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Corby K. Martin, F. Joseph McClernon, Anastasia Chellino, and John B. Correa ...... Halford JC, Boyland EJ, Hughes GM, Stacy L, McKean S, Dovey TM.
Chapter 49

Food Cravings: A Central Construct in Food Intake Behavior, Weight Loss, and the Neurobiology of Appetitive Behavior Corby K. Martin, F. Joseph McClernon, Anastasia Chellino, and John B. Correa

Abbreviations EMA FCCQ-T FCI FCI-J FCQ-S FCQ-T OCQ QCSRF

Ecological momentary assessment Food Chocolate Craving Questionnaire – Trait Food Craving Inventory Food Craving Inventory for Japanese Food Craving Questionnaire – State Food Craving Questionnaire – Trait Orientation to Chocolate Questionnaire Questionnaire on Craving for Sweet or Rich Foods

49.1  Introduction Food craving studies appeared infrequently in the scientific literature until the mid-1980s and important studies on the phenomenology and prevalence of food cravings were conducted in the 1990s. Over the last decade, there has been an increase in food craving research that was likely influenced by the development of new methods to measure food cravings and associated phenomena, such as brain activation. Further, the rise in obesity prevalence led scientists to investigate factors that affect food intake behavior and the association between food cravings and food intake was a logical area of research. The purpose of this chapter is to review the food craving literature and explore the associations between food cravings and food intake, body weight, dieting, and brain activation.

49.2  Food Craving Definition and Etiology The construct of food craving, as well as its definition, has been influenced by research on drug abuse and addiction. Kozlowski and Wilkinson (1987) reviewed the substance abuse literature and concluded that a proper definition of craving requires that the substance be intensely desired. White C.K. Martin (*) Ingestive Behavior Laboratory, Pennington Biomedical Research Center, 6400 Perkins Rd., Baton Rouge, LA, USA e-mail: [email protected] V.R. Preedy et al. (eds.), Handbook of Behavior, Food and Nutrition, DOI 10.1007/978-0-387-92271-3_49, © Springer Science+Business Media, LLC 2011

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et al. (2002) considered this recommendation and defined a food craving as “an intense desire to consume a particular food that is difficult to resist.” Other authors also noted that food cravings represent a strong desire to consume a food (Cepeda-Benito et al. 2000b), and people who report food cravings indicate that it can be difficult to resist eating food in response to cravings. Food cravings differ from hunger by at least one important feature: consumption of a specific food is believed to alleviate food cravings, while consumption of many different types of foods alleviates hunger (Pelchat and Schaefer 2000). The etiology of food cravings has been the subject of considerable debate. It has been hypothesized that food cravings are elicited by a nutrient deficiency or food restriction (Weingarten and Elston 1990). This hypothesis appears logical, but it is not supported by scientific evidence. If this hypothesis were true, food cravings should increase during weight loss diets, yet they decrease (Harvey et al. 1993; Lappalainen et al. 1990; Martin et al. 2006, 2008a) or are unaffected (Gilhooly et al. 2007) by weight loss diets. Further, restriction of certain types of foods results in a decrease, not an increase, in craving for the restricted foods (Martin et al. 2008a), and food deprivation is not a necessary condition for the occurrence of food cravings (Hill et al. 1991). Lastly, nutritional deficiencies are not associated with food cravings, and people crave foods high in certain nutrients, while failing to crave other foods with higher levels of the same nutrient (Weingarten and Elston 1990). This evidence indicates that the etiology of food cravings is not heavily influenced by nutritional deficiencies or food restriction. The role of conditioning in the etiology of food cravings, however, has gained empirical support. Food cravings can develop from pairing consumption of certain foods with hunger, suggesting that food cravings are a conditioned expression of hunger (Gibson and Desmond 1999). In the Gibson and Desmond study, individuals assigned to eat chocolate only when hungry developed greater craving for chocolate over a 2-week period, but chocolate cravings decreased among individuals assigned to only eat chocolate when full. Similarly, the biopsychosocial theory of food cravings suggests that food cravings can also develop by pairing food intake with other conditions, such as physical locations (watching a movie) or internal states (emotional arousal or dysphonic mood) (Rogers and Smit 2000). Conversely, conditioning also appears to influence the development of food aversion. Food aversion during pregnancy appears to be the result of pairing consumption of certain foods with nausea (Bayley et al. 2002; Fairburn et al. 1992). The conditioning model of food cravings is consistent with the above noted finding that food restriction does not increase, and frequently decreases, food cravings (Harvey et al. 1993; Lappalainen et al. 1990, Martin et al. 2006, 2008a). This may occur for a number of reasons. First, when certain foods are restricted during diets, there are limited opportunities to pair consumption of those foods with stimuli that precipitate eating behavior, which limits the development of food cravings. Second, stimuli that once elicited food cravings would no longer be followed by consumption of the craved food, and existing cravings would diminish in frequency or intensity due to extinction. Although the conditioning model of food craving etiology has been supported by experimental evidence (Gibson and Desmond 1999) and the results of trials that involved food restriction (Harvey et  al. 1993; Lappalainen et al. 1990; Martin et al. 2006, 2008a), additional research is warranted to further explicate the role of conditioning in food craving etiology.

