Socio-economic impact in CKD

Ne´phrologie & The´rapeutique 9 (2013) 1–7

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Socio-economic impact in CKD Association statut socioe´conomique et maladie re´nale chronique Laura C. Plantinga Department of Epidemiology, Rollins School of Public Health, Emory University, 1518 Clifton Road NE 3rd Floor, Atlanta, GA 30023, United States of America

A R T I C L E I N F O

A B S T R A C T

Article history: Received 29 April 2012 Accepted 29 July 2012

Background. – Socio-economic status (SES) may be conceptualized as an individual’s position in society, as determined by their income, occupation, education, wealth, and housing situation. This review summarizes the current literature regarding associations of these markers of SES with both chronic kidney disease (CKD) and associated poor outcomes. Methods. – Literature searches were conducted in the US National Library of Medicine, National Institutes of Health, PubMed database using the search terms ‘‘chronic kidney disease’’ and ‘‘chronic renal insufficiency,’’ combined with ‘‘socio-economic status,’’ ‘‘income,’’ ‘‘occupation,’’ ‘‘employment,’’ ‘‘education,’’ ‘‘social class,’’ ‘‘wealth,’’ and ‘‘housing.’’ Articles not in the English language, using nonhuman subjects, or primarily concerning subjects with ESRD or acute kidney injury were excluded. Results. – Income is the most-studied aspect of SES in relation to CKD, but there is increasing literature involving occupation and education as well. Additionally, the associations of CKD and its outcomes with area-level and life course SES are both burgeoning areas of research. There are several research areas that remain mostly unexplored, including the roles of wealth and housing in defining SES-related risk in CKD. Additionally, none have explored the relative utility of composite versus individual indicators of SES in predicting risk of CKD and outcomes. Conclusion. – Given the overwhelming evidence that SES plays an important role in the development and progression of disease, the development and testing of more targeted interventions should be a top priority in CKD research. Continuing examination of these factors, with increased rigor and focus on potentially modifiable intermediate pathways, is needed. ß 2013 Publie´ par Elsevier Masson SAS pour I’Association Socie´te´ de ne´phrologie.

Keywords: Socio-economic status Chronic kidney disease Income Occupation Education Wealth Housing Area-level Life course

R E´ S U M E´

Mots cle´s: Statut socioe´conomique E´ducation Emploi Revenus Logement Biens Insuffisance re´nale chronique

Le statut socioe´conomique repre´sente la place du patient dans la socie´te´, selon l’e´ducation qu’il a rec¸ue, son emploi, ses revenus, son logement et ses biens. La pre´sente revue de la litte´rature explore les liens entre ces diffe´rentes composantes du statut socioe´conomique, d’une part, et le diagnostic et le pronostic de l’insuffisance re´nale chronique, d’autre part. Les articles ont e´te´ recherche´s dans les bases de donne´es : US National Library of Medicine, National Institutes of Health, PubMed database, en utilisant les expressions suivantes : « chronic kidney disease » et « chronic renal insufficiency », associe´es a` « socioeconomic status », « income », « occupation », « employment », « education », « social class », « wealth » et « housing ». Les articles qui n’e´taient pas en langue anglaise, qui n’e´taient pas des e´tudes chez l’homme, ou qui se focalisaient sur l’insuffisance re´nale chronique terminale ou l’insuffisance re´nale aigue¨, n’ont pas e´te´ se´lectionne´s. Concernant l’association : statut socioe´conomique/diagnostic ou pronostic de l’insuffisance re´nale chronique, c’est la composante : Revenus qui a e´te´ la plus e´tudie´e jusqu’a` pre´sent. Mais la litte´rature consacre´e aux composantes : E´ducation et Emploi est de plus en plus significative. E´galement, on constate une augmentation du nombre d’e´tudes consacre´es aux caracte´ristiques des zones ge´ographiques d’habitation et a` l’e´volution du statut socioe´conomique au cours de la vie. En revanche, les composantes : Logement, Biens et les crite`res composites de´finissant le statut socioe´conomique, ne sont pas e´tudie´es. En conclusion, les e´tudes sur les diffe´rentes composantes du statut socioe´conomique doivent eˆtre approfondies. Comme il semble exister un lien tre`s significatif entre le statut socioe´conomique et le diagnostic et le pronostic de l’insuffisance re´nale chronique, l’e´valuation d’interventions cible´es dans ce domaine devrait eˆtre une priorite´. ß 2013 Published by Elsevier Masson SAS on behalf of the Association Socie´te´ de ne´phrologie.

