SES, Chronic Kidney Disease, and Race in the U.S.: A Systematic Review and Meta-analysis

REVIEW ARTICLE

SES, Chronic Kidney Disease, and Race in the U.S.: A Systematic Review and Meta-analysis Priya Vart, PhD,1,2 Sander K.R. van Zon, MSc,1 Ron T. Gansevoort, MD, PhD,3 Ute Bültmann, PhD,1 Sijmen A Reijneveld, MD, PhD1 Context: The risk of chronic kidney disease (CKD) in the U.S. is higher in individuals with low SES than in those with high SES. However, differences in these risks between African Americans and whites are unclear. Evidence acquisition: Studies published through August 30, 2016 in Medline and EMBASE were searched. From the seven studies (1,775,267 participants) that met inclusion criteria, association estimates were pooled by race in meta-analysis. The ratio of association estimates and the corresponding 95% CIs for African Americans and whites were also pooled in meta-analysis. Additionally, meta-regression analysis was used to explore whether race is related to the strength of SES−CKD association. The analysis was conducted in September 2016. Evidence synthesis: The risk of CKD in low-SES people was 58% higher in African Americans (relative risk¼1.58, 95% CI¼1.33, 1.84) and 91% higher in whites (relative risk¼1.91, 95% CI¼1.47, 2.35) compared with their high-SES counterparts. The relative risk of CKD in low SES (versus high SES) was lower in African Americans than in whites (relative risk ratio¼0.71, 95% CI¼0.65, 0.77). Results from meta-regression analyses also indicated that race is potentially related to the strength of the association between low SES and CKD (p for difference between whites and African Americans¼0.001).

Conclusions: The risk of CKD in low SES (versus high SES) is higher in whites than in African Americans. Am J Prev Med 2017;](]):]]]–]]] & 2017 American Journal of Preventive Medicine. Published by Elsevier Inc. All rights reserved.

CONTEXT

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hronic kidney disease (CKD) is a major public health problem. CKD is associated with a number of adverse health outcomes, including progression to end-stage renal disease (ESRD), cardiovascular disease, and all-cause mortality.1,2 In the U.S., about two in three individuals will develop CKD during their life course.3 However, the risk of CKD is not distributed equally among populations. Substantial inequality is observed in prevalence and incidence of CKD across racial/ethnic4–6 and socioeconomic groups.7–9 Understanding racial/ethnic and socioeconomic disparities in CKD risk is important in achieving the Healthy People 2020 aim of eliminating these disparities in CKD by 2020.10 In the U.S., African Americans are suggested to have a higher risk of developing CKD than whites.11 Besides genetic susceptibility (e.g., due to APOL1 polymorphism in African Americans), low SES is a commonly suggested

explanation for the increased CKD risk in African Americans compared with whites because a large proportion of African Americans have low SES, which in itself is a risk factor for CKD.6,12–14 However, for the association between SES and CKD, it remains unclear whether or not the gradient in CKD risk by SES level differs between African Americans and whites. Studies From the 1Department of Health Sciences, Community and Occupational Medicine, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands; 2Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; and 3Department of Internal Medicine, Division of Nephrology, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands Address correspondence to: Priya Vart, PhD, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, 2024 East Monument Street, Baltimore MD 21205. E-mail: [email protected]. 0749-3797/$36.00 https://doi.org/10.1016/j.amepre.2017.06.036

& 2017 American Journal of Preventive Medicine. Published by Elsevier Inc. All rights reserved.

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investigating the association of low SES with CKD across racial groups yielded inconsistent and sometimes conflicting findings. Some studies have shown that, compared with their high-SES counterparts, African Americans with low SES have a higher relative risk (RR) of developing CKD than whites with low SES,9,15 whereas others showed no difference or a lower risk.16,17 Moreover, this inconsistency in association appeared to exist for both early and late stage of CKD.15 Therefore, the aims of this systematic review and metaanalysis were to: (1) summarize the RR of CKD in lowSES groups compared with high-SES groups for African Americans and whites, separately; and (2) assess whether the risk of CKD in low-SES groups versus high-SES groups differs between African Americans and whites.

