Associations of High Density Lipoprotein Cholesterol and Framingham Cardiovascular Risk with Diabetic Retinopathy in African Type 2 Diabetics


Objectives: To assess the associations of high density lipoprotein cholesterol (HDL-C) and Framingham cardiovascular (CVD) with diabetic retinopathy (DR). Methods: A cross-sectional study of random sample of 200 T2DM Central Africans. Sociobiographical, laboratory and eye examination main outcome measures were investigated using Tertiles of HDL-C (stratification = lowest < 40 mg/dL, normal or interdemiate = 40 - 74.9 mg/dL, highest ≥ 75 mg/dL) and Framingham risk stratification (<10% and ≥10%) by logistic regression models. Results: Out of 200 T2DM patients, 120 (35.5%) had DR and out of DR patients, 116 (n = 96.7%) had VD. There was a significant U- shaped relationship between DR rates and HDL-C stratification. In the normal HDL-C group, elevated 8-hydroxydeoxyguanosine and 10-year Framingham risk > 10% were the significant independent determinants for DR. In the highest HDL-C group, smoking status and 10-year Framingham risk ≥ 10% were the significantly independent determinants for DR. In 10-year Framingham risk ≥ 10% group, smoking status, insulin resistance and increasing levels of HDL-C were the significantly independent determinants for DR. Conclusion: DR and VD remain a public health problem in T2DM Central Africans. Some Central Africans with DR and VD appear to have higher HDL-C than T2DM Central Africans without DR and VD. HDL-C in T2DM patients with DR, may be tightly controlled by genetic factors (black Bantu ethnicity) than the other lipoproteins as reported among Indians, African-Americans, and Japanese individuals. The most preventable environmental risk factors for DR were smoking status, global cardiovascular disease risk, insulin resistance and oxidative stress.

Share and Cite:

Longo-Mbenza, B. , Muaka, M. , Gombet, T. , Phemba, I. , Cook, S. and Mengome, E. (2014) Associations of High Density Lipoprotein Cholesterol and Framingham Cardiovascular Risk with Diabetic Retinopathy in African Type 2 Diabetics. World Journal of Cardiovascular Diseases, 4, 179-188. doi: 10.4236/wjcd.2014.44026.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Haffner, S.M., Hazuda, H.P., Stern, M.P., Patterson, J.K., Van Heuven, W.A.J. and Fong, D. (1989) Effect of Socio-economic Status on Hyperglycemia and Retinopathy Levels in Mexican Americans with NIDDM. Diabetes Care, 12, 128-134.
[2] Blaum, C.S., Velez, L., Hiss, R.G. and Halter, J.B. (1997) Characteristics Related to Poor Glycemic Control in NIDDM Patients in Community Practice. Diabetes Care, 20, 7-11.
[3] Harris, M.I., Eastman, R.C., Cowie, C.C., Flegal, K.M. and Eberhardt, M.S. (1999) Racial and Ethnic Differences in Glycemic Control of Adults with Type 2 Diabetes. Diabetes Care, 22, 403-408.
[4] The Expert Committee on the Diagnosis and Classi?cation of Diabetes Mellitus (1977) Report of the Expert Committee on the Diagnosis and Classi?cation of Diabetes Mellitus. Diabetes Care, 20, 1183-1197.
[5] Knuiman, M.W., Welborn, T.A., McCann, V.J., Stanton, K.G. and Constable, I.J. (1986) Prevalence of Diabetic Complications in Relation to Risk Factors. Diabetes, 35, 1332-1339.
[6] Kuusisto, J., Mykkanen, L., Pyorala, K. and Laakso, M. (1994) NIDDM and Its Metabolic Control Predict Coronary Heart Disease in Elderly Subjects. Diabetes, 43, 960-967.
[7] Gilmer, T.P., O’Connor, P.J., Manning, W.G. and Rush, W.A. (1997) The Cost to Health Plans of Poor Glycemic Control. Diabetes Care, 20, 1847-1853.