E-mail address: [email protected] 1769-7255/$ – see front matter ß 2013 Publie´ par Elsevier Masson SAS pour I’Association Socie´te´ de ne´phrologie. http://dx.doi.org/10.1016/j.nephro.2012.07.361

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1. Introduction

2. Search strategy

Chronic kidney disease (CKD), characterized by sustained kidney damage and/or reduced kidney function, is prevalent [1] and is associated with substantial morbidity and mortality [2]. While end-stage renal disease (ESRD), which is defined by the requirement of dialysis or transplant to sustain life, is a wellknown debilitating and expensive outcome of CKD, most adults with CKD will never progress to ESRD. Rather, adults with CKD are likely to suffer various disease-related complications such as anemia, bone disease, cardiovascular disease, and death [2]. In the United States, there are currently greater than 600,000 US adults being treated for ESRD [3], but it is estimated that nearly 26 million may have earlier-stage CKD [1], illustrating the relatively small likelihood of progression to ESRD compared to other outcomes. Additionally, despite the poor consequences of CKD, awareness of disease has been estimated in most populations to be less than 10% [4], which underscores the need for early identification of and intervention in individuals at high risk for CKD. One potential identifiable risk factor is socio-economic status (SES). The two primary risk factors for adult CKD, besides older age, are diabetes mellitus and hypertension. There is a vast international literature linking SES to the incidence and control of both diabetes [5,6] and hypertension [7–9]. It is reasonable to postulate that SES is also an important determinant of CKD (Fig. 1). SES may be conceptualized as an individual’s position in society along a ‘‘SES gradient’’ [10] that is determined by their income, occupation, education, wealth, and/or housing situation. Through such diverse mechanisms as access (to nutrition, physical activity, health information, and/or treatments), stress, and environmental triggers, these markers of SES may be associated–both directly and through diabetes and hypertension–with both CKD and associated poor outcomes. SES has been studied extensively in the context of ESRD [11– 14]. However, it is likely that many SES-related disparities in CKD are established early in disease. Additionally, the association of SES with ESRD, which is treated either with a kidney transplant or dialysis, involves many complex ESRD-specific issues, such as disparities in waitlist referral, kidney allocation, kidney graft survival, choice of dialysis modality, and placement of permanent vascular access for dialysis, that are less relevant earlier in disease. Thus, the focus of the following review is the examination of the current literature regarding associations of SES with adult, earlystage (pre-ESRD) CKD.

