|Year : 2009 | Volume
| Issue : 1 | Page : 77-85
|Microvascular and macrovascular complications in diabetic nephropathy patients referred to nephrology clinic
Jamal S Al-Wakeel, Durdana Hammad, Abdulkaraem Al Suwaida, AH Mitwalli, Nawaz Ali Memon, Fathia Sulimani
Division of Nephrology, Department of Medicine, King Saud University Riyadh, Saudi Arabia
Click here for correspondence address and email
| Abstract|| |
To evaluate the diabetic complications and fate of diabetic nephropathy in Saudi population, we studied 184 diabetic nephropathy (DN) patients who were referred to nephrology clinic of King Khalid University Hospital, Riyadh, Saudi Arabia from January 2003-June 2006. The patients had mean age of 61.9 ± 13.1 years, included 128 (69.6%) males, and were followed up for a mean period of 10.2 ± 1.5 years. The mean duration of diabetes mellitus (DM) was 19.5 ± 5.8 years, and duration of nephropathy was 7.7 ± 3.3 years. Family history of DN was documented in 52 (28.2%) patients. At initial visit, the mean systolic blood pressure was 164 ± 14.5 mmHg, the mean diastolic blood pressure was 97.9 ± 10.4 mmHg. Thirtyseven (20%) patients had normal BMI, 88 (48%) were overweight, while 55 (30%) were obese. Mean creatinine clearance was 51.7 ± 26.3 mL/min, 24 hrs urinary proteins 1.99 ± 2.48 gm/day, HbA1C 9.2 ± 1.8 %, triglyceride 2.1 ± 1.3 mmol/L, and cholesterol 5.17 ± 1.54 mmol/L. Diabetic complications included angiography proven coronary artery disease in 106 (57.6 %) patients, stroke in 21 (11.4%), myocardial infarction (MI) in 27(14.6%), angina in 87 (47.2 %), retinopathy in 82 (44.5%), Blindness in 3 (1.6%), peripheral vascular disease in 121 (65.7%), Neuropathy in 123 (66.8%), hypertension in178 (96.7%), diabetic foot in 25 (13.5%), Amputation in 10 (5.4%), and end-stage renal disease in 70 (38%). Total of 13 (7.05%) patients died in the hospital. Thirty-seven percent of patients developed > 6 concomitant complications. 28% developed 5, 17% developed 4, and the rest developed < 3. DN was relatively refractory to therapy and progressive; 123 (66.8%) patients doubled their serum creatinine in 3.59 ± 2.88 years, 32 (17.3%) maintained stable renal function, 136 (73.6 %) deteriorated, and 12 (6.52%) improved. we conclude that the prevalence of diabetic complications is high among Saudi patients, and many had multiple complications. Baseline creatinine clearance and proteinuria, high systolic blood pressure, advanced age, and longer duration of diabetes were the most significant risk factors for developing complications.
Keywords: Diabetic nephropathy, Diabetic complications, ESRD, Retinopathy, Neuropathy, Diabetic foot, Coronary artery disease
|How to cite this article:|
Al-Wakeel JS, Hammad D, Al Suwaida A, Mitwalli A H, Memon NA, Sulimani F. Microvascular and macrovascular complications in diabetic nephropathy patients referred to nephrology clinic. Saudi J Kidney Dis Transpl 2009;20:77-85
|How to cite this URL:|
Al-Wakeel JS, Hammad D, Al Suwaida A, Mitwalli A H, Memon NA, Sulimani F. Microvascular and macrovascular complications in diabetic nephropathy patients referred to nephrology clinic. Saudi J Kidney Dis Transpl [serial online] 2009 [cited 2020 May 26];20:77-85. Available from: http://www.sjkdt.org/text.asp?2009/20/1/77/44710
| Introduction|| |
Diabetic nephropathy is the leading cause of end stage renal disease (ESRD), ,,, diabetic patients with diabetic nephropathy (DN) are at higher risk of fatal and non fatal cardiovascular and other complications. ,,, Not only stroke and myocardial infarction but retinopathy and peripheral vascular disease have correlation with DN, ,,,,,, which has a genetic and racial predisposition, ,, while environmental and biochemical factors trigger the genetically prone individuals. Increasing modernization with sedentary life style and lack of physical activity is favoring increased incidence of obesity, diabetes and its complications.  In a recent report from U.S.A. released in April 2007 the importance of quantification of diabetic complications was emphasized. 
