CHILD DEVELOPMENT PERSPECTIVES Learning to Eat in an Obesogenic Environment: A Developmental Systems Perspective on Childhood Obesity Leann L. Birch and Stephanie L. Anzman The Pennsylvania State University ABSTRACT—Currently, children are developing in an obesity-promoting, or obesogenic, environment, which has emerged within the past 3 decades. This rapid change provides a rare opportunity to investigate the phenotypic outcomes that result from the expression of human genetic predispositions in a new environment. Unfortunately, the environmental changes that have occurred are associated with epidemic obesity rates in all age groups. Using a developmental perspective, this article argues that this probabilistic outcome is not predetermined, however. The article also provides examples of learning paradigms—familiarization and associative and observational learning—that present opportunities for parents and caregivers to restructure children’s environments in early life, increasing the likelihood of healthy weight-status outcomes in the context of the current obesogenic environment. KEYWORDS—childhood obesity; obesogenic environment; learning; early experience; food preferences; eating behaviors; developmental systems theories Obesity in the United States has increased dramatically since 1980, doubling among adults and tripling among children (Ogden et al., 2006). Young children are included in this The authors thank Mastaneh Sharafi and Brandi Rollins for their assistance in preparing this manuscript. Submitted for publication January 19, 2009; revision received March 18, 2009; accepted March 29, 2009. Correspondence concerning this article should be addressed to Leann L. Birch, The Center for Childhood Obesity Research, The Pennsylvania State University, 129 Noll Laboratory, University Park, PA 16802; e-mail: [email protected]. ª 2010, Copyright the Author(s) Journal Compilation ª 2010, Society for Research in Child Development population, with nearly 25% of 2- to 5-year-olds being overweight (Ogden et al., 2006). Childhood obesity has also reached epidemic proportions worldwide, in developed and developing countries (Lobstein, Baur, & Uauy, 2004). The psychosocial and metabolic comorbidities of childhood obesity begin early, persist into adulthood, and include Type 2 diabetes, hypertension, cardiovascular disease, disordered eating, and social stigmatization (American Academy of Pediatrics [AAP], 2003). Current U.S. health-care costs associated with obesity are estimated at $250 billion per year (Finkelstein, Ruhm, & Kosa, 2005). Given the scope of the problem, preventing childhood obesity has become a priority (Institute of Medicine, 2005). Most prevention efforts have had limited success, focusing almost exclusively on promoting healthy eating and increasing physical activity among school-age children and adolescents (Institute of Medicine, 2007). We argue that waiting until children are school-age misses the best opportunities for prevention. Our argument is focused on the development of children’s food preferences and eating behavior, although we acknowledge the importance of physical activity. Using a developmental systems perspective, we describe how early eating experiences shape behavioral phenotypes and suggest alternative approaches for early obesity prevention. Developmental systems theories (DSTs) posit that phenotypic outcomes are probabilistic; co-actions at multiple levels (e.g., genetic, cellular, physiological, psychological, social, cultural) determine outcomes. Individual trajectories can be altered if any levels of the developing system change enough to trigger a systemic reorganization (Gottlieb, 2002, 2007). Because species tend to stay in broadly stable environments, development can appear to be predetermined. However, experimental evidence, much of which comes from animal models (Harshaw, 2008), demonstrates that a range of seemingly predictable phenotypes (such as species-specific bird calls) can be altered if the speciestypical environment changes. The change from environments Volume 4, Number 2, Pages 138–143 Learning to Eat of scarcity to the obesogenic environment in many societies worldwide provides a rare opportunity to study the effects of dramatic environmental change on human development. For the majority of human history, genetic predispositions to prefer or reject basic tastes and to learn about food and eating evolved and were expressed in environments characterized by food scarcity. In recent years, the food environment has changed markedly in much of the world. The current Western diet is characterized not by food scarcity but by the availability of too much inexpensive, palatable, high-calorie food (Nestle, 2002; Pollan, 2008). During this period of rapid environmental change, we have also seen the emergence of the obesity epidemic, congruent with the developmental