[8] Sasongko, M.B., Wong, T.Y., Nguyen, T.T., Kawasaki, R., Jenkins, A., Shaw, J. and Wang, J.J. (2011) Serum Apolipoprotein AI and B Are Stronger Biomarkers of Diabetic Retinopathy than Traditional Lipids. Diabetes Care, 34, 474-479.
[9] Peter, R., Okoseime, O.E., Rees, A. and Owens, D.R. (2009) Postprandial Glucose—A Potential Therapeutic Target to Reduce Cardiovascular Mortality. Current Vascular Pharmacology, 7, 68-74.
[10] Sivaprasad, S., Gupta, B., Crosby-Nwaobi, R. and Evans, J. (2012) Prevalence of Diabetic Retinopathy in Various Ethnic Groups: A Worldwide Perspective. Survey of Ophthalmology, 57, 347-370.
[11] Harris, M.I. (1995) Health Insurance and Diabetes. In: Harris, M.I., Cowie, C.C., Reiber, G., Boyko, E., Stem, M. and Bennett, P., Eds., Diabetes in America, 2nd Edition, Government Printing Office, Washington DC, 591-600.
[12] Damkondwar, D.R., Raman, R., Suganeswari, G., Kulothungan, V. and Sharma, T. (2012) Assessing Framingham Cardiovascular Risk Scores in Subjects with Diabetes and Their Correlation with Diabetic Retinopathy. Indian Journal of Ophthalmology, 60, 45-48.
[13] Agirbasli, M., Agaoglu, N.B., Ergonul, O., Yagmur, I., Aydogar, H., Oneri, T. and Ozturk, O. (2011) Comparison of Anthropometric Indices in Predicting Metabolic Syndrome Components in Children. Metabolic Syndrome and Related Disorders, 9, 453-459.
[14] Gombet, T., Longo-Mbenza, B., Ellenga-Mbolla, B., Ikama, M.S., Mokondjimobe, E., Kimbally, K.G. and Nkoua, J.L. (2012) Aging, Female Sex, Migration, Elevated HDL-C, and Inflammation Are Associated with Prevalence of Metabolic Syndrome among African Bank Employees. International Journal of General Medicine, 5, 495-503.
[15] Kalk, W.J. and Joffe, B.I. (2008) The Metabolic Syndrome, Insulin Resistance, and Its Surrogates in African and White Subjects with Type 2 Diabetes in South Africa. Metabolic Syndrome and Related Disorders, 6, 247-255.
[16] Davie, S.J., Gould, B.J. and Yudkin, J.S. (1992) Effect of Vitamin C on Glycosylation of Proteins. Diabetes, 41, 167-173.
[17] Longo-Mbenza, B., Muaka, M.M., Yokobo, E.C., Phemba, I.L., Mokondjimobe, E., Gombet, T., Ndembe, D.K., Mona, D.T. and Masamba, S.W. (2012) Effects of Biomarkers of Oxidative Stress Damage on Prevalence and Severity of Visual Disability among Black Central Africans. Molecular Vision, 18, 1619-1628.
[18] Longo-Mbenza, B., Muaka, M.M., Mokondjimobe, E., Ndembe, D.K., Mona, D.T. and Buassabu-Tsumbu, B. (2012) Oxidative Stress Related-Elevated High Gamma Glutamyl Transferase Levels, and Aging, Intake of Tropical Food Plants, Migration and Visual Disability in Central Africans. International Journal of Ophthalmology, 5, 493-498.
[19] Villines, T.C. and Taylor, A.J. (2012) Multi-Ethnic Study of Atherosclerosis Arterial Age versus Framingham 10-Year or Lifetime Cardiovascular Risk. American Journal of Cardiology, 110, 1627-1630.
[20] Myerson, M., Coady, S., Taylor, H., Rosamond, W.D., Goff Jr., D.C. and ARIC Investigators (2009) Declining Severity of Myocardial Infarction from 1987 to 2002: The Atherosclerosis Risk in Communities (ARIC) Study. Circulation, 119, 503-514.