EVIDENCE ACQUISITION Systematic review and meta-analysis were conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines.18,19 Five authors (PV, SKRvZ, RTG, UB, and SAR) formed the systematic review team. Four authors had expertise in social epidemiology (PV, SKRvZ, UB, and SAR), two in renal epidemiology (PV and RTG), and all in epidemiology and biostatistics.

Study Identification Medline and EMBASE were systematically searched to identify observational studies that were focused on SES, CKD, and race, and estimated the association between SES and CKD among racial/ ethnic groups separately in the U.S. Studies that were published between the inception dates of the searched databases and August 30, 2016 were retrieved without language restriction. The search strategy combined terms for individual and area-based socioeconomic indicators with terms for race/ethnicity and for individual measures of CKD. For SES, socioeconomic factors+ was used as a medical subject heading term that inherently covers both individual-level and area-level SES, and additional terms, such as income and education, were used to identify individual-level SES, and social deprivation to identify area-level SES measures. For CKD, chronic renal insufficiency+ as a medical subject heading term and renal insufficiency like other commonly used terms, were employed to identify relevant studies (Appendix Table 1, available online). Dialysis and transplant were not included as search terms because intention was to identify studies that examined CKD irrespective of CKD treatment status, not studies that examined only treated or untreated cases of CKD. Bibliographic information of existing reviews was also examined. Additionally, websites of leading public health, epidemiology, and nephrology journals for studies published in the last 3 months before the start of the systematic review were searched.

Study Selection Criteria The titles and abstracts of potentially relevant studies were screened and eligibility was checked for inclusion. Studies were included if they:

1. examined adult human U.S. populations (aged ≥18 years) of African-American and non-Hispanic white origin; 2. were based on general population or high-risk population (i.e., diabetic, hypertensive, aged ≥65 years, or CKD)20; 3. had a prospective/retrospective cohort design; 4. assessed SES using one or more of the following indicators: individual or household/family income, educational attainment, occupational class/status, available assets/wealth, or a related measure, such as poverty level, composite SES measure (when SES was derived from the combinations of individual’s or household income, education, and occupation), and area deprivation (e.g., average neighborhood income, unemployment rate, and deprivation indices); 5. defined CKD as: Stage 3, 4, or 5 (i.e., estimated glomerular filtration rate level o60 mL/min/1.73 m2 and/or albuminuria/ proteinuria level ≥30 mg/g, or the patient requiring dialysis or a renal transplant); 6. provided risk estimates for both racial groups separately (i.e., performed stratified analysis by race for the association between SES and CKD), or provided crude data enabling to calculate these estimates, (e.g., 2 X 2 tables); and 7. contained the latest published study/data if overlapping studies were published from the same cohort and offered similar outcome messages. Information on Hispanics was not included because of the paucity of data on SES and CKD in this racial/ethnic group in the U.S. Studies were excluded if they: (1) provided risk estimates for one racial group only, as these did not allow comparability of methods of SES, CKD assessment, and covariate adjustment when comparing the RR of CKD in low-SES whites and African Americans; (2) examined parental SES measures and not participant SES; and (3) were identified as conference abstracts, technical reports, and dissertations.