systems perspective’s prediction that phenotypic outcomes will be altered by changes in the species-typical environment (Harshaw, 2008). Although these co-occurring changes show that obesity is a more probable outcome in current obesogenic environments than in the environments that historically preceded them, DSTs also tell us that in any environment, individual level outcomes are not predetermined by any one level of the developing system. Development is plastic, and as noted, even in the case of probabilistic outcomes in a given environment, individuals’ developmental trajectories may be shifted toward more adaptive outcomes if a change in one or more levels of the developing system is sufficient to trigger systemic reorganization (Gottlieb, 2002, 2007). Understanding how children’s genetic predispositions affect developing patterns of food preference and intake may reveal opportunities for early obesity prevention, even in ‘‘obesogenic’’ environments. Although changes in the political and economic conditions that have created an obesogenic environment are essential to reversing population trends in obesity (Brownell & Horgen, 2004), the time scale for macroenvironmental change will require decades. Clearly, the obesity epidemic needs to be addressed now. Early interventions to prevent obesity show particular promise, given evidence that alterations in early dietary experience affect developing neural, metabolic, behavioral, and psychosocial systems, resulting in metabolic and behavioral programming (Harshaw, 2008; Levin, 2006; Waterland, 2006). Research shows that prenatal factors, such as maternal obesity and maternal diet, ‘‘program’’ postnatal neural and metabolic systems that affect eating behavior and obesity risk (Levin, 2006; Lucas, Fewtrell, & Cole, 1999). Additionally, there is experimental evidence that mothers’ diets during pregnancy influence their children’s food preferences later in life (Mennella, Jagnow, & Beauchamp, 2001). Another important developmental period is the transition from the exclusive milk diet of infancy to an omnivorous diet that includes a variety of foods. This transition is rapid and dramatic: Milk provides more than 80% of an American 4-month-old’s total daily calories, but by 18 months of age, 80% of the child’s total calories comes from ‘‘table foods’’ (Fox, Reidy, Novak, & Ziegler, 2006). DSTs propose that periods of rapid transition or instability, like the prenatal period and the 139 postnatal dietary transition just described, are ideal points in development for systemic reorganization. Thus, we argue that these are optimal times for preventive interventions and for early learning about food. CONTEXTUAL INFLUENCES ON CHILD FEEDING A focus on early feeding must consider the various contexts that influence the food environments of infants and young children. Most U.S. families have one or two overweight parents, dramatically increasing children’s obesity risk (Whitaker, Wright, Pepe, Seidel, & Dietz, 1997). This increased risk is related to both genetic and environmental factors (i.e., main effects of genetics and environments, and gene–environment interactions and correlations). In early childhood, parents shape children’s eating patterns by determining which foods are available in what amounts, as well as the timing and frequency of feeding. Parents also make choices about whether to breastfeed or use formula and when to introduce solid foods. In addition, they serve as models for children’s eating. Child-feeding practices are also affected by child characteristics and by perceived environmental threats to healthy development (LeVine, 1988). Traditional child-feeding practices evolved across human history in response to food scarcity. Chief among them was intake beyond satiation. However, in the current obesogenic environment, this practice can be maladaptive, promoting overeating and overweight and creating a major threat to children’s health. Feeding practices are influenced by additional macroenvironmental features, such as the cost and availability of food and cultural customs. Likely as a result of complex combinations of these and other influences, certain demographic groups are at higher risk of obesity, including African Americans, Hispanics, and Native Americans, and families with obese parents and lower levels of income and education. Paradoxically, these groups have the greatest need for early preventive interventions but also experience barriers to their effectiveness, as children in these groups tend to have less exposure to healthy lifestyles and thus fewer opportunities to practice what they may learn via an intervention. Future research must therefore investigate ways to address these barriers in order to facilitate use of the learning paradigms presented herein. Although most of the research we review is from U.S. populations, globalization has resulted