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The prevalence of microalbuminuria in diabetes: a study from North India
Diabetes Research and Clinical Practice,
12 (1991)
125-128 125
Elsevier DIABET 00487
Epidemiological
The prevalence
Note
of microalbuminuria in diabetes: North India
D. K. Gupta I, L. K. Verma2, P. K. Khosla2
a study from
and S. C. Dash ’
‘Departmentof Nephrology, AN India Instilute of Medical Sciences, New Delhi, India and ‘Dr. Rajendra Prasad Centre for Ophthalmic Sciences, New Delhi, India
(Received 8 September 1990) (Revision accepted 6 December 1990)
Summary
Geographic/population variation in the prevalence of diabetic nephropathy is well recognised. In a study of ‘native’ Indians, we screened 102 non-proteinuric diabetes mellitus patients (64 NIDDM, 38 IDDM; mean age and diabetic duration 48.7 and 6.5 years, 21.6 and 6.2 years, respectively) with blood pressure I 170/105 and without congestive heart failure, ketonuria or urinary tract infection, for the presence of microalbuminuria (albumin excretion rate > 20 pg/min). Fifty-six patients (34 NIDDM, 22 IDDM) also underwent detailed fundus examination. Seventeen NIDDM (26.6%) and 3 IDDM (7.9%) patients had microalbuminuria. Glycated hemoglobin was significantly higher in microalbuminurics in the NIDDM group (P < 0.05). Diabetic retinopathy tended to occur more frequently in microalbuminurics (NIDDM and IDDM). Key words:
Diabetes
mellitus; Microalbuminuria;
It is now well established that the stage of microalbuminuria is the forerunner of overt diabetic nephropathy [l] and so screening for microalbuminuria has become routine in many diabetic clinics. Race has been implicated as an important risk Correspondence to: Dr. D. K. Gupta, c/o Prof. S. C. Dash, Dept. of Nephrology, All India Institute of Medical Sciences, New Dehli - 110029, India.
0168-8227/91/$03.50
0 1991 Elsevier Science Publishers
Retinopathy
factor for the development of diabetic nephropathy [2-51. In the WHO multicentre study of vascular disease in diabetics, the prevalence of diabetic nephropathy has shown wide geographic variations [2]. For example, the prevalence of heavy or very heavy proteinuria in males with diabetes of longer than 14 years duration varied from 2.4% (Hong Kong) and 4.2% (London), 21.5 y0 (Switzerland) and 23 % (Delhi, India) to 34% (Tokyo) and 37% (Oklahoma, U.S.A.). In the United States, native Americans and blacks have a relative risk of three for the development
B.V. (Biomedical
Division)
126
of diabetic nephropathy, when compared with the whites [ 31. In a study from the United Kingdom, the prevalence of proteinuria (> 500 mg/24 h) was over twice as high in diabetic patients of Asian origin (14%) as in ‘white’ patients (6%) despite a similar prevalence of hypertension and similar glycemic control [ 41. Furthermore, a study from a different centre in the U.K. showed that the albumin : creatinine ratio in overnight urine samples was significantly higher in Indian diabetics (migrants) than in European diabetics (NIDDM), despite similar age, duration of diabetes, mean blood pressure and glycemic control in the two groups [ 51. However, there is still a paucity of data on the prevalence of microalbuminuria in diabetics in India (native) and so the present study was undertaken.
