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Adaptations of Leptin, Ghrelin Or Insulin During Weight Loss As Predictors of Weight Regain: a Review of Current Literature

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Adaptations of Leptin, Ghrelin Or Insulin During Weight Loss As Predictors of Weight Regain: a Review of Current Literature International Journal of Obesity (2014) 38, 388–396 & 2014 Macmillan Publishers Limited All rights reserved 0307-0565/14 www.nature.com/ijo REVIEW Adaptations of leptin, ghrelin or insulin during weight loss as predictors of weight regain: a review of current literature K Strohacker1, JM McCaffery1, PS MacLean2 and RR Wing1 Numerous laboratory studies involving both animal and human models indicate that weight loss induces changes in leptin, ghrelin and insulin sensitivity, which work to promote weight regain. It is unclear, however, whether these biological changes serve as a biomarker for predicting weight regain in free-living humans in which biological, behavioral and environmental factors are likely at play. We identified 12 studies published between January 1995 and December 2011 that reported changes in leptin, ghrelin or insulin during intentional weight loss with a follow-up period to assess regain. Two of the nine studies examining leptin suggested that larger decreases were associated with greater regain, three studies found the opposite (smaller decreases were associated with greater regain), whereas four studies found no significant relationship; none of the studies supported the hypothesis that increases in ghrelin during weight loss were associated with regain. One study suggested that improvements in insulin resistance were associated with weight gain, but five subsequent studies reported no association. Changes in leptin, ghrelin or insulin sensitivity, taken alone, are not sufficient to predict weight regain following weight loss in free-living humans. In future studies, it is important to include a combination of physiological, behavioral and environmental variables in order to identify subgroups at greatest risk of weight regain. International Journal of Obesity (2014) 38, 388–396; doi:10.1038/ijo.2013.118 Keywords: weight loss; weight regain; appetite hormones; review; free-living humans INTRODUCTION weight loss induce significant increases in the concentration of 33–35 36,37 Sixty-eight percent of men and women in the United States are ghrelin, a potent orexigenic hormone. Elevations in 38 39 classified as overweight (body mass index X25 kg m À 2) or obese ghrelin concentration, either endogenous or exogenous, are (body mass index X30 kg m À 2).1 By promoting dyslipidemia, associated with feelings of hunger and increased food intake. insulin resistance and systemic inflammation, excess adiposity Given the substantial evidence that biological adaptations occur increases risk for poorer health outcomes including cardiovascular with weight loss in a manner that promotes overfeeding and disease or type 2 diabetes.2,3 Moderate, but clinically significant weight regain in tightly controlled laboratory studies, it is weight losses of B5–10% have been shown to reduce disease important to determine whether any of the commonly measured risk.4,5 Although weight loss is achievable through a variety of biomarkers (leptin, insulin or ghrelin) are predictive of weight programs (self-guided, commercial, behavioral or medically regain in free-living humans, in which non-homeostatic behavioral supervised), weight regain is common.6–9 and environmental factors are also at play. Such a biomarker could Weight loss-induced adaptations in several humoral factors have significant value in determining individual risk of weight have been identified and substantial laboratory-based evidence regain in a clinical setting and in subsequently tailoring treatment supports that such adaptations promote weight regain. In rodent programs to improve weight maintenance outcomes in previously models of diet-induced obesity, weight loss triggers biological and overweight or obese individuals. Furthermore, determining a metabolic adaptations that contribute to overfeeding and predictive biomarker could advance pharmacological prevention subsequent weight regain.10–12 In humans, fasting concen- of weight regain. Therefore, the aim of the present review was to trations of adiposity signals leptin and insulin, which are determine whether weight loss-induced changes in leptin, insulin elevated with excessive adiposity, are substantially reduced or ghrelin have been demonstrated to predict human weight during caloric restriction and subsequent weight loss.13–26 regain in the prior literature. Importantly, these reductions are disproportionately low relative to observed fat mass at a stabilized weight,12,24,27–29 which is likely interpreted by the central nervous system as a considerable MATERIALS AND METHODS 30 energy depletion that must be corrected. Indeed, maintenance Search strategies of a