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Original Investigation |

Low Birth Weights Contribute to the High Rates of Early-Onset Chronic Renal Failure in the Southeastern United States FREE

Daniel T. Lackland, DrPH; Holly E. Bendall, MSc; Clive Osmond, PhD; Brent M. Egan, MD; David J. P. Barker, MD, PhD
[+] Author Affiliations

From the Departments of Biometry and Epidemiology (Dr Lackland) and Pharmacology (Dr Egan), Medical University of South Carolina, Charleston, and Medical Research Council, Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, England (Ms Bendall and Drs Osmond and Barker).


Arch Intern Med. 2000;160(10):1472-1476. doi:10.1001/archinte.160.10.1472.
Text Size: A A A
Published online

Background  The southeastern United States is a region in which rates of cardiovascular and renal diseases are excessive. Within the Southeast, South Carolina has unusually high rates of end-stage renal disease (ESRD) in young people, with more than 70% of cases attributed to hypertension and diabetes.

Objective  To determine whether the increased vulnerability to early-onset ESRD might originate through impaired renal development in utero as measured by low birth weight.

Methods  Patients who were diagnosed with renal failure and undergoing dialysis from 1991 through 1996 were identified from the ESRD registry maintained by the Southeastern Kidney Council, Raleigh, NC. Birth weights reported on birth certificates were selected for the ESRD cases and non-ESRD controls who were born in South Carolina in 1950 and later. Birth weights were compared for 1230 cases and 2460 controls who were matched for age, sex, and race.

Results  Low birth weight was associated with ESRD among men and women as well as blacks and whites. Among people whose birth weight was less than 2.5 kg, the odds ratio for ESRD was 1.4 (95% confidence interval, 1.1-1.8) compared with people who weighed 3 to 3.5 kg. This association was present for renal failure resulting from diabetes, hypertension, and other causes.

Conclusions  Low birth weights, which reflect adverse effects on development in utero, contribute to the early onset of ESRD in South Carolina. Since low birth weight increases the risk of ESRD from multiple causes, the data suggest that an adverse environment in utero impairs kidney development and makes it more vulnerable to damage from a range of pathological processes.

Figures in this Article

FOR THE past 60 years, the southeastern region of the United States and South Carolina in particular have had such unusually high death rates from stroke that this region is known as the "stroke belt."1,2 The excessive disease risks are particularly evident with high incidence rates for young black adults.3 More recently, it has also become apparent that an unusually large number of people in South Carolina have chronic renal failure (end-stage renal disease [ESRD]) and require dialysis.4 The age-, race-, and sex-standardized incidence of ESRD in the state is 345 per million compared with an overall rate of 268 per million in the United States.4 The incidence of ESRD in South Carolina doubled from 1987 to 1996.4 While renal failure is considered a late complication of chronic diseases, such as diabetes and hypertension,5,6 40% of patients with ESRD are under age 55 years in South Carolina.7 Similarly high rates and trends are seen in the neighboring states in the southeastern United States.4,7 The disease burden is particularly great for blacks. The black population of the United States has 5-fold higher rates of ESRD than the white population, even after adjusting for differences in socioeconomic status.69 Blacks account for approximately 30% of the South Carolina population but for 69% of the ESRD cases.7

In South Carolina, hypertension and diabetes, the major antecedents of ESRD, are significantly more prevalent among blacks.10,11 Consistent with findings elsewhere in the United States, hypertension and diabetes account for 71% of the ESRD cases in South Carolina, with the remainder being attributed to glomerulonephritis, polycystic disease, and other renal disorders.7

The reasons for the excessive ESRD risks remain unknown, but low birth weight, which serves as an index for impaired development in utero, could be a contributing factor. This notion is supported by observations that high rates of low birth weight have prevailed in South Carolina for many years, especially among the black population.12

Recent studies have shown that non–insulin-dependent diabetes mellitus (NIDDM) and hypertension are more common among people who had low birth weight,1317 although the mechanisms underlying these associations remain unclear. The relationships are independent of socioeconomic status. These observations have led to the hypothesis that the risk for cardiovascular and renal diseases originates through lifelong adaptations in the structure and physiology of the body to undernutrition in utero.18 This article describes the risks of renal failure by birth weight category for young (year of birth, 1950 or later) black and white residents of South Carolina.