Materials and methods 102 patients with diabetes mellitus [64 noninsulin-dependent (NIDDM), 38 insulin-dependent (IDDM), using the National Diabetes Data Group/World Health Organization criteria] attending the Endocrinology and Diabetes clinics of the All India Institute of Medical Sciences, New Delhi, India were included in the study. The inclusion criteria were: (1) absence of congestive heart failure, urinary tract infection, ketonuria and overt proteinuria (1 + or more); (2) blood pressure (BP) I170/105 and serum creatinine < 1.6 mg y0 and (3) duration of diabetes of one month or more. Patients with diabetes secondary to pancreatic diseases, certain endocrine diseases and drugs were excluded. Age of the patients was no bar. Subjects included in the study were not preselected on the grounds of caste or socioeconomic status. Each patient had a brief history taken and physical examination done. The BP of every patient was taken in sitting position by a single investigator (D.K.G.), after at least 10 min of rest. The mean of two readings (taken 3 min apart) from the right arm was recorded; the Korotkoff phase V was used to define the diastolic end point. While
patients rested in the clinic, a timed urine collection was done and used later for estimation of urinary albumin. Urine samples were deep frozen at - 20” C (with sodium azide 2 g/l as preservative) and were thawed just before assay. All patients gave a sample of urine for culture. Glycated hemoglobin (GHb) was determined by the calorimetric (thiobarbituric acid) method [ 61 and serum creatinine by the method of Julie [ 71. Fifty-six patients also underwent detailed fundus examination and fluorescein angiography by a single investigator (L.K.V.). Urinary albumin estimation was done using the immunoturbidimetry method [ 81. 20 ~1 of each urine sample was diluted 40 times in 0.1 M Tris buffer (pH 7.4) containing 40 g/l of polyethylene glycol 6000. Antiserum to human albumin (Serotee, Kidlington, Oxford, U.K.) was diluted lo-fold in the same buffer and 100 ~1 was added to each diluted urine sample in 1 ml quartz cuvettes. The reaction was monitored for 2 min at 292 nm wavelength and the results were calculated from the absorbance of standard solutions of human albumin (2.5-300 mg/l; Serotec). Final results were expressed in terms of albumin excretion rate (AER) in pg/min. Microalbuminuria was considered present when the AER was > 20 pg/min. Statistical analysis was done using the unpaired t-test and chi-square test with Yates correction.
Results Out of 102 patients studied, 64 had NIDDM (male 34, female 30) and 38 had IDDM (male 20, female 18). The mean age and duration of diabetes were 48.7 and 6.5 years in NIDDM and 21.6 and 6.2years in IDDM. A total of 56 patients (34 NIDDM and 22 IDDM) also had an evaluation for diabetic retinopathy. The results are summarized in the Table 1. Results in patients with NIDDM 17 patients (26.6%) had microalbuminuria in the NIDDM group (AER range 22.4-136.8 pg/min). When microalbuminurics were compared with
127 TABLE
1
Summary of the results in NIDDM
Normoalbuminuric
Microalbuminuric
(n = 47) (Mean f SD)
(n = 17) (Mean & SD)
48.68 6.45 128.40 80.11 8.66 3
48.82 6.66 129.41 84.70 10.29 2
P-value
group
Age (years) Duration of diabetes (years) BP-systolic (mmHg) BP-diastolic GHb (glycated hemoglobin) (x) Diabetic retinopathy**
f f f f f +
11.03 5.72 20.83 9.92 2.55 o/21
f f f f + +
9.96 5.24 18.10 10.38 2.89 2113
ns* ns ns ns < 0.05 ns
Summary of the results in IDDM group Age (years) Duration of diabetes BP systolic BP diastolic GHb Diabetic retinopathy
(years)
(n = 35)
(n = 3)
21.63 6.0 112.57 76.28 10.02 4
21.67 8.5 110 76.67 9.65 2
* ns = not significant. ** No of patients with retinopathy, pathy.
f 8.57 k 6.86 & 10.87 & 8.94 * 2.1 + o/20 background
their normoalbuminuric counterparts, the age and duration of diabetes were almost identical. Blood pressure, especially diastolic, was higher in microalbuminurics but was not statistically significant. GHb was significantly higher in microalbuminurics (P < 0.05). Retinopathy (background and proliferative combined) occurred more frequently in microalbuminurics (30% vs 14.2%; P, not significant). Results in patients with IDDM Unlike in the NIDDM group, all IDDM patients were normotensive (maximum BP 130/90). Only 3 patients (7.9%) had microalbuminuria (AER range 46.2-129.2 pg/min). When microalbuminurics were compared with normoalbuminurics, the age, BP (systolic and diastolic) and GHb were almost identical. The duration of diabetes tended to be longer in microalbuninurics (P, not significant). Diabetic retinopathy occurred more frequently in microalbuminurics (100 y0 vs 20%, P, not significant).