Literature searches for primary sources regarding CKD and SES were conducted in the US National Library of Medicine, National Institutes of Health, PubMed database (www.pubmed.gov) using the search terms ‘‘chronic kidney disease’’ and ‘‘chronic renal insufficiency,’’ combined with each of the following: ‘‘socioeconomic status,’’ ‘‘income,’’ ‘‘occupation,’’ ‘‘employment,’’ ‘‘education,’’ ‘‘social class,’’ ‘‘wealth,’’ and ‘‘housing.’’ The search limits included English language and human subjects. Articles that were determined to primarily concern subjects with ESRD or acute kidney injury were not further reviewed. Additional citations were identified secondarily via examination of reference lists in published literature. In general, the combination of CKD and education provided the most initial hits (n = 2324), followed by SES (n = 315), employment (n = 259), income (n = 203), social class (n = 74), occupation (n = 57), wealth (n = 20), and housing (n = 18). After exclusions, additional removal of studies in which SES was used for adjustment only, and recategorization as needed (e.g., ‘‘poverty level’’ being classified more correctly as a measure of income rather than wealth), individual-level income and education were the most commonly examined aspects of SES as potential risk factors for CKD and its outcomes. 3. Individual components of SES and CKD Income, occupation, education, wealth, and housing are individual components of SES that likely overlap considerably but not perfectly (Fig. 2A), such that each component further enhances the complete ‘‘picture’’ of an individual’s SES [15]. SES in CKD has been examined using both individual and multiple components of SES, and these components have also been analyzed as separate and combined factors. 3.1. Income and CKD Although it has only recently been studied in earlier stages of CKD, income is, by far, the most-studied of the SES components with respect to CKD. In 1999, Krop et al. [16] found that reported income less than $16,000 versus greater than $35,000 was associated with 2.4-fold greater risk of incident early kidney function decline ( 0.4 mg/dl increase in creatinine over 3 years) among persons aged 45–64 with diabetes in the longitudinal Atherosclerotic Risk in Communities (ARIC) study. Subsequently, studies have mostly corroborated this observed association

Fig. 1. Proposed pathways through which socio-economic status (SES) influences chronic kidney disease and its outcomes.

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Fig. 2. Dimensions of socio-economic status (SES). A. Cross-section of various components of SES. B. Population dimension of SES. C. Time dimension of SES.

between income and the burden of CKD in various populations. A community-based study of African-Americans in Jackson, Mississippi, showed that the odds of CKD (either albuminuria or reduced kidney function) were 41% lower in the more affluent participants [17]. In a cross-sectional study of low- and highincome (defined by 125% of the US poverty threshold) white and African-American participants in Baltimore, Maryland, low income was associated with 59% greater odds of reduced kidney function among the African-Americans only [18]. Even among a cohort of persons with CKD [the Chronic Renal Insufficiency Cohort (CRIC) study], the prevalence of having eGFR less than 30 was 37% in those with income less than $25,000 but only 6% in those with income greater than $100,000 [19]. Outside the United States, results are mixed. Studies of community-level data suggest that poverty is not as strong a predictor in the Australian and Thai populations, relative to the US population [20]. However, in an Indian CKD registry, lower income was associated with more advanced CKD at presentation [21]. Complications and outcomes, as well as burden, of CKD have been associated with lower income. In the REasons for Geographic Differences in Stroke (REGARDS) study, the odds of anemia among those reporting income less than $25,000 were 2.6-fold the odds in those reporting income greater than $75,000 (1.2-fold after adjustment for education) [22]. Gutierrez and colleagues [23,24] found that odds of phosphatemia were greatest among those with lowest income both in a longitudinal cohort (CRIC) and in a national survey [National Health and Nutrition Examination Survey (NHANES)]. Disability was also shown to be more common in those with lower income in NHANES [25]. Similarly, lower physical (but not mental) health-related quality of life (HRQOL) scores were associated with lower income among participants with CKD in the African-American Study of Kidney Disease and Hypertension (AASK) Trial [26]. Depressive symptoms were shown to be more common with lower income in the AASK study [27] and also in a Brazilian study of patients with CKD [28]. Progression to

ESRD, even in a disadvantaged safety-net urban patient population, was still greater among those with lowest income [29]. Finally, income less than $15,000 was a significant predictor of cardiovascular disease incidence in the AASK study, even after adjustment for several clinical factors [30]. Note that the use of income as a predictor for CKD and its outcomes can be problematic for many reasons. First, most researchers have used cutoffs rather than continuous income, despite the abundance of evidence for a SES gradient in health [10]. When dichotomous cutoffs were used, they were often poverty thresholds, which may differ dramatically by country or region, reflect definitions that are primarily politically driven, and/or lack generalizability. Second, information on income can be difficult to obtain, and missing information may be correlated with risk factors for or outcomes of CKD. At least one study has suggested that failure to disclose income is associated with less adherence to blood pressure control regimens in those with CKD [31]; however, baseline data from CRIC showed that, while missing income information is prevalent (15% refusal), refusal did not differ by CKD severity [19]. Finally, in cross-sectional studies, the possibility that CKD and its effects have caused a decline in income, rather than vice versa, cannot be excluded [25,32]. 3.2. Occupation and CKD Information on occupation as a risk factor for CKD or its outcomes is less abundant. A case-control study in Sweden [33] showed that individuals with CKD were more likely to come from families with only unskilled workers compared to families with professional workers. In a Brazilian study [28], among those with CKD, those in the lowest occupational grades, including those who did only unskilled work or casual or no work, were more likely to have depressive symptoms relative to those in higher grades with CKD. Similarly, lower occupational grade was cross-sectionally associated with greater odds of decreased eGFR in a United