The Southeast Kidney Council (Network 6 of the United States Renal Data System, Raleigh, NC) maintains a registry of all people receiving dialysis for chronic renal failure in the states of South Carolina, North Carolina, and Georgia. The network implements and maintains a data collection and management system that includes quality assurance and monitoring to assure complete case ascertainment.6 The database includes the name, race, sex, and date of birth of each subject, as well as the nephrologist's diagnosis of the primary cause of renal failure. The primary disease causing renal failure for each patient with ESRD is identified from the nephrologist's diagnosis, which is recorded during the application and certification process for Medicare benefits. For the analyses in this study, the primary diagnoses were categorized in 3 groupings: hypertension, diabetes, and other.

Birth weight was determined from the weight reported on the South Carolina birth certificate. Since 1950, the birth weight of babies born in South Carolina has been recorded on the birth certificate, which also records the race of each child's mother.

The years 1991 through 1996 constitute the most recent period for which ESRD data were available. The ESRD registry identified 2446 South Carolina residents (1374 men and 1072 women) who had renal dialysis during these years. The identification data on the dialysis record were sent to the Office of Vital Records at the South Carolina Department of Health and Environmental Control in Columbia. Visual matching on name and birth date followed initial computer matching. The second phase of the matching process was a manual search for the birth certificates of the successful computer matches. Birth certificates were identified and located for 1345 (55%) of the 2446 subjects. Birth weight was recorded on 1230 of the 1345 birth certificates, including 892 men and 338 women. In most cases, nonmatches were probably the result of individuals who were born outside South Carolina and women who changed their surnames with marriage.

The birth weights were recorded in pounds and ounces and converted to grams for analyses. Subjects were categorized according to birth weight (ie, <2500, 2500-2999, 3000-3499, 3500-3999, or ≥4000 g). Two controls matched for sex and race were selected for each of these 1230 cases. Since birth certificates are registered in sequential order, the next 2 certificates with the same sex and race were selected. This procedure controlled for age. When a birth weight was not reported on a selected control certificate, the next certificate in sequence was selected. Age was calculated in completed years as of January 1, 1994. The Mann-Whitney test was used to compare the ages of case subjects according to sex, race, and cause of ESRD. Matching was preserved during the analysis of the data using conditional logistic regression in STATA, release 5 (STATA Corp, College Station, Tex). Odds ratios for renal failure were calculated for each birth weight category. The most common birth weight group, 3000 to 3499 g, was chosen as the reference interval to provide stable odds ratio estimates.

Of the 1230 cases with ESRD, 70% of patients (858) were black, 72% (892) were male, 19% (233) had diabetes, 29% (359) had hypertension, and 46% (571) were "other." For only 67 (5%), the cause of renal failure was unknown. The comorbid conditions and/or primary diagnoses were based on the reports from the nephrologist at the time of first dialysis. A substantial racial difference in the cause of ESRD was found in this study population, with 53% of ESRD cases among blacks caused by hypertension or diabetes vs 36% among whites.

The median age for all case subjects was 34 years but varied according to cause. The median age was 37 years for case subjects with diabetes, 36 years for those with hypertension, and 31 years for those with other causes of ESRD. Black case subjects with hypertension or diabetes were younger than corresponding white case subjects, with a median age of 36 years vs 38 years (P=.02). No significant age differences were detected for black and white case subjects with other causes of ESRD.

