tardiness among “hungry” children than children reported as “not hungry” and “at- risk of hunger”, and that even intermittent experiences of household food insufficiency and child “hunger” were associated with less optimal behavioral and academic functioning in low-income children.56 Other studies suggested that FI was correlated with a number of mental health-related outcomes and symp- toms.
For instance, Alaimo et al.8 found that 6 to 11 years old children from food insufficient households had a 2-fold increase in likelihood of having seen a psychol- ogist.
In addition, in a longitudinal study covering chil- dren between 4 and 14 years old at recruitment and at 5 and 16 years old at follow-up, Slopen et al.41 found that persistently food insecure school-aged children were 1.5 times more likely than those in never food insecure households to show internalizing behavior and twice as likely to show externalizing behavior.
Children in this study transitioning from food secure to food insecure were also 1.8 times more likely to have externalizing problems at follow-up.

Slack and Yoo31 similarly found that “food hardship” is positively associated with in- ternalizing behavior problems at 6 to 12 years of age.
However, once controls for parental characteristics were added to the analysis, the effect of food hardship dis- appeared, suggesting only an indirect association be- tween food hardship and behavior problems.31 Of note, in contrast to Slopen et al., Slack and Yoo31 did not find a statistically significant association between food in- security and externalizing behaviors among school-aged children.
Concurrent and previous FI has also been found to be correlated at school age with less optimal academic outcomes.

Among children aged 6 to 11 years from food insufficient households, Alaimo et al.
found lower read- ing and arithmetic scores on the Wide Range Achieve- ment Test-Revised (WRAT-R)22 and a higher likelihood of repeating a grade.8 Kleinman et al.40 noted that care- givers of “hungry” school-aged children reported that their children had elevated rates of grade repetition and use of special education services compared with their “at-risk-for hunger” and “non-hungry” peers.
Jyoti et al.42 found that even marginal FI predicted lower test scores in both reading and math among children between kin- dergarten to third grade.
In addition, children whose households transitioned from food secure to food in- secure exhibited worse reading performance, especially food insecure among girls, and the persistence of through third grade was correlated with a delay in reading relative to the effect of FI in kindergarten alone.42 Moreover, the associated decrease in reading scores with kindergarten FI was reversed if a household was no longer FI by third grade.

A cross-sectional study by Winicki et al.


found a trend toward a dose-response relationship between household FI and academic per- formance, with lower math scores obtained with in- creasing levels of FI43; the threshold for a statistically significant effect was marginal food insecurity.

In addi- tion, the gain in math scores from fall to spring was less for children from food insecure households compared with food secure households.
Adolescents As Table 4 summarizes, among adolescents, the major correlates of household FI were psychosocial.

FI was associated with mental health symptoms and diagnoses 140 Food Insecurity with Children Journal of Developmental & Behavioral Pediatrics Copyright 2017 Wolters Kluwer Health, Inc.

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Table 2.
Preschoolers Author Kimbro et al.32 Slack and Yoo31 (see Table 3 for School- Aged) Weinreb et al.33 (see Table 3 for School- Aged) Longitudinal/ Cross- sectional N 5 Study Population, Age Informants Outcome Results Limitations Longitudinal 6300 Early Childhood FI: parents Academic performance: math, Longitudinal Survey- Kindergarten (ECLS-K) and first grade Longitudinal 458 Illinois Families FI: parents reading, and science achievement scores; child behavior: teachers’ rating through Social Skills Rating System (SSRS) Child behavior: parents assessed children through SSRS,28 Parenting Stress Index (PSI)59 Cross-sectional FI: mothers Internalizing behavior/anxiety: mothers assessed children through the Child Behavior Checklist (CBCL)20 Negative impacts of transitions to FI on teachers’ report of children’s externalizing behaviors, self-control, and interpersonal skills.
Persistent FI associated with internalizing behaviors.

“Food hardship” [internalizing and externalizing behavior problems for children 3–5 yr. Parental stress, depression, and warmth mediate FI effects on externalizing behaviors; only parental stress affects in- ternalizing behaviors.