In Saudi Arabia, trends of diabetes and diabetic nephropathy are increasing tremendously. Al Wakeel et al reported diabetic nephropathy to be the leading cause of Chronic renal failure (CRF). ,,, The incidence of DN signals a medical catastrophe in dialysis units in ESRD patients whose original kidney disease is DN in addition to consumption of economic resources.  Management of diabetes is a national issue, and a reassessment besides urgent action is needed.
Studies on diabetic complications conducted in Saudi Arabia are very few. In 1995, Huraib et al have addressed the pattern of DN in the region. While Al Khader  followed 28 diabetic nephropathy patients and reported the outcome that 42.8% became dialysis dependent and similar percentage doubled their serum creatinine. There is no recent systematic and detailed report on diabetic complications with reference to DN in Saudi population, and this is the first comprehensive study report from this region.
| Patients and Methods|| |
Present study is a cross sectional retrospecttive study of patients referred to nephrology clinic of King Khalid University Hospital, a tertiary hospital in Riyadh-Saudi Arabia, from Jan 2003-June 2006. Eligible patients screened were clinically diagnosed DN patients according to World Health Organization (WHO) criteria.  There were 184 diabetic nephropathy patients included in the study.
Demographics and patients' height and weight were recorded, and body mass index (BMI) was calculated.
Blood investigations included blood glucose, HbA1C, cholesterol, Triglycerides (TG), serum creatinine, creatinine clearance, and24-hour urinary protein.
Glomerular filtration rate (GFR) was calculated using Kockroft and Gualt equation:
GFR= (140-Age (yrs) × Weight (kg) × 1.23/Serum Creatinine µmol (for males)
GFR= (140-Age (yrs) × Weight (kg) × 1.02/Serum Creatinine µmol (for females)
Rate of change of GFR was calculated. Renal function was considered to be stable if yearly change of GFR was 1-2.5 mL, and it was considered deteriorated if yearly decrease of GFR was > 2.5 mL. While renal function was considered improved if yearly change of GFR was < 1 mL. Duration of follow-up, age at onset of diabetes, duration of complications, time for doubling of serum creatinine, and ESRD were recorded. Time course of all the above parameters were followed up carefully.
The target levels definitions were based on the guidelines of the American Diabetic Association, European Society of Hypertension, European Society of cardiology, the following recommended target levels were adopted: < 135/85 mmHg for blood pressure,< 7 % for HbA1C, < 1.4 mmol/L of TG,  and < 5.2 mmol/ L for cholesterol.
| Statistical Analysis|| |
SPSS for Windows Version 11 statistical package was used for analysis. ANOVA, Pearson's Correlation, followed by Regression analysis were performed as required. P value of < 0.05 was considered statistically significant.
| Results|| |
Of 184 diabetic nephropathy patients included in the study, 128 (69.6 %) were males patients, and mean age at the enrolment was 61.97 ± 13.1 years, (range, 19-85 years). The mean age for onset of diabetes was 42.4 ± 12.1 years with the (range, 6-68 years) .The mean duration of diabetes was 19.5 ± 5.8 years (range, 6-40 years), the mean follow-up in our hospital was 10.2 ± 1.5 years, and the mean age at the onset of nephropathy was 54.3 ± 12.5 years (range, 15-83 years). The mean duration of nephropathy was 7.7 ± 3.3 years (range, 2-14years). Family history of diabetic nephropathy was documented in 52 (39.6%) patients, and there were 6 (3.3%) active smokers in the study patients.
