EMPIRICAL ARTICLE

Is Disordered Eating Behavior More Prevalent in Adolescents with Early-Onset Type 1 Diabetes than in Their Representative Peers? Christina Baechle, M.Sc1* Katty Castillo, Ph.D1 Klaus Straßburger, Ph.D1 Anna Stahl-Pehe, Ph.D1 Thomas Meissner, M.D2 Reinhard W. Holl, M.D3 Guido Giani, Ph.D1 Joachim Rosenbauer, M.D1 In Cooperation with the German Paediatric Surveillance Unit (ESPED) and the DPV-Science Initiative

ABSTRACT Objective: Despite modern therapeutic regimens, youths with Type 1 diabetes may be at increased risk of mental and behavioral disorders. In this study, the prevalence of disordered eating behavior (DEB) in intensely treated children and adolescents with early-onset Type 1 diabetes and peers from the general population was compared. Method: Data from 629 patients from a population-based, nationwide survey (54.1% male, mean age 15.3 years) with early-onset Type 1 diabetes of at least 10 years duration were compared with data from 6,813 participants of the German KiGGS study (51.3% male, mean age 14.6 years). The generic SCOFF questionnaire was used as screening instrument to identify participants with symptoms of DEB. Both groups were compared with multivariable regression analysis adjusting for sociodemographic covariates. Results: 31.2% of the female and 11.7% of the male diabetic patients and 28.9% of the females and 15.2% of the males in the comparison group were SCOFF-

Introduction The term “disordered eating behavior” (DEB) comprises a wide spectrum of eating disorder pathologies, ranging from dieting for weight control, binge

positive (SCOFF score 2; p > .05). The odds for symptoms of eating disorders were 3.7% higher in female and 4.3% lower in male patients with diabetes than in the comparison group, but the differences were not significant. 20.5% of the female and 18.5% of the male diabetic patients reported insulin restriction at least three times per week. Discussion: Children and adolescents with early-onset Type 1 diabetes of long duration do not seem to be more frequently SCOFF-positive than peers. However, as insulin restriction is practiced in a substantial portion of patients, attention for insulin restriction in diabetes C 2013 Wiley Periodicals, care is essential. V Inc. Keywords: eating disorders; disordered eating behavior; childhood type 1 diabetes; early onset; long duration; insulin purging; insulin restriction (Int J Eat Disord 2014; 47:342–352)

eating and purging behaviors to subthreshold and full-syndrome eating disorders (ED). DEB is common in adolescents and young adults.1–4 According to a recent survey, 3.9%

Accepted 5 December 2013 Study results were presented as a poster at the 48th annual meeting of the EASD in Berlin 2012. Supported by the Competence Network Diabetes Mellitus by the German Federal Ministry of Education and Research (FKZ 01GI0802, 01GI1109A, 01GI0859, 01GI1106), by the German Ministry of Health and the Ministry of Innovation, Sciences and Research of the Federal State of North Rhine-Westphalia, European Foundation for the Study of Diabetes (EFSD), the Dr. B€ urger-B€ using Foundation, and Novo Nordisk Germany. *Correspondence to: Christina Baechle, Institute for Biometrics and Epidemiology, German Diabetes Centre, Leibniz Institute for Diabetes Research at Heinrich Heine University, Auf’m Hennekamp 65, D 40225 D€ usseldorf, Germany. E-mail: [email protected] 1 German Diabetes Centre, Institute for Biometrics and Epidemiology, D€ usseldorf, Germany 2 Department of General Paediatrics, Neonatology and Paediatric Cardiology, Heinrich Heine University, D€ usseldorf, Germany 3 University of Ulm, Institute of Epidemiology and Medical Biometry, Faculty of Medicine, Ulm, Germany C.B. researched the data, designed the study, assisted in the analyses and wrote the article. K.C. researched the data and performed the analyses. K.S. contributed to the analyses and reviewed the article. A.S.-P. researched the data, contributed to the discussion and reviewed the article. T.M. and G.G. reviewed the article. R.W.H. is the principal investigator of the DPV Initiative and reviewed the article. J.R. is the principal investigator of the diabetes study and contributed to every aspect of this article. Published online 22 December 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/eat.22238 C 2013 Wiley Periodicals, Inc. V