The mean birth weight was 3210 g for black and 3361 g for white case subjects, and it was higher in men (3295 g) than women (3149 g). Table 1 shows the odds ratios for renal failure from all causes of ESRD according to birth weight in men and women. Among all cases, the highest odds ratio is in the lowest birth weight group (ie, <2500 g). However, there is evidence of a U-shaped trend (quadratic trend), with elevated odds ratios at either end of the birth weight distribution (P=.02 for quadratic trend). The pattern is similar in men and women when analyzed separately.

Table Graphic Jump LocationTable 1. Odds Ratios for Renal Failure by Sex and Birth Weight Group*

Table 2 shows the odds ratios for renal failure according to cause of ESRD. For hypertension, diabetes, and other causes, there are elevated odds ratios among those with birth weights of 2500 g or less. In addition, the U-shaped trend is evident among case subjects with diabetes (P=.02 for quadratic trend). The quadratic trend is less evident in case subjects with hypertension or other causes of renal failure, in which case the trends are more linear. Figure 1, which omits the small number of cases of unknown cause, illustrates these patterns.

Table Graphic Jump LocationTable 2. Odds Ratios for Renal Failure by Primary Cause and Birth Weight Group*
Place holder to copy figure label and caption

Odds ratios for renal failure by primary cause and birth weight group; the reference birth-weight group is 3000 to 3499 g.

Graphic Jump Location

Table 3 shows that high odds ratios in association with low birth weight are seen in black and white case subjects. In separate models, for quadratic trends P=.03 for white and P=.19 for black case subjects. However, the quadratic trends for the 2 races did not differ significantly.

Table Graphic Jump LocationTable 3. Odds Ratios for Renal Failure by Race and Birth Weight Group*

Among men and women as well as among blacks and whites, chronic renal failure was significantly associated with low birth weight. One of the strengths of this study was the inclusion of black and white case subjects with ESRD in the southeastern United States. The analyses involved 1230 people who were born in South Carolina, developed chronic renal failure at a young age (<50 years), and required dialysis. This study was possible because a registry of all patients on dialysis has been maintained. Moreover, birth weight has been routinely recorded on birth certificates since 1950. Birth weights were ascertained for 65% of men receiving dialysis for ESRD. Based on our previous study of birthplace and stroke deaths in South Carolina, most of the remaining 35% were probably born outside the state.19 Birth weights were obtained for only 32% of women, which reflects the difficulty encountered when attempting to trace women, who usually change surnames at marriage. This would only introduce bias and limit extrapolations if associations between birth weight and ESRD were different in men and women who were born outside South Carolina or between women who were married or single. In our case-control study, we were able to match for sex, age, and race but not for socioeconomic status. The association of ESRD with low birth weight could, therefore, reflect associations with other aspects of low socioeconomic status. However, the links between low birth weight and both hypertension and NIDDM are independent of socioeconomic status.1317 Another limitation of the study was the inability to determine the level of blood pressure and glycemic control as well as the duration of hypertension and diabetes for the cases. However, the significant association with low birth weight was consistent for all causes of ESRD.

Low birth weight was found to be associated with cases of ESRD that were attributed to a range of causes, including those cases for which no cause was identified. One possible explanation for this was that reduced fetal growth is associated with defects in the development of the kidney that make it more vulnerable to a number of pathological processes. Brenner and colleagues2023 have proposed that chronic renal failure is associated with a reduced number of nephrons in the kidneys of individuals who had low birth weights. The number of nephrons in the normal population varies widely, from 300,000 to 1.1 million or more.24 In humans, 60% of the normal complement of nephrons are laid down during the last trimester, and kidney development ceases at around week 35.25 In addition, urinary albumin-creatinine ratios were higher among adult Aborigines who had low birth weights than those who had normal birth weights.26 Animal and human studies have shown that low rates of intrauterine growth are associated with reduced numbers of nephrons.27 Brenner and Mackenzie28 have suggested that retarded fetal growth leads to a reduced number of nephrons, which in turn leads to increased hydrostatic pressure in the glomerular capillaries, glomerular hyperfiltration, and the development of glomerular sclerosis.28 This sclerosis could in turn lead to further loss of nephrons as the glomerular hypertension and hyperfiltration worsen.