“Hunger” associated with[ levels of internalizing behavior problems.
Data only on children in kindergarten and 1st grade; limited set of covariates Incomplete data on alternative food sources; single-site study; USDA FI scale focuses on household; no discussion of families experiencing VLFS Small sample; cross-sectional; I educational outcomes only among older children Whitaker et al.34 Cross-sectional FI: mothers Child behavior: mothers assessed through CBCL20 subscales aggressive, anxious/depressed, inattentive/hyperactive [ behavior problems in children with [ FI even after adjustment for maternal mental health.
Nonmarital births oversampled; English- or Spanish-speaking mothers only, mothers ,18 yr excluded Study (IFS), 3–5 yr, families transitioning from welfare to work 180 Homeless and low-income mothers and their children; 180 children 2.5–6 yr 2870 The Fragile Families and Child Wellbeing Study, 3 yr V o l .

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Table 3.
School-aged children Longitudinal/ Cross- sectional Cross-sectional N 5 Study Population, Age 3286 NHANES III, children 6–11 yr Author Alaimo et al.8 (see Table 4 for Adolescents) Informants Outcome Results Limitations Food insufficiency: parents Cognitive Function: WIS21 and WRAT-R22; social skills: school records Belsky et al.38 Longitudinal 1116 Environmental Risk FI: parents Longitudinal Twin Study (ERLTS), children 5–12 yr Cognitive function: WISC21; anxiety and depression: Multidimensional Anxiety Scale for children, Children’s Depression Inventory23; emotional problems: Teacher Report Form (TRF) Cross-sectional 216 Children 3–11 yr FI: parents Child Health Related Quality of Casey et al.51 (see Table 4 for Adolescents) Life (HRQOL): parents responded for children 3–8 yr; 9–11 yr responded with parent assistance Child behavior/skill outcomes: teachers asked to report how often student exhibited noncognitive skills Howard et al.39 Longitudinal 4710 Early Childhood FI: parents Longitudinal Survey- Kindergarten (ECLS-K), children 6–13 yr Jyoti et al.42 Longitudinal 21,260 ECLS-K FI: parents Academic performance: children; social skills: teachers Food insufficiency Y reading and arithmetic scores, [ likelihood to have repeated a grade and to have seen a psychologist.
Food insufficiency rather than FI scale used; Mexican and African- Americans oversampled; homeless children excluded FI [emotional problems, but not cognitive or behavior problems after controlling for home environments.

Only twins; not all measures at every data collection; lacked measures of fathers’ characteristics Children in FI households have poorer HRQOL, Yphysical functioning and borderline Ypsychosocial functioning.
FI Y noncognitive skill development; dose-response relationship between FI severity, self-control, and externalizing behaviors; children transitioning from FI in 1st grade to food secure in 3rd grade have large skill impairments persisting through 5th grade.

FI [ impaired academic performance in reading and math for girls and boys; persistent FI through 3rd grade [[[ delay in reading.
Unmeasured covariates; both measures self/proxy reported; exclusion of highest need group by reliance on telephone survey collection; small “n” in some categories No control for age, race/ ethnicity None noted (Table continues , I n c .

 .
& B e h a v o r a i l i P e d a t r i c s Table 3.
Continued Longitudinal/ Cross- sectional Cross-sectional Author Kleinman et al.40 N 5 Study Population, Age Informants Outcome Results Limitations 328 Families with at least 1 child ,12 yrs FI: parents Child behavior: parents through Pediatric Symptom Checklist (PSC)24 Melchior et al.52 Longitudinal 1116 ERLTS, children $5 yr FI: mothers Child behavior: teachers through TRF; mothers through CBCL20 Melchior et al.35 Longitudinal Murphy et al.36 Cross-sectional 1682 Children born in 1997–98 and evaluated at 1½, 4½, and 8 yr 204 Collaborative study of free breakfast program in Philadelphia and Baltimore, children grades 3–8 FI: mothers Mental health symptoms: FI: children and parents parental reports through adapted Preschool Behavior Questionnaire, CBCL,20 and Ontario Child Health Study Scales Psychosocial problems: parents used CBCL,20 PSC; teachers used Conners Teacher Rating Scale-39; investigators used CGAS26; academic functioning: school records of attendance and tardiness Dose-response relationship between “hunger” and special education services, mental health counseling, repeating a grade; “hungry” children [ clinical levels of psychosocial dysfunction, especially aggression and anxiety.
FI [ rates of clinically significant behavioral problems after controlling for maternal mental health.

FI children [ hyperactivity/ inattention but not aggression.

