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(Demmer RT, Zuk AM, Rosenbaum M, Desvarieux M. Prevalence of diagnosed and undiagnosed type 2 diabetes mellitus among US adolescents: results from the continuous NHANES, 1999-2010. Am J Epidemiol 2013;178:1106-13.)

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Original Contribution Prevalence of Diagnosed and Undiagnosed Type 2 Diabetes Mellitus Among US Adolescents: Results From the Continuous NHANES, 1999 2010 Ryan T. Demmer * , Aleksandra M. Zuk, Michael Rosenbaum, and Moïse Desvarieux * Correspondence to Dr. Ryan T. Demmer, Department of Epidemiology, Mailman School of Public Health, Columbia University, 722 West 168th Street, New York, NY 10040 (e-mail: [email protected]). Initially submitted January 18, 2013; accepted for publication April 16, 2013. Although prevalence and incidence of type 2 diabetes mellitus (T2DM) are reportedly increasing among adoles- cents, national data are lacking, particularly in regard to undiagnosed T2DM. To estimate the prevalence of diag- nosed and undiagnosed T2DM among US adolescents, we analyzed a nationally representative cross-section of 11,888 adolescents aged 12 19 years who received a diabetes interview in the Continuous National Health and Nutrition Examination Survey during 1999 2010. Among them, a random subsample of 4,661 adolescents also had fasting blood samples collected. Persons who reported a previous diabetes diagnosis and were either taking no medication or taking an oral hypoglycemic agent (with or without insulin) were classified as having T2DM; persons who reported using insulin alone were classified as having type 1 diabetes. Undiagnosed diabetes was defined as a fasting plasma glucose concentration of 126 mg/dL and was assumed to be type 2. In the fasting subsample, 31 diabetes cases (types 1 and 2) were identified, representing a prevalence of 0.84% (weighted 95% confidence interval (CI): 0.51, 1.40) (276,638 cases; 95% CI: 134,255, 419,020). Estimates of the prevalences of type 1 and type 2 diabetes were 0.48% (95% CI: 0.23, 1.02) and 0.36% (95% CI: 0.20, 0.67), respectively, indicat- ing that T2DM accounted for 43% of all cases. Further, undiagnosed T2DM prevalence was 0.12% (95% CI: 0.05, 0.31), representing 34% of T2DM cases (40,611 cases; 95% CI: 2,850, 78,373). T2DM accounts for approxi- mately half of adolescent diabetes in the United States, and one-third of these cases are undiagnosed. adolescents; diabetes mellitus; etiology; prevalence; undiagnosed diabetes Abbreviations: CDC, Centers for Disease Control and Prevention; CI, confidence interval; MODY, maturity-onset diabetes of the young; NHANES, National Health and Nutrition Examination Survey; SEARCH, SEARCH for Diabetes in Youth Study; T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus. Diabetes mellitus is a serious disease which is linked to substantial morbidity and mortality in the United States and globally ( 1 ). Type 2 diabetes mellitus (T2DM) among adoles- cents is particularly concerning, since recent reports suggest that early-onset T2DM is challenging to control and repre- sents a more aggressive disease phenotype than the later-onset form (i.e., more rapid decline in β -cell function and accrual of comorbid conditions) ( 2 4 ). Therefore, increased prevalence and incidence of early-onset T2DM would portend increased health-care costs, morbidity, and premature mortality ( 5 , 6 ). Although evidence suggests that the prevalence of T2DM has been increasing among US adolescents ( 7 16 ) as a result of the overweight/obesity epidemic ( 17 19 ), there are very few reports from population-based studies that can provide reliable estimates, because the overall prevalence of adoles- cent diabetes remains very low (<1%) ( 7 , 8 ). In the largest nationally representative sample examining T2DM preva- lence in US adolescents to date, Fagot-Campagna et al. ( 7 ) reported a total of only 4 cases, 2 of which were undiagnosed, making it dif cult to generate precise upper and lower preva- lence bounds or to consider variation by sex or race/ethnic- ity. Alternatively, the SEARCH for Diabetes in Youth Study (SEARCH) has identi ed more than 6,000 ( 9 ) cases of dia- betes in youth through an innovative study design, which has attempted to identify all cases of diabetes in de ned geo- graphic areas ( 20 ). However, the SEARCH sample was recruited 1106 Am J Epidemiol. 2013;178(7):1106 1113 American Journal of Epidemiology © The Author 2013. Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: [email protected] Vol. 178, No. 7 DOI: 10.1093/aje/kwt088 Advance Access publication: July 25, 2013 at Harvard University on March 16, 2014 Downloaded from
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from 6 distinct geographic areas ( 9 ) that are not completely representative of the US adolescent population, and estimates of undiagnosed diabetes cannot be obtained from SEARCH. Obtaining nationally representative, reliable prevalence esti- mates for undiagnosed T2DM is important because it is possi- ble that some of the reported increase in T2DM prevalence might be due to changing diagnostic standards across time and region (diagnostic bias), as well as increased awareness resulting in surveillance bias ( 16 ). The literature on autism incidence provides a recent and compelling example of how diagnostic and surveillance bias can misrepresent secular trends in pediatric conditions ( 21 , 22 ). An accurate prevalence esti- mate of adolescent diabetes is necessary for informing public health prevention efforts and screening policy. The purpose of this study was to determine the prevalence of diagnosed and undiagnosed T2DM among adolescents. These results arise from 6 nationally representative serial cross-sections of US adolescents enrolled in the Continuous National Health and Nutrition Examination Survey (NHANES) during a 12- year time period from 1999 to 2010. MATERIALS AND METHODS The Continuous NHANES is a complex, multistage prob- ability sample of US noninstitutionalized civilians