Body Mass Index (kg/m 2 )
At the initial visit, BMI normal (18.5-25) in only 37 (20%) patients 88 (8%) patients were overweight (BMI 25.1-30), 55 (30%) patients were obese (BMI 30.1-40), and only 3 (1.6%) patients were underweight. At the last visit, 2 (1%) patients were underweight, 34 (18.4%) patients remained stable, 80 (43.4%) patients were overweight, while 65 (33%) patients were obese (trend toward more weight gain).
At the initial visit, only 2 (1.1%) patients had the recommended systolic blood pressure (SBP) < 135 mmHg, while 182 (98.9%) had elevated SBP including 92 (50%) patients who had SBP between 135-160 mmHg, 82 (44.6%) between 160-190 mmHg, and 6 (3.3%) > 190 mmHg. At the last visit, 76 (41.3%) patients attained the recommended target level of SBP < 135 mmHg, (p= 0.0000), 86 (46.7%) between 135160 mmHg, 18 (9.8%) between 160-190 mmHg, and 1 (0.5%) > 190 mmHg.
Regarding the diastolic blood pressure (DBP), at the initial visit, 62 (33.7%) patients had the recommended DBP < 85 mmHg, 70 (38%) between 85-90 mmHg, 35 (19%) between 90100 mmHg, and 14 (7.6%) > 100 mmHg. At the last visit, 142 (77.2 %) patients had DBP < 85 mmHg, p= 0.0000, 33 (17.9%) between 8590 mmHg, 5 (2.7%) between 90-100 mmHg, and 2 (1.1%) > 100 mmHg.
Prevalence of Health Complications in Diabetic Nephropathy Patients
[Figure 1] and [Table 1] show the prevalence and frequencies of the associated complications in the DN Patients. The most common complication was hypertension (HTN) in 178 (96.7%) patients followed by neuropathy in 124 (67.3%), angiography proven coronary artery disease (CAD) in 106 (57.6%), and peripheral vascular disease (PVD) in 121 (65.7%) patients, and diabetic retinopathy in 82 (44.6%).
Kidney failure was frequent and 70 (38.0%) patients advanced to ESRD, and 13 (7.2%) deaths occurred in the hospital.
The mean time to onset of diabetic complications from the diagnosis of diabetes in our study patients was8.9 ± 4.9 years for CAD, 16.4 ± 5.9 years for PVD, 2.52 ± 1.3yrs for retinopathy, 11.7 ± 4.7 years for neuropathy, and 5.4 ± 2.36 years for diabetic foot. In addition, it took 20-25years for amputations after diabetes was diagnosed, 3-22 years for blindness, and > 25 years for ESRD.
Prevalence of multiple health complications in DN patients
[Figure 2] shows the frequency of multiple complications in our study patients. Only (1%) of the patients had 1 concomitant complication, 5% had 2, 11% had 3, 17% had 4, 28% had 5, and 37% patients had > 6 and more complications. Reduced Creatinine clearance at base line had impact on the future development of health complications in DN patients.
In the present study a significant correlation was found between baseline creatinine clearance and coronary artery disease (r=-0.15, p = 0.04), neuropathy (r=-.194, p = .01), hypertension (r=-.193, p = 0.01), ESRD (r=-.274, p = 0.005), and Death (r=-.168, p = 0.028),[Table 2].
Changes in the serum creatinine during followup
In the present study, there was a constant deterioration of renal function of the patients over time. The mean serum creatinine increased from 138 ± 91.0 µmol/L at the baseline to 175 ± 111 µmol/L in 12 months, 218 ± 141 µmol/L in 24 months, 259 ± 165 µmol/L in 3 years, 289 ± 176 µmol/L in 4 years, 361± 245 µmol/L in 5 years, 390 ± 274 µmol/L, in 10 years, 431 ± 300 µmol/L in 15 years, and 441 ± 325 µmol/L at last follow-up.