“Hungry” and at risk for “hunger” children 2x more likely to have impaired functioning; [ hyperactivity, absenteeism, tardiness; intermittent food insufficiency and “hunger” associated with poor behavioral and academic functioning.
No control variables All twins; does not analyze sex or twin discordance Excludes twins and persons with major diseases or handicaps; no control for race/ethnicity; 4 part questionnaire for FI rather than USDA scale Sampling bias; “hunger”- related feeding intervention between 1st and 2nd rounds of survey may have influenced parents’ rating of children’s “hunger” Ramsey et al.37 Cross-sectional 185 Families in Y FI: parents Child behavior: parents Children in food insecure Only sampled from lower 5% socioeconomic status (SES) suburbs, children 3–17 yr Strength and Difficulties Questionnaire27 households more likely to miss school/activities, have borderline or atypical emotional symptoms.
of SES of Australians; mailed survey biased against non-English speaking/poor literacy (Table continues) V o l .

3 8 , N o .

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1 4 3 Table 3.
Continued Author Slack and Yoo31 (see Table 2 for Preschoolers) Longitudinal/ Cross- sectional N 5 Study Population, Age Informants Outcome Results Longitudinal 754 Illinois Families FI: parents Child behavior: parents through SSRS,28 Parenting Stress Index (PSI)59 Slopen et al.41 Longitudinal FI: primary caregiver Child behavior: primary caregivers through the CBCL20 Study (IFS), children 6–12 yr, families tran- sitioning from welfare to work 2810 Project on Human Development in Chicago neighborhoods, children 4–14 yr at baseline and 5– 16 yr at follow-up Cross-sectional 228 Children 6–17 yr FI: mothers Weinreb et al.33 (see Table 2 for Preschoolers) Internalizing behavior/anxiety: mothers through the CBCL20; academic performance: Weschler Individual Achievement Test (WIAT)60 screener Winicki et al.43 Longitudinal 21,260 ECLS-K FI: parents Academic performance: compared fall school- administered math test scores to spring scores Limitations (see Table 2) Not validated measure of FI; relatively short observation period with infrequent assessments; incomplete data and loss to follow-up (see Table 2) No control for race/ethnicity Food hardship [ internalizing behavior problems for children 6–12 yr; parental stress, depression, and warmth mediate FI effects on externalizing behaviors, only parental stress affects in- ternalizing behaviors.
Persistent FI [internalizing and externalizing problems; children moving from food secure to insecure had [ externalizing problems at follow-up; caregiver depression significant predictor of internalizing and externalizing problems Children with severe hunger” had 2x [anxiety and depression scores; no relationship between “hunger” and academic achievement; severe “hunger” associated with[ levels of internalizing behavior problems; mothers of children with severe “hunger” [ lifetime diagnosis of PTSD, anxiety, or substance abuse.
Math scores Y with [levels of FI; average gain in math scores from fall to spring $ for children in food secure households , I n c .

 .

 & B e h a v o r a i l i P e d a t r i c s V o l .

3 8 , N o .
3 8 , N o .

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Table 4.
Adolescents Longitudinal/ Cross- sectional (see Table 3) Author Alaimo et al.8 Study Population, Age N 5 2063 National Health and Nutrition Examination Survey (NHANES), 12–16 yr Informants Outcome Results (see Table 3) (see Table 3) Alaimo et al.44 Cross-sectional 754 NHANES III, 15–16 yr Mental health: Diagnostic Interview scale (DIS)61 Food insufficiency: respondent to family questionnaire Casey et al.51 (see Table 3) 183 Children 12–17 yr (see Table 3) FI: person most knowledgeable Longitudinal 22,831 Canadian National Longitudinal Survey of children and youth, 0– 11 yr, 14– 25 yr McIntyre et al.45 McLaughlin et al.46 Child Health Related Quality of Life (HRQOL): children 12– 17 yrs responded on their own Mental health: Center for Epidemiologic Studies Depression Rating Scale (CES-D), General Self Image, Emotional Quotient scale45 Children divided into low-risk and high-risk groups.
Food insecure adolescents did not have YWRAT-R22 or WISC21 scores in either the low- or high-risk FI groups; lower risk food insecure teens [ likelihood to have worse psychosocial outcomes (difficulty getting along with others, having fewer friends); both risk groups more likely to have been suspended from school.
Adolescents from food insecure households: 4x more likely: dysthymia; 2x more likely: thoughts of death; 3.4x more likely: desire to die; 5x more likely: attempted suicide; Food insecure children more likely to report losing and gaining weight without trying; 21% of suicide attempts attributable to FI.

