help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Monteleone, P.
Right arrow Articles by Maj, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Monteleone, P.
Right arrow Articles by Maj, M.
The Journal of Clinical Endocrinology & Metabolism Vol. 88, No. 11 5387-5391
Copyright © 2003 by The Endocrine Society

Opposite Changes in Circulating Adiponectin in Women With Bulimia Nervosa or Binge Eating Disorder

Palmiero Monteleone, Michele Fabrazzo, Vassilis Martiadis, Antonio Fuschino, Cristina Serritella, Nicola Milici and Mario Maj

Departments of Psychiatry (P.M., M.F., V.M., A.F., C.S., M.M.) and Biochemistry and Biophysics (N.M.), University of Naples SUN, 80138 Naples, Italy

Address all correspondence and requests for reprints to: Palmiero Monteleone, M.D., Department of Psychiatry, University of Naples SUN, Largo Madonna delle Grazie, 80138 Naples, Italy. E-mail: monteri{at}tin.it.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Adiponectin is a recently discovered peripheral peptide that is secreted exclusively by differentiated adipocytes. It has been shown to enhance insulin sensitivity, control body weight, regulate lipid homeostasis, and prevent atherosclerosis. Dysregulation of both lipid and glucose metabolism and changes in body weight and body fat mass have been reported in bulimia nervosa (BN) and/or binge eating disorder (BED); hence, investigation of adiponectin secretion is of obvious interest in these eating disorders. To this purpose, we measured plasma levels of adiponectin, glucose, cholesterol, triglycerides, and thyroid hormones in 60 drug-free women, including 20 patients with BN, 20 patients with BED, and 20 healthy controls. Compared with healthy women, BN women exhibited significantly increased circulating adiponectin levels (P < 0.002) and cholesterol concentrations (P < 0.005), whereas BED women had significantly reduced plasma levels of adiponectin (P < 0.005) and increased concentrations of glucose (P < 0.01), cholesterol (P < 0.05), and triglycerides (P < 0.02). Moreover, plasma levels of adiponectin were significantly correlated to the frequency of binge/vomiting episodes (r = 0.65, P = 0.002) in bulimics but not to the frequency of bingeing in BED patients. Because we did not include a group of obese patients who did not binge eat, the specificity of our findings in the BED should be considered cautiously. However, on the basis of present results, it is tempting to speculate that the increased production of adiponectin in BN may represent a compensatory mechanism to counteract the possible development of insulin resistance, whereas the decreased secretion of adiponectin in individuals with BED may be a risk factor for the development of glucose intolerance.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
ADIPOSE TISSUE HAS been traditionally considered an inert storage depot for lipids to be released in conditions of hardship such as starvation. Now it is becoming more and more clear that adipocytes operate as endocrine cells that release a number of peptide hormones actively involved in the regulation of body weight (BW) and energy homeostasis. These peptides share some structural properties of cytokines and are therefore referred to as adipocytokines (1). One of the latest arrivals in the family of adipocytokines is adiponectin, a 30-kDa protein that is secreted exclusively by differentiated adipocytes (2).

Several recent studies suggest that adiponectin plays an important role in the metabolic homeostasis of the organism. In vitro, adiponectin facilitates reduction of hepatocyte glucose production by insulin (3) and attenuates TNF-{alpha} signal transduction in macrophages, and TNF-{alpha} is one factor that potentially induces insulin resistance (4). In vivo, the administration of purified adiponectin to obese mice improves glucose metabolism and fatty acid utilization in the liver and skeletal muscles (3, 5, 6). Moreover, serum levels of adiponectin have been found to be significantly decreased in obese humans (7) and in patients with type 2 diabetes mellitus (8, 9), conditions commonly associated with insulin resistance. Similarly, reduced adiponectin concentrations have been detected in women with dyslipidemia (10). Taken together, all these data suggest that maintenance of stable systemic adiponectin levels might be critical to glucose and lipid homeostasis and modulation of insulin sensitivity.

Bulimia nervosa (BN) and binge eating disorder (BED) are two relatively recently categorized eating disorders (EDs). BN is characterized by multiple binge episodes followed by compensatory behaviors, such as purging, excessive exercising, and prolonged starvation, which aim to prevent the BW increase that would follow the massive calorie ingestion in the binge episodes. As a consequence of the abnormal eating patterns and compensatory behaviors, multiple physiological aberrations occur in BN. In particular, although normal glucose and insulin responses to oral glucose (11, 12) have been elicited in bulimic patients, exaggerated insulin peaks after test meals (13, 14), reduced insulin sensitivity (15), and glucose intolerance (16) have all been reported. Similarly, either increased or normal levels of cholesterol and triglycerides have been detected in symptomatic bulimic individuals (17, 18, 19, 20, 21).