49.3  Assessment of Food Cravings Food cravings can be quickly and affordably measured by self-report inventories. Studies prior to 2000 primarily relied on instruments created to measure cravings for specific studies, and the psychometric properties of many of these instruments were not thoroughly examined. In recent years,

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Table 49.1  List of self-report inventories designed to quantify food cravings, including the type of cravings measured (general craving vs. cravings for specific types of foods), if the questionnaire measures state or trait cravings, and the reference article Type of craving Trait or state cravings Questionnaire General Specific Trait State Reference FCQ-T x x Cepeda-Benito et al. (2000b) FCQ-S x x Cepeda-Benito et al. (2000b) FCCQ-T x x Rodriguez et al. (2007) FCI x x White et al. (2002) FCI-J x x Komatsu (2008) QCSRF x x Toll et al. (2008) OCQ x x Cartwright and Stritzke (2008) Note. Abbreviations: FCQ-T Food Craving Questionnaire – Trait, FCQ-S Food Craving Questionnaire – State, FCCQ-T Food Chocolate Craving Questionnaire – Trait, FCI Food Craving Inventory, FCI-J Food Craving Inventory for Japanese, QCSRF Questionnaire on Craving for Sweet or Rich Foods, OCQ Orientation to Chocolate Questionnaire

however, inventories have been developed and validated to measure many aspects of cravings, including cravings for specific types of foods (White et al. 2002) and state and trait food cravings (CepedaBenito et al. 2000b). Furthermore, at least two of these instruments have been modified to measure food cravings in non-English speaking samples (Cepeda-Benito et al. 2000a; Komatsu 2008). The properties of existing self-report instruments to measure food cravings are reviewed here in the order in which the first version of the instrument was published. Additionally, Table 49.1 provides a summary of the characteristics of the inventories.

49.3.1  F  ood Craving Questionnaire – Trait (FCQ-T) and State (FCQ-S) Versions The Food Craving Questionnaire has two forms to measure trait (FCQ-T) and state (FCQ-S) food cravings (Cepeda-Benito et al. 2000b). Ratings for the FCQ-T are made on a six-point scale, with “Never” scored as 1 and “Always” scored as 6. Ratings for the FCQ-S are made on a five-point scale, with “Strongly disagree” scored as 1 and “Strongly agree” scored as 5. The FCQ measures the phenomenological aspects of food cravings, and does not measure cravings for specific foods. The FCQ-T includes nine subscales used to measure trait cravings: intention and planning to consume food, positive reinforcement resulting from eating, negative reinforcement resulting from eating, lack of control of eating, preoccupation with foods, craving as a physiological state, emotions caused by cravings, environmentally induced cravings, and guilt-triggered cravings. The FCQ-S measures state cravings or cravings that are occurring “at this moment.” The FCQ-S has five subscales: desire to eat, positive reinforcement from eating, negative reinforcement from eating, lack of control of eating, and craving as a physiological state. The subscales of the FCQ-T exhibit acceptable test-retest reliability coefficients (0.72–0.88). The FCQ-S has lower test-retest reliability coefficients (0.40–0.63), reflecting the expected instability of state cravings (Cepeda-Benito et al. 2000b). Both the FCQ-T and FCQ-S have adequate internal consistency (coefficient-alpha 0.81–0.94) and discriminant validity (Cepeda-Benito et al. 2000b). The validity of a Spanish language version of the FCQ has also been supported (CepedaBenito et al. 2000a).