The association between birth weight and diabetic ESRD was U-shaped and may reflect a mixture of insulin-dependent childhood-onset diabetes and NIDDM. These data do not distinguish between these forms of diabetes. The risk of ESRD is 4 times greater in patients with insulin-dependent diabetes,29 which is associated with high birth weight. In a large study of children in Sweden, the relative risk of insulin-dependent diabetes rose progressively from 0.81 to 1.20 across the range of birth weight, after adjusting for gestational age.30 Likewise, an association between maternal undernutrition, retarded fetal growth, and the subsequent development of NIDDM has been demonstrated.31 Since this study involves the early onset of ESRD, maturity-onset diabetes of the young may be a significant contributor. This syndrome is defined clinically by the early onset of NIDDM.32 While somewhat different in physical and demographic characteristics from the black-white population in our study, an investigation of Japanese patients with early-onset NIDDM (diagnosed before age 30 years) found a high incidence of diabetic nephropathy consistent with rates among Pima Indian patients with NIDDM and white patients with insulin-dependent diabetes mellitus.33 A U-shaped association between birth weights and elevated urinary albumin excretion was identified in Pima Indians with NIDDM.34

The results of this study suggest that the high rates of ESRD among young people in South Carolina originate through an adverse environment in utero, which may impair the development of the kidney and make it more vulnerable to damage by a range of pathological processes. While the association between low birth weight and ESRD extends across race and sex, the high rates of ESRD in South Carolina are concentrated in the black population. Low birth weight is more common in South Carolina and the Southeast than in other states and regions, and it is more common among blacks than whites.12 Thus, the results of these analyses could provide one explanation for the high rates of chronic renal failure in the southeastern region of the United States as well as the excessive rates of ESRD among the black population. The earlier age of onset of renal failure in blacks with diabetes and hypertension compared with whites may reflect an accelerated progression of these diseases in blacks and/or a greater vulnerability of the kidney to their effects. The number of people who will be treated with long-term dialysis is predicted to increase over the next 40 years.35 The economic burden to Medicare, which covers the costs of ESRD, will continue to grow with an increasing disease rate and aging population. This economic drain may be reduced by the implementation of programs to improve perinatal health.

Accepted for publication October 6, 1999.

The study was partly funded by a grant from the Oriana Bethea Research Endowment, Medical University of South Carolina, Charleston.

The data in this report were supplied by the Southeastern Kidney Council, ESRD Network 6, Raleigh, NC, under Health Care Financing Administration contract 500-97-EO24.

We thank James Ferguson, DrPH, Yiling Cheng, PhD, Murray Hudson, MPH, Linda Jacobs, MPH, and the Office of Public Health Statistics and Information Systems, South Carolina Department of Health and Environmental Control, Columbia, for carrying out record linkage.

The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as an official policy or interpretation of the Southeastern Kidney Council or the Health Care Financing Administration, Washington, DC.

Corresponding author: Daniel T. Lackland, DrPH, Department of Biometry and Epidemiology, Medical University of South Carolina, Rutledge Tower 1125, Charleston, SC 29425 (e-mail: lackland@musc.edu).