BED is characterized by multiple binge episodes, as in BN, but with no compensatory behaviors; therefore, patients with this disorder incur BW gain and fat accumulation. This considerable increase of adipose tissue is expected to be associated with changes in adiponectin secretion in BED patients. Furthermore, an intriguing association has been reported between BED and type 2 diabetes mellitus (22). Finally, alterations in the physiology of other adipose-borne peptide hormones, such as leptin, have been clearly documented in both BN and BED (23, 24, 25, 26). Therefore, investigation of circulating adiponectin in patients with BN or BED seems to be of obvious interest.

In the present study, we measured circulating adiponectin and investigated its relationships to anthropometrics and metabolic and hormonal parameters in a cohort of subjects including patients with BN, patients with BED, and healthy controls.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

A total of 60 women were recruited for the study. Forty women were outpatients attending the Eating Disorder Center in the Department of Psychiatry (University of Naples, Naples, Italy), and 20 women were healthy controls. According to the criteria of the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) (27), 20 patients fulfilled the diagnosis of BN (five of the patients had a previous history of anorexia nervosa), and 20 fulfilled the diagnosis of BED. Diagnostic assessment was made by a trained interviewer using the Structured Clinical Interview for DSM-IV (28). Moreover, all the patients underwent a structured clinical interview that is used in our department to collect information about the patients’ demographic and historical characteristics and to specifically assess past and/or current eating-related symptomatology, including the number of daily objective bingeing and purging episodes in the 4 wk preceding the assessment. Patients with BN were all of the purging subtype, with binge episodes always followed by self-induced vomiting; five of the patients also abused laxatives, one abused diuretics, and two exercised excessively. Five bulimic patients were amenorrheic; the remaining patients with BN and the patients with BED had normal, regular menses. At the time of the study, all patients had been drug free for more than 6 wk.

The control women were mentally healthy, as assessed by the M.I.N.I. International Neuropsychiatric Interview (29), and had no positive family history of mental disorders, as assessed by the Family History Research Diagnostic Criteria (30). The control subjects were regularly menstruating, had normal diets, and took no medication for at least 6 wk before the study.

Both patients and healthy volunteers had normal physical examinations, normal values of routine blood and urine tests, and normal electrocardiograms. Female controls and patients who were normally menstruating were tested in the follicular phase of their menstrual cycle (d 5–10 from menses). None of the subjects was taking oral contraceptives or had a past history of alcohol or drug abuse.

Procedure

The study was approved by the local ethics committee, and subjects gave written informed consent before study participation.

Each subject underwent a blood sample collection in the morning, between 0800 and 0900 h, after an overnight fast. Patients were instructed to not binge from 2000 h of the day before blood sampling, and their behavior was carefully checked by a relative. Blood was collected in tubes with lithium heparin as anticoagulant. Plasma was separated by centrifugation and stored at -20 C.

In each subject, BW and height were measured, and the body mass index (BMI) was calculated. Moreover, body composition was evaluated by means of a bioelectrical impedance analyzer (STA/BIA, Akern Srl, Florence, Italy).

Biochemical analyses

Plasma adiponectin values were determined by a sandwich ELISA using a commercial kit purchased from B-Bridge International, Inc. (San Jose, CA). The sensitivity of the method was 23.4 pg/ml, and the intra- and interassay coefficients of variation were 4.6 and 7.3%, respectively. Plasma free T3 (FT3) and free T4 (FT4) levels were determined by an ELISA using commercial kits purchased from Adaltis Italia (Bologna, Italy). The sensitivities of the assays were 0.05 pg/ml for FT3 and 0.05 ng/dl for FT4, and the intra- and interassay coefficients of variation were 4.1 and 5.2% for FT3, and 6.1 and 9.6% for FT4, respectively.

Plasma glucose, cholesterol, and triglycerides were determined by commercial enzymatic colorimetric methods (Roche Diagnostics GmbH, Mannheim, Germany) on an automated clinical chemistry analyzer (Hitachi 717, Boheringer Biochemia Robin, Monza, Italy).

