Prediabetes among HIV-infected individuals receiving antiretroviral therapy: prevalence, diagnostic tests, and associated factors

Angsana Phuphuakrat, Hataikarn Nimitphong, Sirimon Reutrakul, Somnuek Sungkanuparph, Angsana Phuphuakrat, Hataikarn Nimitphong, Sirimon Reutrakul, Somnuek Sungkanuparph

Abstract

Background: Metabolic complications in human immunodeficiency virus (HIV)-infected individuals are common. Prediabetes represents a high risk for future diabetes development. This study aimed to determine the prevalence, diagnostic methods, and associated factors of prediabetes among HIV-infected individuals receiving antiretroviral therapy (ART).

Methods: A cross-sectional study was conducted among HIV-infected adults without a history of diabetes who were receiving ART. Fasting plasma glucose (FPG), 2-hour plasma glucose (2-h PG) after a 75-g oral glucose tolerance test, and hemoglobin A1c (HbA1c) were assessed.

Results: A total of 397 patients with a mean age of 47.0 ± 9.8 years and 55.7% male, were studied. All received ART with undetectable plasma viral load. The mean duration of ART was 9.6 ± 5.2 years, and the mean CD4 cell count was 554 ± 235 cells/mm3. Among the patients, 28 (7.1%) had first-diagnosed diabetes, and 133 (33.5%) patients had prediabetes. Glycemia estimation by FPG, 2-h PG, and HbA1c showed a prediabetes prevalence of 17.4%, 14.7%, and 12.5%, respectively. The kappa statistics for the agreement of FPG and 2-h PG, HbA1c and 2-h PG, and HbA1c and FPG were 0.317, 0.429, and 0.396, respectively. In multivariate analysis, hypertension [odds ratio (OR) 3.38; 95% confidence interval (CI), 1.16-9.91; p = 0.026), and triglycerides > 150 mg/dL (OR 2.11; 95% CI, 1.01-4.44; p = 0.047) were factors significantly associated with prediabetes.

Conclusions: Prediabetes among HIV-infected individuals receiving ART is common. The agreements of glycemia estimation methods are minimal to weak. HbA1c may underestimate prediabetes prevalence. Using FPG together with HbA1c increases the detection rate to approximately three-quarters of prediabetes patients. HIV-infected individuals who had hypertension and hypertriglyceridemia should be regularly assessed for prediabetes. Trial registration ClinicalTrial.gov, NCT03545217. Registered 1 June 2018-Retrospectively registered, https://ichgcp.net/clinical-trials-registry/NCT03545217.

Keywords: Antiretroviral therapy; Associated factors; Diagnostic test; HIV; Prediabetes; Prevalence.

Conflict of interest statement

The authors declare no conflict of interest for this article.

Figures

Fig. 1
Fig. 1
Diagnosis of prediabetes in HIV-infected individuals using fasting plasma glucose (FPG), 2-hour plasma glucose (2-h PG) after performing 75-g oral glucose tolerance test (OGTT), and hemoglobin A1c (HbA1c)