+ proliferative/total
k 8.08 f 3.97 * 8.66 k 5.77 k 3.78 + o/2
ns ns ns ns ns ns
no. of patients evaluated for retino-
Discussion
In the present study, microalbuminuria was found in 26.6% of NIDDM patients, with a mean diabetic duration of 6.5 years. Similar results have been reported in the literature [ 9,101. Mattock et al. from London reported microalbuminuria in 26% of 103 NIDDM patients with a mean diabetic duration of 7.5 years [ 91. Anita Schmitz from Denmark analysed 416 NIDDM patients (mean diabetic duration 6.5 years) with AER I200 pg/ml and found microalbuminuria (15 < AER < 200 pg/ml) in 27.4% patients [IO]. In the IDDM group, we found microalbuminuria in 7.9% patients; all the IDDM patients in our study were normotensive with a mean diabetic duration of only 6.2 years. In a recent study from the U.S.A. [ 1 l] of 135 normotensive IDDM patients, the prevalence of microalbuminuria (AER > 20 pg/min) was 11.8 %. However, the mean duration of diabetes in this study was 15.7 years. One study from England [ 121 has reported microalbuminuria
128
(AER > 30 pg/min) in only 6”/, of non-proteinuric and normotensive IDDM patients (mean duration of diabetes 15 years); but the study used stricter inclusion criteria (no BP > 160/95, < 3 episodes of ketoacidosis per year, < 120 units insulin/day and no major illness) and a higher cut-off point for definition of microalbuminuria (30 pg/min vs 20 pg/min). Diabetic retinopathy tended to occur more frequently in microalbuminurics in both groups 100% vs 20”,‘, in (30% vs 14.2% in NIDDM; IDDM). The same has been reported in the literature [ 131. The observed geographic/population variation in the prevalence of diabetic nephropathy could be due to real ethnic differences in the susceptibility to diabetic nephropathy (‘genetic’) or due to poor control of diabetes, hypertension or other socio-economic and cultural factors (‘environmental’). Quality and quantity of protein intake may also play an important role in the evolution of diabetic nephropathy. Indian (native) diabetics consume a diet, rich in carbohydrates and low in proteins [ 141. Studies show that a lower intake of proteins is accompanied by lesser albuminuria in healthy volunteers and also in diabetics with and without microalbuminuria [ 151. In a preliminary study of 19 diabetics (both IDDM and NIDDM), we have found that microproteinuria (using Commassie blue dye binding assay) had a positive correlation with the average daily intake of class I proteins (p. = 0.48, P < 0.005) and total proteins (Y = 0.26, P < 0.02) [ 161.
3
4
5
6
7 8
9
10
11
12
13
14
Acknowledgement
The authors are grateful to the Department of Endocrinology and Metabolism of All India Institute of Medical Sciences, New Delhi, India for its invaluable help throughout the study.
References 1 Mogensen, C. E. (1987) Microalbuminuria as a predictor of clinical diabetic nephropathy. Kidney Int. 3 1,673-689. 2 The World Health Organisation Multinational Study of Vascular Disease in Diabetics. (1985) Prevalence of small
15
16
vessel and large vessel disease in diabetic patients from 14 centres. Diabetologia 28: 615-640. West, K. M. (1974) Diabetes in American Indians and other native population of the new world. Diabetes 23, 841-855. Samanta, A., Burden, A. C., Feehally. J. and Walls, J. (1986) Diabetic renal disease: difference between Asian and white patients. Br. Med. J. 293, 366-367. Allawi, J., Rao, P. V., Gilbert, R. et al. (1988) Microalbuminuria in non-insulin dependent diabetes: its prevalence in Indian compared with Europid patients. Br. Med. J. 296, 462-464. Gabbuy, K. H., Sosenko, J. M., Banuchi, G. A. et al. (1979) Glycosylated hemoglobins: increased glycosylation of hemoglobin A in diabetic patients. Diabetes 28, 337-340. Husdan, H. and Rapoport, A. (1968) Estimation of creatinine by the Jaffe reaction. Clin. Chem. 14,222-226. Teppo, A.