Data analysis

The BMDP statistical software package (University of California, Berkeley, CA) was used for data analysis (31). In each subject group, adiponectin values were analyzed for normality of distribution; because there were no significant deviations from normality in the data, parametric statistical analyses were used. Where one-way ANOVA showed significant differences among the groups, the post hoc Tuckey’s test was used to assess differences between patients and controls. The Pearson’s product x moment correlation test was used to examine the relationships between adiponectin values and demographic, metabolic, or hormonal data.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Demographic and clinical data

ANOVA showed significant intergroup differences in mean age [F(2,57) = 10.19, P < 0.0001], BW [F(2,57) = 44.03, P < 0.0001], BMI [F(2,57) = 43.39, P < 0.0001], body fat mass [F(2,57) = 48.92, P < 0.0001], and body lean mass [F(2,57) = 20.52, P < 0.0001]. With respect to healthy women, patients with BED had significantly higher mean age, BW, BMI, body fat mass, and body lean mass. No significant differences in these variables were observed between patients with BN and healthy women (Table 1Go).


View this table:
[in this window]
[in a new window]
  		TABLE 1. Anthropometrics and metabolic parameters of healthy female controls and women with BN or BED

 
For the BN group, the mean binge/vomiting frequency and the mean duration of the illness were 17.8 ± 8.2 episodes/wk and 5.9 ± 2.8 yr, respectively. For the BED group, the mean binge frequency and the mean duration of the illness were 15.4 ± 9.3 episodes/wk and 8.9 ± 6.5 yr, respectively.

Biochemical data

ANOVA showed significant intergroup differences in plasma levels of adiponectin [F(2,57) = 23.53, P < 0.0001], cholesterol [F(2,57) = 6.71, P < 0.003], triglycerides [F(2,57) = 4.58, P < 0.02], glucose [F(2,57) = 4.68, P < 0.02], and FT4 [F(2,57) = 13.78, P < 0.0001] but not in plasma levels of FT3 [F(2,57) = 2.09, P = 0.1].

Compared with healthy women, BN patients exhibited significantly increased plasma levels of adiponectin (Fig. 1Go) and cholesterol but similar plasma concentrations of triglycerides, glucose, FT3 and FT4 (Table 1Go). Circulating adiponectin was higher in the five patients with BN who had a previous history of anorexia nervosa than in BN patients without this history (15.8 ± 5.6 µg/ml vs. 11.8 ± 3.4 µg/ml, respectively), although this difference did not reach a statistical significance [F(1,18) = 3.63, P = 0.07]. After excluding these five patients, in BN patients, plasma adiponectin levels were still higher than in healthy controls [F(1,33) = 6.43, P = 0.01].



View larger version (31K):
[in this window]
[in a new window]
  		FIG. 1. Plasma adiponectin concentrations in healthy women, women with BN, and women with BED. Data are expressed as mean ± SD. *, P < 0.005; and **, P < 0.002 compared with healthy women (post hoc Tukey’s test).

 
Women with BED had significantly reduced blood concentrations of adiponectin (Fig. 1Go) and FT4 but increased plasma levels of cholesterol, triglycerides, glucose, and normal levels of FT3 (Table 1Go). Regarding cholesterol data, eight women with BN (40% of the sample) and five women with BED (25% of the sample), but none of the healthy controls, showed plasma concentrations of cholesterol above the desirable value of 5.172 mmol/liter, as defined by the National Cholesterol Education Program Expert Panel (31). Regarding triglycerides, only one BED patient exhibited plasma levels above the normal value of 1.80 mmol/liter.

To evaluate whether differences in adiponectin levels among the groups persisted after adjustments for age, BW, and plasma levels of glucose, cholesterol, and triglycerides, analyses of covariance were performed with adiponectin as the dependent variable. These analyses showed that age [F(2,56) = 0.06, P = 0.8], BW [F(2,56) = 1.54, P = 0.2], and plasma levels of glucose [F(2,56) = 0.016, P = 0.9], cholesterol [F(2,56) = 1.63, P = 0.2], and triglycerides [F(2,56) = 0.07, P = 0.8] were not significantly associated with adiponectin.