reduced body weight has been related to leptin-reversible A systematic search was conducted through the PubMed electronic neural activity in part of the brain responsible for energy 31 database. The database was searched for human studies from January homeostasis, and leptin administration in weight-reduced 1990 to January 2012. The inclusion criteria were that studies (i) reported 32 subjects improves satiety. In addition, caloric restriction and intentional weight loss with a follow-up period to assess weight regain, 1Department of Psychiatry and Human Behavior, The Miriam Hospital and Warren Alpert School of Medicine at Brown University, Providence, RI, USA and 2Department of Medicine, Division of Endocrinology, Metabolism, and Diabetes, Center for Human Nutrition, University of Colorado Anschutz Medical Campus, Denver, CO, USA. Correspondence: Dr RR Wing, Weight Control and Diabetes Research Center, The Miriam Hospital, 196 Richmond Street, Providence, RI 02904, USA. E-mail: [email protected] Received 11 March 2013; revised 21 May 2013; accepted 14 June 2013; accepted article preview online 26 June 2013; advance online publication, 23 July 2013 Leptin, ghrelin, insulin and weight regain K Strohacker et al 389 (ii) were published in English or with an English abstract, (iii) reported Do reductions in leptin during weight loss predict weight regain? original research on the relationships between weight loss-induced The nine articles examining relationships between changes in changes in leptin, ghrelin and indices of insulin sensitivity (glucose clamp, leptin during weight loss and weight regain are summarized in fasting insulin, and so on) and weight regain or weight maintenance. Multiple keywords and word combinations were used in searches, Table 1. Overall, the results are mixed. Only two of nine studies supported the hypothesis that decreases in leptin predict weight including weight, regain, maintenance, leptin, ghrelin, insulin, insulin 40 sensitivity, predict, future and weight change. The references of articles regain in free-living humans. Erez et al. found that weight regain were also screened for potentially relevant studies. The study selection was greatest in individuals with larger decreases in leptin during process is shown in Figure 1. weight loss, supporting the hypothesis that decreases in leptin may be a determinant of weight regain. Soni et al.41 provided mixed support of their hypothesis. Decreases in leptin during the Data synthesis weight-loss phase were associated with weight regain during the The studies’ diversity in sample, design, data analysis, variables and maintenance phase; however, this association was lost when follow-up time-frame (3 months–4 years after weight loss) precluded analyses were limited to participants who lost X10 lbs during the meta-analysis. The data are summarized descriptively and synthesized in 41 Tables 1–3. The tables are organized by author group and publication year initial weight-loss phase. Three studies reported opposite results, such that a smaller decline in leptin during weight loss was from earliest to most recent, and then alphabetically. They include 42–44 descriptions of the sample populations if available (age and body mass associated with a larger weight regain. In the largest and 43 index upon entry to study and gender stratification) and descriptions of most recent of these studies, the authors found that smaller the intervention (approach to weight loss and durations of weight loss/ decreases in leptin were significantly related to regain among maintenance phases). Initial weight loss is described referring to weight men and women who had lost on average 5% of their weight change during the initial weight loss phase compared with baseline. during a low-calorie diet.43 Finally, four additional studies reported Follow-up weight loss is also described referring to weight change during no association between leptin reductions during weight loss and the maintenance phase compared with baseline. If quantitative data for subsequent weight change.45–48 follow-up weights were not provided, the tables provide descriptive information on weight change patterns stratified by successful main- A number of these studies also examined the association tenance or quartiles. Finally, tables provide determinations (‘yes’, ‘no’ or between baseline and/or post-weight loss leptin and weight ‘not tested’) on the basis of study outcomes of whether decreases in leptin, regain; these findings are also mixed (Table 1). One study found increases in ghrelin or increases in insulin sensitivity during weight loss that low baseline leptin levels were associated with weight were related to weight regain. Within the reviewed studies, we also regain.44 However, two studies demonstrated opposing findings, determined whether low leptin, high ghrelin or high insulin sensitivity at such that relatively higher baseline leptin concentrations
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