-M. (1982) Immunoturbidimetry of albumin and immunoglobulin G in urine. Clin. Chem. 28, 1359-1361. Mattock, M. B., Scott, G. S., Elgohari, R. et al. (1986) High prevalence of ischaemic heart disease and hyperlipidaemia in type II (non-insulin-dependent) diabetic patients with microalbuminuria. Diabetologia 29, 570 A. Schmitz A. (1988) Microalbuminuria and mortality in non-insulin-diabetes. In: C. E. Mogensen (Ed.), The kidney and Hypertension in Diabetes Mellitus, Martinus Nijhoff Publishing, Boston, p. 65. Ramirez, L., Rios, J., Hellen Brand, D., Rosenstock, J. and Raskin, P. (1989) Low prevalence of microalbuminuria in normotensive insulin dependent diabetic subjects. Diabetes 38 (Suppl. 2) 16 A. Microalbuminuria Collaborative Study group, U.K. (1987) Microalbuminuria and glycaemic control. In: Diabetic Complications ‘87. Multicentre and/or Prospective Study Session on Diabetic Complications. Consiglio Nazionale dell Ricerche, Rome. Marre, M., Claudel, J. P., Ciret, P. et al. (1987) Laser immunonephelometry for routine quantification of urinary albumin excretion. Clin. Chem. 33, 209-213. Ahuja. M. M. S. (1979) Epidemiological studies on diabetes mellitus in India. In: M. M. S. Ahuja (Ed.), Epidemiology of Diabetes in Developing Countries. lnterprint, New Delhi. p. 29. Viberti, G. C., Dodds, R. A., Bending, J. J. and Bognetti, E. (1988) Nonglycemic intervention in diabetic nephropathy: the role of dietary protein intake. In: C. E. Mogensen (Ed.), The Kidney and Hypertension in Diabetes Mellitus, Martinus Nijhoff Publishing, Boston, p. 205. Rustagi, G., Raju, R.. Gupta, D. K.. Dash, S. C., Kochupillai, N. and Sharma, R. (1989) Evaluation of a simple dye binding method for measurement of microproteinuria in diabetic patients and its correlation with microalbuminuria (Turbidi-Immunoassay) and clinical parameters. Diabetes Bull. 9 (Suppl. 1) 16-17.
12 (1991)
125-128 125
Elsevier DIABET 00487
Epidemiological
The prevalence
Note
of microalbuminuria in diabetes: North India
D. K. Gupta I, L. K. Verma2, P. K. Khosla2
a study from
and S. C. Dash ’
‘Departmentof Nephrology, AN India Instilute of Medical Sciences, New Delhi, India and ‘Dr. Rajendra Prasad Centre for Ophthalmic Sciences, New Delhi, India
(Received 8 September 1990) (Revision accepted 6 December 1990)
Summary
Geographic/population variation in the prevalence of diabetic nephropathy is well recognised. In a study of ‘native’ Indians, we screened 102 non-proteinuric diabetes mellitus patients (64 NIDDM, 38 IDDM; mean age and diabetic duration 48.7 and 6.5 years, 21.6 and 6.2 years, respectively) with blood pressure I 170/105 and without congestive heart failure, ketonuria or urinary tract infection, for the presence of microalbuminuria (albumin excretion rate > 20 pg/min). Fifty-six patients (34 NIDDM, 22 IDDM) also underwent detailed fundus examination. Seventeen NIDDM (26.6%) and 3 IDDM (7.9%) patients had microalbuminuria. Glycated hemoglobin was significantly higher in microalbuminurics in the NIDDM group (P < 0.05). Diabetic retinopathy tended to occur more frequently in microalbuminurics (NIDDM and IDDM). Key words:
Diabetes
mellitus; Microalbuminuria;
It is now well established that the stage of microalbuminuria is the forerunner of overt diabetic nephropathy [l] and so screening for microalbuminuria has become routine in many diabetic clinics. Race has been implicated as an important risk Correspondence to: Dr. D. K. Gupta, c/o Prof. S. C. Dash, Dept. of Nephrology, All India Institute of Medical Sciences, New Dehli - 110029, India.