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49.3.2  Food Chocolate Craving Questionnaire-Trait (FCCQ-T) The Food Chocolate Craving Questionnaire-Trait (FCCQ-T) (Rodriguez et al. 2007) is a modified version of the Food Craving Questionnaire-Trait (FCQ-T) (Cepeda-Benito et  al. 2000b). The FCCQ-T utilizes nine subscales similar to the FCQ-T, but the questions within these subscales are specific to chocolate cravings. Both English (coefficient-alpha 0.76–0.92) and Spanish (coefficientalpha 0.69–0.90) versions of the FCCQ-T have adequate internal consistency, a stable factor structure, and support for their construct validity (Rodriguez et al. 2007).

49.3.3  Food Craving Inventory (FCI) The FCI measures cravings for specific types of foods by asking respondents to rate the frequency of cravings over the previous month for 28 food items (White et al. 2002). Ratings are made on a fivepoint scale ranging from “Never,” scored as 1, to “Always/almost every day,” scored as 5. Higher scores indicate more frequent food cravings. The FCI has four scales that constitute the higher-order construct of food craving, which is represented by the total score. The four scales are: sweets (e.g., brownies, ice cream), high fats (e.g., bacon, fried fish), carbohydrates/starches (e.g., baked potatoes, pasta), and fast-food fats (e.g., pizza, French fries). The FCI has acceptable internal consistency (coefficient-alpha 0.76–0.93) and test–retest reliability coefficients (0.79–0.91), and a stable factor structure (White et al. 2002). Lastly, a state version of the FCI is undergoing validation. This version of the FCI measures cravings for specific types of foods that are occurring “at this moment.”

49.3.4  Food Craving Inventory for Japanese (FCI-J) The FCI was modified to measure food cravings in Japanese females by removing food items unfamiliar to Japanese culture and adding items eaten in Japan. The resulting FCI-J (Komatsu 2008) was validated in samples of Japanese female undergraduate students, and the following five-factor model was supported: sweets, snacks, western foods, sushi, and rice (Komatsu 2008). Support was found for the reliability and validity of the FCI-J and it serves as a valuable tool to quantify culture-specific aspects of food cravings.

49.3.5  Questionnaire on Craving for Sweet or Rich Foods (QCSRF) The QCSRF measures cravings for sweet or rich foods in smokers. The QCSRF has nine items and a two-factor structure (Toll et al. 2008). The first factor (Relief/Control) assesses the expectation that sweet or rich foods will alleviate negative affect and perceptions of self-control over eating. The second factor (Intensity) measures the intensity of cravings. Higher scores on the Relief/Control factor indicate greater endorsement that the food may relieve negative affect and lower self-control over eating. Higher scores on the Intensity factor indicate more intense cravings. Both factors of the QCSRF show adequate internal consistency (coefficient alpha = 0.87–0.90). The Intensity scale was positively correlated with weight gain from previous attempts to quit smoking (Toll et al. 2008).

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49.3.6  Orientation to Chocolate Questionnaire (OCQ) The OCQ is a 14-item self-report inventory that measures three dimensions of chocolate cravings: avoidance of chocolate, approach to chocolate, and guilt related to chocolate consumption. Agreement with each item is rated using a Likert scale (1 = “not at all” to 9 = “very strongly”) (Cartwright and Stritzke 2008). When administered to young adults, the three dimensions of the OCQ were found to differentially correlate with frequency and quantity of chocolate consumption, supporting its concurrent validity (Cartwright and Stritzke 2008).

49.4  Food Craving Prevalence The estimated prevalence of food cravings varies among studies and the discrepant estimates are likely due to the use of different definitions and methods to measure food cravings, as well as demographic differences among the study samples. Nevertheless, there is a consensus that food cravings are common, and occur in 58–97% of adults sampled from industrialized countries (Gendall et al. 1997; Weingarten and Elston 1991). More women report food cravings than men (Weingarten and Elston 1991), and food cravings and food intake increase during the luteal phase of the menstrual cycle (Dye and Blundell 1997; Johnson et al. 1994). The majority of pregnant women report food cravings, primarily for sweet foods (chocolate, fruit, fruit juice, etc.) (Bayley et al. 2002; Fairburn et al. 1992). People report approximately 3–4 food cravings per week (Hill and Heaton-Brown 1994; Hill et  al. 1991), with the majority of food cravings occurring in the evening (Hill et  al. 1991). Craved foods are frequently high in energy density and fat (Gilhooly et al. 2007), and the most frequently craved food in industrialized countries, particularly among women, is chocolate (Weingarten and Elston 1991). Indeed, the majority (90%) of people who report cravings crave chocolate; further, chocolate cravings comprise 49–60% of food cravings (Hill and Heaton-Brown 1994; Hill et al. 1991).