Perry  HMRoccella  EJ Conference report on stroke mortality in the southeastern United States. Hypertension. 1998;311206- 1215
Link to Article
Lackland  DTMoore  MA Hypertension-related mortality and morbidity in the Southeast. South Med J. 1997;90191- 198
Link to Article
Lackland  DTBachman  DLCarter  TDBarker  DLTimms  SKohli  H The geographic variation in stroke incidence in two areas of the southeastern stroke belt: the Anderson and Pee Dee Stroke Study. Stroke. 1998;292061- 2068
Link to Article
US Renal Data System, USRDS 1998 Annual Data Report.  USRDS Bethesda, Md National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health April1998;
Brancati  FLWhittle  JCWhelton  PKSeidler  AJKlag  MJ The excess incidence of diabetic end-stage renal disease among blacks: a population-based study of potential explanatory factors. JAMA. 1992;2683079- 3084
Link to Article
McClellan  W Hypertensive end-stage renal disease in blacks: the role of end-stage renal disease surveillance. Am J Kidney Dis. 1993;2125- 30
Link to Article
Not Available, End-Stage Renal Disease Network 6, 1997 Annual Report.  Raleigh, NC Southeastern Kidney Council Inc1998;
Perneger  TVWhelton  PKKlag  MJ Race and end-stage renal disease: socioeconomic status and access to health care as mediating factors. Arch Intern Med. 1995;1551201- 1208
Link to Article
Rostand  SG US minority groups and end-stage renal disease: a disproportionate share. Am J Kidney Dis. 1992;19411- 413
Link to Article
Lackland  DTOrchard  TJKeil  JE  et al.  Are race differences in the prevalence of hypertension explained by body mass and fat distribution? a survey in a biracial population. Int J Epidemiol. 1992;21236- 246
Link to Article
Eberhardt  MSLackland  DTWheeler  FCGerman  RRTeutsch  SM Is race related to glycemic control? an assessment of glycosylated hemoglobin in two South Carolina communities. J Clin Epidemiol. 1994;471181- 1189
Link to Article
Ventura  SJAnderson  RNMartin  JASmith  BL Births and deaths: preliminary data for 1997. Natl Vital Stat Rep. October7 1998;471- 41
Hales  CNBarker  DJPClark  PMS  et al.  Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;3031019- 1022
Link to Article
Lithell  HOMcKeigue  PMBerglund  LMohsen  RLithell  UBLeon  DA Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ. 1996;312406- 410
Link to Article
Barker  DJPOsmond  CGloding  JKuh  DWadsworth  MEJ Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298564- 567
Link to Article
Nilsson  PMOstergren  PONyberg  PSoderstrom  MAllebeck  P Low birth weight is associated with elevated systolic blood pressure in adolescence: a prospective study of a birth cohort of 149,378 Swedish boys. J Hypertens. 1997;151627- 1631
Link to Article
Barker  DJP Fetal origins of coronary heart disease. BMJ. 1995;311171- 174
Link to Article
Law  CMShiell  AW Is blood pressure inversely related to birth weight? the strength of evidence from a systematic review of the literature. J Hypertens. 1996;14935- 941
Link to Article
Lackland  DTEgan  BMJones  PJ Impact of nativity and race on "Stroke Belt" mortality. Hypertension. 1999;3457- 62
Link to Article
Brenner  BMChertow  GM Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis. 1994;23171- 175
Link to Article
Brenner  BMMilford  EL Nephron underdosing: a programmed cause of chronic renal allograft failure. Am J Kidney Dis. 1993;2166- 72
Link to Article
Brenner  BMChertow  GM Congenital oligonephropathy: an inborn cause of adult hypertension and progressive renal injury? Curr Opin Nephrol Hypertens. 1993;2691- 695
Link to Article
Brenner  BMCohen  RAMilford  EL In renal transplantation, one size may not fit all. J Am Soc Nephrol. 1992;3162- 169
Mackenzie  HSBrenner  BM Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis. 1995;2691- 98
Link to Article
Hinchliffe  SALynch  MRJSargent  PHHoward  CVVan Velzen  D The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynaecol. 1992;99296- 301
Link to Article
Hoy  WERees  MKile  E  et al.  Low birthweight and renal disease in Australian aborigines. Lancet. 1998;3521826- 1827
Link to Article
Merlet-Benichou  CLeroy  BGilbert  TLelievre-Pegorier  M Intrauterine growth retardation and inborn nephron deficit. Med Sci. 1993;9777- 780
Brenner  BMMackenzie  HS Nephron mass as a risk factor for progression of renal disease. Kidney Int. 1997;52(suppl 63)124- 127
Perneger  TVBrancati  FLWhelton  PKKlag  MJ End-stage renal disease attributable to diabetes mellitus. Ann Intern Med. 1994;121912- 918
Link to Article
Dahlquist  GBennich  SSKallen  B Intrauterine growth pattern and risk of childhood onset insulin dependent (type 1) diabetes: population based case-control study. BMJ. 1996;3131174- 1177
Link to Article
Barker  DJP The fetal origins of type 2 diabetes mellitus. Ann Intern Med. 1999;130322- 324
Link to Article
Hattersley  AT Maturity-onset diabetes of the young: clinical heterogeneity explained by genetic heterogeneity. Diabet Med. 1998;1515- 24
Link to Article
Yokoyama  HOkudaira  MOtani  T  et al.  High incidence of diabetic nephropathy in early-onset Japanese NIDDM patients: risk analysis. Diabetes Care. 1998;211080- 1085
Link to Article
Nelson  RGMorgenstern  HPennet  PH Birth weight and renal disease in Pima Indians with type 2 diabetes mellitus. Am J Epidemiol. 1998;148650- 656
Link to Article
Whelton  PKKlag  MJ Hypertension as a risk factor for renal disease: review of clinical and epidemiological evidence. Hypertension. May1989;13(5 suppl)I19- I27
Link to Article