Data Extraction and Synthesis Two authors (PV and SKRvZ) extracted the following data from each study: characteristics of participants (number, age, sex, and race), type of SES measure, type of CKD measure, number of covariates adjusted for in the analysis, number of SES categories, comorbidities, length of follow-up, risk estimate with 95% CIs, and data on events and non-events in exposed and unexposed groups from studies that did not provide association estimates. For studies presenting estimates for SES assessed at various ages, estimates for SES assessed at the youngest age group were used to allow for longer follow-up time for CKD development. A risk estimate for the overall population was calculated for studies that reported association estimates overall and by age groups or sex. When a study reported association estimates for more than one SES measure, information was extracted on association estimates for all SES measures separately. To facilitate comparability between studies, the lowest- versus the highest-SES category risk estimate was extracted from each article, using highest SES as the reference group. For level of covariate adjustment, the maximally adjusted estimate was included where possible, but not adjusted for other SES measures. In the analyses, the level of covariate adjustment was categorized as crude (not adjusted for any covariate), minimally adjusted (only adjusted for age or sex), and maximally adjusted (adjusted for covariates in addition to age and sex). The number of SES categories were divided into categories of: two, www.ajpmonline.org

Vart et al / Am J Prev Med 2017;](]):]]]–]]] three, and four or more. When it was possible, the data to calculate RRs instead of ORs was extracted.21

Study Quality Assessment Three authors (PV, SKRvZ, and UB) assessed the quality of all included studies. Quality of the included studies was assessed using the criteria suggested by Hayden et al.22,23 Using these quality criteria, six potential sources of bias are examined: (1) representativeness of the study sample, (2) study attrition, (3) exposure assessment, (4) appropriateness of outcome measurement, (5) measurement of and accounting for covariates, and (6) appropriateness of analytic methods and of reporting of results (i.e., not selective). Each of these sources of bias was examined and assigned low, moderate, or high risk of bias. Using all six scores assigned to six potential sources of bias, each study was then assigned an overall low (no moderate or high risk of bias), moderate (one or more moderate risks of bias and no high risk of bias), or high risk of bias (one or more high risks of bias). The authors resolved disagreement on ratings by discussion.

Statistical Analysis Data analysis was conducted in September 2016. Risk estimates were pooled in a meta-analysis using the random effects model of DerSimonian and Laird (using the metan command specifying random in Stata, version 14.0) that incorporates both within- and betweenstudy variability, based on the initial assumptions of between-study heterogeneity.24 In case a study provided more than one estimate for a racial group (e.g., estimates for different SES measures), only one estimate per racial group at a time was included in the meta-analysis, to avoid potential collinearity between estimates from the same study. To handle multiple estimates arising from different SES measures in a single study, the effect estimate that was presented first was included in the meta-analyses and analyses were repeated when including the following estimate that was presented next in place of the estimate that was presented first. The log RRs from the individual studies and corresponding SE (presented or calculated from the confidence limits) were used to perform the analysis. The pooled estimates were then converted back to RRs and 95% CIs for presentation. Statistical heterogeneity among studies was evaluated using the I2 statistics. A series of random effect meta-analyses were performed to meet study objectives. First, to assess the RR of CKD in low SES African Americans and whites, the relationship between SES and CKD was quantified by racial subgroups (i.e., African Americans and whites). Second, to test the difference between African Americans and whites for their RRs of CKD due to low SES, the ratio of their RRs and the corresponding 95% CIs were calculated25 and these ratios were subsequently pooled in a random effect meta-analysis. Because heterogeneity may influence the funnel plot symmetry for reasons other than publication bias, and the interpretation of funnel plot is subjective,26 Egger’s and Begg’s tests were performed to determine possible publication bias.27,28 To further assess the robustness of findings in this review, a number of additional analyses were performed. Univariable and multivariable meta-regression analyses were performed to assess whether the RR for the association between low SES and CKD differed by race or any other relevant study characteristic. The multivariable meta-regression model included race, type of SES measure, level of covariate adjustment, and number of SES categories as covariates. In addition, subgroup analyses by the aforementioned covariates were presented. For the purpose of ] 2017

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meta-regression and subgroup analysis, types of SES measures were divided into two groups (i.e., individual-level and area-level) because there were few estimates for income, education, and occupation as a separate category. Moreover, within-study clustering of estimates was accounted for while performing metaregression analyses.29 Furthermore, the robustness of the findings was assessed by repetition of the overall analyses only for studies with low risk of bias, by using fixed effect models instead of random effect models and when using the effect estimate for subsequent SES measure(s) presented after first SES measure that was included in the primary analysis. Finally, low SES by definition may capture a narrow SES group and probably represents a reasonable approximation of low SES for both African Americans and whites, whereas the non−low-SES groups probably do not represent similar SES groups for African Americans and whites, particularly when SES is categorized in fewer categories. Thus, studies with four or more SES categories were analyzed separately to have a more representative approximation of an SES group for both African Americans and whites. All statistical analyses were performed using Stata, version 13.1. A p-value o0.05 was considered to be statistically significant.