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(female 5.9%, male 1.5%) of the German population older than 13 years reported DEB.5 The longterm consequences of DEB/ED are considerable. DEB and ED are associated with an increased risk of medical complications, psychiatric comorbidities, and the highest mortality rate among psychiatric disorders.6 In patients with DEB/ED and Type 1 diabetes (referred to as “diabetes”), poor metabolic control7,8 and an increased risk for diabetesrelated complications may be additional consequences.2,9 The etiology of DEB/ED is complex and multifactorial.6,10 Individual, familial, and sociocultural factors can contribute to cause or prevent the development of DEB depending on their type or constellation.10 Diabetes can increase the risk of ED or subthreshold ED due to specific characteristics of the disease itself and its management. Daneman et al. established a model of the association between diabetes, eating, and weight psychopathology.11 Accordingly, the provision of insulin may result in weight gain, followed by body dissatisfaction and a drive for thinness among Type 1 diabetic patients.1,6,11,12 Intensive insulin management11,13– 15 and insulin resistance during puberty16,17 may increase the need for insulin and thus exacerbate the problems of weight gain and body dissatisfaction. The dietary management of diabetes and the preoccupation with food may further predispose the development of an ED.1,6,11,18 Other risk factors include high discipline and a strong sense of control behavior, which are necessary to achieve optimal metabolic control and prevent late diabetic complications.2,18 A frequent specific purging behavior (as sign of a DEB) in patients with diabetes is the so-called insulin purging (reduction or omission of insulin dose for weight control). Several studies have reported that up to 36% of patients with diabetes practice this purging behavior.19–22 Insulin purging may be favored in patients with diabetes compared with other DEB. To date, it is not clear if there is an association between DEB/ED and diabetes. Some studies show an increased risk of DEB/ED in patients with diabetes compared with the general population.1,6,12,18,23 For example, Jones et al. compared the prevalence of ED in 361 adolescent diabetic females (mean age at onset 8.1 years, mean diabetes duration 6.7 years) with 1,114 age-matched nondiabetic controls using a two-stage study design.1 Participants who were considered to have an ED according to their answers to the diabetes-modified Eating Disorder Inventory (EDI) and Eating Attitudes Test International Journal of Eating Disorders 47:4 342–352 2014

(EAT-26) questionnaires were asked to take part in a diagnostic interview (Eating Disorder Examination [EDE]). Female patients with diabetes had an increased prevalence of ED (10% vs. 4%) and subthreshold ED (14% vs. 8%). € m et al. used a Similar to Jones et al., Engstro two-stage procedure to compare the prevalence of ED in 89 adolescent girls with diabetes (mean age 16.3 years, mean diabetes duration 7.7 years) with 89 age-matched, healthy controls.23 A total of 83.1% of the female patients were on multiple daily injections; 11.2% used continuous subcutaneous insulin infusion (CSII). According to the results of the questionnaire, female patients with diabetes had higher scores for drive for thinness and body dissatisfaction. Based on the subsequent interview, 6.9% of the diabetic girls, but none of the control group, were diagnosed with ED. Other studies are inconclusive8,24–26 or do not report an increased risk of DEB/ED in diabetic patients.27 Ackard et al. compared the prevalence of disordered eating in 143 diabetic patients (mean age 15.3 years, mean diabetes duration >1 year) with a population-based sample of 4,746 adolescents using the Project Eating Among Teens (EAT) survey.25 Adjusted for age, race, socioeconomic status, and BMI, the prevalence of ED was lower in patients with diabetes than in the comparison group, and there were no significant differences between the male and the female groups. Using the Eating Disorder Inventory (EDI), Meltzer et al. even reported fewer symptoms of bulimia in male diabetic patients and less body dissatisfaction in female diabetic adolescents than in the normative comparison group.27 The mean diabetes duration was 6.1 years, and all patients were on a conventional insulin regimen (CT) with two daily injections. Studies comparing the frequency of DEB or ED in male participants with and without diabetes are € m et al., scarce. Using the same design as Engstro Svensson et al. compared 109 male diabetic patients (mean age 16.6 years, mean diabetes duration 7.2 years, all patients on intensified conventional therapy [ICT] or CSII) with 139 controls.24 According to the results of the questionnaire, male patients with diabetes had an increased score for drive for thinness, but a decreased score for bulimia compared with nondiabetic peers. No participants were identified with ED in either the diabetic or the control group. A recently published systematic review and meta-analysis conducted by Young et al. summarized the results of 13 empirical studies published between 1999 and 2011.28 The mean age of the 343