Figures

Place holder to copy figure label and caption

Odds ratios for renal failure by primary cause and birth weight group; the reference birth-weight group is 3000 to 3499 g.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Odds Ratios for Renal Failure by Sex and Birth Weight Group*
Table Graphic Jump LocationTable 2. Odds Ratios for Renal Failure by Primary Cause and Birth Weight Group*
Table Graphic Jump LocationTable 3. Odds Ratios for Renal Failure by Race and Birth Weight Group*

References

Perry  HMRoccella  EJ Conference report on stroke mortality in the southeastern United States. Hypertension. 1998;311206- 1215
Link to Article
Lackland  DTMoore  MA Hypertension-related mortality and morbidity in the Southeast. South Med J. 1997;90191- 198
Link to Article
Lackland  DTBachman  DLCarter  TDBarker  DLTimms  SKohli  H The geographic variation in stroke incidence in two areas of the southeastern stroke belt: the Anderson and Pee Dee Stroke Study. Stroke. 1998;292061- 2068
Link to Article
US Renal Data System, USRDS 1998 Annual Data Report.  USRDS Bethesda, Md National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health April1998;
Brancati  FLWhittle  JCWhelton  PKSeidler  AJKlag  MJ The excess incidence of diabetic end-stage renal disease among blacks: a population-based study of potential explanatory factors. JAMA. 1992;2683079- 3084
Link to Article
McClellan  W Hypertensive end-stage renal disease in blacks: the role of end-stage renal disease surveillance. Am J Kidney Dis. 1993;2125- 30
Link to Article
Not Available, End-Stage Renal Disease Network 6, 1997 Annual Report.  Raleigh, NC Southeastern Kidney Council Inc1998;
Perneger  TVWhelton  PKKlag  MJ Race and end-stage renal disease: socioeconomic status and access to health care as mediating factors. Arch Intern Med. 1995;1551201- 1208
Link to Article
Rostand  SG US minority groups and end-stage renal disease: a disproportionate share. Am J Kidney Dis. 1992;19411- 413
Link to Article
Lackland  DTOrchard  TJKeil  JE  et al.  Are race differences in the prevalence of hypertension explained by body mass and fat distribution? a survey in a biracial population. Int J Epidemiol. 1992;21236- 246
Link to Article
Eberhardt  MSLackland  DTWheeler  FCGerman  RRTeutsch  SM Is race related to glycemic control? an assessment of glycosylated hemoglobin in two South Carolina communities. J Clin Epidemiol. 1994;471181- 1189
Link to Article
Ventura  SJAnderson  RNMartin  JASmith  BL Births and deaths: preliminary data for 1997. Natl Vital Stat Rep. October7 1998;471- 41
Hales  CNBarker  DJPClark  PMS  et al.  Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;3031019- 1022
Link to Article
Lithell  HOMcKeigue  PMBerglund  LMohsen  RLithell  UBLeon  DA Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ. 1996;312406- 410
Link to Article
Barker  DJPOsmond  CGloding  JKuh  DWadsworth  MEJ Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298564- 567
Link to Article