49.5  The Association Between Food Cravings, Hunger, and Food Intake Conceptual differences exist between food cravings and hunger (Pelchat and Schaefer 2000), though the two constructs are associated with each other (Cepeda-Benito et al. 2000b; Steel et al. 2006; White et al. 2002). Food cravings are believed to precipitate eating behavior (Weingarten and Elston 1990) and frequently result in consumption of the craved food (Hill and Heaton-Brown 1994; Weingarten and Elston 1991). Among females diagnosed with bulimia nervosa, food cravings can also precipitate binge eating (Waters et al. 2001), which implies that a large amount of food can be ingested in response to food cravings. In other samples and in laboratory settings, however, it appears that food cravings do not always lead to the consumption of a large amount of food (Martin et al. 2008b), though additional research is needed to more thoroughly explore the amount of food eaten in response to food cravings in naturalistic settings. In the laboratory, cravings for specific types of foods were associated with consumption of similar foods (Martin et al. 2008b). In this study, the association was examined between the four scales of the FCI and consumption of M&M’s® chocolate candies, jelly beans, regular (high-fat) potato chips, and low-fat potato chips. The sweets scale correlated significantly with intake of jelly beans and M&M’s®, and the high fats scale correlated with intake of regular potato chips, but not low fat chips (Table 49.2).

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Table 49.2  Pearson correlation coefficients between food craving (FCI scales) and consumption (g) of specific foods (Reprinted from Martin et al. (2008b, p. 325). Copyright 2008, with permission from Elsevier) Grams consumed FCI scales Baked Lay’s® Jelly beans Regular Lay’s® M&M’s® Total intake High fats −0.04 −0.03 0.27** 0.16 0.13 Sweets 0.01 0.20* 0.13 0.19* 0.20* Carbohydrates 0.02 0.10 0.14 0.13 0.14 Fast food fats 0.06 0.05 0.13 0.18* 0.15 Total score 0.01 0.13 0.23* 0.23* 0.22* Note. *p < 0.05, **p < 0.01 (1-tailed)

49.6  The Association Between Food Cravings and Body Mass The association between food cravings and food intake suggests that food cravings might also be associated with body mass, and evidence suggests that this is the case. Food cravings are associated with body mass index among people diagnosed with type 2 diabetes (Delahanty et al. 2002). Further, obesity is associated with cravings for high fat foods (White et al. 2002), and obesity is associated with sweet cravings among people diagnosed with binge eating disorder (White and Grilo 2005). Weight loss diets reduce food cravings, but no robust relations have been found between baseline levels of cravings or change in cravings and weight loss (Martin et al. 2006). People who lose more weight during a diet, however, do not indulge in cravings as frequently as those who lose less weight (Gilhooly et al. 2007). Despite the lack of scientific evidence suggesting that food cravings are associated with weight loss treatment outcome, participants most frequently reported food cravings as the reason for failing to adhere to a diet during controlled feeding studies (Hall and Most 2005). Therefore, clinicians are encouraged to explore peoples’ beliefs and fears about food cravings before and during weight loss treatment. Research is also warranted to determine the temporal relation between food cravings and food intake or poor adherence to dietary recommendations. This research is possible with the use of ecological momentary assessment (EMA) methodology (Stone and Shiffman 1994), which utilizes communication technology (e.g., cell phones, Smartphones) to collect data from participants in real-time while they reside in their natural environment. EMA data can be used to identify the antecedents and consequences of behavior without relying on retrospective recall, which can introduce bias.

49.7  T  he Effect of Dietary Restraint, Food Restriction, and Dieting on Food Cravings The effect of food restriction and dieting on food cravings is an important consideration in the etiology of cravings. Furthermore, anecdotal reports from clinical settings suggest that people frequently believe that food restriction during dieting will increase food cravings, and fear of increased food cravings can affect the likelihood of enrolling in a weight loss program. Research in this area has been complicated by a number of factors, such as the use of different methods to measure food cravings and induce food restriction, and studies appear to produce discrepant findings. The seemingly discrepant findings are not necessarily incompatible, however, as described in this section.