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participants ranged between 11.8 and 16.4 years, the mean diabetes duration was 1.5 to 7.7 years. DEB (39.3% vs. 32.5%) and ED (7.0% vs. 2.8%) were significantly more common in Type 1 diabetic adolescents than in their peers, respectively. However, after restricting the analysis to the four (n 5 1 DEB and ED, n 5 3 ED) studies using diabetes-adapted assessment tools, the difference in the prevalence of eating problems remained but was no longer significant between the two groups (DEB: 51.8% vs. 48.1%; ED: 6.4% vs. 3.0%).28 Over the last 15 years, diabetes management has changed considerably, with increased use of multiple daily injection regimens and in most recent years of continuous subcutaneous insulin infusion (CSII).29 This medical advance has resulted in less restrictive dietary regimens, allowing patients with diabetes to lead a more normal lifestyle.30,31 To date, it has not been established whether these therapeutic advances have affected potential correlations between DEB/ED and diabetes. While there are several studies comparing the prevalence of ED or DEB in diabetic populations and in the general population, there has been no special focus on patients with early-onset and long-duration T1D. Patients in this group are of special interest because they are predisposed to suffer from late diabetes-related complications arising from the long duration of diabetes.32 In the presence of DEB, health problems may be exacerbated. The aim of this study was to compare the prevalence of symptoms of DEB in intensely treated male and female patients with early-onset and long-duration diabetes with representative peers in Germany using large population-based samples and to assess insulin restriction in Type 1 diabetic patients.

this analysis represent the 11- to 17-year-old subgroup of the total diabetes study population (629 participants, response rate 42%). The study was approved by the local commissioner for data protection and the ethical review € sseldorf. Furboard of the Heinrich Heine University Du ther details on the study design have been published recently.33 For the comparison, data from the Public Use File of The German Health Survey for Children and Adolescents (KiGGS, Robert Koch Institute, Berlin, Germany, 2008) were used. The KiGGS is a nationwide survey that was conducted between May 2003 and May 2006 (baseline survey). The survey is representative of all noninstitutionalized children less than 18 years of age living in Germany. Altogether, 17,641 participants were included in the final KiGGS sample. 6,813 KiGGS participants were between 11 and 17 years old (response rate 67%). The design and methods of the KiGGS study have been previously described.34 In both studies, the participants received extensive, standardized, self-administered questionnaires. The participants in the diabetes study completed the questionnaires at home, while the KiGGS participants completed the questionnaires at the study centers. The questionnaire for the diabetes study corresponded to the KiGGS study questionnaire, but it was supplemented by diabetes-specific questions.

Assessment of Variables To assess the frequency of DEB, the SCOFF questionnaire was used.35,36 Five questions with dichotomous response options (yes/no) focused on the core symptoms of anorexia and bulimia nervosa.

Study Population

1. Do you make yourself Sick because you feel uncomfortably full? 2. Do you worry you have lost Control over how much you eat? 3. Have you recently lost more than One stone in a 3-month period? 4. Do you believe yourself to be Fat when others say that you are too thin? 5. Would you say that Food dominates your life?

The data for the diabetic patients were derived from the German nationwide, population-based cohort study “Clinical Course of Type 1 Diabetes in Children, Adolescents and Young Adults with Disease Onset in Preschool Age” (diabetes study). Inclusion criteria were an early onset of diabetes (age 0–4 years) during the period 1993 to 1999. Between September 2009 and December 2010, all eligible patients and their parents were contacted via their treatment facilities and asked to complete a standardized questionnaire. All participants stated their written informed consent. The diabetic patients included in

Each affirmative answer is scored as 1 point. If two or more of the questions are answered with “yes” (SCOFFpositive), this is defined as indicative of an ED. The questionnaire was originally developed as a brief screening tool for ED. In a validation study among a primary care population (341 women, age 18–50 years), the questionnaire had 100% sensitivity to detect anorexia or bulimia nervosa using two or more questions answered with yes as cut-off (i.e., a score of at least 2) and a clinical diagnostic interview as reference method.37 In other