that began in 1999. It consists of 6 unique data sets that have been gen- erated in 2-year cycles (i.e., 1999 2000, 2001 2002, 2003 2004, 2005 5006, 2007 2008, and 2009 2010) ( 23 ). Each 2-year survey cycle examines a nationally representative sam- ple of approximately 10,000 persons and collects a variety of health-related data via questionnaire, physical examination, andlaboratoryassessments.Participationratesforthe6survey cycles have ranged from 78% to 84%. The current analysis included 11,888 adolescents aged 12 19 years who responded to a diabetes questionnaire (the inter- view sample). Among these 11,888 adolescents, a randomly selected subgroup of 4,661 also provided a fasting blood sam- ple (the fasting subsample). Therefore, all 11,888 participants responded to interviewer-administered questionnaires, while only 4,661 participants also provided a fasting blood sample. Responses to interviewer-administered questionnaires were provided by a proxy for participants under 16 years of age; all other participants provided self-report responses. The NHANES protocol was approved by the National Center for Health Statistics institutional review board, and written informed consent was obtained from all participants. Fasting glucose assessments Fasting status was veri ed via interview prior to blood collection. During the years 1999 2004, glucose measure- ments for NHANES were performed by the Diabetes Diag- nostic Laboratory at the University of Missouri-Columbia using the Cobas Mira Chemistry System (Roche Diagnostic Systems, Inc., Montclair, New Jersey). In 2005 2006, mea- surements were performed by the Fairview Medical Center Laboratory at the University of Minnesota using a Roche/ Hitachi 911 Analyzer (Roche Diagnostics, Indianapolis, Indi- ana). In the NHANES 2007 2010 survey cycle, glucose mea- surements were still performed at the University of Minnesota, but the Roche Modular P Chemistry Analyzer (Roche Diag- nostics) was used. In all surveycycles and laboratories, fasting glucose was measured according to a hexokinase enzymatic method ( 24 ). All glucose values measured from 2005 to 2010 were standardized to the 1999 2004 values using regression equations provided in the analytical notes of the NHANES data documentation for glucose measurement ( 25 , 26 ). Diabetes classification Diagnosed diabetes was de ned on the basis of a partici- pant self-report of a previous diabetes diagnosis by a physician or health professional, as has been done in previous studies ( 7 , 8 ). Two respondents who reported no or borderline for diabetes but reported that they were taking diabetic pills to lower blood sugar were conservatively classi ed as diabetes- free. Participants who reported either no medication use or use of any blood glucose-lowering medication (with or without insulin) were de ned as having T2DM, while participants who reported only insulin use were de ned as having type 1 diabe- tes mellitus (T1DM). This approach differs from previously used epidemiologic case de nitions of diabetes ( 7 , 8 )intha t participants receiving both insulin and oral hypoglycemic agents were classi ed as having T2DM, whereas in previous studies all subjects receiving any insulin therapy had been classi ed as having T1DM. Approximately 25% 30% of per- sons with T2DM are treated with insulin (usually along with oral hypoglycemic agents) ( 27 , 28 ), while very few persons with T1DM are treated with oral hypoglycemic agents ( 29 , 30 ). Therefore, our current approach, while not perfect, was less likely to underestimate the prevalence of T2DM while having little impact on the underestimation of T1DM, as previously discussed ( 14 ). In the fasting subsample, diagnosed diabetes was de ned as above (irrespective of fasting glucose values) and undiag- nosed diabetes was de ned by a fasting blood glucose con- centration of 126 mg/dL among participants who did not report a previous diabetes diagnosis during the interview ( 31 ). All undiagnosed diabetes cases were classi ed as T2DM ( 7 ). Estimates of the prevalence of diagnosed diabetes were derived from both the interview sample (diagnosed) and the fasting subsample (undiagnosed) for comparative purposes, but we based all nal inferences regarding the prevalence of undiagnosed diabetes on the results obtained from the inter- view sample because the sample size was approximately 3 times larger, resulting in more precise estimates. Statistical analysis Survey procedures in SAS, version 9.3 (SAS Institute, Inc., Cary, North Carolina), were used for all analyses to obtain the correct variance estimates and corresponding 95% con - dence intervals. Publicly available survey weights were gen- erated for all 6 continuous NHANES survey cycles by the Centers for Disease Control and Prevention (CDC). These survey weights were used to create a nal analysis survey weight, per the CDC protocol ( 32 ), enabling the generation of prevalence estimates and absolute counts representative of US adolescents aged 12 19 years at the midpoint of the combined 12-year survey period. Survey weights are necessary Diabetes Prevalence Among Adolescents 1107 Am J Epidemiol. 2013;178(7):1106 1113 at Harvard University on March 16, 2014 Downloaded from
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1. What is the research question (aim of the research)? 2. Describe how the participants for this study were chosen. 3. What type of epidemiologic study design is this? 4. Was this an appropriate design give the aim of the study? 5. What was the main outcome (dependent variable) of interest and what type of variable is it? How was the outcome assessed/operationally defined for the analysis? 6. What were the independent variables included in the main analyses? How were they operationally defned/assessed? What types oF variables are they? 7. What are the key findings from table 1? 8. How does table 3 differ from table 1? 9. What are the key points from table 3? 10. What are the potential limitations of this study?
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