Adolescents 12–17 yr reportedY psychosocial function.
Limitations (see Table 3) Oversampling of Mexican-American and African-American children; sample limited to children 15–16 yrs (see Table 3) Child hunger was robust, Single question used to assess child hunger independent predictor of depression and suicidal ideation in late adolescence and young adulthood; females had [ odds of depression/suicidal ideation in late adolescence/young adulthood.
Cross-sectional 6483 National Comorbidity Survey Replication Adolescent Supplement, 13–17 yr FI: child and parents Mental health: Composite International Diagnostic Interview (CIDI) and parental reports60 Higher or more severe FI is significantly associated with[ odds of any mental disorder in the last year and [ odds of DSM- IV mood, anxiety, behavior, and substance disorders.
Dramatic [in child poverty since survey conduction (2001–2004); underrepresentation of homeless teens; non-English speaking participants; unable to determine if FI is risk or risk marker (Table continues , s m e l b o r p , l a n o i t o m e , h t l a e h r e e p [ .

s m e l b o r p ; [ d a h s t n e c s e l o d a I F .
: : I F d o o h d l i h C y l r a E 0 0 6 8 - s s o r C i D - e l o o P l a n d u i t i g n o L - y e v r u S t h 8 n i n e r d l i h c , ) K - S L C E ( .
, n o i t a l u p o P e g A 5 N / l a n i d u t i g n o L - s s o r C l a n o i t c e s r o h t u A d e u n i t n o C .

4 e l b a T including anxiety, depression, dysthymia, seeing a coun- ideation.
Alaimo et al.8 ob- selor, and having suicidal served that 12 to 16 years olds, even those with a lower background demographic risk whose households expe- rienced food insufficiency, were more likely to have seen a psychologist, been suspended, had difficulty getting along with others, and had fewer friends.
Another study by Alaimo et al.44 found a 4-fold increase in food in- sufficient households in dysthymia as well as an increase in the adolescent’s reported desire to die, history of loss or attempted suicide, and unintentional weight weight gain.

In a Canadian longitudinal study by McIntyre et al.,45 child/youth “hunger” at ages 0 to 11 and 14 to 18 was a predictor of depression and suicidal ideation in late adolescence and young adulthood up to age 25 with a greater impact among females.
Using a sample from the United States, McLaughlin et al.46 similarly described how higher FI in the last 12 months was associated with in- creased odds of any mental disorder and with diagnoses of mood, anxiety, behavior, and substance use disorders over the same period.
Finally, in another study from the United States by Poole-Di Salvo et al.,62 adolescents from food insecure households had higher rates of overall mental health problems, emotional problems, conduct problems, hyperactivity, and peer problems.

SUMMARY levels, In summary, across developed countries, household FI, even at marginal identified by a variety of measures, is associated with children’s behavioral, aca- demic, and emotional problems beginning as early as infancy.
Correlates of FI differ by developmental stage.