0168-8227/91/$03.50
0 1991 Elsevier Science Publishers
Retinopathy
factor for the development of diabetic nephropathy [2-51. In the WHO multicentre study of vascular disease in diabetics, the prevalence of diabetic nephropathy has shown wide geographic variations [2]. For example, the prevalence of heavy or very heavy proteinuria in males with diabetes of longer than 14 years duration varied from 2.4% (Hong Kong) and 4.2% (London), 21.5 y0 (Switzerland) and 23 % (Delhi, India) to 34% (Tokyo) and 37% (Oklahoma, U.S.A.). In the United States, native Americans and blacks have a relative risk of three for the development
B.V. (Biomedical
Division)
126
of diabetic nephropathy, when compared with the whites [ 31. In a study from the United Kingdom, the prevalence of proteinuria (> 500 mg/24 h) was over twice as high in diabetic patients of Asian origin (14%) as in ‘white’ patients (6%) despite a similar prevalence of hypertension and similar glycemic control [ 41. Furthermore, a study from a different centre in the U.K. showed that the albumin : creatinine ratio in overnight urine samples was significantly higher in Indian diabetics (migrants) than in European diabetics (NIDDM), despite similar age, duration of diabetes, mean blood pressure and glycemic control in the two groups [ 51. However, there is still a paucity of data on the prevalence of microalbuminuria in diabetics in India (native) and so the present study was undertaken.
Materials and methods 102 patients with diabetes mellitus [64 noninsulin-dependent (NIDDM), 38 insulin-dependent (IDDM), using the National Diabetes Data Group/World Health Organization criteria] attending the Endocrinology and Diabetes clinics of the All India Institute of Medical Sciences, New Delhi, India were included in the study. The inclusion criteria were: (1) absence of congestive heart failure, urinary tract infection, ketonuria and overt proteinuria (1 + or more); (2) blood pressure (BP) I170/105 and serum creatinine < 1.6 mg y0 and (3) duration of diabetes of one month or more. Patients with diabetes secondary to pancreatic diseases, certain endocrine diseases and drugs were excluded. Age of the patients was no bar. Subjects included in the study were not preselected on the grounds of caste or socioeconomic status. Each patient had a brief history taken and physical examination done. The BP of every patient was taken in sitting position by a single investigator (D.K.G.), after at least 10 min of rest. The mean of two readings (taken 3 min apart) from the right arm was recorded; the Korotkoff phase V was used to define the diastolic end point. While
patients rested in the clinic, a timed urine collection was done and used later for estimation of urinary albumin. Urine samples were deep frozen at - 20” C (with sodium azide 2 g/l as preservative) and were thawed just before assay. All patients gave a sample of urine for culture. Glycated hemoglobin (GHb) was determined by the calorimetric (thiobarbituric acid) method [ 61 and serum creatinine by the method of Julie [ 71. Fifty-six patients also underwent detailed fundus examination and fluorescein angiography by a single investigator (L.K.V.). Urinary albumin estimation was done using the immunoturbidimetry method [ 81. 20 ~1 of each urine sample was diluted 40 times in 0.1 M Tris buffer (pH 7.4) containing 40 g/l of polyethylene glycol 6000. Antiserum to human albumin (Serotee, Kidlington, Oxford, U.K.) was diluted lo-fold in the same buffer and 100 ~1 was added to each diluted urine sample in 1 ml quartz cuvettes. The reaction was monitored for 2 min at 292 nm wavelength and the results were calculated from the absorbance of standard solutions of human albumin (2.5-300 mg/l; Serotec). Final results were expressed in terms of albumin excretion rate (AER) in pg/min. Microalbuminuria was considered present when the AER was > 20 pg/min. Statistical analysis was done using the unpaired t-test and chi-square test with Yates correction.