[21] Chamnan, P., Simmons, R.K., Sharp, S.J., Griffin, S.J. and Wareham, N.J. (2009) Cardiovascular Risk Assessment Scores for People with Diabetes: A Systemic Review. Diabetologia, 52, 2001-2014.
[22] Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care, 26, S5-S20.
[23] IDF (2006) A Consensus Statement from the International Diabetes Federation. Diabet Med, 23, 469-480.
[24] Friedwald, W.T., Levy, R.I. and Fredrickson, D.S. (1972) Estimation of the Concentration of Low-Density Lipoprotein Cholesterol in Plasma, without Use of the Preparative Ultracentrifuge. Clinical Chemistry, 18, 499-502.
[25] Longo-Mbenza, B., Nkongo Mvindu, H., Kasiam On’kin, J.B., Bikuku, N., Kianu Phanzu, B., Nge Okwe, A. and Kabangu, N. (2011) The Deleterious Effects of Physical Inactivity on Elements of Insulin Resistance and Metabolic Syndrome in Central Africans at High Cardiovascular Risk. Diabetes & Metabolic Syndrome: Clinical Research Review, 5, 1-6.
[26] Agarwal, S., Raman, R., Paul, P.G., et al. (2005) Sankara Nethralaya—Diabetic Retinopathy Epidemiology and Molecular Genetic Study (SN—DREAMS 1): Study Design and Research Methodology. Ophthalmic Epidemiology, 12, 143-153.
[27] Kawasaki, R., Cheung, N., Islam, F.M., Klein, R., Klein, B.E., Cotch, M.F., Sharrett, A.R., O’Leary, D. and Wong, T.Y. (2011) Is Diabetic Retinopathy Related to Subclinical Cardiovascular Disease? Ophthalmology, 118, 860-865.
[28] Yau, J.W., Rogers, S.L., Kawasaki, R., Lamoureux, E.L., Kowalski, J.W., Bek, T., Chen, S.J., Dekker, J.M., Fletcher, A., Grauslund, J., Haffner, S., Hamman, R.F., Ikram, M.K., Kayama, T., Klein, B.E., Klein, R., Krishnaiah, S., Mayurasakorn, K., O’Hare, J.P., Orchard, T.J., Porta, M., Rema, M., Roy, M.S., Sharma, T., Shaw, J., Taylor, H., Tielsch, J.M., Varma, R., Wang, J.J., Wang, N., West, S., Xu, L., Yasuda, M., Zhang, X., Mitchell, P., Wong, T.Y. and Meta-Analysis for Eye Disease (META-EYE) Study Group (2012) Global Prevalence and Major Risk Factors of Diabetic Retinopathy. Diabetes Care, 35, 556-564.
[29] Liew, G., Klein, R. and Wong, T.Y. (2009) The Role of Genetics in Susceptibility to Diabetic Retinopathy. International Ophthalmology Clinics, 49, 35-52.
[30] Zhang, X., Saaddine, J.B., Chou, C.F., Cotch, M.F., Cheng, Y.J., Geiss, L.S., Gregg, E.W., Albright, A.L., Klein, B.E. and Klein, R. (2010) Prevalence of Diabetic Retinopathy in the United States, 2005-2008. JAMA, 304, 649-656.
[31] Sivaprasad, S., Gupta, B., Crosby-Nwaobi, R. and Evans, J. (2010) Prevalence of Diabetic Retinopathy in Various Ethnic Groups: A Worldwide Perspective. Survey of Ophthalmology, 57, 347-370.
[32] Sivaprasad, S., Gupta, B., Gulliford, M.C., Dodhia, H., Mann, S., Nagi, D. and Evans, J. (2012) Ethnic Variation in the Prevalence of Visual Impairment in People Attending Diabetic Retinopathy Screening in the United Kingdom (DRIVE UK). PLoS ONE, 7, Article ID: e39608.