EVIDENCE SYNTHESIS Selected Studies and Characteristics After removing duplicates, 769 study abstracts were reviewed. Of them, 40 articles qualified for full text review (Figure 1). In the full text review process, seven studies, comprising 1,775,267 participants, met the inclusion and exclusion criteria.13,17,30–34 From the included studies, a total of 20 risk estimates were obtained (ten each for African Americans and whites) (Table 1). Two of the included studies were prospective cohorts and five were retrospective cohorts. The majority of the studies used area and composite SES measures. Less frequently used SES measures were individual income, education, and occupation. Six studies assessed CKD as ESRD and one study assessed CKD as estimated glomerular filtration rate o45 mL/min/1.73 m2. Three studies had a crude level of covariate adjustment and two studies each had minimal and maximal level of covariate adjustment. Three studies had two SES categories; two studies had three SES categories; and two studies had four or more SES categories. In the study quality assessment, four studies were graded as having a low risk of bias, two studies as having a moderate risk of bias, and one study as having a high risk of bias (Appendix Table 3, available online). At all levels of SES, the incidence rates of CKD tended to be higher in African Americans than whites (Appendix Figure 1, available online). Meta-analysis Low SES was significantly associated with CKD in both African Americans and whites. In African Americans, the overall CKD risk was 58% higher in low SES groups compared with high SES groups (RR¼1.58, 95%

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Figure 1. Flow chart of the selection of studies. a Websites of leading public health, epidemiology, and nephrology journals were searched for relevant articles published in the last 3 months before start of the systematic review. CKD, chronic kidney disease.

CI¼1.33, 1.84). Among whites, the overall CKD risk was 91% higher in low-SES groups compared with high-SES groups (RR¼1.91, 95% CI¼1.47, 2.35; Figure 2). A high heterogeneity was observed in the meta-analyses (I2¼97.2%, po0.001 and I2¼96.4%, po0.001 for African Americans and whites, respectively). The RR of CKD in low SES (versus high SES) was 29% lower in African Americans compared with whites (RR ratio of African Americans versus whites¼0.71, 95% CI¼ 0.65, 0.77; Figure 3). The level of heterogeneity was high when pooling these estimates (I2¼87.8%, po0.001).

Egger’s test and Begg’s test for publication bias were not significant (p¼0.52 and p¼0.13, respectively). In random effect meta-regression analyses, the test for subgroup difference for African Americans versus whites was statistically significant. Among other study characteristics, a statistically significant subgroup difference was observed for level of covariate adjustment, but not for type of SES measure and number of SES categories (Appendix Table 2, available online). When using the following: high-quality studies only, fixed effect models instead of random effect models, ESRD studies only, effect estimate for subsequent SES

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Table 1. Characteristics of the Studies Included in the Systematic Review First author/ year

SES measure

CKD Study measure design

Area (income)

ESRD

Cohort (retro)

Klag, 199732

Area (income)

ESRD

Cohort (prosp)

Shoham, 200733

Education and occupation

Low eGFR

Volkova, 200813

Area (income)

Ward, 200834

Lipworth, 201218

Garrity, 201635

Sex

Comorbidities

ESRD type

Followup, years

Covariate adjustmenta

80,172 (whites¼49,781; AA¼30,391) 320,867 (whites¼300,645; AA¼20,222)

NP (o60)