Patterns of change of serum creatinine at baseline and at last follow-up
A total of 80 (43.5%) patients had serum creatinine < 110 µmol/L, 39 (21.2%) between 110-140 µmol/L, 17 (9.2%) between 141-165 µmol/L, 35 (19%) between 166-220 µmol/L, and 12 (6.5%) > 220 µmol/L. At the last visit 68.5% of patients had their serum creatinine > 220 µmol/L, [Table 3].
Percent of change and doubling of serum creatinine in DN Patients
There were 123 (67 %) patients who doubled serum creatinine after 3.95 ± 2.88 years of follow-up. However, time to doubling was significantly (p=< .05) influenced by certain factors such as initial creatinine clearance (r=0.58, p=0.000), baseline proteinuria (r=- 0.36, p= 0.004), baseline serum creatinine (r=0.334, p= 0.000), age at the onset of diabetes (r=-0.264, p= 0.000), advance age of the patients (r=0.234, p= 0.001), SBP (r=0.239, p= 0.001), TG (r= 0.171 p= .026), [Table 4].
Time course of creatinine clearance in DN patients
In the present study FN patients showed a continued decline in renal function the creatinine clearance (ml/min) deteriorated gradually from 51.7 ± 26.3 at the base line to 41.7 ± 23.2 in 1 year, 33.4 ± 21.5 in 2 years, 26.5 ± 24.3 in 3 years, 26.0 ± 26.2 in 4 years, 25.8 ± 26.2 in 5 years, and further reduced to 20.1 ± 17.1 in 10 years, and 24.8 ± 28.1 at the last follow-up.
Patterns of GFR
There were 19 (10 %) patients who had GFR < 30 mL/min, 78 (43.8%) between 31-60 mL/ min, 41 (23%) between 61-89 mL/min, and 40 (22.4%) > 90 mL/min. A total of 12 (6.5%) patients improved their GFR, 32 (17.7%) remained stable, and 134 (72.8%) deteriorated their GFR. A total of 70 (68.6%) patients developed ESRD; 53 (28.8%) males and 17 (9.2%) females.
Baseline health status was detrimental in present study for renal outcome. Baseline creatinine clearance (r=0.58, p= 0.000), 24-hour urinary protein (r=-0.36, p= 0.004), Base line serum creatinine (r=-0.334, p= 0.000), age at the onset of diabetes (r=-0.264, p= 0.000), high systolic blood pressure (r=-0.239, p= 0.001), age (r=-0.234, p= 0.001), TG (r= -0.17, p= 0.001) were had a statistically significant correlation with poor renal outcome and ESRD, [Table 5].
24-hour urinary proteins in DN patients
The mean proteinuria in our DN patients (gm/24 hrs) was 1.99 ± 2.5 gm/L (Range 0.0222.1) at baseline. Protein excretion < 0.5 was found in 55 (29.9%) patients, between 0.5-3 in 90 (48.9%), > 3 in 39 (21.1%). At the last visit, protein excretion of < 0.5 was found in 32 (17.4%) patients, between 0.5-3 in 105 (57.1%), >3 in 47 (25.5%). Thus number of the patients with lower range (< 0.5) of proteinuria were reduced from 55 (29.9%) at baseline to 32 (17.4%) at the last visit, p= 0.04. Similarly, the number of the patients with proteinuria > 3 gm/24hrs increased from 39 (21.1%) at baseline to 47 (25.5%) at the last visit, however, the change was not statistically significant.
Other laboratory investigations
The mean HbA1C was 9.2 ± 1.8 % (Range 5.4-15.9) at base line and 8.93 ± 2.08 % (6.512.5) at the last visit.
