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General and Abdominal Obesity and Incident Distal Sensorimotor 240 Diabetes Care Volume 42, February 2019 SabrinaSchlesinger,1,2 ChristianHerder,2,3,4 General and Abdominal Obesity Julia M. Kannenberg,2,3 Cornelia Huth,2,5 Maren Carstensen-Kirberg,2,3 and Incident Distal Sensorimotor Wolfgang Rathmann,1,2,4 Gidon J. Bonhof,¨ 3 Wolfgang Koenig,6,7,8 Margit Heier,5 Polyneuropathy: Insights Into Annette Peters,2,5 Christa Meisinger,5,9 fl Michael Roden,2,3,10 Barbara Thorand,2,5 In ammatory Biomarkers as and Dan Ziegler2,3,10 Potential Mediators in the KORA F4/FF4 Cohort Diabetes Care 2019;42:240–247 | https://doi.org/10.2337/dc18-1842 1Institute for Biometrics and Epidemiology, German Diabetes Center, Leibniz Center for Di- abetes Research at Heinrich Heine University OBJECTIVE Dusseldorf,¨ Dusseldorf,¨ Germany 2 To investigate the associations between different anthropometric measurements German Center for Diabetes Research, Munchen-Neuherberg,¨ Germany and development of distal sensorimotor polyneuropathy (DSPN) considering 3Institute for Clinical Diabetology, German Di- fl EPIDEMIOLOGY/HEALTH SERVICES RESEARCH interaction effects with prediabetes/diabetes and to evaluate subclinical in am- abetes Center, Leibniz Center for Diabetes Re- mation as a potential mediator. search at Heinrich Heine University Dusseldorf,¨ Dusseldorf,¨ Germany RESEARCH DESIGN AND METHODS 4Medical Faculty, Heinrich Heine University Dusseldorf,¨ Dusseldorf,¨ Germany This study was conducted among 513 participants from the Cooperative Health 5Institute of Epidemiology, Helmholtz Zentrum Research in the Region of Augsburg (KORA) F4/FF4 cohort (aged 62–81 years). Munchen,¨ German Research Center for Environ- Anthropometry was measured at baseline. Incident DSPN was defined by neu- mental Health, Neuherberg, Germany 6 ropathic impairments using the Michigan Neuropathy Screening Instrument at Deutsches Herzzentrum Munchen,¨ Technische Universitat¨ Munchen,¨ Munich, Germany baseline and follow-up. Associations between anthropometric measurements and 7German Center for Cardiovascular Research, DSPN were estimated by multivariable logistic regression. Potential differences by Partner Site Munich Heart Alliance, Munich, diabetes status were assessed using interaction terms. Mediation analysis was Germany 8 conducted to determine the mediation effect of subclinical inflammation in these Department of Internal Medicine II-Cardiology, University of Ulm Medical Center, Ulm, Germany associations. 9Chair of Epidemiology, Ludwig-Maximilians- Universitat¨ Munchen¨ am UNIKA-T Augsburg, RESULTS Augsburg, Germany After a mean follow-up of 6.5 years, 127 cases with incident DSPN were detected. 10Division of Endocrinology and Diabetology, Both general and abdominal obesity were associated with development of DSPN. Medical Faculty, Heinrich Heine University Dusseldorf,¨ Dusseldorf,¨ Germany The odds ratios (95% CI) of DSPN were 3.06 (1.57; 5.97) for overweight, 3.47 (1.72; Corresponding author: Sabrina Schlesinger, 7.00) for obesity (reference: normal BMI), and 1.22 (1.07; 1.38) for 5-cm differences [email protected] in waist circumference, respectively. Interaction analyses did not indicate any Received 31 August 2018 and accepted 4 differences by diabetes status. Two chemokines (C-C motif chemokine ligand 7 November 2018 [CCL7] and C-X-C motif chemokine ligand 10 [CXCL10]) and one neuron-specific This article contains Supplementary Data online marker (Delta/Notch-like epidermal growth factor–related receptor [DNER]) were at http://care.diabetesjournals.org/lookup/suppl/ identified as potential mediators, which explained a proportion of the total effect doi:10.2337/dc18-1842/-/DC1. up to 11% per biomarker. S.S. and C.He. contributed equally to this work. B.T. and D.Z. contributed equally to this work. CONCLUSIONS © 2018 by the American Diabetes Association. General and abdominal obesity were associated with incident DSPN among in- Readers may use this article as long as the work is properly cited, the use is educational and not dividuals with and without diabetes, and this association was partly mediated by fi fl for pro t, and the work is not altered. More infor- in ammatory markers. However, further mechanisms and biomarkers should be mation is available at http://www.diabetesjournals investigated as additional mediators to explain the remainder of this association. .org/content/license. care.diabetesjournals.org Schlesinger and Associates 241 Distal sensorimotor polyneuropathy (DSPN) cohort (9,10). It remains to be answered foot ulceration, ankle reflexes, and vi- is associated with several adverse health whether and to what extent these bio- bration perception threshold using the outcomes, including increased morbidity markers may explain the link between C 64 Hz Rydel-Seiffer tuning fork at