M/F

NP

Dialysis/ 6 transplant

Maximum

whites: 46 AA: 45.3 (35–57)

M/F

Dialysis/ 16 transplant

Crude (unadjusted)

Cohort (retro)

12,631 (whites¼9,449; AA¼3,182)

67.4(NP)

M/F

Whites: DM¼1.4% Heart attack¼1.5% AA: DM¼3.2%, Heart attack¼1.4% NP

NA

Minimum

ESRD

Cohort (retro)

61 (419)

M/F

NP

Dialysis/ 5 transplant

Crude (unadjusted)

ESRD Composite (income, wealth, education, and occupation) Income and ESRD education

Cohort (retro)

34,767 (whites¼15,020; AA¼19,747) 704,946 (whites¼487,372; AA¼217,574)

NP (419)

M/F

NP

Dialysis/ 8.5 transplant

Minimum

Cohort (prosp)

79,943 (white¼25,192; AA¼54,751)

White: 51 AA: M/F 54(40–79)

DM¼21% HT¼56% MI/coronary artery bypass¼7%

Dialysis/ 329,003 transplant person years

Maximum

Area (income)

Cohort (retro)

541,941 (white¼392,307; AA¼149,634)

NP (20–110)

NP

Dialysis/ ∽5 transplant

Minimum

ESRD

M/F

NP

Resultsb RR (whites)¼1.57 (1.22– 2.03) RR (AA)¼1.59 (1.29–1.97) RR (whites)¼1.81 (1.17– 2.80) RR (AA)¼1.73 (1.00–3.00)

RR (low-education whites)¼ 1.46 (1.06–2.01) RR (low-education AA)¼ 1.35 (0.99–1.83) RR (unskilled whites)¼1.45 (1.11–1.88) RR (unskilled AA)¼1.89 (1.34–2.66) RR (whites)¼2.92 (2.72– 3.13) RR (AA)¼1.99 (1.86–2.13) RR (white)¼1.72 (1.54– 1.91) RR (AA)¼1.26 (1.20–1.33)

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Young, 199431

Sample size

Age, years, M (range)

HR (low-education whites)¼ 0.90 (0.40–2.00) HR (low-education AA)¼ 1.12 (0.88–1.44) HR (low-income whites)¼ 1.60 (0.97–2.80) HR (low-income AA)¼1.40 (1.20–1.70) RR (whites)¼2.56 (2.55– 2.57) RR (AA)¼1.71 (1.70–1.72)

a

Maximum, adjusted for covariates in addition to age and sex; minimum, adjusted for age and sex; crude, unadjusted. RR of HR with 95% CI for the lowest SES category compared to the highest SES category. AA, African Americans; CKD, chronic kidney disease; DM, diabetes mellitus; eGFR, estimated glomerular filtration rate; ESRD, end-stage kidney disease; F, females; HR, hazard ratio; HT, hypertension; M, males; MI, myocardial infarction; NA, not applicable; NP, not provided; prosp, prospective; RR, relative risk; retro, retrospective. b

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Figure 2. Meta-analysis of the relative risk (RR) of chronic kidney disease in low SES: (A) overall and (B) by race. ES, effect size.

measure(s) (data not shown), or studies with four or more SES categories, the results tended to show a higher RR of CKD in whites of low SES compared with African Americans of low SES (Appendix Table 4, available online).

DISCUSSION In this systematic review and meta-analysis, risk of CKD in low-SES groups compared with high-SES groups was observed to be 58% higher in African Americans and www.ajpmonline.org

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Figure 3. RRR of chronic kidney disease due to low SES in African Americans versus whites. ES, effect size; RRR, ratio of relative risk.