The mean cholesterol was 5.17 ± 1.5 mmol/L (range 2.2-11.9 mmol/L) at baseline versus 4.22 ± 1.1 mmol/L (1.4-9.9) at the last visit. Hypercholesteremia was reported in 152 (82.6%) patients at base line. At the initial visit, there were 102 (55.4%) patients who had cholesterol < 5.2 mmol/L; 70 (38%) patients were on statins. At the last visit, 159 (86.4%) patients had serum cholesterol < 5.2mmol/L; 116 (63%) patients were on statins. There were 25 (13.5%) patients who had serum cholesterol > 5.2 mmol/L at the last visit in comparison with 82 (44.6%) at base line (p= 0.000).
TG were elevated in patients with DN at the initial visit. Only 14 (7.6%) patients had targeted recommended TG, 86 (47%) between 12 mmol/L, 41 (22%) between 2.01-3 mmol/L, and 43 (23.4%) > 3 mmol/L. The mean TG at the baseline was 2.1 ± 1.33 mmol/L. TG levels improved significantly at the last visit (p< 0 05) At the last visit, 22 (12%) patients had TG < 1 mmol/L, 123 (66.8%) between 1-2 mmol/L, 27 (14.7%) between 2.01-3 mmol/L, and 12 (6.5%) > 3 mmol/L.
| Discussion|| |
The present study is by far the biggest comprehensive overview and recent insight on the diabetic complications present in diabetic nephropathy patients. It reveals that the Saudi population has aggressive course of diabetic nephropathy and other health complications than western world. Multiple complications were present in both male and females As many as more than six complications were present in some of the individuals. Similar multiple complications were also reported by Mitka et al. 
CAD is a quite serious complication that affects a great majority (57.6%) of patients with DN, especially in the older age group. Incidence of CAD is lower in western countries being 25% in patients 45-59 yrs of age in a study from Finland,  and 9.1% in USA,  than 57.6% in the present study, which may be attributed to DN, high serum creatinine, dietary preferences favoring dyslipedemia, and sedentary life style.
Diabetic retinopathy was present in 82 (47.8%) in our study and complete loss of vision was found in 3 (1.6%) patients. Prevalence of retinopathy among Saudi patients with diabetes was reported previously as 31%.  Similar findings were reported by some other studies. ,,, another study from Saudi Arabia emphasized that presence of retinopathy could predict other diabetes complications.  In 2002, 11.5% prevalence of retinopathy in was reported in Saudi diabetic patients including both types of diabetes. 
The prevalence of neuropathy in the present study was 67.3%, and there was no significant gender difference. A similar high rate of diabetic neuropathy was reported in western provinces of Saudi Arabia in 2000. ,, Prevalence of painful diabetic neuropathy was 26.4% as reported by Davies et al et al from UK in 2006. 
In the present study, problems of lower extremities were in 25 (13.6 %) patients. However, there was a trend of improvement in the diabetic foot disease, and the percentage in the present study was much less than that reported from Saudi Arabia in year 2000(23.5%), , and from USA (22.8%). 
In the present study the prevalence of HTN (96.7%) was high compared to previous reports in which prevalence of hypertension was 25%  and 62.6%. 
Susceptibility for diabetic complications varies from one ethnic to another, and also from one individual to another. ,, For instance black Hispanics and Pima Indians are more susceptible for diabetic complication than white Americans.  Such differences might be present with other races, necessitating research in different races to pool the data for future reforms and special care of high risk groups. The present study reveals that the Saudi population has progressive and aggressive course of DN, indicating and anticipating a future burden on dialysis units. A similar aggressive course is reported in Pima tribes.  The peak incidence of diabetic nephropathy was present between 50 to70 yrs of age. The mean age of the onset of diabetes is early and the majority have diabetes in their forties.