such as foot ulcers and lower-extremity obesity and DSPN. the great toes. Age-dependent lower amputation, occurrence of chronic pain, The aims of this study were threefold. limits of normal for vibration perception depression, impaired quality of life, and First, we investigated the association be- threshold at the fifth percentile were risk of premature death (1,2). The prev- tween general and abdominal obesity and computed according to Martina et al. alence and incidence vary according to incident DSPN. Second, potential differen- (14) using the equation y = 5.75 2 assessment method of DSPN, prediabe- ces in these associations between individ- 0.026 3 age. The neuropathy assessment tes/diabetes status, and diabetes dura- uals with and without prediabetes/diabetes also included a bilateral examination of tion. The prevalence of DSPN has been were assessed. Third, inflammatory bio- sensory perception with a 10-g mono- estimated to be ;30% for hospital-based markers were considered as potential filament (Neuropen) (9). Thus, the total populations, 20% for the general pop- mediators of the observed associations. MNSI score ranged from 0 (all aspects ulation, and 10–15% for newly diagnosed normal) to a maximum of 10 points. patients with type 2 diabetes, whereas RESEARCH DESIGN AND METHODS Prevalent or incident DSPN were defined with longer duration of diabetes (.10 Study Design and Participants basedonacutoffvalueof.3pointsas years), the prevalence increases up to The study design has been described described in our previous study (9). 50% (3,4). Evidence has emerged sug- previously in detail (9,11). Briefly, this gesting that the prevalence of DSPN is prospective cohort study is based on the Assessment of Anthropometry increased even in individuals with pre- KORA F4 (2006–2008) and KORA FF4 Body weight, height, and waist and hip diabetes compared to those with normal studies (2013 to 2014), which are both circumferenceweremeasuredbytrained glucose tolerance (1). Major risk factors follow-up examinations of the KORA S4 personnel based on standard protocols of DSPN include advanced age, smoking, study (1999–2001), a population-based (12). Body weight was assessed in light and metabolic factors, such as diabetes, cohort study conducted in the region of clothing to the nearest 0.1 kg. BMI hyperglycemia, and obesity (5). Augsburg, Germany. (kg/m2) was calculated as a measure Previous studies that reported asso- The study sample is identical to the of general body fatness, and individ- ciations between obesity, measured by sample used for a comprehensive anal- uals with a BMI of 18.5 to ,25 kg/m2 BMI or waist circumference, and DSPN ysis of associations between biomarkers were defined as normal weight, 25 to were mostly cross-sectional (2–6). Only of inflammation and incident DSPN (10). ,30 kg/m2 as overweight, and $30 one recent prospective study reported Briefly, out of the 1,161 KORA F4 study kg/m2 as obese (15). Waist circumfer- a positive association between obesity participants aged 62–81 years, we ex- ence was measured at the minimum and increased risk of diabetic polyneu- cluded participants with missing in- abdominal girth, and hip circumference ropathy (7,8). Further data on this relation- formation of exposure variables and was assessed at the maximum protrusion ship are lacking, and the previous study covariates (n = 113), missing follow-up of the hips at the level of the symphysis focused only on DSPN in patients with information (n = 452), and prevalent pubis to the nearest 0.1 cm (16). Ab- type 2 diabetes. It remains unclear DSPN (n = 83), resulting in an analysis dominal obesity was defined by the waist whether diabetes or prediabetes, de- sample of 513 participants. circumference according to the classifi- fined as impaired fasting glucose (IFG) Characteristics of the cohort, including cation of the International Diabetes and/or impaired glucose tolerance (IGT), age, sex, socioeconomic status, anthro- Federation (IDF) with sex-specific cutoff are effect modifiers of the relationship pometry, metabolic variables, lifestyle points (,94 vs. $94 cm for men and ,80 between obesity and DSPN. Moreover, factors, and glucose tolerance status vs. $80 cm for women) (17) and accord- the underlying mechanisms explaining using standard 75-g oral glucose toler- ing to the classification of the World this association are not well understood. ance tests were assessed as previously Health Organization (WHO) (,102 vs. A possible mediator for this relationship reported. Prediabetes was defined as the $102 cm for men and ,88 vs. $88 might be a low-grade inflammatory state. presence of IFG and/or IGT (12,13). DSPN cm for women) (15). Further measures In two recent reports, two proinflamma- was assessed at baseline and follow- for abdominal obesity were defined by
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