in the Westernization of many countries’ food supplies and dietary patterns, with accompanying increases in obesity. Thus, this research could be applied in many contexts, with culturally appropriate alterations to feeding interactions. EARLY EXPERIENCE: LEARNING ABOUT FOOD AND EATING The child brings a set of predispositions to early feeding interactions—a preference for sweet and salty tastes, a tendency to Child Development Perspectives, Volume 4, Number 2, Pages 138–143 140 Leann L. Birch and Stephanie L. Anzman reject bitter and sour tastes, and a neophobic rejection of novel foods and flavors. In addition, during prenatal and postnatal development, infants are biologically prepared to learn to eat what is available in the environment (Rozin & Vollmecke, 1986) and to learn food and flavor preferences, initially through familiarization, and later through familiarization and associative and observational learning (Birch, 1999). The current Western diet is obesogenic because it is attuned to these predispositions: Foods and beverages high in sugar and foods with added salt are readily available. Because children learn to prefer and eat what is available, accessible, and being eaten by others, it is not surprising that children’s diets are too high in added sugars, fat, and salt, although their consumption of complex carbohydrates, fruits, and vegetables is well below recommended levels (Kranz, Findeis, & Shrestha, 2008). Whether or not children learn to like and eat their vegetables will depend on the prenatal and postnatal food environments that caregivers create for the expression of children’s predispositions. THREE LEARNING PARADIGMS THAT INFLUENCE CHILDREN’S EATING Familiarization Learning Rheingold (1985) described development in terms of becoming familiar with the world. In familiarization learning, the evaluation of a stimulus increases following an individual’s repeated exposure to it. Aspects of the environment are reflected in phenotypic outcomes, as individuals come to prefer and select those foods that they have repeatedly experienced in their environment. Initially, all foods are unfamiliar, but infants can distinguish among flavors at birth (Mennella & Beauchamp, 1996; Mennella, Nicklaus, Jagolino, & Yourshaw, 2008) and develop flavor preferences quickly. Familiarization learning begins during the prenatal period, when flavors from the maternal diet are present in mothers’ amniotic fluid, and continues postnatally, when these flavors are present in breast milk. Such learning was demonstrated in a study in which infants whose mothers drank carrot juice during either pregnancy or lactation showed greater acceptance of carrot-flavored cereal compared with infants who did not experience either type of familiarization (Mennella et al., 2001). Thus, one potential advantage of breastfeeding is early familiarization with a variety of flavors from the maternal diet (Forestell & Mennella, 2007). Additionally, repeated exposure to a variety of solid foods in infancy enhances the acceptance of fruits and vegetables in childhood (Mennella et al., 2008), and familiarization generalizes to other, similar foods in early life (Birch, Gunder, Grimm-Thomas, & Laing, 1998; Pepino & Mennella, 2005). Repeated exposure continues to affect acceptance and preference for flavors in childhood. When 2-year-old children were exposed to novel fruits and cheeses, preference increased with increased exposure (Birch & Marlin, 1982). Preschoolers who were repeatedly fed tofu prepared one of three ways (sweet, salty, or plain) learned to prefer the familiar version over others (Sullivan & Birch, 1990). Furthermore, repeated exposure to a novel vegetable (red bell pepper) increased school-age children’s consumption, whereas rewarding children for consuming the food did not (Wardle, Herrera, Cooke, & Gibson, 2003). Birch, McPhee, Shoba, Pirok, and Steinberg (1987) also showed that increased preference was contingent on repeated experience with the taste of the food; looking at novel fruits did not affect preference. Familiarization may occur more quickly as additional foods are added to a child’s repertoire and neophobia decreases with further development (Williams, Paul, Pizzo, & Riegel, 2008). Consistent with broader developmental theories related to familiarization learning (Rheingold, 1985) and with the epigenetic framework, individuals learn to like what becomes familiar, highlighting the critical role of food availability. If children have frequent experience with healthy foods in early life, it is possible to promote acceptance of healthier choices, even amidst an abundance of energy-dense foods, changing individual ontogeny toward healthier eating and weight outcomes. Associative Learning In associative learning, an initially neutral stimulus (conditioned stimulus [CS]) begins to elicit responses after repeated pairings