Large number of patients presented at the time of start of the study without recommended target levels of blood pressure, cholesterol, TG, serum creatinine, or urinary protein. During the study, strict medical control of cholesterol, triglyceride, and blood pressure were attained in the vast majority, but renal function was refractory to the treatment in DN patients who progressed to ESRD. Time to doubling of serum creatinine was significantly influenced by certain factors such as initial creatinine clearance, base line proteinuria, baseline serum creatinine, age at the onset of diabetes, age of the patient, SBP, and TG. The incidence of ESRD in the present study was 70 (38%) as compared to 27.8% in USA.  In another study from the region reported an incidence of 43% ESRD. Only 15 % patients had stable course of DN, indicating an alarming fast progression of DN in Saudi population. 
Mortality was low (7.2%) in the present study as compared to other studies, since we have reported only those deaths that occurred in the hospital and did not include the mortality at home.
Finally, the world is facing a huge epidemic of diabetes and its complications consuming health resources and compelling to recognize the problem and galvanize action for the benefit of people. In 2007, a report from USA estimated the total direct costs spent on diabetes complications as 57 billion US dollars yearly.  Heart attack costs $ 14150 per person followed by chronic kidney disease $ 9002 per person, foot problems $ 4687 per person, and eye damage $ 1,785 per person.  In addition, there are added costs attributed to lost employment, lost productivity, disability and premature death of earning head of the family. 
We conclude that DN in Saudi population is aggressive. Patients are having high prevalence of diabetic complications, multiple complications are frequent, and cardiovascular complications are very high. Progression to chronic renal failure and ESRD is fast. Age, male gender, duration of diabetes, baseline HbA1C, systolic blood pressure, and renal function are risk factors for renal outcome and diabetic complications. Frequent screenings in addition to tight glycemic, lipid, and blood pressure control may be helpful. Saudi males are at a higher risk of having retinopathy, diabetic foot, amputation, and CAD, which should be studied further in future.
| References|| |
|1.||Al-Wakeel JS, Mitwalli AH, Abu-Aisha H, et al. Single center experience with pre-dialysis patients. Saudi J Kidney Dis Transpl 2002;13 (3):363-70. |
|2.||Centers for Diseases Control and Prevention (CDC). Incidence of end-stage renal diseases among persons with diabetes United States, 1992-2002. MMWR Morb Mortal Wkly Rep 2005;54(43):1097-100. |
|3.||Lin CH, Yang WC, Tsai ST, Tung TH, Chou P. A Community-based study of chronic kidney disease among type 2 diabetics in Kinmen, Taiwan. Diabetes Res Clin Pract 2007;75(3): - 12. |
|4.||Keane WF, Lyle PA. Reduction of Endpoints in NIDDM with the Angiotensin II Receptor Antagonist Losartan study: Recent advances in management of type 2 diabetes and Nephropathy: Lessons from the Renal study. Am J Kidney Dis 2003;41(3 Suppl 1):S22-5. |
|5.||Gaede P, Vedel P, Larsen N, Jensen GV, Parving HH, Pedersen O. Multifactor intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med 2003;348(5): 383-93. |
|6.||Hirata-Dulas CA, Rith-Najarian SJ, Mcintyre MC, et al. Risk factors for nephropathy and cardiovascular diseases in diabetic Northern Minnesota American Indians. Clin Nephrol 1996;46(2):92-8. |