Method

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validation studies, sensitivity coefficients ranged between 73% and 98%, and specificity coefficients were between 21% and 94% for the same cut-off score.38 The German version of the SCOFF was validated in a sample of 807 pupils aged 12 years with the reference method EAT-26D.39 Sensitivity and specificity of the German SCOFF version were 79% and 74% in detecting highly risky eating behaviors and 59% and 51% in detecting moderately risky eating behaviors. Muro-Sans et al. and Hautala et al. assigned the five SCOFF questions to two typical eating disorder-related behaviors. Loss of control over food includes questions 2, 4, and 5 and comprises cognitive aspects of DEB like control over food and body image. In contrast, purging behavior (SCOFF questions 1 and 3) contains the behavior-related items intentional vomiting and weight loss.38,40 However, the questionnaire does not allow to determine the type of ED. Using assessment tools originally developed for the general population in patients with diabetes may result in an overestimation of ED.9,41 This detection bias can be attributed to the fact that patients with diabetes have to deal intensively with their diet to balance their food intake and insulin dosage. Questions such as SCOFF question 5 may be answered in the affirmative solely because of the diabetes treatment-related behaviors and may not be a valid indication of DEB. For this reason, in this analysis, the total SCOFF and a SCOFF excluding question 5 were used to compare the eating behaviors of children with and without diabetes. In addition, each SCOFF question and the two subscores for purging behavior and loss of control over food (subscore 1: with question 5, subscore 2: excluding question 5) were analyzed. As generic instrument, the SCOFF questionnaire does naturally not cover insulin restriction. Therefore, we assessed insulin restriction in diabetes patients by the additional question “How often did you inject too little or no insulin after carbohydrate intake during the last week?” with the response categories “never,” “once or twice a week,” “3 to 5 times a week,” “(almost) every day,” or “more than once a day.” All variables were derived from the questionnaires of the children and their parents, respectively. Socioeconomic status was divided into three categories (i.e., low, middle, and high) according to the total scores from a composite social status index commonly used in Germany.34,42 This index summarizes information on parents’ education levels, parents’ professional statuses, and household income. Immigration background was considered if the participants had emigrated from another country and if at least one of their parents was born abroad or was of non-German nationality. Furthermore, the region of residence (Western or Eastern Germany), and the family structure (e.g., living with both International Journal of Eating Disorders 47:4 342–352 2014

parents or one parent [and partner]) were determined. Health-related data included body mass index (BMI), age, smoking and, if applicable, age at diabetes onset, diabetes duration, HbA1c (average of self-reported and parentreported value), and insulin regimen (conventional therapy (CT): one to three daily injections; intensified conventional therapy (ICT): 4 daily injections; or continuous subcutaneous insulin infusion [CSII]). The BMIs were converted to standard deviation scores (BMI-SDS) using age- and sex-specific German reference data43,44 and BMI-SD scores were then categorized according to the BMI-SDS terciles of the KiGGS participants. Statistical Analyses Continuous and categorical variables are described as the means and standard deviations (SD) or percentages, respectively. To ensure representativeness of the comparison group, all analyses of the KiGGS group were weighted with a survey weighting factor according to a current KiGGS recommendation.45 Multivariable logistic regression (SAS survey logistic) was used to analyze the association between the dependent variable (SCOFF, cut-off 2) and the independent variable study group, adjusting for potential confounders and stratified by gender. Two separate models were applied. Model 1 (M1) included age group as potential confounder. Model 2 (M2) added variables with indicated differences (p < .1) between groups (immigration background, region of residence, familial structure, socioeconomic status, BMI-SDS category, and smoking) as additional covariates. All analyses were repeated with the SCOFF results excluding question 5 as outcome variable (cut-off 2), the SCOFF sub-scores (cut-offs 1 and 2, respectively, and excluding question 5) and separately for each SCOFF question. p Values of two-sided tests .05 were considered statistically significant. For statistical analyses, SAS for Windows version 9.3 (SAS Institute, Cary, NC) was used.

Results Description of the Study Populations

Table 1 provides an overview of the participants’ characteristics in both groups and summarizes the diabetes-specific characteristics of the diabetes group. Prevalence of Disordered Eating Behavior Based on SCOFF results

In total, 31.2% of the female diabetic patients and 28.9% of the female comparison group were SCOFF-positive (Table 2). Among boys, 11.7% of the patients and 15.2% of the male comparison 345

BAECHLE ET AL. TABLE 1.

Description of the two cohorts

No. participants Boys (%) Age (yr) 11–13 yrs (%) 14–17 yrs (%) Socioeconomic status Low (%) Middle (%) High (%) Immigration background (%) Region of residence West (%) Familial structure Biological parents (%) Mother and partner/father and partner (%) Single mother/single father (%) Other (relatives, foster parents, youth institutions) (%) BMI mean (SD) (kg/m2) BMI-SDS (SD) Smoker (%) Mean age at diabetes onset (SD) (yr) Mean diabetes duration (SD, range) HbA1c mean (SD) (%) HbA1c mean (SD) (mmol/mol) Proportion 9.0% (75 mmol/mol) Insulin therapy regimen Continuous subcutaneous insulin infusion (CSII) (%) Intensified conventional therapy (4 daily injections, ICT) (%) Conventional therapy (1–3 daily injections, CT) (%) a

Diabetes Studya

KiGGSb

629 54.1 15.3 (1.7) 24.0 76.0

6,813 51.3 14.6 (2.0) 39.6 60.4

17.9 48.2 34.0 1.8

27.4 47.2 25.3 17.5

Is disordered eating behavior more prevalent in adolescents with early-onset type 1 diabetes than in their representative peers?

Despite modern therapeutic regimens, youths with Type 1 diabetes may be at increased risk of mental and behavioral disorders. In this study, the preva...
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