Correlations

Adiponectin levels were negatively correlated with BW (r = -0.50, P < 0.001), BMI (r = -0.53, P < 0.001), and body fat mass (r = -0.50, P < 0.001) in the entire population (i.e., the BN, BED, and control groups combined). These correlations were no longer observed when data were assessed in each group separately. This may be explained by the narrow ranges of anthropometrics values within each group. Moreover, no significant correlations emerged between plasma levels of adiponectin and metabolic or hormonal variables in both the entire population and each diagnostic group. To the contrary, a strong positive correlation emerged between circulating adiponectin and the frequency of bingeing/vomiting in the BN group (r = 0.65, P = 0.002) but did not emerge between the hormone and the frequency of bingeing in the BED group (r = 0.29, P = 0.2, Fig. 2Go). Finally, no significant correlations emerged between cholesterol or triglycerides plasma levels and thyroid hormone concentrations.



View larger version (15K):
[in this window]
[in a new window]
  		FIG. 2. Correlation between plasma adiponectin values and the frequency of binge/vomiting in women with BN (left panel) and correlation between plasma adiponectin values and the frequency of binge episodes in women with BED (right panel).

 
Given the significant inverse correlations between adiponectin levels and BW, BMI, and body fat mass in the whole group and the positive correlation between adiponectin and the frequency of bingeing/purging in the BN group, a stepwise multiple regression analysis was carried out to clarify the simultaneous effect of nutritional and clinical variables on circulating adiponectin in women with BN. This analysis showed that the bingeing/purging frequency was the only variable significantly associated with circulating adiponectin [F(1,18) = 13.19, P = 0.001], which explains 42% of the variability in plasma adiponectin concentrations (R2 = 0.42). After removing this effect, no further variable entered into the analysis.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
There most original and striking primary results from this study are: 1) normal-weight patients with BN had circulating adiponectin higher than normal-weight healthy women of similar age, whereas obese women with BED had significantly decreased plasma levels of this adipocytokine; and 2) circulating adiponectin strongly correlated with the frequency of binge/purging episodes in BN patients but not with the frequency of binge eating in women with BED. Secondary results of this investigation were the finding of significantly enhanced plasma levels of cholesterol in bulimic individuals and the presence of significantly increased plasma concentrations of cholesterol, triglycerides, and glucose in BED patients.

At present, we are not aware of studies exploring adiponectin production in people with BN or BED; therefore, we cannot compare our data with those of other research groups. However, the finding of decreased levels of circulating adiponectin in our obese binge eaters does agree with studies reporting decreased plasma levels of this adipocytokine in obese individuals (7, 33). It has been shown that adipose tissue produces a factor that destabilizes adiponectin mRNA (34), thus exerting a negative feedback on its own adiponectin production. Therefore, the increased fat mass in our obese women with BED could enhance such a negative feedback, contributing to hypoadiponectinemia.

Two studies have reported increased concentrations of adiponectin in underweight women with anorexia nervosa (35, 36). Therefore, our findings of enhanced plasma levels of adiponectin in BN suggest that a similar derangement in the production of this adipocytokine occurs in both EDs. This is not surprising because analogous findings have been reported for other hormones, including cortisol (37, 38), neuroactive steroids (39), and leptin (23, 24, 25, 26). The finding of similar biochemical alterations in anorexia nervosa and BN likely suggests that common pathophysiological mechanisms could underlie these dysfunctions. In particular, malnutrition and energy restriction have been claimed to be the major determinants of physiological aberrations in EDs, and it is well known that, despite no significant BW change in BN patients, bulimics do incur malnutrition and energy restriction because of their abnormal eating patterns, purging behaviors, prolonged starvation, and incorrect selection of food. Furthermore, in those bulimics with a previous history of anorexia nervosa, which likely implies a more severe malnutrition, circulating adiponectin was higher than in bulimics without such a history. Finally, it has been recently reported that a significant increase in plasma adiponectin occurs in young women in response to 7-d energy restriction (39).

It has been shown that, in both healthy subjects and bulimic patients, experimental binge eating dramatically increases insulin plasma levels despite a normal glucose response (13, 16, 40), which suggests an incoming insulin resistance. Therefore, it is possible to speculate that in our bulimic patients, who binged with a frequency ranging from 7 to 28 times a wk, a persistent insulin resistance could develop. Because adiponectin has been shown to have insulin-sensitizing properties (2, 3), its increased production might counteract the occurrence of such a persistent insulin resistance, thus preserving bulimic patients from dysregulation of glucose metabolism. In support of this idea, a strong positive correlation was found in our BN women between circulating adiponectin values and the frequency of binge-purging episodes, and no significant difference emerged in the mean fasting levels of plasma glucose between BN patients and healthy controls.