References

    1. Brown TT, Cole SR, Li X, Kingsley LA, Palella FJ, Riddler SA, et al. Antiretroviral therapy and the prevalence and incidence of diabetes mellitus in the multicenter AIDS cohort study. Arch Intern Med. 2005;165:1179–1184. doi: 10.1001/archinte.165.10.1179.
    1. Kalayjian RC, Machekano RN, Rizk N, Robbins GK, Gandhi RT, Rodriguez BA, et al. Pretreatment levels of soluble cellular receptors and interleukin-6 are associated with HIV disease progression in subjects treated with highly active antiretroviral therapy. J Infect Dis. 2010;201:1796–1805. doi: 10.1086/652750.
    1. Neuhaus J, Jacobs DR, Jr, Baker JV, Calmy A, Duprez D, La Rosa A, et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis. 2010;201:1788–1795. doi: 10.1086/652749.
    1. Bourgi K, Wanjalla C, Koethe JR. Inflammation and metabolic complications in HIV. Curr HIV/AIDS Rep. 2018;15:371–381. doi: 10.1007/s11904-018-0411-2.
    1. Betene ADC, De Wit S, Neuhaus J, Palfreeman A, Pepe R, Pankow JS, et al. Interleukin-6, high sensitivity C-reactive protein, and the development of type 2 diabetes among HIV-positive patients taking antiretroviral therapy. J Acquir Immune Defic Syndr. 2014;67:538–546. doi: 10.1097/QAI.0000000000000354.
    1. Diabetes Prevention Program Research Group. Knowler WC, Fowler SE, Hamman RF, Christophi CA, Hoffman HJ, et al. 10-year follow-up of diabetes incidence and weight loss in the diabetes prevention program outcomes study. Lancet. 2009;374:1677–1686. doi: 10.1016/S0140-6736(09)61457-4.
    1. Forouhi NG, Luan J, Hennings S, Wareham NJ. Incidence of Type 2 diabetes in England and its association with baseline impaired fasting glucose: the Ely study 1990-2000. Diabet Med. 2007;24:200–207. doi: 10.1111/j.1464-5491.2007.02068.x.
    1. Nathan DM, Davidson MB, DeFronzo RA, Heine RJ, Henry RR, Pratley R, et al. Impaired fasting glucose and impaired glucose tolerance: implications for care. Diabetes Care. 2007;30:753–759. doi: 10.2337/dc07-9920.
    1. Barr EL, Zimmet PZ, Welborn TA, Jolley D, Magliano DJ, Dunstan DW, et al. Risk of cardiovascular and all-cause mortality in individuals with diabetes mellitus, impaired fasting glucose, and impaired glucose tolerance: the Australian Diabetes, Obesity, and Lifestyle Study (AusDiab) Circulation. 2007;116:151–157. doi: 10.1161/CIRCULATIONAHA.106.685628.
    1. Emerging Risk Factors Collaboration. Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375:2215–2222. doi: 10.1016/S0140-6736(10)60484-9.
    1. Hoehner CM, Greenlund KJ, Rith-Najarian S, Casper ML, McClellan WM. Association of the insulin resistance syndrome and microalbuminuria among nondiabetic native Americans. The Inter-Tribal Heart Project. J Am Soc Nephrol. 2002;13:1626–1634. doi: 10.1097/01.ASN.0000015762.92814.85.
    1. Melsom T, Mathisen UD, Ingebretsen OC, Jenssen TG, Njolstad I, Solbu MD, et al. Impaired fasting glucose is associated with renal hyperfiltration in the general population. Diabetes Care. 2011;34:1546–1551. doi: 10.2337/dc11-0235.
    1. Nguyen TT, Wang JJ, Wong TY. Retinal vascular changes in pre-diabetes and prehypertension: new findings and their research and clinical implications. Diabetes Care. 2007;30:2708–2715. doi: 10.2337/dc07-0732.
    1. Plantinga LC, Crews DC, Coresh J, Miller ER, 3rd, Saran R, Yee J, et al. Prevalence of chronic kidney disease in US adults with undiagnosed diabetes or prediabetes. Clin J Am Soc Nephrol. 2010;5:673–682. doi: 10.2215/CJN.07891109.
    1. Dream Trial Investigators. Gerstein HC, Yusuf S, Bosch J, Pogue J, Sheridan P, et al. Effect of rosiglitazone on the frequency of diabetes in patients with impaired glucose tolerance or impaired fasting glucose: a randomised controlled trial. Lancet. 2006;368:1096–1105. doi: 10.1016/S0140-6736(06)69420-8.
    1. Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002;346:393–403. doi: 10.1056/NEJMoa012512.
    1. Chantrathamachart P, Sungkanuparph S, Kiertiburanakul S, Malathum K. Diabetes mellitus and hypertension in HIV-infected patients receiving antiretroviral therapy: a pilot study. J Infect Dis Antimicrob Agent. 2006;23:131–138.
    1. Kim PS, Woods C, Georgoff P, Crum D, Rosenberg A, Smith M, et al. A1C underestimates glycemia in HIV infection. Diabetes Care. 2009;32:1591–1593. doi: 10.2337/dc09-0177.