91% higher in whites. In addition, it was found that compared with African Americans, whites were at higher risk of CKD in low SES groups (versus high SES), suggesting that socioeconomic gradients in CKD risk may be steeper in whites than in African Americans. Some reviews previously investigated the association between SES and CKD but did not formally summarize this association for African Americans and whites.14,35–37 This is the first systematic review and meta-analysis quantifying the risk of CKD in low-SES African Americans and whites. This review expands understanding in a number of aspects. First, in a quantitative review of the association between SES and CKD risk, this review provides separate summary risk estimates for African Americans and whites. Of note, findings show that despite improvement in management of CKD risk factors, substantial SES disparities in CKD continue to exist in both African Americans and whites. Second, findings suggest that the socioeconomic gradient in CKD risk in the U.S. tends to differ between African Americans and whites, and this difference is unlikely due to methodologic differences in studies (e.g., differences in SES measures). Finally, findings from this review show that, although in African Americans RR for CKD by low SES is lower, the absolute risk is actually higher in African Americans than in whites, independent of whether African Americans have low SES or high SES. A number of factors might explain findings observed in this systematic review and meta-analysis. First, the prevalence of CKD risk factors, such as diabetes, hypertension, and poor diet, is generally higher in African Americans than in whites. This is true even independent of their SES group. Consequently, at any SES level, the ] 2017

absolute risk of CKD is higher in African Americans compared with whites (as can be seen from CKD incidence rates across SES groups in Appendix Figure 1, available online). Thereby, the RR at a given level of SES is lower in African Americans than whites.38 A second potential explanation relates to the difference in the coping mechanisms of African Americans and whites with low SES. Although African Americans may be economically disadvantaged compared with whites across SES levels, their reliance on particular coping resources may make them less vulnerable to the impact of chronic strains, particularly economic problems.39,40 Because chronic psychosocial distress is a risk factor for CKD,41,42 better coping with psychosocial distress could contribute to the lower RR of CKD from low SES among African Americans compared with whites. In addition, smaller SES differences in chronic psychosocial distress in African Americans than whites43 would also contribute to a lower RR for CKD among low-SES African Americans than low-SES whites. Finally, it is equally possible that African Americans retain some of the adverse health behaviors (e.g., poor diet),44 despite being in high-SES groups compared with whites in high-SES groups. In this review, besides race, the level of covariate adjustment was also related to the association between SES and risk of CKD, such that adjustment for covariates attenuated the association. Results from meta-regression analysis should be interpreted with caution, as the included studies were heterogeneous and the power to detect differences in the SES−CKD association by study characteristics was limited because of the small number of studies included in the review. However, these findings

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are in line with those from an earlier review showing the relationship between the level of covariate adjustment and the strength of SES–CKD association.35 It should be noted that, besides demographic factors, the factors adjusted for in the association between SES and risk of CKD were mostly CKD risk factors, such as smoking status, diabetes, and hypertension, which are more likely to be mediators than confounders. Future studies investigating the association between SES and CKD should make a clearer distinction between mediators and confounders. The results of this systematic review and meta-analysis may have important implications on future public health practice and research. They suggest that, despite efforts to manage hypertension, diabetes, and other CKD risk factors (which predominantly take place in healthcare settings), SES disparities in CKD continue to exist (both in African Americans and whites) and stress the need for interventions targeted at low-SES groups to reduce these disparities. In addition, if public health policy aims to achieve equality among groups with no consideration of absolute rates, findings observed in the present review suggest that the reduction of inequalities in CKD risk requires larger relative reductions in CKD in low-SES whites than in low-SES African Americans. However, in a more pragmatic view, high RR matters the most when absolute risk is also high.45 Given that people in low-SES groups and African Americans have high absolute risks of CKD (as also noted in this review) and resources are limited to reduce overall risk and RR, it might be preferred to reduce the absolute CKD risk among African Americans with low SES. Actions to prevent and manage CKD risk factors might first consider improving access to primary care for people in low-SES groups and African Americans (e.g., by extending their access to health insurance). In addition, preventive policies might be directed at including the full population, such as reduction of salt levels in food, like bread and fast food. Preventive policies should further aim to improve the reach of preventive messages among people in low-SES groups and among African Americans by targeted community-level interventions (e.g., National Implementation and Dissemination for Chronic Disease Prevention)46 that are focused on improving physical activity, tobacco control, and access to disease management in disadvantaged communities.