Articles that examine infants and toddlers suggest that FI poses a developmental risk, impairs child attach- ment, mental proficiency, and cognitive assessment scores.5,29,30 Studies also demonstrate the impact of temporary FI on subsequent child outcomes.
In pre- school years, studies have found an association between FI, externalizing and internalizing behaviors and mental health symptoms,31–33 and less optimal self-control and interpersonal skills.32 In school-aged children, an asso- ciation is found between FI and impaired academic inattention,34–36 performance, increased hyperactivity, aggressive behavior,34 missing school,36 borderline emotional problems,37 less adaptive interpersonal rela- tions, self-control and approaches to learning,39 more internalizing and greater likelihood of having seen a psychologist.8 In ad- dition, some of the studies demonstrate a dose-response relationship between length of time experiencing FI or level of FI and developmental-behavioral domains in areas such as academic performance, utilization of mental health services, grade repetition, and use of special education services.40,43 Finally, studies involving adolescents indicate associations between FI and anxi- ety,46 depression and suicidal ideation,45 attempted sui- cide,8 dysthymia,8 seeing a counselor,8 suspension from and externalizing behaviors,31,41 146 Food Insecurity with Children Journal of Developmental & Behavioral Pediatrics Copyright 2017 Wolters Kluwer Health, Inc.
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school,8 difficulty getting along with others,8 and sub- stance use disorders.46 DISCUSSION Despite a clear and consistent bivariate association between FI and adverse childhood behavioral, emo- tional, and cognitive function, the exact pathways by which FI may have an impact remains unclear.
Many studies have found that maternal depression is associated with the household’s experience of FI and may partially or fully mediate negative cognitive, be- havior, and mental health–related consequences.30 Par- ticularly, maternal distress, whether a predictor or an outcome of FI, may be associated with childhood de- velopmental and behavioral problems through parental anxiety and parenting behavior, i.e.
“the stresses that accumulate on parents can affect how well they are able to care for their children.”47 In parallel, as noted by Radimer, parents from food insecure families attempt to buffer their children and may deprive themselves of food to allow their children to eat; parental nutritional depri- vation and the constant effort to buffer children may induce parental anxiety and irritability which may in turn affect children.50 This point is further examined in the article by Hernandez and Jacknowitz,5 which found that while temporary FI was associated with a negative im- pact on toddler development, toddlers seem to be buff- ered in families that are persistently food insecure, perhaps because of parents evolving coping strategies to assure children receive an adequate diet.
Alaimo et al.8 suggests that FI may be an independent physiologic predictor of behavioral, emotional, or aca- demic consequences given that going even briefly without food causes irritability, distractibility, and emo- tional changes, which in turn affect children’s achieve- ment scores or psychosocial behaviors.
However, the author also describes another possibility that food in- sufficiency can perhaps be likened to experiences such as homelessness, such that the absence of basic family necessities like food or housing could cause anxiety and other emotional problems in children, even if the mechanism does not result from disrupted physiologic processes.8,47 LIMITATIONS important limitations.
Eleven of Of note, the articles in this systematic review have a number of these studies use cross-sectional8,29,33,34,36,37,40,44,46,51,62 and twelve use longitudinal designs.5,31,32,35,38,39,41–43,45,52,54 Longitudinal studies provide stronger, but not conclu- sive, evidence that FI is on a causal pathway to negative developmental and behavioral outcomes.
Other limi- tations these studies used several of idiosyncratic,8,35,41,44,45 or nonstandard older,33,36,40 versions Security of scale.5,31,34,37,38,46 Some studies on FI are not nationally representative and may not be generalizable to a larger the USDA 18-item Food include that population or to other contexts.
In addition, many of the older articles with relatively small samples describe only bivariate associations, without statistical control for po- tential confounders.8,36,40 Also, although the parents are asked in the USDA Food Security Survey about the fre- quency of providing children a balanced meal, the food security measures do not characterize the nutritional quality of the food, nor the frequency with which chil- dren receive meals in schools and day care center, or the homes of other relatives or friends.
Except for Howard et al., Alaimo et al., Jyoti, et al., Winicki et al., Murphy et al., and Casey et al., all of the articles are limited by shared-method variance, as caregivers report not only FI but all outcomes.39,42–44,51,56 In McIntyre et al.,45 there was some degree of shared-method variance, particularly in the older age group where the youth reported both “hunger” and their symptoms.
In addition, as in much infant research, the infant studies, such as Hernandez et al., are constrained by the fact that standardized assessments used under a year may be insufficiently sensitive to distinguish early developmental differences.53 CONCLUSION The available peer-reviewed literature consistently identifies a bivariate relationship in the United States, Canada, United Kingdom, and Australia between FI and concurrent and future negative developmental and be- havioral outcomes.
In general, multivariate analyses show that this relationship persists but is attenuated after controlling for background characteristics including pa- rental distress, although at least 2 studies find that the relationship is no longer significant after controlling for maternal mental health symptoms.30,31 Clinically obvious malnutrition has visible effects on brain size and structure, but the impact of food in- security without severe anthropometric or biochemical deficits on the developing brain is less well understood.
According to Cook et al., recent research has suggested that the “toxic stress” of FI has adverse consequences for brain architecture,47–49 but no research has yet been performed to confirm or disconfirm this hypothesis.
Whether the mechanisms of effect are direct, indirect, or both, food insecurity in households with children constitutes a preventable and remediable threat to the behavioral and emotional health of children in all stages of childhood, from infancy to adolescence, with addi- tional negative associations with cognitive and academic development identified through school age but not in adolescence.
The Council on Community Pediatrics and the Com- mittee on Nutrition of the American Academy of Pedi- atrics have recommended routine screening for food insecurity at pediatric health maintenance visits.57 From a clinical perspective, findings summarized here also suggest that families presenting to specialty clinics with children for evaluation of developmental and behavioral diagnoses should be screened for FI and conversely that Vol.