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49.7.1  Dietary Restraint and Food Cravings Dietary restraint is measured with self-report questionnaires and refers to the intent to restrict caloric intake, though people that report high levels of dietary restraint are not necessarily in energy deficit or losing weight (Stice et al. 2007). Dietary restraint has been found to be associated with the development of binge eating pathology (Field et al. 1999) and obesity onset (Stice et al. 2005), particularly among adolescent or college-aged female samples; therefore, dietary restraint is an important construct worthy of investigation. Cross-sectional studies provide mixed support for an association between self-reported dietary restraint and food cravings. Some (Hill et al. 1991) but not all (Rodin et al. 1991) studies report a significant association between dietary restraint and food cravings.

49.7.2  Short-Term Food Restriction The effect of short-term food restriction was examined in at least two studies that enrolled samples of college-aged females (Coelho et al. 2006; Polivy et al. 2005). In one study, restrained and unrestrained female participants were assigned to a chocolate deprivation, vanilla deprivation, or no deprivation condition for 1 week (Polivy et al. 2005). Deprivation had no effect on reported food cravings, but restrained participants in the chocolate deprivation condition ate more chocolate than restrained and unrestrained participants in the other groups (Polivy et al. 2005). In another study, female undergraduates were randomly assigned to a carbohydrate restriction, protein restriction, or no restriction control group for 3 days (Coelho et al. 2006). Carbohydrate restriction was associated with more carbohydrate cravings during the study and increased carbohydrate intake during a food intake test. Protein restriction was associated with more cravings for protein-rich foods, but was not associated with increased protein intake during the food intake test (Coelho et al. 2006). These studies provide important data on short-term restriction of certain types of food and the study designs merit discussion. First, as previously noted, the studies measured changes in cravings that occurred over the short-term (days) in response to food restriction. Second, although neither energy balance nor weight change were measured, it is unlikely that participants would have experienced a significant energy deficit or weight loss if they followed the study instructions. These details and study strengths are important when considering the effects of dieting/weight loss on food cravings, as outlined in the following section.

49.7.3  F  ood Restriction During Diets Marked by Energy Deficit and Weight Loss Food restriction and dieting, which is marked by energy deficit and weight loss, decreases food cravings (Harvey et al. 1993; Lappalainen et al. 1990; Martin et al. 2006, 2008a). However, some studies find that dieting increases (Pelchat and Schaefer 2000) or has no effect on food cravings (Gilhooly et al. 2007). More restrictive diets result in larger reductions in food cravings (Harvey et  al. 1993; Lappalainen et al. 1990; Martin et al. 2006), as illustrated in Fig. 49.1, and food cravings remain suppressed even after a varied diet is restored following a restrictive monotonous diet (Fig. 49.2). Recent evidence also suggests that the macronutrient content of the diet affects changes in cravings

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Fig. 49.1  Change in food cravings (estimated marginal means), measured with the Food Craving Inventory (FCI), from baseline (BL) to week 12 of a food-based low calorie diet (LCD) and very low calorie diet (VLCD) that relied on liquid shakes for the first 12 weeks. The VLCD group demonstrated significantly larger decreases on all craving scores compared to the LCD group (p < 0.01) (Reprinted from Martin et al. (2006, p. 119). Copyright 2006, with permission from Nature Publishing Group)

Fig. 49.2  Mean Food Craving Inventory (FCI) scores of VLCD participants who completed an FCI at baseline, VLCD Weeks 6 and 12, and Refeeding Week 6. By Refeeding Week 6, participants had transitioned off of liquid shakes and were consuming a solid food-based diet. All FCI scores decreased significantly between baseline and VLCD Week 6 and did not change significantly thereafter. Additionally, all FCI scores were significantly lower at all three dieting points than at baseline (Reprinted from Martin et al. (2006, p. 119). Copyright 2006, with permission from Nature Publishing Group)

for specific types of foods. Over 2 years, a low-fat diet reduced cravings for high-fat foods, while a low-carbohydrate diet reduced cravings and preferences for foods high in carbohydrate (Martin et al. 2008a). These results indicate that restricting consumption of certain types of foods results in decreased cravings and preferences for the restricted foods. Although the effect of weight loss on food cravings might appear counterintuitive, it provides some support for the conditioning model of food craving etiology, as previously discussed. The effect of dieting on hunger levels should also be considered in interpreting these findings. Hunger is