Limitations The results of this meta-analysis, however, should be interpreted with some caution. First, there was high heterogeneity for the pooled risk of CKD in low SES in both African Americans and whites that suggests that other factors than SES and race may also affect the risk of

CKD. Although the level of heterogeneity was similar for both African Americans and whites (i.e., variation in studies within a racial group was high, but minimal between them). Given that African Americans and whites were being compared within the same study (i.e., same study comparison), high heterogeneity should not influence the findings on the difference in CKD risk in lowSES African Americans and whites. Second, six of seven studies included in this meta-analysis examined CKD as ESRD and only one small study (n¼12,361) contributed evidence to risk of early-stage CKD. This may explain the lower RR of CKD in African Americans than in whites, as relatively more low-SES African Americans than low-SES whites die before reaching ESRD.47 Moreover, because six of the seven identified studies were ESRD studies, the results are predominantly applicable to late-stage CKD. Third, this systematic review is focused on the NorthAmerican populations, where some of the studies included in the review examined about 90% of all cases of the renal failure in the U.S. in a certain period.30,31 However, such studies were performed on participant SES data collected 10 to 20 years ago, which may have led to misclassification of SES. Fourth, average SES (e.g., average income) within low- or high-SES groups might vary between two races, especially when SES is categorized into fewer categories. This may influence results of this review. Though when studies with four or more SES categories were analyzed separately, they were found to have more similar approximations of an SES group for both African Americans and whites, essentially similar results were obtained. Finally, access to individual patient data was not available and thus it was not possible to explore which factors might explain differences in the socioeconomic gradient in CKD risk by race. Despite these limitations, the present systematic review and meta-analysis also has several strengths that merit mentioning. First, studies that measured CKD risk in low SES for African Americans and whites separately in the same study were examined. Within these studies, the definition of SES, the definition of CKD, and the level of covariate adjustment were the same for African Americans and whites, preventing their possible effect on the difference in CKD risk because of low SES in these racial groups. Second, as comprehensive searching of electronic databases may not retrieve all the pertinent literature, the literature search in this systematic review was supplemented by checking the reference lists on relevant search results. Third, to limit the possibility of reverse causation, only prospective and retrospective cohort studies were included. Fourth, to test the validity of findings, the quality of the included studies was assessed and separate meta-analyses were performed on high-quality studies only. Finally, the results of the tests for publication bias provide evidence that it is www.ajpmonline.org

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unlikely to have missed studies that could have altered the meta-analysis results.

CONCLUSIONS The risk of CKD in low SES groups is substantially higher than in high SES groups, both in African Americans and in whites. Importantly, the RR of CKD in low SES (versus high SES) differs between African Americans and whites, with the RR being higher in low SES whites. These findings reaffirm the importance of the socioeconomic factors and the concomitant role of race that are associated with the development of CKD.

ACKNOWLEDGMENTS This study did not receive any specific funding. All authors received funding from their respective institutes. The funding bodies had no role in the design and conduct of this study; in the collection, analysis, and interpretation of the data; or in the preparation, review, or approval of the manuscript. Research idea and study design: PV; data acquisition: PV, SKRvZ; data analysis/interpretation: PV, SKRvZ, UB, SAR; statistical analysis: PV, SKRvZ; supervision or mentorship: RTG, UB, SAR. Each author contributed important intellectual content during manuscript drafting or revision and accepts accountability for the overall work by ensuring that questions pertaining to the accuracy or integrity of any portion of the work are appropriately investigated and resolved. PV takes responsibility that this study has been reported honestly, accurately, and transparently; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned have been explained. No financial disclosures were reported by the authors of this paper.

SUPPLEMENTAL MATERIAL Supplemental materials associated with this article can be found in the online version at https://doi.org/10.1016/j. amepre.2017.06.036.

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