with a meaningful stimulus (unconditioned stimulus [UCS]). For example, if a novel food (CS) is followed temporally by nausea and vomiting (UCS), the negative valence of the sickness becomes paired with the novel, previously neutral food, even if the food did not cause the sickness (e.g., Garcia, Kimeldorf, & Koelling, 1955). The food then serves as a cue for the consequences of its ingestion and is subsequently avoided. In a similar fashion, associative learning can also shape children’s food preferences. Conditioned preferences are more common than conditioned aversions and require more CS–UCS pairings. When this type of learning occurs, food cues come to predict the positive postingestive consequences of satiety that result from the ingestion of needed nutrients (Sclafani, 1999, 2001). Most evidence of this was obtained in research with rats (Myers, Ferris, & Sclafani, 2005; Sclafani, 1999, 2001), but young children also learn to prefer foods paired with positive postingestive consequences. When 3- and 4-year-old children had repeated exposure to high- and low-calorie versions of two novel drinks paired with different flavors, their preference increased for the drink flavor paired with the high-calorie version but not for the flavor paired with the low-calorie version (Birch, McPhee, Steinberg, & Sullivan, 1990; Johnson, McPhee, & Birch, 1991; Kern, McPhee, Fisher, Johnson, & Birch, 1993). As noted, learned preferences for energy-dense foods would be adaptive in environments where food is scarce and insufficient energy intake threatens children’s health, but in an obesogenic environment, such preferences can be maladaptive by promoting excessive intake. Child Development Perspectives, Volume 4, Number 2, Pages 138–143 Learning to Eat Children also learn food preferences by associating foods with the social contexts in which they are eaten. Depending on the emotional valence of the context, foods eaten may become more or less preferred. When children were pressured to eat a food (e.g., ‘‘Finish your soup’’) or were offered rewards for eating a food (e.g., ‘‘If you finish your peas, you can watch TV’’), preference and intake of the food decreased (Birch, Birch, Marlin, & Kramer, 1982; Galloway, Fiorito, Francis, & Birch, 2006). Evidence suggests that the use of coercion to promote children’s intake of healthy foods is particularly likely to be counterproductive, producing dislikes. In one retrospective study, young adults reported that the foods they had been coerced to eat as young children were the ones they came to dislike the most (Batsell, Brown, Ansfield, & Paschall, 2002). In contrast, positive social contexts can promote the development of food preferences. In one study, for example, providing food rewards paired with praise and positive attention increased preschool children’s preferences for the foods (initially neutral sweet and nonsweet snacks) used as rewards (Birch, Zimmerman, & Hind, 1980). Positive social contexts can also lead to counterproductive associative learning, however. For example, cultural traditions often dictate the serving of special, highly palatable foods at celebrations. In the United States, this means that cake and ice cream, not peas and carrots, are traditional fare at birthday parties. Such learned associations may also potentiate liking for palatable, energy-dense foods that should be consumed in moderation. Observational Learning Because children usually eat in social contexts, there are many opportunities for children to be influenced by the eating behaviors of others. Observational learning may have positive or negative effects, depending on what models are eating. If adult and peer models are consuming fast foods and sweetened beverages rather than healthier options, they are promoting children’s intake of those foods, with negative effects on diet quality. For example, in one study, French fries, the most frequently consumed vegetable among adults (Block, 2004), were also the most frequently consumed vegetable among 15-month-olds (Fox, Pac, Devaney, & Jankowski, 2004). Models can also have positive effects: For example, a comparative study of mother–daughter beverage choices found that daughters whose mothers drank more milk drank more milk themselves, were more likely to meet dietary recommendations for dairy-related nutrients, and had higher bone density (Fisher, Mitchell, Smiciklas-Wright, Mannino, & Birch, 2004). Adult models can also be effective at increasing children’s willingness to try novel foods (Addessi, Galloway, Visalberghi, & Birch, 2005; Harper & Sanders, 1975; Hendy & Raudenbush, 2000; Highberger & Carothers, 1977). Peers are also effective models (Dunker, 1938; Hendy, 2002; Marinho, 1942); indeed, they can be more effective than adults (Hendy, 2002), as suggested by the social cognitive view that children are most likely to change their behaviors