Results Out of 102 patients studied, 64 had NIDDM (male 34, female 30) and 38 had IDDM (male 20, female 18). The mean age and duration of diabetes were 48.7 and 6.5 years in NIDDM and 21.6 and 6.2years in IDDM. A total of 56 patients (34 NIDDM and 22 IDDM) also had an evaluation for diabetic retinopathy. The results are summarized in the Table 1. Results in patients with NIDDM 17 patients (26.6%) had microalbuminuria in the NIDDM group (AER range 22.4-136.8 pg/min). When microalbuminurics were compared with
127 TABLE
1
Summary of the results in NIDDM
Normoalbuminuric
Microalbuminuric
(n = 47) (Mean f SD)
(n = 17) (Mean & SD)
48.68 6.45 128.40 80.11 8.66 3
48.82 6.66 129.41 84.70 10.29 2
P-value
group
Age (years) Duration of diabetes (years) BP-systolic (mmHg) BP-diastolic GHb (glycated hemoglobin) (x) Diabetic retinopathy**
f f f f f +
11.03 5.72 20.83 9.92 2.55 o/21
f f f f + +
9.96 5.24 18.10 10.38 2.89 2113
ns* ns ns ns < 0.05 ns
Summary of the results in IDDM group Age (years) Duration of diabetes BP systolic BP diastolic GHb Diabetic retinopathy
(years)
(n = 35)
(n = 3)
21.63 6.0 112.57 76.28 10.02 4
21.67 8.5 110 76.67 9.65 2
* ns = not significant. ** No of patients with retinopathy, pathy.
f 8.57 k 6.86 & 10.87 & 8.94 * 2.1 + o/20 background
their normoalbuminuric counterparts, the age and duration of diabetes were almost identical. Blood pressure, especially diastolic, was higher in microalbuminurics but was not statistically significant. GHb was significantly higher in microalbuminurics (P < 0.05). Retinopathy (background and proliferative combined) occurred more frequently in microalbuminurics (30% vs 14.2%; P, not significant). Results in patients with IDDM Unlike in the NIDDM group, all IDDM patients were normotensive (maximum BP 130/90). Only 3 patients (7.9%) had microalbuminuria (AER range 46.2-129.2 pg/min). When microalbuminurics were compared with normoalbuminurics, the age, BP (systolic and diastolic) and GHb were almost identical. The duration of diabetes tended to be longer in microalbuninurics (P, not significant). Diabetic retinopathy occurred more frequently in microalbuminurics (100 y0 vs 20%, P, not significant).
+ proliferative/total
k 8.08 f 3.97 * 8.66 k 5.77 k 3.78 + o/2
ns ns ns ns ns ns
no. of patients evaluated for retino-
Discussion
In the present study, microalbuminuria was found in 26.6% of NIDDM patients, with a mean diabetic duration of 6.5 years. Similar results have been reported in the literature [ 9,101. Mattock et al. from London reported microalbuminuria in 26% of 103 NIDDM patients with a mean diabetic duration of 7.5 years [ 91. Anita Schmitz from Denmark analysed 416 NIDDM patients (mean diabetic duration 6.5 years) with AER I200 pg/ml and found microalbuminuria (15 < AER < 200 pg/ml) in 27.4% patients [IO]. In the IDDM group, we found microalbuminuria in 7.9% patients; all the IDDM patients in our study were normotensive with a mean diabetic duration of only 6.2 years. In a recent study from the U.S.A. [ 1 l] of 135 normotensive IDDM patients, the prevalence of microalbuminuria (AER > 20 pg/min) was 11.8 %. However, the mean duration of diabetes in this study was 15.7 years. One study from England [ 121 has reported microalbuminuria
128
(AER > 30 pg/min) in only 6”/, of non-proteinuric and normotensive IDDM patients (mean duration of diabetes 15 years); but the study used stricter inclusion criteria (no BP > 160/95, < 3 episodes of ketoacidosis per year, < 120 units insulin/day and no major illness) and a higher cut-off point for definition of microalbuminuria (30 pg/min vs 20 pg/min). Diabetic retinopathy tended to occur more frequently in microalbuminurics in both groups 100% vs 20”,‘, in (30% vs 14.2% in NIDDM; IDDM). The same has been reported in the literature [ 131. The observed geographic/population variation in the prevalence of diabetic nephropathy could be due to real ethnic differences in the susceptibility to diabetic nephropathy (‘genetic’) or due to poor control of diabetes, hypertension or other socio-economic and cultural factors (‘environmental’). Quality and quantity of protein intake may also play an important role in the evolution of diabetic nephropathy. Indian (native) diabetics consume a diet, rich in carbohydrates and low in proteins [ 141. Studies show that a lower intake of proteins is accompanied by lesser albuminuria in healthy volunteers and also in diabetics with and without microalbuminuria [ 151. In a preliminary study of 19 diabetics (both IDDM and NIDDM), we have found that microproteinuria (using Commassie blue dye binding assay) had a positive correlation with the average daily intake of class I proteins (p. = 0.48, P < 0.005) and total proteins (Y = 0.26, P < 0.02) [ 161.