|7.||Ritz E, Rychlic I, Locatelli F, Halimi S. End stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions. Am J Kidney Dis 1999;34(5):795-808. |
|8.||Girach A, Manner D, Porta M. Diabetic Micro vascular complications: Can patients at risk be identified? Int J Clin Pract 2006;60(11):147183. |
|9.||Sarnak MJ, Levey AS, Schoolwerth AS, et al. Kidney disease as a risk factor for development of cardiovascular disease. Hypertension 2003;42(5):1050-65. |
|10.||Hsieh MS, Hsiao JY, Tien KJ, et al. Chronic kidney disease as a risk factor for coronary artery disease in Chinese with type 2 diabetes. Am J Nephrol 2007;28(2):317-23. |
|11.||Wirta O, Pasternak A, Mustonen J, et al. Retinopathy is independently related to microalbuminuria in type 2 diabetes mellitus. Clin Nephrol 1999;51(6):329-34. |
|12.||Czekalski S. Diabetic nephropathy and cardiovascular diseases. Rocz Akad Med Bialymst 2005;50:122-5. [PUBMED] |
|13.||Toriyama T, Yokoya M, Nishida Y. Increased incidence of coronary artery disease and cardiac death in elderly patients undergoing chronic dialysis. J Cardiol 2000;36(3):165-71. |
|14.||Lee KU, Park JY, Kim SW, et al. Prevalence and associated features of albuminuria in Koreans with NIDDM. Diabetes Care 1995; 18(6):793-9. |
|15.||Hsieh MS, Hsiao JY, Tien KJ, et al. Chronic disease as a risk factor for coronary artery disease in chinese with type 2 diabetes. Am J Nephrol 2007;28(2):317-23. |
|16.||Young BA, Maynard C, Bokyko EJ. Racial differences in diabetic nephropathy, cardiovascular disease, and mortality in a national population of veterans. Diabetes Care 2003;26 (8):2392-9. |
|17.||Cowie CC, Port FK, Wolfe RA, Savage PJ, Moll PP, Hawthorne VM. Disparities in incidence of diabetic end-stage renal disease according to race and type of diabetes. N Engl J Med 1982;321(16):1074-9. |
|18.||Rostand SG, Kirk KA Rutsky EA, Pate BA. Racial differences in the incidence of treatment for end-stage renal disease. N Engl J Med 1982;306(21):1276-9. |
|19.||al-Nuaim AA, Bamgboye EA, al-Rubeaan KA, al-Mazrou Y. Over weight and obesity in Saudi Arabian adult population, Role of socio demographic variables. J Community Health 1997;22(3):211-23. |
|20.||Mitka M. Report quantifies diabetes complications. JAMA 2007;297(21):2337-8. |
|21.||Alzaid AA, Sobki S, De Silva V. Prevalence of microalbuminuria in Saudi Arabians with non insulin dependent diabetes mellitus: a clinic based study. Diabetes Res Clin Pract 1994;26 2):115-20. |
|22.||Al Khader AA. Impact of diabetes in renal disease in Saudi Arabia. Nephrol Dial Transplant 2001;16(11):2132-5. |
|23.||Koivisto VA, Stevens Lk, Mattaock M, et al. Cardiovascular disease and its risk factors in IDDM Complications Study Group. Diabetes Care 1996;19(7):689-97. |
|24.||El-Asrar AM, Al-Rubeaan KA, Al-Amro SA, Kangave D, Moharram OA. Risk factors for diabetic retinophaty among Saudi diabetics. Int Ophthalmol 1998-1999;22(3);155-61. |
|25.||Guiffre G, Lodato G, Dardanoni G. Prevalence and risk factors of diabetic retinopathy in adult and elderly subjects: The Casteldaccia eye study. Graefes Arch Clin Exp Ophthalmol 2004;242(7):535-40. |
|26.||Rotimi C, Daniel H, Zhou J, et al. Prevalence and determinants of diabetic retinopathy and cataracts in West African type 2 diabetics. Ethn Dis 2003;13(S2):S110-7. |
|27.||Tajunasah I, Nabilah H, Reddy SC. Prevalence and risk factors for diabetic retinopathy: a study of 217 patients from University of Malaya Medical center. Med J Malaysia 2006; 61(4):451-6. |