    1. Slama L, Palella FJ, Jr, Abraham AG, Li X, Vigouroux C, Pialoux G, et al. Inaccuracy of haemoglobin A1c among HIV-infected men: effects of CD4 cell count, antiretroviral therapies and haematological parameters. J Antimicrob Chemother. 2014;69:3360–3367. doi: 10.1093/jac/dku295.
    1. Hoffman R, Benz EJJ, Shatti SJ, Furie B. Hematology: basic principles and practice. New York: Churchill-Livingstone; 2004.
    1. American Diabetes Association. 2. Classification and Diagnosis of Diabetes. Diabetes Care. 2017;40:S11-S24.
    1. Aekplakorn W, Chariyalertsak S, Kessomboon P, Sangthong R, Inthawong R, Putwatana P, et al. Prevalence and management of diabetes and metabolic risk factors in Thai adults: the Thai National Health Examination Survey IV, 2009. Diabetes Care. 2011;34:1980–1985. doi: 10.2337/dc11-0099.
    1. Rhee JY, Bahtila TD, Palmer D, Tih PM, Aberg JA, LeRoith D, et al. Prediabetes and diabetes among HIV-infected adults in Cameroon. Diabetes Metab Res Rev. 2016;32:544–549. doi: 10.1002/dmrr.2792.
    1. Njuguna B, Kiplagat J, Bloomfield GS, Pastakia SD, Vedanthan R, Koethe JR. Prevalence, risk factors, and pathophysiology of dysglycemia among people living with HIV in sub-Saharan Africa. J Diabetes Res. 2018;2018:6916497. doi: 10.1155/2018/6916497.
    1. Srivanich N, Ngarmukos C, Sungkanuparph S. Prevalence of and risk factors for pre-diabetes in HIV-1-infected patients in Bangkok, Thailand. J Int Assoc Physicians AIDS Care (Chic). 2010;9:358–361. doi: 10.1177/1545109710373832.
    1. Camacho JE, Shah VO, Schrader R, Wong CS, Burge MR. Performance of A1c versus Ogtt for the diagnosis of prediabetes in a community-based screening. Endocr Pract. 2016;22:1288–1295. doi: 10.4158/EP161267.OR.
    1. Pinelli NR, Jantz AS, Martin ET, Jaber LA. Sensitivity and specificity of glycated hemoglobin as a diagnostic test for diabetes and prediabetes in Arabs. J Clin Endocrinol Metab. 2011;96:E1680–E1683. doi: 10.1210/jc.2011-1148.
    1. McHugh ML. Interrater reliability: the kappa statistic. Biochem Med (Zagreb). 2012;22:276–282. doi: 10.11613/BM.2012.031.
    1. Aekplakorn W, Tantayotai V, Numsangkul S, Sripho W, Tatsato N, Burapasiriwat T, et al. Detecting prediabetes and diabetes: agreement between fasting plasma glucose and oral glucose tolerance test in Thai adults. J Diabetes Res. 2015;2015:396505. doi: 10.1155/2015/396505.
    1. Coelho AR, Moreira FA, Santos AC, Silva-Pinto A, Sarmento A, Carvalho D, et al. Diabetes mellitus in HIV-infected patients: fasting glucose, A1c, or oral glucose tolerance test—which method to choose for the diagnosis? BMC Infect Dis. 2018;18:309. doi: 10.1186/s12879-018-3221-7.
    1. Sakamoto N, Hu H, Nanri A, Mizoue T, Eguchi M, Kochi T, et al. Associations of anemia and hemoglobin with hemoglobin A1c among non-diabetic workers in Japan. J Diabetes Investig. 2019.
    1. George C, Matsha TE, Korf M, Zemlin AE, Erasmus RT, Kengne AP. The agreement between fasting glucose and markers of chronic glycaemic exposure in individuals with and without chronic kidney disease: a cross-sectional study. BMC Nephrol. 2020;21:32. doi: 10.1186/s12882-020-1697-z.
    1. Jung M, Warren B, Grams M, Kwong YD, Shafi T, Coresh J, et al. Performance of non-traditional hyperglycemia biomarkers by chronic kidney disease status in older adults with diabetes: results from the Atherosclerosis Risk in Communities Study. J Diabetes. 2018;10:276–285. doi: 10.1111/1753-0407.12618.
    1. Rhee MK, Ho YL, Raghavan S, Vassy JL, Cho K, Gagnon D, et al. Random plasma glucose predicts the diagnosis of diabetes. PLoS ONE. 2019;14:e0219964. doi: 10.1371/journal.pone.0219964.
    1. Liu HH, Cao YX, Li S, Guo YL, Zhu CG, Wu NQ, et al. Impacts of prediabetes mellitus alone or plus hypertension on the coronary severity and cardiovascular outcomes. Hypertension. 2018;71:1039–1046. doi: 10.1161/HYPERTENSIONAHA.118.11063.
    1. Bhowmik B, Siddiquee T, Mujumder A, Afsana F, Ahmed T, Mdala IA, et al. Serum lipid profile and its association with diabetes and prediabetes in a rural Bangladeshi population. Int J Environ Res Public Health. 2018;15:1944. doi: 10.3390/ijerph15091944.
    1. Desouky DE, Kasemy Z, Abdel-Hamid AE, Omar MS. Insulin resistance and prediabetes in hepatitis C virus patients. Am J Med Sci. 2015;350:77–80. doi: 10.1097/MAJ.0000000000000513.

Source: PubMed

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