[33] Nsiah-Kumi, P., Ortmeier, S.R. and Brown, A.E. (2009) Disparities in Diabetic Retinopathy Screening and Disease for Racial and Ethnic Minority Populations: A Literature Review. Journal of the National Medical Association, 101, 430-437.
[34] Muaka, M.M., Longo-Mbenza, B. and Kaimbo wa Kaimbo, D. (2009) Frequency and the Causes of Blindness and Visual Impairment among Patients with Diabetes Mellitus from DR Congo. Le Mali Médical, 24, 22-26.
[35] Moukouri, E.D.N., Moli, T. and Nouedoui, C. (1992) Les aspects épidémiologiques de la rétinopathie diabétique à Yaoundé. Médecine d’Afrique Noire, 39, 327-334.
[36] Longo-Mbenza, B., Muaka, M.M., Mbenza, G., Mbungu-Fuele, S., Mabwa-Mbalanda, L., Nzuzi Babeki, V. and Mbadi-A-Sungu, J. (2008) Risk Factors of Poor Control of HBA1c and Diabetic Retinopathy: Paradox with Insulin Therapy and High Values of HDL in African Diabetic Patients. International Journal of Diabetes and Metabolism, 16, 69-78.
[37] Longo-Mbenza, B., Kasiam Lasi On’kin, J.B., Nge Okwe, A. and Kangola Kabangu, N. (2011) The Metabolic Syndrome in a Congolese Population and Its Implications for Metabolic Syndrome Definitions. Diabetes & Metabolic Syndrome: Clinical Research & Reviews, 5, 17-24.
[38] Isezuo, S.A. (2005) Is High Density Lipoprotein Cholesterol Useful in Diagnosis of Metabolic Syndrome in Native Africans with Type 2 Diabetes? Ethnicity & Disease, 15, 6-10.
[39] Omolase, C.O., Adekanle, O., Owoeye, J.F.A. and Omolase, B.O. (2010) Diabetic Retinopathy in a Nigerian Community. Singapore Medical Journal, 51, 56-59.
[40] Longo-Mbenza, B., Nkondi Nsenga, J. and Vangu Ngoma, D. (2007) Prevention of the Metabolic Syndrome Insulin Resistance and the Atherosclerotic Diseases in Africans Infected by Helicobacter pylori Infection and Treated by Antibiotics. International Journal of Cardiology, 121, 229-238.
[41] Damkondwar, D.R., Raman, R., Suganeswari, G., Kulothungan, V. and Sharma, T. (2012) Assessing Framingham Cardiovascular Risk Scores in Subjects with Diabetes and Their Correlation with Diabetic Retinopathy. Indian Journal of Ophthalmology, 60, 45-48.
[42] Hartnett, M.E., Stratton, R.D., Browne, R.W., Rosner, B.A., Lanham, R.J. and Armstrong, D. (2000) Serum Markers of Oxidative Stress and Severity of Diabetic Retinopathy. Diabetes Care, 23, 234-240.
[43] Mancino, R., Di Pierro, D., Varesi, C., Cerulli, A., Feraco, A., Cedrone, C., Pinazo-Duran, M., Coletta, M. and Nucci, C. (2011) Lipid Peroxidation and Total Antioxidant Capacity in Vitreous, Aqueous Humor, and Blood Samples from Patients with Diabetic Retinopathy. Molecular Vision, 17, 1298-1304.
[44] Aldebasi, Y., Mohieldein, A., Almansour, Y. and Almoteri, B. (2011) Imbalance of Oxidant/Antioxidant Status and Risk Factors for Saudi Type 2 Diabetic Patients with Retinopathy. British Journal of Medicine & Medical Research, 1, 371-384.
[45] Kowluru, R.A. and Koppolu, P. (2002) Termination of Experimental Galactosemia in Rats, and Progression of Retinal Metabolic Abnormalities. Investigative Ophthalmology & Visual Science, 43, 3287-3291.