Nilsson  PMOstergren  PONyberg  PSoderstrom  MAllebeck  P Low birth weight is associated with elevated systolic blood pressure in adolescence: a prospective study of a birth cohort of 149,378 Swedish boys. J Hypertens. 1997;151627- 1631
Link to Article
Barker  DJP Fetal origins of coronary heart disease. BMJ. 1995;311171- 174
Link to Article
Law  CMShiell  AW Is blood pressure inversely related to birth weight? the strength of evidence from a systematic review of the literature. J Hypertens. 1996;14935- 941
Link to Article
Lackland  DTEgan  BMJones  PJ Impact of nativity and race on "Stroke Belt" mortality. Hypertension. 1999;3457- 62
Link to Article
Brenner  BMChertow  GM Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis. 1994;23171- 175
Link to Article
Brenner  BMMilford  EL Nephron underdosing: a programmed cause of chronic renal allograft failure. Am J Kidney Dis. 1993;2166- 72
Link to Article
Brenner  BMChertow  GM Congenital oligonephropathy: an inborn cause of adult hypertension and progressive renal injury? Curr Opin Nephrol Hypertens. 1993;2691- 695
Link to Article
Brenner  BMCohen  RAMilford  EL In renal transplantation, one size may not fit all. J Am Soc Nephrol. 1992;3162- 169
Mackenzie  HSBrenner  BM Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis. 1995;2691- 98
Link to Article
Hinchliffe  SALynch  MRJSargent  PHHoward  CVVan Velzen  D The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynaecol. 1992;99296- 301
Link to Article
Hoy  WERees  MKile  E  et al.  Low birthweight and renal disease in Australian aborigines. Lancet. 1998;3521826- 1827
Link to Article
Merlet-Benichou  CLeroy  BGilbert  TLelievre-Pegorier  M Intrauterine growth retardation and inborn nephron deficit. Med Sci. 1993;9777- 780
Brenner  BMMackenzie  HS Nephron mass as a risk factor for progression of renal disease. Kidney Int. 1997;52(suppl 63)124- 127
Perneger  TVBrancati  FLWhelton  PKKlag  MJ End-stage renal disease attributable to diabetes mellitus. Ann Intern Med. 1994;121912- 918
Link to Article
Dahlquist  GBennich  SSKallen  B Intrauterine growth pattern and risk of childhood onset insulin dependent (type 1) diabetes: population based case-control study. BMJ. 1996;3131174- 1177
Link to Article
Barker  DJP The fetal origins of type 2 diabetes mellitus. Ann Intern Med. 1999;130322- 324
Link to Article
Hattersley  AT Maturity-onset diabetes of the young: clinical heterogeneity explained by genetic heterogeneity. Diabet Med. 1998;1515- 24
Link to Article
Yokoyama  HOkudaira  MOtani  T  et al.  High incidence of diabetic nephropathy in early-onset Japanese NIDDM patients: risk analysis. Diabetes Care. 1998;211080- 1085
Link to Article
Nelson  RGMorgenstern  HPennet  PH Birth weight and renal disease in Pima Indians with type 2 diabetes mellitus. Am J Epidemiol. 1998;148650- 656
Link to Article
Whelton  PKKlag  MJ Hypertension as a risk factor for renal disease: review of clinical and epidemiological evidence. Hypertension. May1989;13(5 suppl)I19- I27
Link to Article

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