Because of the association of bingeing and purging, bulimics do not gain BW or incur body fat accumulation as BED patients do. Therefore, it is likely that in the condition of increased fat mass, as in BED individuals, the negative feedback exerted by the adipose tissue on adiponectin biosynthesis (34) leads to a decreased adiponectin production with a consequent increase in the risk for glucose dismetabolism. Therefore, there have been suggestions that binge eating may contribute to the onset of diabetes mellitus (41), possibly via its impact on BW (42). Indeed, it has been proposed that BED is more typical of the population with type 2 diabetes mellitus, and it has been shown that, in this population, binge eating started, on average, at a significantly earlier age than the age at diagnosis of type 2 diabetes (22). Furthermore, a recent article focusing on adiponectin levels during the progression of type 2 diabetes in Rhesus monkeys genetically predisposed to develop insulin resistance evidentiated that adiponectin levels decreased at the onset of the obesity and that this decrease preceded overt hyperglycemia (9). Therefore, we can suggest that, in women with BED, the decrease in circulating adiponectin may represent a risk factor for the development of glucose intolerance.

A secondary finding of the present investigation was that, compared with healthy controls, both women with BN and those with BED exhibited significantly enhanced mean plasma levels of cholesterol, with 40% of BN patients and 25% of BED patients showing circulating cholesterol concentrations above the desirable value of 5.172 mmol/liter (32). These findings agree with those of previous studies that found enhanced blood levels of cholesterol in nonfasted bulimic subjects (17, 18, 19, 20) but disagree with the results of a single study reporting normal morning levels of cholesterol in 12-hr fasted bulimic women (21). However, in the latter study, only 10 bulimics and 10 healthy controls older than our subjects were studied; differences in the sample sizes and age of the subjects may explain these discrepancies. Therefore, present findings do extend the knowledge in the field because they confirm that increased blood concentrations of cholesterol also occur in fasted bulimic patients.

Some limitations of the present study need to be discussed. First, we did not assess plasma insulin concentrations and oral glucose tolerance or undertake sensitive tests of insulin resistance; therefore, we can only speculate about the compensatory role of hypoadiponectinemia in BN subjects and the putative diabetic risk of hypoadiponectinemia in BED individuals. Second, we did not include a BMI-matched control group for the BED subjects. Therefore, although a decrease in circulating adiponectin has been consistently reported in obese non-binge-eating individuals (7, 32), we cannot conclude that the changes observed in BED patients were attributable exclusively to their obesity rather than to their behaviors.

Notwithstanding these limitations, our findings show for the first time that fasting adiponectin levels are increased in the blood of drug-free symptomatic women with BN, whereas they are decreased in the blood of women with BED. The pathophysiological significance of these alterations awaits further studies to be clarified. However, these data, together with other findings showing changes in the physiology of other adipocytokines in people with EDs, suggest the need to deeply investigate peripheral mechanisms in disordered eating.


   Footnotes
 
Abbreviations: BED, Binge ED; BMI, body mass index; BN, bulimia nervosa; BW, body weight; ED, eating disorder; FT3, free T3; FT4, free T4.

Received June 3, 2003.