3
4
5
6
7 8
9
10
11
12
13
14
Acknowledgement
The authors are grateful to the Department of Endocrinology and Metabolism of All India Institute of Medical Sciences, New Delhi, India for its invaluable help throughout the study.
References 1 Mogensen, C. E. (1987) Microalbuminuria as a predictor of clinical diabetic nephropathy. Kidney Int. 3 1,673-689. 2 The World Health Organisation Multinational Study of Vascular Disease in Diabetics. (1985) Prevalence of small
15
16
vessel and large vessel disease in diabetic patients from 14 centres. Diabetologia 28: 615-640. West, K. M. (1974) Diabetes in American Indians and other native population of the new world. Diabetes 23, 841-855. Samanta, A., Burden, A. C., Feehally. J. and Walls, J. (1986) Diabetic renal disease: difference between Asian and white patients. Br. Med. J. 293, 366-367. Allawi, J., Rao, P. V., Gilbert, R. et al. (1988) Microalbuminuria in non-insulin dependent diabetes: its prevalence in Indian compared with Europid patients. Br. Med. J. 296, 462-464. Gabbuy, K. H., Sosenko, J. M., Banuchi, G. A. et al. (1979) Glycosylated hemoglobins: increased glycosylation of hemoglobin A in diabetic patients. Diabetes 28, 337-340. Husdan, H. and Rapoport, A. (1968) Estimation of creatinine by the Jaffe reaction. Clin. Chem. 14,222-226. Teppo, A.-M. (1982) Immunoturbidimetry of albumin and immunoglobulin G in urine. Clin. Chem. 28, 1359-1361. Mattock, M. B., Scott, G. S., Elgohari, R. et al. (1986) High prevalence of ischaemic heart disease and hyperlipidaemia in type II (non-insulin-dependent) diabetic patients with microalbuminuria. Diabetologia 29, 570 A. Schmitz A. (1988) Microalbuminuria and mortality in non-insulin-diabetes. In: C. E. Mogensen (Ed.), The kidney and Hypertension in Diabetes Mellitus, Martinus Nijhoff Publishing, Boston, p. 65. Ramirez, L., Rios, J., Hellen Brand, D., Rosenstock, J. and Raskin, P. (1989) Low prevalence of microalbuminuria in normotensive insulin dependent diabetic subjects. Diabetes 38 (Suppl. 2) 16 A. Microalbuminuria Collaborative Study group, U.K. (1987) Microalbuminuria and glycaemic control. In: Diabetic Complications ‘87. Multicentre and/or Prospective Study Session on Diabetic Complications. Consiglio Nazionale dell Ricerche, Rome. Marre, M., Claudel, J. P., Ciret, P. et al. (1987) Laser immunonephelometry for routine quantification of urinary albumin excretion. Clin. Chem. 33, 209-213. Ahuja. M. M. S. (1979) Epidemiological studies on diabetes mellitus in India. In: M. M. S. Ahuja (Ed.), Epidemiology of Diabetes in Developing Countries. lnterprint, New Delhi. p. 29. Viberti, G. C., Dodds, R. A., Bending, J. J. and Bognetti, E. (1988) Nonglycemic intervention in diabetic nephropathy: the role of dietary protein intake. In: C. E. Mogensen (Ed.), The Kidney and Hypertension in Diabetes Mellitus, Martinus Nijhoff Publishing, Boston, p. 205. Rustagi, G., Raju, R.. Gupta, D. K.. Dash, S. C., Kochupillai, N. and Sharma, R. (1989) Evaluation of a simple dye binding method for measurement of microproteinuria in diabetic patients and its correlation with microalbuminuria (Turbidi-Immunoassay) and clinical parameters. Diabetes Bull. 9 (Suppl. 1) 16-17.