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Kingdom study [34]. American studies have focused more on the state of unemployment rather than particular occupational grades or classes. For example, greater prevalence of hyperphosphatemia [23], depressive symptoms [27], and lower mental and physical HRQOL [26,35] have all been associated with unemployed status in populations with CKD in the United States. Additionally, NHANES data showed that unemployed non-Hispanic black and MexicanAmericans in the United States had greater than 2-fold greater prevalence of CKD relative to their employed counterparts [20]. In general, longitudinal studies on occupation and CKD are lacking, and, particularly in the United States, the focus is primarily on unemployed status. Recent economic developments worldwide, which have led to changing occupational and employment status for many, may provide opportunities to explore these associations more closely. Of course, specific occupational exposures, which are more common in lower occupational grades, have been examined as risk factors for CKD. Lead exposure has been associated with CKD in the general [36] and lead worker [37,38] populations in the United States; however, occupational lead exposure was not associated with CKD in a Swedish case-control and cohort studies [39]. The mixed evidence may be the result of true differences in either exposure or risk or may be due to differences in study design and power. Similarly, greater burden of CKD has recently been seen among agricultural workers (particularly, those working with sugar cane) in Central America [40–42], but the specific exposures associated with this local epidemic remain unknown. 3.3. Education and CKD Education has been studied frequently as a potential risk factor for CKD, but rarely in isolation. In the ARIC study [16], individuals with less than a high school education had 1.7 times the risk of kidney function decline versus those with a college education. Similar associations were seen in the Jackson Heart Study [17] and in a population-based case-control study in Sweden [33]. Low education was also associated cross-sectionally with lower physical HRQOL on both the mental and physical scales in African-Americans with CKD [26]. Disability in persons with CKD was also more common among those with lower education in NHANES [25]. This study demonstrates the possibly greater utility of education as compared to income as a risk factor in crosssectional studies of outcomes that may both be a cause and result of income, such as disability–in other words, given that CKD may lead to a loss in income but is unlikely to affect educational status, the possibility of reverse causation is lessened. Finally, in an observational cohort of the Kidney Early Evaluation Program (KEEP) study, Choi et al. [43] found that lower educational attainment was associated with greater prevalence of CKD and higher mortality in those in the cohort who had chronic disease, including CKD. 3.4. Wealth and CKD While income has been examined extensively in CKD, wealth remains virtually unexplored, particularly at the individual level, possibly due to difficulties in obtaining information about net worth. Wealth is distinct from income, in that it represents the accumulation of assets and worth, rather than the flow of resources (income) or the potential for accumulation of resources (education and occupation). Its importance in health is related to its ability to act as a buffer in times of hardship, including stressful life events and associated health outcomes, particularly in places with fewer social welfare programs [44]. Additionally, in older individuals, wealth could act as a proxy for lifetime SES, although the impact of extant chronic disease on wealth must be considered. Although