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unchanged or reduced during dieting (Rosen et al. 1982) and more restrictive diets result in larger decreases in hunger (Wadden et al. 1987). These results suggest that dieting has similar effects on food cravings and hunger, which is not necessarily surprising since hunger and food cravings are associated with each other (Cepeda-Benito et  al. 2000b; Steel et  al. 2006; White et  al. 2002). Moreover, these findings can guide research to identify the mechanism by which food cravings decrease during dieting. For example, it has been hypothesized that change in hunger mediates the relation between dieting and change in food cravings (Martin et al. 2006), but this hypothesis has not been fully tested. The studies reviewed in this section provide data on the course of food cravings (and hunger) during long-term (weeks to years) food restriction in the context of weight loss diets. It is unclear, however, if similar food craving reductions would be observed when certain types of foods are restricted and weight is maintained. Moreover, change in food cravings over the short-term (days) was not thoroughly assessed in the studies reviewed in this section. The studies reported by Polivy et al. (2005) and Coelho et al. (2006) suggest that short-term food restriction during energy balance might have very different effects on food cravings, and this is an area worthy of future investigation. Moreover, the possibility that change in hunger might mediate the relation between dieting and food craving change requires examination.

49.7.4  Reconciling the Empirical Findings To summarize, there is mixed support for an association between self-reported dietary restraint and food cravings, and the effect on food cravings of short-term food restriction, which is not likely associated with an energy deficit or weight loss, is inconsistent. Longer-term food restriction that is accompanied by a significant energy deficit and weight loss is associated with a decrease in food cravings. Although these findings appear discrepant, they are not necessarily incompatible when the following issues are considered. First, the dietary restraint studies, which inconsistently found an association between restraint and food cravings, were primarily cross-sectional and when an association was found the magnitude of the association was modest (Hill et al. 1991). Additionally people who report high levels of dietary restraint are not necessarily in energy deficit or losing weight (Stice et al. 2007). In some samples, dietary restraint is predictive of pathological eating behavior. Therefore, the investigation of food cravings and dietary restraint is warranted, but equating dietary restraint with dieting marked by weight loss is not supported by the research and, similarly, the results from studies on food cravings and dietary restraint will not necessarily be reflective of findings from studies where food cravings were assessed during weight loss. Second, important differences exist between the studies on short-term food restriction and longerterm food restriction that is also accompanied by weight loss. Participants in the short-term food restriction studies were young college-age females who were presumably not actively losing weight during the study. These samples also appeared to be relatively lean or healthy weight, with a smaller proportion of the samples being overweight or obese. Importantly, these studies measured food cravings in the days following food restriction. The longer-term food restriction studies involved an energy deficit sufficient of promoting significant weight loss and relied on samples of predominantly middle-aged overweight/obese males and females. These studies are limited, however, because they rarely included assessment of craving change after only a few days of food restriction or energy deficit. Consequently, it is possible that food cravings remain stable or increase in the days following the onset of food restriction and energy deficit, and subsequently decrease.

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Fig. 49.3  Key features of food cravings

Third, very few studies used the same instrument to measure food cravings, making comparisons among studies problematic. As outlined in this chapter, inventories are available that have good support for their factor structure and psychometric properties. Investigators are encouraged to rely on these or other instruments whose reliability and validity has been supported in future research. Moreover, the cited studies relied on mostly retrospective reports of craving (e.g., questionnaires filled out at weekly sessions). Ecological momentary assessment (EMA) studies should be conducted to more precisely evaluate the temporal course of food craving in the context of ad libitum and restricted food intake. Although it is difficult to compare the results among some studies due to their differences, these differences demonstrate the importance of each type of study and the how the results can guide future research. For instance, it appears food restriction in the absence of an energy deficit or weight loss has a limited or inconsistent effect on food cravings, while the degree of calorie restriction during weight loss diets appears to be associated with the degree to which food cravings decrease. The findings indicate that future research is needed to quantify the extent to which cravings are affected by: (1) longer-term restriction of specific types of foods during weight maintenance and (2) restriction of specific types of foods during diets that vary in the size of the energy deficit or magnitude of weight loss. Our results suggest that both the degree of energy restriction (Martin et al. 2006) and the macronutrient content of the restricted foods (Martin et al. 2008a) have a direct impact on craving reductions, yet the relative contribution of each manipulation is unknown. Key features of food cravings are summarized in Fig. 49.3.