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children from families identified by any method as food insecure should be evaluated for developmental and behavioral risk, as well as need for intervention for caregivers’ psychological symptoms.
In the United States, clinicians should be aware of and ensure families are connected with available food assis- tance programs which supplement the diets of parents and children in their homes like Supplemental Nutrition Assistance Program (SNAP, formerly known as food stamps) the Special Supplemental Nutrition Program for Women, Infants, and Children (WIC), and community providers such as food pantries.
In addition, families should be assisted in accessing public child nutrition programs designed to feed children in congregate set- tings, including the National School Breakfast and Lunch Programs, Child and Adult Care Food Program (CACFP), and Summer Food Service Program (SFSP).

Developmental, behavioral, and psychiatric professionals also have a role in addressing parental distress, particularly maternal de- pression, and FI given the potential link of both with ad- verse childhood outcomes.
Although this systematic review begins to explore the relationships cited in the current literature between FI and developmental and behavioral outcomes, there is a need for formal meta-analysis, which will provide a greater understanding of the “strength and consistency of the effects of FI on child outcomes in the social and cognitive domains.”54 Although randomly assigning families to experience FI is clearly neither ethical nor feasible, randomized studies could be performed to de- crease FI by sustained macronutrient or micronutrient supplementation in at-risk families similar to those that have already been performed in the developing world.55 These studies may be useful in evaluating to what extent enhancing a family’s food security may lead to improved behavioral or cognitive outcomes in children.
There are also several suggestive observational but not randomized studies that describe measurable, although not always large, improvements in academic and behavioral out- comes among low-income children who gain access to public nutrition programs.

Notably, there is one study that identifies deterioration among children whose fam- ilies cease receiving benefits.56 There are many other potential areas for multigener- ational research and intervention to address the impact of FI on childhood outcomes.
Family-focused multigen- erational studies that use longitudinal design and explore the dose-response between degree and duration as well as the developmental timing of FI and childhood be- havioral, emotional, and academic outcomes can provide an evidence base for program implementation.
Zaslow et al.30 suggests that we may further extend research by fathers in food insecure examining the impact of households on the development and behavioral out- comes of their children given the potential that FI may affect “depression and parenting in both parents.” In addition, only 3 of the articles analyzed in this systematic review assessed the effects of FI during the sensitive period of brain development of infants, reflecting the need to increase the number of studies undertaken in this population and to extend research to early behav- ioral problems.
The long-term sequelae of experiencing FI in childhood may persist over a lifetime and into the next generation as young adults, who have experienced and may still experience food insecurity, themselves become parents.63 However, multigenerational relation- ships are not well understood; longitudinal studies into young adulthood or old age have not yet been undertaken.
At a policy level, also suggested in a statement by the Council on Community Pediatrics and the Com- mittee on Nutrition of the American Academy of Pe- diatrics, developmental and behavioral professionals can educate policymakers that preventing and reme- diating FI in families with children has the potential to decrease costly adverse developmental and behavioral outcomes in America’s children.57 Although FI is cer- tainly not the sole mechanism by which poverty impacts child development and behavior, it seems to have incremental effects on childhood outcomes after controlling for poverty.
FI is also the most rapidly re- mediable social determinant of child health simply by enhancing public resources for and increasing fami- lies’ access to already available public nutrition pro- grams including WIC, SNAP, CACFP, and school and summer meals.54 Further research could also assess whether the effectiveness on developmental and be- havioral outcomes of these programs would be en- hanced by raising benefits to the levels recommended by the National Academy of Sciences (2013), which are more consistent with the current nutritional science.58 levels Ultimately, in America and other developed nations, the reality that food insecurity remains a pervasive and persistent threat to families and to the developmental and psychosocial health of children does not reflect a lack of informative research, but a failure of politi- cal will.
ACKNOWLEDGMENTS The authors acknowledge the editorial support of Ricky Sharma.

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