wealth has generally not been explored as a predictor in studies of CKD, related conditions like stroke [45] and cardiovascular disease [46] have been shown to be independently associated with wealth. Research exploring the feasibility and predictive value of wealth as an indicator of SES is likely warranted in CKD. 3.5. Housing and CKD Housing is the final individual indicator of SES examined here. Housing tenure (or home ownership), amenities (running water, heating, refrigerator, etc.), environment (pests, lead, etc.), and overcrowding are all household-level indicators that may be related to health and, particularly, CKD. A 30-year ecologic analysis of national survey data showed that asthma, obesity, and diabetes trends in the United States tracked with improvements in housing characteristics over time [47]. Housing instability has also been associated with decreased self-efficacy in persons with diabetes [48]. Certain exposures such as lead and cadmium have been associated with CKD [49–52], and these exposures may be more likely in poorer housing. These intriguing trends suggest further research into housing as a potential risk factor for CKD. 3.6. Composite measures of individual SES While most studies have examined individual factors of SES in relation to CKD, often in the same study, a few have used composite scores that combine multiple factors. For example, in a singlecenter German study of diabetic patients, Wolf et al. [53] found that reduced kidney function, but not albuminuria, was associated with a low score on a composite indicator including household net income, highest professional position achieved, and education. Additionally, composite scores have been frequently used in arealevel and life course studies of SES and CKD, described below. Such composite measures may be advantageous because they take multiple factors into account, which is likely a more accurate representation of the complete SES picture. However, these composite scores are often sums of indicators or z scores, which assume equal weight for each component of the score. The validity of this assumption requires further research into the relative contributions of each SES component to CKD-related risk. 4. Area-level SES and CKD Interest in the effects of individuals’ surroundings on their health has grown substantially in the last 15 years. The socioeconomic features of a neighborhood, community, or other geographic area could affect health through various environmental and social pathways, above and beyond individual SES and other risk factors [54,55]. The various components of SES that have been described above at an individual level can be considered along a ‘‘population’’ dimension, from the individual to household to community to society (Fig. 2B) [56]. Merkin and colleagues were pioneers in the study of the effect of area-level SES on CKD [57,58]. In the ARIC study, they examined progressive CKD (i.e., declines in kidney function over follow-up) by US. Census block-stratified SES. Using a composite SES score–a sum of z scores for six census-derived SES indicators, including median household income, median value of housing units; percentage of households with interest, dividend, or rental income, percentage of residents older than 25 years with a complete high school education, percentage of residents older than 25 years with a complete college education, and percentage of residents in executive, managerial, or professional specialty occupations–they found that, with adjustment for individual SES and other confounders, area-level poverty was associated with 60% higher risk in white men (associations in women and African-American

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men were not statistically significant after adjustment) [57]. Similarly, in the elderly population of the Cardiovascular Health Study, the same group [58] found 50% increased risk for progressive CKD among elderly participants living in Census blocks with the lowest SES scores. In contrast, in the REGARDS study, McClellan et al. [59], using single measures of poverty (< $15,000 household income or 25% of households in neighborhood below poverty), found that household but not neighborhood-level poverty was associated with CKD. All three studies employed similar hierarchical modeling techniques to account for both individual- and area-level SES; the differences in results may reflect the use of multiple- versus single-component SES at both levels. In a United Kingdom study [60], being in the lowest versus highest quintile of social deprivation at the arealevel, as measured by the British Index of Multiple Deprivation (http://www.communities.gov.uk/publications/communities/ indiciesdeprivation07), was associated with greater severity of CKD at presentation to renal service. Not only burden but also poor outcomes of CKD have also been associated with neighborhood SES. Neighborhood poverty has been associated with greater risk of progression to ESRD in the southern United States [61,62]. In Australia, area measures of social disadvantage (examining multiple SES factors) have been associated with delayed nephrology referral (a measure of access to care) and disease progression risk [63,64]. While high levels of SES inequality at the area-level have been associated with poor health overall, albeit modestly [65–67], no specific studies of SES inequality and CKD or its outcomes were identified in this literature search. 5. Life course SES and CKD In addition to the population dimension, SES may be considered over the dimension of time (Fig. 2C) [56], from gestation to death (‘‘life course’’). The examination of life course SES rather than static measures of SES as risk factors for chronic disease is a relatively nascent but growing field [68]. In 2005, Shoham et al. [69] presented the current literature of CKD and SES at various stages of life, arguing for a life course SES perspective in CKD research. Later, the same authors presented data from the ARIC study [70,71], in which SES was measures at various time points (e.g., working vs. non-working class, based on occupation, at ages 30, 40, and 50; area-level SES based, on summed z scores from corresponding census data, at ages 10, 30, 40, and 50). In general, there were positive but non-statistically significant responses for low versus high tertiles of SES at the various time points. The authors also noted that the effects of area SES were strongest at the older ages. Such results begin to suggest the accumulation of effects of deprivation over time, which is an underlying mechanism behind the hypothesis that SES over the life course affects later health. 6. Summary and implications Much of the research on SES and CKD focuses on its explanatory role in observed racial disparities in CKD [16,18,59,72,73], particularly in the United States. However, increasingly, low SES is being viewed as an independent potential risk factor for CKD. Income is the most-studied aspect of SES in relation to CKD, but there is increasing literature involving occupation and education as well. Additionally, the associations of CKD and its outcomes with area-level and life course SES are both burgeoning areas of research. As noted, there are several research areas that remain mostly unexplored, including the roles of wealth and housing in defining SES-related risk in CKD. Another area for possible research includes the determination of the relative utility of composite versus individual indicators of SES in predicting risk of CKD and outcomes.