49.8  Neurobiology of Food Cravings Exposure to visual and/or olfactory cues associated with preferred foods can elicit craving for those foods. Cues have been shown to drive appetitive behavior (Jansen 1998) and are used to great advantage by advertisers (Halford et al. 2008). Even non-food visual cues (e.g., fast food restaurant logos) can become associated with food reward and promote consumption (Robinson et al. 2007), demonstrating the role of conditioning in appetitive behavior. Recently, neuroimaging studies have demonstrated that exposure to food cues results in activation of a network of brain regions subserving attention, appetitive motivation, and reward (Killgore et al. 2003; LaBar et al. 2001; Simmons et al. 2005; Stoeckel et al. 2008; St-Onge et al. 2005; Wang et al. 2004). At a functional level, this network evaluates information about the potential reward value of environmental cues and initiates behavioral responses aimed at obtaining and consuming food. Specific nodes of this network include the

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ventral striatum, which is involved in reward signaling, prefrontal cortex areas involved in the initiation and control of behavior, memory areas including the hippocampus, and regions involved in both stimulus driven and willful attention including the anterior cingulate cortex and fusiform gyrus. Interestingly, exposure to visual cues activates brain regions that are also activated by taste stimuli including the orbitorfrontal cortex and operculum-insula (Rolls 2006). Activation in these regions in response to visual cues (in the absence of taste cues) suggests that visual food information potentially modulates taste and other gustatory information processing. The specific neural underpinnings of food craving are beginning to be elucidated. In a recent study, brain responses to chocolate taste and visual cues were examined in women who endorsed being cravers or noncravers of chocolate (Rolls and McCabe 2007). Compared to noncravers, cravers exhibited greater activation in response to the sight of chocolate in the orbitorfrontal cortex and ventral striatum, and greater activation to the combined taste and sight of chocolate in the anterior cingulate cortex. In addition to identifying neural correlates of specific food preferences, neuroimaging techniques have been used to examine brain activation during imagining craved foods versus imagining a monotonous diet among subjects who just completed a 2-day bout of a monotonous diet. Compared to individuals who maintained their normal diet, individuals on the monotonous diet exhibited greater activation while imagining liked foods in the hippocampus, insula, and the caudate nucleus (part of the dorsal striatum) (Pelchat et al. 2004). The studies above provide a first look at the neurobiological basis of food craving. Neuroimaging studies suggest that food cravings appear idiosyncratic and distinct from the subjective experience of hunger. Thus, the findings of the above studies should be considered distinct from those that have examined brain responses to cues depicting foods generally agreed to be appetitive (e.g., donuts, hamburgers) since such foods may not be craved universally (Killgore et al. 2003; Stoeckel et al. 2008). For similar reasons they are distinct from studies which have evaluated the effects of food deprivation and/or overfeeding on brain responses to food cues (Cornier et al. 2007; LaBar et al. 2001; Siep et al. 2009) since these studies manipulate hunger, not necessarily craving. The extant data thus suggest that exposure to imagined or actual craved foods increases activation in brain regions subserving reward, motivation, and memory. Additional work is necessary to evaluate whether dietary interventions change brain responses to craved foods and whether this modulation can be delineated from those caused by changes in hunger. Asked another way, does the neural circuitry that underlies food craving differ from that underlying hunger and do the two overlap? To the degree that food craving might represent a “liking” of food rather than “wanting,” it could be hypothesized that food craving would elicit activation of reward regions (e.g., ventral striatum), whereas hunger would elicit activation of areas subserving compulsive responding (e.g., dorsal striatum). Regions involved in the selection, planning, initiation, and control of behaviors may serve as a final common pathway of both circuits. Additional studies that specifically manipulate both craving and hunger will be necessary to address this question.