Accepted July 22, 2003.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. Trayhum P, Beattie JH 2001 Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc Nutr Soc 60:329–339[Medline]
  2. Berg AH, Combs TP, Scherer PE 2002 ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13:84–89[CrossRef][Medline]
  3. Berg AH, Du Combs TPX, Brownlee M, Scherer PE 2001 The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 2001 7:947–953[CrossRef][Medline]
  4. Ouchi N, Kihara S, Arita Y, Okamoto Y, Maeda K, Kuriyama H, Hotta K, Nishida M, Takahashi M, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y 2000 Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-{kappa}B signaling trough a cAMP-dependent pathway. Circulation 102:1296–1301[Abstract/Free Full Text]
  5. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF 2001 Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98:2005–2010[Abstract/Free Full Text]
  6. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T 2001 The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 7:941–946[CrossRef][Medline]
  7. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y 1999 Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257:79–83[CrossRef][Medline]
  8. Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, Iwahashi H, Kuriyama H, Ouchi N, Maeda K, Nishida M, Kihara S, Sakai N, Nakajima T, Hasegawa K, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Hanafusa T, Matsuzawa Y 2000 Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol 20:1595–1599[Abstract/Free Full Text]
  9. Hotta K, Funahashi T, Bodkin NL, Ortmeyer HK, Arita Y, Hansen BC, Matsuzawa Y 2001 Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes 50:1126–1133[Abstract/Free Full Text]
  10. Matsubara M, Maruoka S, Katayose S 2002 Decreased plasma adiponectin concentration in women with dyslipidemia. J Clin Endocrinol Metab 87:2764–2769[Abstract/Free Full Text]
  11. Mitchell JE, Bantle JP 1983 Metabolic and endocrine investigations in women of normal weight with the bulimia syndrome. Biol Psychiatry 18:355–366[Medline]
  12. Taniguchi A, Nakai Y, Fukushima M, Doi K, Tokuyama K, Kawamura H, Suzuki M, Higaki Y, Tanaka H, Sakai M, Nagata I 1997 Intravenous glucose tolerance test-derived glucose effectiveness in bulimia nervosa. Metabolism 46:484–486[CrossRef][Medline]
  13. Kaye WH, Gwirtsman HE, George DT 1989 The effect of bingeing and vomiting on hormonal secretion. Biol Psychiatry 25:768–780[CrossRef][Medline]
  14. Schweiger V, Poellinger J, Laessle R, Wolfram G, Fichter MM, Pirke KM 1986 Altered insulin responses to a balanced test meal in bulimic patients. Int J Eat Disord 6:551–556
  15. Kiriike N, Nishiwaki S, Nagata T, Okuno Y, Yamada J, Tanaka S, Fujii A, Kawakita Y 1990 Insulin sensitivity in patients with anorexia and bulimia. Acta Psychiatr Scand 81:236–239[Medline]
  16. Russell J, Hooper M, Hunt G 1996 Insulin response in bulimia nervosa as a marker of nutritional depletion. Int J Eat Disord 20:307–313[CrossRef][Medline]
  17. Mira M, Stewart PM, Vizzard J, Abraham S 1987 Biochemical abnormalities in anorexia and bulimia. Ann Clin Biochem 24:29–35
  18. Vize CM, Coker S 1994 Hypercholesterolemia in bulimia nervosa. Int J Eat Disord 15:293–295[Medline]
  19. Sullivan PF, Gendall KA, Bulik CM, Carter FA, Joyce PR 1998 Elevated total cholesterol in bulimia nervosa. Int J Eat Disord 23:425–432[CrossRef][Medline]
  20. Pauporte J, Walsh BT 2001 Serum cholesterol in bulimia nervosa. Int J Eat Disord 30:294–298[CrossRef][Medline]
  21. Case T, Lemieux S, Kennedy SH, Lewis GF 1999 Elevated plasma lipids in patients with binge eating disorders are found only in those who are anorexic. Int J Eat Disord 25:187–193[CrossRef][Medline]
  22. Kenardy J, Mensch M, Bowen K, Green B, Walton J, Dalton M 2001 Disordered eating behaviours in women with type 2 diabetes mellitus. Eat Behav 2:183–192
  23. Monteleone P, Di Lieto A, Tortorella A, Longobardi N, Maj M 2000 Circulating leptin in patients with anorexia nervosa, bulimia nervosa or binge-eating disorder: relationship to body weight, eating patterns, psychopathology and endocrine changes. Psychiatry Res 94:121–129[CrossRef][Medline]
  24. Monteleone P, Fabrazzo M, Tortorella A, Fuschino A, Maj M 2002 Opposite modifications in circulating leptin and soluble leptin receptor across the eating disorder spectrum. Mol Psychiatry 7:641–646[CrossRef][Medline]