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The current literature has limitations, including a general lack of longitudinal studies, use of arbitrary dichotomous cutoffs, possibly differentially missing data (particularly for income), and likely geographic variations in the relative importance of various SES indicators to individual health, making the standardization of measures difficult. In general, SES was not a primary question in the studies examined, and available data may not necessarily the most relevant or informative data for the research question. Despite these problems, the preponderance of evidence points to a strong role of SES in the development and progression of CKD. Of course, the ultimate goal of such research would be to inform potential interventions that prevent CKD and its outcomes in those who may be at higher risk due to SES. In general, such interventions are lacking. Clinical practice guidelines for CKD, such as those presented by the National Kidney Foundation’s Kidney Disease Quality in Outcomes Initiative [74], focus on treatment aspects only. Recent Australian guidelines discuss the role of SES in increasing the risk of CKD but fail to provide specific interventions for disadvantaged populations [75]. US education initiatives such as National Kidney Foundation’s KEEP, the National Institutes of Health’s National Kidney Disease Education Program (http:// nkdep.nih.gov/), and the Centers for Medicare and Medicaid’s mandated free education program for stage 4 CKD patients [76] may provide greater access to information to those with low SES. Additionally, housing projects such as the Seattle-King County Healthy Homes Project [77] and Oklahoma Healthy Homes Initiative [78] might improve overall health–and decrease risk of CKD specifically–in those with poor housing opportunities. However, the effects of such programs on CKD risk specifically remains unexplored. Given the overwhelming evidence that SES plays an important role in the development and progression of disease, the development and testing of more targeted interventions that might mitigate the effects of SES on CKD and its outcomes should be a top priority in CKD research. Such a process necessitates the continuing examination of these factors, with increased rigor– particularly with respect to the development and validation of composite measures in all SES dimensions–to identify potentially modifiable intermediate pathways that could be amenable to interventions to decrease CKD risk. Disclosure of interest The author declares that she has no conflicts of interest concerning this article. Acknowledgements The author would like to thank Drs. William McClellan and Julie Gazmararian for their critical reading of earlier versions of the manuscript. References [1] Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, et al. Prevalence of chronic kidney disease in the United States. JAMA 2007;298(17):2038–47. [2] Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 2004;351(13):1296–305. [3] United States Renal Data System, USRDS 2011 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, 2011. [4] Plantinga LC, Tuot DS, Powe NR. Awareness of chronic kidney disease among patients and providers. Adv Chronic Kidney Dis 2010;17(3):225–36. [5] Agardh E, Allebeck P, Hallqvist J, Moradi T, Sidorchuk A. Type 2 diabetes incidence and socio-economic position: a systematic review and meta-analysis. Int J Epidemiol 2011;40(3):804–18.

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