when observ- 141 ing models similar to themselves (Bandura, 1986). In quasiexperimental research, Birch (1980) demonstrated that peer models were effective at altering preschoolers’ vegetable preferences and intake at lunch. After 4 days of observing the peer models choosing and eating vegetables that the observers disliked, observers’ preference for, and intake of, those vegetables increased significantly. Although the use of multiple learning modalities might be particularly effective in changing children’s food preferences, little research has tested this hypothesis. In a rare multimodal study, Jansen and Tenney (2001) examined how children’s preference for a sweetened drink was affected by pairing flavornutrient conditioning with teacher attention and parental modeling. Preference increased only when flavor-nutrient conditioning, teacher attention, and parental modeling were used in combination. Food marketing to children, which employs all three learning modes, provides a powerful demonstration of the potential impact of early learning and experience on children’s food preferences and intake patterns. Children spend 3–5 hr per day watching television, exposing themselves to more than 40,000 television commercials annually, the majority of which feature confectionary, presweetened cereals, and snacks (Vandewater, 2008). Children are repeatedly exposed to the same advertisements (familiarization), in which they witness foods paired with positive social settings and music (associative conditioning) and enjoyed by exuberant and attractive peer models (observational learning). Television advertisements are successful in changing children’s food preferences, requests, and consumption (see McGinnis, Gootman, & Kraak, 2006). Because 90% of food commercials advertise foods high in fat, sugar, and sodium and low in other nutrients (Batada, Seitz, Wootan, & Story, 2008), these findings are particularly problematic with respect to promoting healthier diets to prevent obesity. It is clear that these three learning paradigms could easily lead to preferences for unhealthy foods in the current environment. However, these learning paradigms could also present the potential to shift developmental trajectories, pending conscious efforts to shape children’s environments, so that healthy preferences may be learned when many foods are still unfamiliar. CONCLUSIONS The centrality of early learning and experience in the acquisition of food preferences and eating behaviors points to the pivotal role of children’s eating environments in shaping children’s obesity risk. Research is needed to identify key environmental features that affect early obesity risk by persistently influencing children’s early learning and experience with food and eating. Increasing the availability and accessibility of healthy nutrientdense foods early in life is one promising avenue to altering phenotypic outcomes by means of the learning paradigms reviewed herein. The emergence of new phenotypes is particularly likely during developmental transitions, including the prenatal period Child Development Perspectives, Volume 4, Number 2, Pages 138–143 142 Leann L. Birch and Stephanie L. Anzman and the rapid and dramatic dietary transition that occurs in infancy and early childhood. The potential plasticity of food preferences and intake patterns during the first years of life provides relatively unexplored opportunities for influencing development during a transition when phenotypic patterns of preferences and intake can be ‘‘built into our bodies’’ (Hougan, 2008; Shonkoff & Phillips, 2000), affecting subsequent neural, behavioral, and metabolic outcomes, and potentially leading to overall systemic reorganization as developing children continue to choose and consume healthier food options within an overall obesogenic context. Systemic reorganization toward healthier phenotypic outcomes can be facilitated by targeting multiple levels of the developing system simultaneously. Parents’ decisions about what to feed their children are affected by food marketing, availability, cultural traditions and preferences, and the relatively higher costs of fruits and vegetables compared with those of energy-dense foods (Caprio et al., 2008), all of which are potential macrolevel barriers to parents’ exposing their children to healthy foods early in life. Likely as a result of complex combinations of these and other influences, certain demographic groups are at higher risk for obesity, including African Americans, Hispanics, and Native Americans, as well as families with obese parents and lower levels of income and education. These groups seem particularly likely to not only experience the various barriers just described but also to lack opportunities for the modeling necessary to promote the early liking of healthy foods. 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