[46] Lepira, F.B., M’buyamba Kabangu, J.R., Kayembe, K.P. and Nseka, M.N. (2005) Correlates of Serum Lipids and Lipoprotein in Congolese Patients with Arterial Hypertension. Cardiovascular Journal of South Africa, 16, 249-255.
[47] Seedat, Y.K., Mayet, F.G.H., Latiff, G.H. and Joubert, G. (1993) Study of Risk Factors Leading to Coronary Heart Disease in Urban Zulus. Journal of Human Hypertension, 7, 529-532.
[48] Longo-Mbenza, B., Agongola Mambune, H.F., Kasiam, J.B., Kintoki Vita, E., Mbungu Fuele, S., Nkondi Senga, J., Mabwa, L. and Nzuzi, V. (2008) Positive Correlation between Waist Circumference, HDL-Cholesterol and Total Cholesterol in Central Africans with Congestive Heart Failure: Reverse Epidemiology and U-Shaped Relationship in Cardiovascular Risk. Circulation, 117, 677.
[49] Bruce, C., Sarp, D.S. and Tall, A.R. (1998) A Relationship of HDL and Coronary Heart Disease to a Common Amino-Acid Polymorphism in the Cholesteryl Ester Transfer Protein in Men with and without Hypertriglyceridemia. Journal of Lipid Research, 39, 1071-1078.
[50] Klos, K.L. and Kullo, I.J. (2007) Genetic Determinants of HDL: Monogenic Disorders and Contributions to Variation. Current Opinion in Cardiology, 22, 344-351.
[51] Guyard-Dangremont, V., Lagrost, L., Gambert, P. and Lallemant, C. (1994) Competitive Enzyme-Linked Immunosorbent Assay of the Human Cholesteryl Ester Transfer Protein (CETP). Clinica Chimica Acta, 231, 147-160.
[52] Brunham, L.R., Singaraja, R.R. and Hayden, M.R. (2006) Variations on a Gene: Rare and Common Variants in ABCA1 and Their Impact on HDL Cholesterol Levels and Atherosclerosis. Annual Review of Nutrition, 26, 105-129.
[53] Moss, S.E., Klein, R. and Kelin, B.E. (1996) Cigarette Smoking and Ten-Year Progression of Diabetic Retinopathy. Ophthalmology, 103, 1438-1442.
[54] Sich, D., Saidi, Y., Giral, P., Lagrost, L., Elgloff, M., Auer, C., Gautier, V., Turpin, G. and Beucler, I. (1998) Hyperal-phalipoproteinemia: Characterization of a Cardioprotective Profile Associating Increased High-Density Lipoprotein2 Levels and Decreased Hepatic Lipase Activity. Metabolism, 47, 965-973.
[55] Tyroler, H.A., Glueck, C.J., Christensen, B. and Kwiterovich Jr., P.O. (1980) Plasma High-Density Lipoprotein Cholesterol Comparisons in Black and White Populations. The Lipid Research Clinics Program Prevalence Study. Circulation, 62, IV99-IV107.
[56] Bower, J.F., Deshaies, Y., Pfeifer, M., Tanenberg, R.J. and Brarkat, H.A. (2002) Ethnic Differences in Postprandial Triglyceride Response to a Fatty Meal and Lipoprotein Lipase in Lean and Obese African American and Caucasian Women. Metabolism, 51, 211-217.
[57] Jaichander, P., Selvarajan, K., Garelnabi, M. and Parthasarathy, S. (2008) Induction of Paraoxonase 1 and Apolipo-protein A-1 Gene Expression by Aspririn. Journal of Lipid Research, 49, 2142-2148.
[58] Aviram, M., Rosenblat, M., Bisgaier, C.L., Newton, R.S., Primo-Parmo, S.L. and La Du, B.N. (1998) Paraoxonase Inhibits High-Density Lipoprotein Oxidation and Preserves Its Functions. A Possible Peroxidative Role for Paraoxonase. Journal of Clinical Investigation, 101, 1581-1590.

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.