49.9  Treatment of Food Cravings Food cravings are frequently addressed or treated in the context of weight management programs, where techniques are used to reduce the frequency and severity of food cravings and to minimize subsequent food intake. This approach relies on cognitive-behavioral techniques, including distraction and confrontation (Brownell 2000). Patients are also trained to distinguish the difference between food cravings and hunger, and to identify situations or stimuli that elicit food cravings. Once these stimuli are identified, the antecedents and consequences of food cravings and subsequent

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food intake can be evaluated and cognitive-behavioral techniques can be used to modify these contingencies. For example, if watching a movie in the evening is associated with a craving for popcorn, patients can prepare and be trained to use relaxation or distraction techniques during the movie to avoid eating popcorn until the food craving diminishes. Assuming the patient successfully avoids eating popcorn during movies, the association between movie watching and cravings will decrease over time. Stimulus control techniques can also be utilized, and stimuli that elicit food cravings can be avoided. The relation between food cravings and hunger, and the theory that food cravings develop from pairing food intake with external or internal stimuli (e.g., hunger, physical locations, emotions) (Gibson and Desmond 1999; Rogers and Smit 2000) suggest that following a healthy meal plan (three meals per day with planned snacks) and managing hunger will reduce the frequency of food cravings. Other aspects of following a healthy meal plan are also hypothesized to reduce food cravings, such as eating in the same location in the absence of other stimuli, e.g., television or music. The finding that food cravings decrease during weight loss diets, during which participants follow a healthy meal plan (Martin et al. 2006, 2008a), supports this hypothesis, but the effect of meal regulation and hunger management in the absence of weight loss is unclear. Indeed, understanding the independent effects of energy deficit/weight loss and meal regulation/hunger management on food cravings would significantly improve our understanding of the etiology of food cravings and how to most effectively address them. Acceptance-based approaches (Hayes et al. 1999) can also be used to cope with food cravings. This approach involves cognitive-behavioral principles, but it does not attempt to directly reduce the frequency of food cravings. Rather, the patient is trained to be mindful, and to experience and accept the phenomenon of food cravings with the recognition that the ability to control internal experience is limited. To our knowledge, there are only two studies that empirically examined the efficacy of specific treatments to manage food cravings. First, an acceptance-based approach was found to help participants who were sensitive to food-rich environments manage food cravings and food intake (Forman et al. 2007). This study also found that cognitive strategies helped participants manage food cravings. Second, acute vagus nerve stimulation in depressed participants was found to change cravings for sweet foods, with approximately half the participants experiencing an increase, and half a decrease, in sweet cravings (Bodenlos et al. 2007). In reviewing the literature on food cravings, directions for future research are apparent. These directions for future research are outlined in Fig. 49.4.

Fig. 49.4  Directions for future research

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49.10  Applications to Other Areas of Health and Disease Food cravings are an important construct for patients and clinicians involved in weight management and the treatment of conditions associated with weight gain or obesity (e.g., cardiovascular disease, type 2 diabetes, and hypertension). The food craving literature is also relevant to other conditions, such as renal insufficiency, that require modification and management of the amounts and types of foods eaten. Finally, the role of food cravings in the etiology of overeating or binge eating in certain subsamples is worthy of further investigation.

Summary Points • In industrialized countries, 58–97% of the population report food cravings (Gendall et al. 1997; Weingarten and Elston 1991). • Chocolate is the most frequently craved food, particularly among women (Weingarten and Elston 1991). • Several self-report instruments with acceptable psychometric properties are available to quantify food cravings. • Overweight and obesity are associated with cravings for high fat foods in individuals with type 2 diabetes (Delahanty et al. 2002) and cravings for sweets in individuals diagnosed with binge eating disorder (White and Grilo 2005). • In laboratory settings, food cravings are associated with the consumption of similar foods (Martin et al. 2008b). • Food restriction accompanied by an energy deficit and weight loss reduces food cravings, and more restrictive diets result in larger decreases in food cravings (Harvey et al. 1993; Lappalainen et al. 1990; Martin et al. 2006, 2008a). • Neuroimaging studies indicate that exposure to imagined or actual craved foods increases activation in brain regions subserving reward, motivation, and memory (Killgore et al. 2003; Simmons et al. 2005; Wang et al. 2004; St-Onge et al. 2005; LaBar et al. 2001; Stoeckel et al. 2008).

Key Terms Food craving:  a desire to consume a specific food or beverage that is difficult to ignore or satisfy with consumption of an alternative food or beverage. Energy deficit:  a state of negative energy balance, where energy expenditure exceeds energy intake. Dietary restraint:  the intent to limit food intake; dietary restraint is not necessarily synonymous with calorie restriction or an energy deficit. Food restriction:  limiting the intake of specific types of foods; food restriction can occur in the presence or the absence of an energy deficit. Neuroimaging:  indirectly or directly measuring the structure and activation of the brain.

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Acknowledgments  Corby K. Martin, Ph.D. is supported by National Institutes of Health Grant 1 K23 DK068052.

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