|28.||Prasad S, Klamath GG, Jones K, Clearkin LG, Phillips RP. Prevalence of blindness and visual impairment in a population of people with diabetes. Eye 2001;15(.5):640-3. |
|29.||Abu El Asrar AM, Al-Rubean KA, Al-Amro SA, Moharram OA, Kangave D. Retinopathy as a predictor for other diabetic complications. Int Ophthalmol 2001;24(1):1-11. |
|30.||Nielsen JV. Peripheral neuropathy, hypertension, foot ulcers and amputations among Saudi Arabian patients with Type-2 diabetes. Diabetes Res Clin Pract 1998;41(1):63-9. |
|31.||Akbar DH, Mira SA, Zawawi TH, Malibary HM. Sub clinical neuropathy: a common complications in Saudi diabetics. Saudi Med J 2000;21(5):433-7. |
|32.||Foncesca V, Laajam MA, Tongia RK. Asymptomatic autonomic neuropathy in Saudi diabetics. Saudi Med J 1985;6(1):38-42. |
|33.||Davies M, Brophy S, Williams R, Taylor A. The prevalence, severity, and impact of painful diabetic peripheral neuropathy in type 2 diabetes. Diabetes Care 2006;29(7):1518-22. |
|34.||Elhadd TA, Al Amoudi AA, AlZahrani AS. Epidemiology, clinical and complications profile of diabetes in Saudi Arabia: a review. Ann Saudi Med 2007;27(4):241-50. |
|35.||Qari FA, Akbar D. Diabetic foot: presentation and treatment. Saudi Med J 2000;21(5):443-6. |
|36.||Famuyiwa OO, Sulimani RR, Laajam MA, AlJasser J, Mekki MO. Diabetes mellitus in Saudi Arabia. The clinical pattern and complications in 1000 patients. Ann Saudi Med 1992;12(2):140-51. |
|37.||Earle KK, Porter KA, Ostberg J, Yudkin JS. Variation in the progression of diabetic nephropathy according to racial origin. Nephrol Dial Transplant 2001;16(2):286-90. |
Jamal S Al-Wakeel
Nephrology Unit, Department of Medicine, King Khalid University Hospital, King Saud University, Riyadh
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
|This article has been cited by|
||Awareness, Attitude, And distribution of high blood pressure among health professionals
| ||Mitwalli, A.H. and Harthi, A.A. and Mitwalli, H. and Juwayed, A.A. and Turaif, N.A. and Mitwalli, M.A. |
| ||Journal of the Saudi Heart Association. 2013; 25(1): 19-24 |
||Complications and characteristics of patients referred to a joint diabetes renal clinic in Ireland
| ||Thabit, H. and Besharatian, B. and Conlon, P.J. and Smith, D. |
| ||Irish Journal of Medical Science. 2012; 181(4): 549-553 |
||Risk factors of diabetic foot in central Saudi Arabia
| ||Abolfotouh, M.A. and Alfaif, S.A. and Al-Gannas, A.S. |
| ||Saudi Medical Journal. 2011; 32(7): 708-713 |
||Relationship between the severity of albuminuria and vibration perception threshold in patients with type 2 diabetics
| ||Shen, J. and Liu, F. and Zeng, H. and Yu, J. and Li, Q. and Zhang, F. and Bao, Y.-Q. and Jia, W.-P. |
| ||Fudan University Journal of Medical Sciences. 2011; 38(3): 251-256 |
||Role of endothelin receptor A and NADPH oxidase in vascular abnormalities
| ||Dai, D.-Z. and Dai, Y. |
| ||Vascular Health and Risk Management. 2010; 6(1): 787-794 |
||Protective effects of HMG-CoA reducase inhibitor atorvastatin on nephridial tissues of diabetic rats and its related mechanism
| ||Zhao, X.-L. and Xu, W.-W. and Jiang, G.-P. and Liu, X.-I. and Fang, J. |
| ||Journal of Xięan Jiaotong University (Medical Sciences). 2010; 31(4): 459-462 |
||Epidemiology of diabetes mellitus and diabetic foot problems in Saudi Arabia
| ||Ahmed, A.A. |
| ||Avances en Diabetologia. 2010; 26(1): 29-35 |
||Chronic complications of diabetes in Iraq: Experience from Southern Iraq
| ||Mansour, A.A. |
| ||Clinical Medicine Insights: Endocrinology and Diabetes. 2009; 2: 89-97 |