  25. Monteleone P, Bortolotti F, Fabrazzo M, La Rocca A, Fuschino A, Maj M 2000 Plasma leptin response to acute fasting and refeeding in untreated women with bulimia nervosa. J Clin Endocrinol Metab 85:2499–2503[Abstract/Free Full Text]
  26. Jimerson DC, Mantzoros C, Wolfe BE, Metzger BD 2000 Decreased serum leptin in bulimia nervosa. J Clin Endocrinol Metab 85:4511–4514[Abstract/Free Full Text]
  27. American Psychiatric Association 1990 Diagnostic and statistical manual of mental disorders, 4th ed. Washington, DC: American Psychiatric Press
  28. First MB, Spitzer RL, Gibbon M, Williams JB 1995 Structured clinical interview for DSM-IV axis I disorders (SCID-I). New York: Research Version Biometrics, Research Department, New York State Psychiatric Institute
  29. Lecrubier Y, Sheehan D, Weller E, Amorim P, Bonora I, Sheehan K, Janavs J, Dunbar GC 1997 The Mini International Neuropsychiatric Interview (M.I.N.I.). A short diagnostic structured interview: reliability and validity according to the CIDI. Eur Psychiatry 12:224–231[CrossRef]
  30. Andreasen NC, Endicott J, Spitzer RL, Winokur G 1997 The family history method using diagnostic criteria: reliability and validity. Arch Gen Psychiatry 34:1229–1235
  31. Dixon J 1985 BMDP statistical software. Berkeley, CA: University of California Press
  32. The National Cholesterol Education Program Expert Panel 1988 Report of the National Cholesterol Education Program Expert Panel on the detection, evaluation, treatment of high blood cholesterol in adults. Arch Intern Med 148:36–69[Abstract]
  33. Matsubara M, Maruoka S, Katayose S 2002 Inverse relationship between plasma adiponectin and leptin concentrations in normal-weight and obese woman. Eur J Endocrinol 147:173–180[Abstract]
  34. Halleux CM, Takahashi M, Delporte ML, Detry R, Funahashi T, Matsuzawa Y, Brichard SM 2001 Secretion of adiponectin and regulation of apM1 gene expression in human visceral adipose tissue. Biochem Biophys Res Commun 288:1102–1107[CrossRef][Medline]
  35. Delporte ML, Brichard SM, Hermans MP, Beguin C, Lambert M 2003 Hyperadiponectinaemia in anorexia nervosa. Clin Endocrinol (Oxf) 58:22–29[CrossRef][Medline]
  36. Pannacciulli N, Vettor R, Milan G, Granzotto M, Catucci A, Federspil G 2003 Anorexia nervosa is characterized by increased adiponectin plasma levels and reduced nonoxidative glucose metabolism. J Clin Endocrinol Metab 88:1748–1752[Abstract/Free Full Text]
  37. Brambilla F, Monteleone P 2003 Physical complications and physiological aberrations in eating disorders: a review. In: Maj M, Halmi K, Lòpez-Ibor JJ, Sartorius N, eds. Eating disorders. Hoboken, NJ: John Wiley & Sons Ltd.; 139–192
  38. Monteleone P, Luisi M, Colurcio B, Casarosa E, Monteleone P, Ioime R, Genazzani AR, Maj M 2001 Plasma levels of neuroactive steroids are increased in untreated women with anorexia nervosa or bulimia nervosa. Psychosom Med 63:62–68[Abstract/Free Full Text]
  39. Havel PJ, Stanhope KL, Sinha M, Dubuc GR, Phinney SD Gender differences in circulating adiponectin concentrations and in adiponectin responses to 7 d of energy restriction in normal weight men and women. Proc Annual Meeting of the American Diabetes Association, San Francisco, CA, 2002, p 1867
  40. Taylor AE, Hubbard J, Anderson EJ 1999 Impact of binge eating on metabolic and leptin dynamics in normal young women. J Clin Endocrinol Metab 84:428–434[Abstract/Free Full Text]
  41. Kenardy J, Mensch M, Bowen K, Pearson S 1994 A comparison of eating behaviors in newly diagnosed non-insulin-dependent diabetes mellitus and case-matched controls. Diabetes Care 17:1197–1199[Abstract]
  42. Herpertz S, Albus C, Wagener R, Kocnar M, Wagner R, Henning A, Best F, Foerster H, Schulze Schleppinghoff B, Thomas W, Kohle K, Mann K, Senf W 1998 Does diabetes control reflect disturbed eating behavior? Diabetes Care 21:1110–1116[Abstract]



This article has been cited by other articles:


Home page
 J. Clin. Endocrinol. Metab.Home page
J. Housova, K. Anderlova, J. Krizova, D. Haluzikova, J. Kremen, T. Kumstyrova, H. Papezova, and M. Haluzik
Serum Adiponectin and Resistin Concentrations in Patients with Restrictive and Binge/Purge Form of Anorexia Nervosa and Bulimia Nervosa
J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1366 - 1370.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Monteleone, P.
Right arrow Articles by Maj, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Monteleone, P.
Right arrow Articles by Maj, M.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals