Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
Associations between socioeconomic status and
chronic kidney disease: a meta-analysis
Xiaoxi Zeng,1,2 Jing Liu,1 Sibei Tao,1 Hyokyoung G Hong,3 Yi Li,4 Ping Fu1,2

►► Additional material is ABSTRACT These can differ substantially in their associations

published online only. To view Background Socioeconomic status (SES) has long been and effect size.10 In the absence of a uniform defi-
please visit the journal online
(http://d​ x.​doi.o​ rg/​10.​1136/​ conjectured to be associated with the incidence and nition of SES, various substitutes have been used,
jech-​2017-​209815). progression of chronic kidney disease (CKD), but few including income, education level, occupation,
studies have examined this quantitatively. This meta- wealth or geographic location. Second, many
1
Division of Nephrology, Kidney analysis aims to fill this gap. studies have been confined to particular regions, so
Research Institute, West China the results may not be generalisable. Studies have
Methods A systematic literature review was performed
Hospital of Sichuan University,
Chengdu, China using Medline and EMBASE to identify observational therefore provided inconsistent results about the
2
West China Biomedical Big studies on associations between SES and incidence magnitude of associations, making it hard to under-
Data Center, Sichuan University, and progression of CKD, published between 1974 and stand the true association between SES and CKD
Chengdu, China March 2017. Individual results were meta-analysed using in the general population. Vart et al5 performed a
3
Department of Statistics and
Probability, Michigan State a random effects model, in line with Meta-analysis of meta-analysis to explore the association between
University, East Lansing, Observational Studies in Epidemiology guidelines. the two, combining estimates from different socio-
Michigan, USA Results In total, 43 articles met our inclusion criteria. economic indicators. However, the mechanisms
4
Department of Biostatistics, CKD prevalence was associated with several indicators underlying the association between individual indi-
University of Michigan, Ann cators and the onset and progression of CKD need
of SES, particularly lower income (OR 1.34, 95% CI (1.18
Arbor, Michigan, USA
to 1.53), P<0.001; I2=73.0%, P=0.05); lower education further investigation. We therefore carried out a
Correspondence to (OR 1.21, 95% CI (1.11 to 1.32), P<0.001; I2=45.20%, meta-analysis to examine the association between
Professor Ping Fu, Division of P=0.034); and lower combined SES (OR 2.18, 95% CI CKD and several individual indicators of SES.
Nephrology, Kidney Research (1.64 to 2.89), P<0.001; I2=0.0%, P=0.326). Lower
Institute, West China Hospital levels of income, occupation and combined SES were
of Sichuan University, Chengdu, Materials and methods
also significantly associated with progression to end-
Sichuan 610041, China; ​ Study identification
fupinghx@​163.​com stage renal disease (risk ratio (RR) 1.24, 95% CI (1.12 to
1.37), P<0.001; I2=66.6%, P=0.006; RR 1.05, 95% CI Information source and search strategy
XZ and JL contributed equally. (1.01 to 1.09), P=0.012; I2=0.0%, P=0.796; and RR Eligible studies on associations between SES and
1.39, 95% CI (1.09 to 1.79), P=0.009; I2=74.2%, CKD were found by searching four electronic data-
Received 4 August 2017
P=0.009). Subgroup analyses generally confirmed bases: PubMed/Medline, OV/EMBASE, Cochrane
Revised 22 November 2017 Library and Chinese Biomedicine Database from
Accepted 6 January 2018 these results, except in a few cases, such as an inverse
Published Online First association related to particular socioeconomic 1974 to March 2017.
2 February 2018 backgrounds and where results were adjusted by more Suitable studies involved associations between
disease-related risk factors. individual indicators (income, educational attain-
Conclusion Lower income was most closely ment or occupation) or a combined index of
SES and CKD.11 12 Keywords included ‘social class’,
associated with prevalence and progression of CKD,
and lower education was significantly associated ‘socioeconomic status, position, factors’, ‘income’,
with its prevalence. Evidence for other indicators was ‘education level’, ‘occupations’, ‘chronic kidney
inconclusive. disease’, ‘chronic renal insufficiency’, ‘chronic
kidney failure’ and ‘chronic renal dysfunction’
(see online supplementary material/search strategy).
There were no restrictions on languages or coun-
tries of publication. Unpublished or non-peer-re-
Introduction
viewed articles were excluded. The review complied
Chronic kidney disease (CKD) has become a global
strictly with Meta-analysis of Observational Studies
issue because of its rapidly increasing prevalence and
in Epidemiology guidelines for meta-analyses13
cost. Its worldwide prevalence ranges from 10.2%
(online supplementary table 1).
to 13%,1–3 and middle-aged and older people with
a history of hypertension or diabetes are more
susceptible.4 Individuals with lower socioeconomic Selection criteria
status (SES) may suffer from unrecognised and Studies were independently screened by two
untreated CKD as well as end-stage renal disease reviewers (JL and ST) using the following criteria:
in both low-income and middle-income countries Inclusion criteria: (1) prospective, retrospective
and developed countries.5–7 This may be because of and cross-sectional observational studies; (2) adult
poor access to healthy diets, physical activity, health population or adult patients diagnosed with CKD;
information and quality healthcare.8 9 (3) reported associations between at least one deter-
To cite: Zeng X, Liu J, Tao S, Studies on the overall impact of SES on CKD minant of SES and CKD, using adjusted HR, risk
et al. J Epidemiol Community have obvious limitations. SES is a multidimensional ratio (RR) or OR with 95% CIs or sufficient infor-
Health 2018;72:270–279. concept incorporating material and social factors. mation to calculate these statistics.
270 Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815
 Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
Exclusion criteria: (1) abstracts, protocols, letters, expert and 95% CIs as metrics for pooled estimates in case–control or
opinions, case reports and reviews; (2) studies on acute renal cross-sectional studies, and RR and 95% CIs in cohort studies.
failure or unrepresented CKD. To evaluate the heterogeneity, we used Cochrane’s Q test. This
Any disagreements were resolved through discussion with is statistically significant if P<0.1; I2 below 30% is defined as
another reviewer (XZ). unimportant, 30%–50% as moderate, 50%–75% as substantial
and >75% as considerable heterogeneity.29 30
Data abstraction We also used subgroup analyses by geographic area, national
Two independent reviewers (XZ and JL) extracted informa- income level, different degrees of adjustment for important
tion about each article including the first author’s name, year disease-related risk factors (eg, comorbid conditions, access to
of publication, country where the study was conducted, type of healthcare and health behaviours) based on studies that had
study design, covariate adjustment degree, sample size, dura- maximum adjustment, study design, study quality and estimated
tion of study, indicators of SES (income, education, occupation, glomerular filtration rate (eGFR) calculation equation (only for
combined SES), development and progression of CKD, mean incidence). ORs or RRs were compared using the Q test to assess
age, sex and risk estimates (OR or RR) with corresponding the difference.
95% CIs. To evaluate the stability of the results and to test whether a
Measurements of the indicators of SES were all categorised study had excessive influence on the final result, we used a leave-
(dichotomised or multicategorised). Combined SES was an one-study-out sensitivity analysis,31 especially for pooled studies
indicator which incorporated more than one individual SES with considerable heterogeneity. The presence of publication
indicator. It could be a comprehensive indicator determined bias for the hypothesis of an association between low SES and
by income, education and occupation,14 by Index of Multiple CKD was assessed by funnel plots, coupled by Egger’s regression
Deprivation (IMD) at practice level,15–17 or by summary score of asymmetry test32 and Begg’s adjusted rank correlation test.33
area-level SES constructed summing z scores 6–7 census-derived The statistical software was Stata V.13 (Stata, College Station,
SES indicators.18–20 Outcomes were not restricted, but included Texas, USA), and a two-sided P<0.05 was considered statisti-
prevalence, incidence and progression of CKD. To augment cally significant in all tests.
between-study comparability using different indicator catego-
ries, we also compared the lowest and highest SES categories. Results
The national income level was classified into high, middle or Search results
low using the World Bank’s 2003 World Development Indi- In total, 3140 articles were identified from electronic databases.
cator.21 The degree of adjustment was categorised as ‘minimal’ After removing duplicates, 2142 unique articles remained, of
or ‘maximal’ depending on whether a model used three or fewer which 989 did not address the issue of interest, and 898 were
(age, gender or ethnicity), or more than three control covari- not related to the incidence and progression of CKD, leaving
ates.11 22 43 articles that met our selection criteria and were therefore
included in our meta-analysis (online supplementary figure 1).
Quality assessment The mean age of participants in the studies ranged from
The quality of studies was assessed using the Newcastle-Ottawa 39.7 to 72.7 years. The studies took place in America,
Quality Assessment Scale for cohort or case–control studies, and Europe, Asia and Africa. Seventeen articles defined CKD as
the Cross-Sectional/Prevalence Study Quality Assessment recom- eGFR<60 mL/min/1.73 m2, as in the CKD-Modification of Diet
mended by the Agency for Healthcare Research and Quality for in Renal Disease Study.8 14 17 26 34–46 Eight articles used Epidemi-
cross-sectional studies. For Newcastle-Ottawa, the maximum ology Collaboration (EPI),15 24 47–52 one used Cockcroft-Gault
numbers of points awarded in the selection, comparability and normalised to body surface area equation,53 two used creatinine
exposure (for cohort studies) or outcome (for case–control level25 54 and the rest eGFR<45 mL/min/1.73 m2.55
studies) categories were 4, 2 and 3. The Cross-Sectional/Prev- A total of 29 articles8 14 15 17 24–26 35–38 40–57 focused on associa-
alence Study Quality Assessment contains 11 items covering tions between SES and prevalence and incidence of CKD, with a
information source, subject quality, study design and outcome total of 584 805 participants. The majority were cross-sectional
completeness. Each item has ‘Yes/No/Unclear’ response options: studies (n=21) on the association between SES and CKD prev-
‘Yes’ scored one point and ‘No’ or ‘Unclear’ zero, and the scores alence. Nineteen studies8 15 17 24 35–38 40–42 44 45 47 49–51 54 57 were
were summed (online supplementary tables 2–4). There is no of moderate quality, nine14 25 26 43 46 52 53 55 56 high and only one48
agreed level of study quality, so we rated it as ‘High’, ‘Moderate’ low (online supplementary tables 2–4). Fourteen articles16 58–66
or ‘Low’, if it had values of 7–9, 4–6 and 0–3 for cohort or examined the relationship between SES and CKD progression,
case–control studies, and 8–11, 5–7 and 0–4 for cross-sectional across more than 6 978 082 participants (two articles60 65 did not
studies. provide the number of participants). Of these, six studies7 16 60 63–65
were of moderate quality, and eight18–20 23 58 60–62 high. Table 1
shows the characteristics of the studies on prevalence, incidence
Statistical analysis
and progression of CKD. The between-researcher agreement
The estimated associations were obtained using either logistic
levels on the quality of cross-sectional, case–control and cohort
regressions or Cox proportional hazards models with reported
studies were 19/21, 4/5 and 15/17, respectively. The final quality
adjusted ORs, HRs or RRs. For studies8 18 20 23–26 reporting
assessments are shown in online supplementary tables 2–4.
separate estimates by gender, the risk estimates were pooled
(weighted by the inverse of the variance) to obtain summarised
estimates. Overall results
The meta-analyses used the DerSimonian and Laird27 Associations of SES with CKD prevalence and incidence
random effects model, which takes into account within-study and A total of 21 articles14 15 17 24 35–38 40–44 47–49 51–53 56 57 reporting
between-study variations, stratified by study design28 (cohort, 24 cross-sectional studies (two articles43 52 reported five of these),
case–control or cross-sectional studies). We used adjusted OR and conducted in the USA,15 35–38 43 51 52 56 57 Europe,14 17 24 48 49 52
Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815 271
272
Table 1 Characteristics and results of included studies on incidence and progression of CKD
Age Duration
Author (year) Country Design/settings Sample size (year) (years) Indicators Criteria for CKD and ESRD
Included studies on the association between SES and incidence of CKD
Al-Qaoud et al (2011)24 UK Cross-sectional/population 5533 65.6 – Occupation eGFR<60 mL/min/1.73 m2—EPI
53
Amato et al (2005) Mexico Cross-sectional/population 3564 47 – Income/education/occupation eGFR<60 mL/min/1.73 m2—CG/BSA
37
Choi et al (2011) USA Cross-sectional/population 61 457 54 – Education GFR<60 mL/min/1.73 m3
48
Chudek et al (2014) Poland Cross-sectional/population 3797 ≥65 – Income/education/occupation eGFR<60 mL/min/1.73 m2—EPI; ACR>30 mg/g
36
Crews et al (2010) USA Cross-sectional/population 2375 48.3 – Combined eGFR<60 mL/min/1.73 m2
Chronic kidney disease

Fisher et al (2008)38 USA Cross-sectional/population 12 947 – – Income eGFR<60 mL/min/1.73 m2—MDRD

Flessner et al (2009)35 USA Cross-sectional/population 3431 52.7 – Income/education eGFR<60 mL/min/1.73 m2—EPI; ACR>30 mg/g
Fraser et al (2014)49 England Cross-sectional/population 13 065 – – Income eGFR<60 mL/min/1.73 m2
39
Kim et al (2015) Korea Cross-sectional/population 45 208 – – Income/education/occupation GFR<60 mL/min/1.73 m2
40
Lin et al (2013) Taiwan Cross-sectional/population 3352 47.5 – Income/education eGFR<60 mL/min/1.73 m2 or proteinuria
41
Liu et al (2012) China Cross-sectional/population 1214 49.4 – Education eGFR<60 mL/min/1.73 m2 or albuminuria
Martins et al (2006)56 USA Cross-sectional/population 14 484 – – Income ACR>300 mg/day (>200 µg/min)
Seck et al (2014)42 Senegal Cross-sectional/population 1037 47.9 – Education eGFR<60 mL/min/1.73 m2— MDRD; albuminuria >1 g/L
Seck et al (2014)34 Senegal Cross-sectional/population 1036 48.0 – Education eGFR<60 mL/min/1.73 m2
81
Singh et al (2009) India Cross-sectional/population 3155 40.1 – Education eGFR<60 mL/min/1.73 m2—CG/BSA
17
So et al (2015) Scotland Cross-sectional/population 313 639 50.0 – SES eGFR<60 mL/min/1.73 m2—MDRD
57
Tamrat et al (2015) USA Cross-sectional/population 462 47.3 – Income eGFR<60 mL/min/1.73 m2
52
Vart et al (2013) USA Cross-sectional/population 6428 47.3 – Income/education eGFR<60 mL/min/1.73 m2—EPI; AER>30 mg/24 hours; ACR>30 mg/g
52
Vart et al (2013) Netherlands Cross-sectional/population 7983 48.9 – Income/education eGFR<60 mL/min/1.73 m2—EPI; AER>30 mg/24 hours; ACR>30 mg/g
Vart et al (2015)15 USA Cross-sectional/population 9823 49.0 – Combined eGFR<60 mL/min/1.73 m2 or ACR>30 mg/day
43
White et al (2008) USA Cross-sectional/population 9098 – – Income/education/occupation eGFR<60 mL/min/1.73 m2—MDRD
43
White et al (2008) Australia Cross-sectional/population 9329 – – Income/education/occupation eGFR<60 mL/min/1.73 m2—MDRD
43
White et al (2008) Thailand Cross-sectional/population 5063 – – Income/education/occupation eGFR<60 mL/min/1.73 m2—MDRD
14
Wolf et al (2011) Germany Cross-sectional/hospital 825 62.9 – Combined eGFR<60 mL/min/1.73 m2
44
Xue et al (2014) China Cross-sectional/hospital 14 399 49.0 – Education eGFR<60 mL/min/1.73 m2
Hsieh et al (2012)45 Taiwan Case–control/hospital 424 66.8 3.5 Education GFR<60 mL/min/1.73 m2 or with proteinuria
Fored et al (2003)25 Sweden Case–control/population 1924 57.6 2 Occupation/education Male (Scr≥300 μmol/L), female (Scr≥250 µmol/L)
46
Su et al (2015) Taiwan Case–control/hospital 10 463 57.0 2.5 Income eGFR<60 mL/min/1.73 m2 or with proteinuria
8
Bruce et al (2010) USA Cohort/population 3430 54.3 3.5 Income/education eGFR<60 mL/min/1.73 m2 or with proteinuria
54
Drey et al (2003) Britain Cohort/population 1076 – 6 Combined Scr≥150 μmol/L
Guessous et al (2014)50 Switzerland Cohort/population 4441 52.6 5 Education eGFR<60 mL/min/1.73 m2 or with proteinuria
Shoham et al (2008)55 USA Cohort/population 15 792 53.6 15 Income/occupation eGFR<45 mL/min/1.73 m2 or hospital discharge diagnosis
Tohidi et al (2012)26 Iran Cohort/population 3313 39.7 9.9 Education eGFR<60 mL/min/1.73 m2
Included studies on the association between SES and progression of CKD

Continued

Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815

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 Table 1 Continued
Age Duration
Author (year) Country Design/settings Sample size (year) (years) Indicators Criteria for CKD and ESRD
Akrawi et al (2014)23 Sweden Prospective cohort study/population-based 5 593 516 43.5 10 Neighbourhood deprivation/ ESRD (surgical codes for transplantation or dialysis)
education/family income
Couchoud et al (2012)60 France Prospective cohort study/population-based – – 1 Individual income, education/ ESRD (initiation of dialysis or receiving a renal graft)
occupation
Crews et al (2014)7 USA Prospective cohort study/population-based 23 314 64.8 6 County poverty level/household ESRD (initiation of renal replacement therapy)
income/education
Hossain et al (2012)16 UK Retrospective cohort study/hospital-based 918 67 3 Area SES/education/occupation ESRD (initiation of dialysis)
Hsu et al (2009)58 USA Retrospective cohort study/population-based 177 570 40.7 25.7 Education ESRD (treated with maintenance dialysis or renal transplantation)
Klag et al (1997)61 USA Prospective cohort study/population-based 332 544 45.9 16 Household income ESRD (treatment for ESRD or death from renal failure)
Lipworth et al (2012)62 USA Prospective cohort study/population-based 79 943 52.1 8 Household income/education ESRD (initiation of renal replacement therapy)

Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815

20
Ward (2008) USA Retrospective cohort study/population-based 747 556 >20 8.5 SES ESRD (treated with maintenance dialysis or renal transplantation)
Young et al (1994)65 USA Retrospective cohort study/population-based – <60 6 Individual income ESRD (treated with maintenance dialysis or renal transplantation)
Young et al (2016)66 USA Prospective cohort study/population-based 3653 54 8.04 Income/education 30% decline in eGFR during follow-up
Merkin et al (2007)19 USA Retrospective cohort/population 4735 72.7 7 Income/education/area SES Scr elevation ≥35 μmol/L or CKD hospitalisation
Merkin et al (2005)18 USA Retrospective cohort/population 12 856 54.1 9 Combined Scr elevation ≥35 μmol/L or CKD hospitalisation
Tsai et al (2009)64 Taiwan Case–control study/hospital-based 400 46.0 1 Household income/education ESRD (new diagnosed patients dialysis dependent)
63
Perneger et al (1995) USA Case–control study/population-based 1077 47.4 0.5 Household income/education ESRD (initiation of renal replacement therapy)
ACR, albumin creatinine ratio; AER, albumin excretion rate; CG/BSA, Cockcroft-Gault normalised to body surface area equation; CKD, chronic kidney disease; eGFR, estimated glomerular filtration rate; EPI, epidemiology collaboration ; ESRD, end-stage renal
disease; MDRD, Modification of Diet in Renal Disease Study equation; Scr, serum creatinine; SES, socioeconomic status.
Chronic kidney disease

273
J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
 Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
Figure 1 Associations between socioeconomic status (SES) and chronic kidney disease (CKD) prevalence. (Parts A–D demonstrate different
associations between SES indicators and CKD incidence in the form of lower income, education level, occupation status and combined SES,
respectively.)

Asia,40 41 43 44 Africa,42 Mexico,53 Brazil47 and Australia43 were (1.09 to 1.79), P=0.009; I2=74.2%, P=0.009). There was no
published between 2003 and 2016. Most studies focused on significant association with education (RR 1.11, 95% CI (0.94 to
associations between CKD prevalence and income (n=17) or 1.30), P=0.218; I2=71.3%, P=0.002) (figure 3A–D). Two case–
education (n=14). Significant associations were found between control studies63 64 showed significant associations between
prevalence and most indicators of SES: lower income (OR lower income and CKD progression (OR 3.83, 95% CI (2.28 to
1.34, 95% CI (1.18 to 1.53), P<0.001; I2=73.0%, P=0.05);
lower education (OR 1.21, 95% CI (1.11 to 1.32), P<0.001;
I2=45.20%, P=0.034); and lower combined index (OR
2.18, 95% CI (1.64 to 2.89), P<0.001; I2=0.0%, P=0.326)
(figure 1A–D). Lower level occupations were not associated
with prevalence (OR 1.09, 95% CI (0.96 to 1.23), P=0.168;
I2=26.4%, P=0.227).
Five cohort studies8 26 50 54 55 and three case–control
studies25 45 46 explored the relationship between SES and CKD
incidence. Incidence was significantly associated with lower
income (RR 1.59, 95% CI (1.23 to 2.04), P<0.01; I2=0.0%,
P=0.5/OR 2.00, 95% CI (1.49 to 2.60), P<0.001; n=1),
occupation level (RR 1.72, 95% CI (1.31 to 2.25), P<0.01;
n=1/OR 1.70, 95% CI (1.18 to 2.45), P=0.005; n=1) and
combined index (RR 1.17, 95% CI (1.12 to 1.23), P<0.01; n=1/
OR 2.18, 95% CI (1.64 to 2.89), P=0.003), but had no associ-
ation with lower educational level (RR 1.16, 95% CI (0.82 to
1.63), P=0.4; I2=71.8%, P=0.03/OR 2.66, 95% CI (0.57 to
12.43), P=0.212; I2=89.5%, P=0.002) (figure 2).

The association between SES and CKD progression

Twelve cohort studies7 16 18–20 23 58 60–62 65 66 provided RRs for
the association between CKD progression and indicators of
SES, mostly income (n=7) or education (n=7). Progression was
significantly associated with lower income (RR 1.24, 95% CI
(1.12 to 1.37), P<0.001; I2=66.6%, P=0.006), lower level Figure 2 Associations between socioeconomic status (SES) and
occupation (RR 1.05, 95% CI (1.01 to 1.09), P=0.012; chronic kidney disease (CKD) incidence (by different study designs with
I2=0.0%, P=0.796) and lower combined SES (RR 1.39, 95% CI each SES indicator). ES, effect size.
274 Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815
 Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
Figure 3 Associations between socioeconomic status (SES) and chronic kidney disease (CKD) progression to end-stage renal disease (ESRD). (Parts
A–D demonstrate different associations between SES indicators and CKD progression in the form of lower income, education level, occupation status
and combined SES, respectively.) RR, risk ratio.

6.42), P<0.001; I2=30.0%, P=0.232). No single studies exerted and progression in several geographic areas (USA: RR 1.27,
an obviously excessive influence on the associations. 95% CI (1.08 to 1.50), P=0.004; European countries: RR 1.19,
95% CI (1.13 to 1.26), P<0.001). The association between
Subgroup analyses lower educational attainment and disease progression in Europe
The associations between CKD prevalence and progression and (RR 1.23, 95% CI (1.17 to 1.30), P<0.001; I2=0.0%, P=0.861)
the indicators of SES varied across several factors (see table 2). was statistically significant but inconsistent with the overall
We also planned to use gender but there were insufficient data. trend. If the analysis was limited to studies that fully adjusted for
When relative estimations were fully adjusted for comorbid disease-related risk factors, the associations between progression
conditions, health access and health-related behaviours, the and lower income and education level were insignificant (OR
associations between CKD prevalence and lower income and 1.29 vs 1.06, P=0.276 vs 0.742). More studies were published
education level were still significant, with lower heterogeneity after 2010, accounting for more than half of the eligible studies
(income: OR 1.46, 95% CI (1.23 to 1.74), P<0.001; I2=49.4%, on both income and education, with similar results (RR 1.39,
P=0.139; education: OR 1.11, 95% CI (1.03 to 1.20), P=0.008; 95% CI (1.11 to 1.74), P=0.004; RR 1.07, P=0.454) with
I2=0.0%, P=0.398). All the significant associations between substantial heterogeneity (I2=75.0%, P=0.007; I2=68.1%,
lower income, education and occupation and SES prevalence P=0.014). (See table 3.)
were observed in high-income (income: OR 1.49, 95% CI The publication bias funnel plots and results of Begg’s test and
(1.32 to 1.67), P<0.001; I2=50.1%, P=0.024; education: OR Egger’s test (online supplementary figures 2.1–2.3, 3.1, 3.2)
1.19, 95% CI (1.06 to 1.34), P=0.003; I2=40.7%, P=0.120; showed no publication bias except for studies on the association
occupation: OR 1.21, 95% CI (1.06 to 1.38), P=0.004; I2=0.0%, between income and disease progression (Egger’s test P=0.05).
P=0.849), but not upper middle-income countries (income: Publication bias analysis was not possible on other indicators of
OR 1.20, P=0.340; education: OR 1.28, P=0.163; occupa- SES because of the limited number of studies.67
tion: OR 0.91, P=0.293). The association between prevalence
and education was similar in the USA, Europe and Asia-Pacific Discussion
Region (OR=1.17, 1.18, 1.21; P=0.783), but the association This meta-analysis has shown several associations between indi-
between prevalence and lower income was more marked in the vidual indicators of SES and CKD prevalence and progression.
USA than Europe (OR=1.55 vs 1.14; P=0.013). The results of The effect sizes of these associations varied by national income,
studies from the 2000s and 2010s were similar (comparison of geographic location and level of adjustment. Lower income and
ORs from subgroups of 2000s vs 2010s in income (P=0.809), in education level were strongly associated with CKD prevalence in
education (P=0.974) and occupation (P=0.353)). high-income countries, except Europe. Disease progression was
All the cohort studies on the association between SES and associated with lower income in the USA and Europe, but the
disease progression were conducted in high-income countries, association with lower educational attainment was only signif-
and there was a significant association between lower income icant in Europe.
Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815 275
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Table 2 Pooled OR (from cross-sectional) of CKD prevalence in the lower SES indicators compared with the higher in series of subgroup analyses
Income Education Occupation
Subgroup (prevalence) n OR (95% CI) I2 (P) n OR (95% CI) I2 (P) n OR (95% CI) I2 (P)
Overall 17 1.34 (1.18 to 1.53) 73.0% (0.050) 14 1.21 (1.11 to 1.32) 45.2% (0.034) 7 1.09 (0.96 to 1.23) 26.4% (0.227)
Geographic area
 USA 9 1.55 (1.37 to 1.75) 47.8% (0.053) 4 1.17 (1.01 to 1.36) 38.8% (0.179) 1 1.12 (0.82 to 1.52) –
 Europe 3 1.14 (0.93 to 1.41) 33.3% (0.223) 2 1.18 (0.74 to 1.88) 82.0% (0.018) 2 1.12 (0.89 to 1.41) 55.0% (0.136)
 Asian-Pacific Region 3 1.01 (0.85 to 1.20) 0.0% (0.516) 5 1.21 (1.09 to 1.33) 2.6% (0.392) 2 1.27 (0.99 to 1.62) 0.0% (0.975)
 Latin America 2 1.35 (0.70 to 2.59) 88.3% (0.003) – – – 2 0.87 (0.69 to 1.09) 0.0% (0.780)
 Africa 0 – – 1 1.18 (0.46 to 3.03) – 0 – –
Country’s income level
 High 12 1.49 (1.32 to 1.67) 50.1% (0.024) 6 1.18 (1.04 to 1.35) 46.0% (0.099) 3 1.21 (1.06 to 1.38) 0.0% (0.8490)
 Upper middle 3 1.20 (0.83 to 1.74) 79.6% (0.007) 3 1.28 (0.90 to 1.82) 81.3% (0.005) 3 0.91 (0.76 to 1.08) 0.0% (0.802)
 Lower middle 2 0.98 (0.81 to 1.17) 0.0% (0.779) 4 1.25 (1.13 to 1.39) 0.0% (0.695) 1 1.27 (0.92 to 1.76) –
 Low 0 – – 1 1.18 (0.46 to 3.03) – 0 – –
Adjustments for CKD-related risk factors
 None 5 1.66 (1.25 to 2.20) 72.7% (0.005) 3 1.67 (1.34 to 2.06) 0.0% (0.398) 1 0.83 (0.56 to 1.24) –
 Health behaviours 1 0.99 (0.76 to 1.30) – 1 0.93 (0.71 to 1.21) – 1 0.97 (0.74 to 1.27) –
 Comorbid conditions 1 1.24 (0.94 to 1.65) – 0 – – 1 1.23 (1.05 to 1.44) –
 +Health behaviours 7 1.20 (0.99 to 1.45) 74.7% (<0.001) 8 1.23 (1.14 to 1.33) 0.0% (0.630) 4 1.10 (0.93 to 1.30) 14.3% (0.321)
 +Healthcare access 3 1.46 (1.23 to 1.74) 49.4% (0.139) 2 1.11 (1.03 to 1.20) 0.0% (0.398) 0 – –
Study period
 2000s 7 1.35 (1.14 to 1.60) 42.2% (0.109) 5 1.24 (0.97 to 1.57) 68.3% (0.013) 4 1.13 (0.94 to 1.34) 3.2% (0.376)
 2010s 10 1.34 (1.11 to 1.62) 81.6% (<0.001) 9 1.20 (1.10 to 1.30) 27.4% (0.200) 3 1.05 (0.85 to 1.29) 60.0% (0.082)
CKD definitions
 MDRD equation 9 1.24 (1.08 to 1.43) 40.2% (0.099) 9 1.16 (1.09 to 1.25) 9.9% (0.352) 3 1.21 (1.00 to 1.46) 0.0% (0.83)
 EPI equation 7 1.40 (1.13 to 1.75) 83.6% (<0.001) 4 1.23 (0.99 to 1.53) 55.0% (0.084) 3 1.05 (0.85 to 1.29) 60.0% (0.082)
 CG/BSA equation 1 1.91 (1.32 to 2.78) – 1 1.97 (1.37 to 2.83) – 1 0.83 (0.56 to 1.25) –
CG/BSA, Cockcroft-Gault normalised to body surface area equation; CKD, chronic kidney disease; EPI, epidemiology collaboration equation; MDRD, Modification of Diet in Renal Disease
Study; SES, socioeconomic status.

Interactions between indicators of SES may bring statistical and a publicly financed healthcare system in most European
artefacts, especially for parameters with significant associations Union member states.71
such as income and education level. A previous study clarified The association between lower educational attainment and
that indicators of SES are only modestly correlated with each CKD was complex, as it may be mediated by behavioural risk
other, and we found that income was still associated with CKD factors. For example, several studies72–74 have found that lower
prevalence even after full adjustment for other indicators. Indi- education is linked to various CKD-related behavioural risk
cators of SES are therefore not directly comparable and may be factors (smoking and alcohol, poor diet planning ability and lack
independently associated with health outcomes to some degree. of physical activity), and chronic conditions leading to secondary
The association between lower income and CKD preva- CKD, such as diabetes and hypertension. Better education
lence could be attributed to food insufficiency, inadequate enables individuals to make better healthcare decisions and
nutritional intake, exposure to environmental toxins, infection obtain better access to healthcare interventions and plans,75 so
and/or inflammation, distress or anxiety over income disadvan- helps to improve general health in individuals and their chil-
tage, inadequate health insurance and poorer access to quality dren.37 Interestingly, awareness of CKD is not linked to educa-
healthcare services.15 43 53 56 Inadequate diet and unhealthy life- tion level. For example, one study35 found that the majority of
styles were likely to be associated with obesity, diabetes mellitus subjects with more than high school education were unaware of
and hypertension, which may be causally linked to kidney their CKD status
disease.35 68 There was a significant association in high-income Only a few studies have examined the association between
but not upper middle-income countries. This might be partly occupation and CKD, and occupation categories were not stan-
explained by differences in healthcare and insurance systems.25 dard, but each OR or RR maximised the comparability. Individ-
Socialised medicine systems in some upper middle-income coun- uals with lower level occupations were more likely to be exposed
tries might attenuate the association between income and CKD. to hazardous working conditions,25 and blue collar workers were
Income-related and education-related inequalities might also more likely to be obese than white collar workers.68 76 77 Obesity
be smaller in countries providing relatively generous universal is a significant risk factor for diabetes and hypertension,78 and
welfare, such as Scandinavian countries.69 The effect size was in turn to CKD. The potential mechanisms linking lower level
larger in the USA than in Europe, which might be partly because occupations to CKD onset included fewer nephrons, neph-
of stricter guidelines on comorbidity management in Europe,70 rotoxins (analgesics), and poor diet and health behaviours.55
276 Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815
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Table 3 Pooled RR (from cohort studies) of CKD progression in the lower SES compared with the higher in series of subgroup analyses
Income Education
Subgroup (progression) n RR (95% CI) I2 n RR (95% CI) I2
Overall 7 1.24 (1.12 to 1.37) 66.6% (0.006) 7 1.11 (0.94 to 1.30) 71.3% (0.002)
Geographic area
 USA 6 1.27 (1.08 to 1.50) 72.5% (0.003) 5 1.06 (0.86 to 1.32) 71.3% (0.002)
 Europe 1 1.19 (1.13 to 1.26) – 2 1.23 (1.17 to 1.30) 0.0% (0.861)
 Asia 0 – – 0 – –
Country's income group
 High 7 1.24 (1.12 to 1.37) 66.6% (0.006) 7 1.11 (0.94 to 1.30) 75.6% (0.001)
 Middle 0 – – 0 – –
SES-related risk factor adjustments
 None 3 1.19 (1.03 to 1.37) 78.4% (0.010) 3 1.23 (1.16 to 1.29) 0.0% (0.579)
 Health behaviours 0 – – 1 0.90 (0.69 to 0.18) –
 Comorbid conditions 1 1.45 (1.23 to 1.71) – 1 1.11 (0.93 to 1.33) 75.6% (0.001)
 +Health behaviours 2 1.18 (0.93 to 1.52) 54.6% (0.138) 1 0.93 (0.80 to 1.09) –
 +Healthcare access 1 1.29 (0.82 to 2.04) – 1 1.06 (0.75 to 1.50) –
CKD progression definitions
 Initiation of RRT 4 1.26 (1.10 to 1.45) 80.4% (0.002) 5 1.16 (0.96 to 1.41) 75.2% (0.003)
 Initiation of RRT or death from renal failure 1 1.30 (1.12 to 1.50) ß 0 – –
 Scr elevation 1 1.00 (0.73 to 1.37) – 1 0.90 (0.69 to 0.18)
 30% eGFR decline 1 1.29 (0.82 to 2.04) – 1 1.06 (0.75 to 1.50) –
Study design
 Prospective 6 1.26 (1.13 to 1.40) 70.1% (0.005) 4 1.07 (0.88 to 1.29) 76.0% (0.006)
 Retrospective 1 1.00 (0.80 to 1.50) – 3 1.20 (0.76 to 1.91) 76.25 (0.015)
Time period
 1990s 2 1.19 (1.02 to 1.38) 70.1% (0.067) 0 – –
 2000s 1 1.00 (0.80 to 1.50) – 2 1.18 (0.69 to 2.02) 88.0% (0.004)
 2010s 4 1.39 (1.11 to 1.74) 75.0% (0.007) 5 1.07 (0.89 to 1.29) 68.1% (0.014)
CKD, chronic kidney disease; eGFR, estimated glomerular filtration rate; RR, risk ratio; RRT, renal replacement therapy; Scr, serum creatinine; SES, socioeconomic status.

Finally, social status itself might confer health benefits, possibly This paper has several limitations. First, income, education
via psychosocial mechanisms, regardless of economic elements.79 level, occupation and the combined index were defined and clas-
Our review was rigorous in maximising its completeness sified differently in the studies analysed. Second, the definition
and quality of evidence. To explore potential confounders, of CKD also varied, which may lead to overdispersion of the
we conducted subgroup and sensitivity analyses to distinguish estimated effects. Third, there might have been some selection
and diminish heterogeneity. Substantial heterogeneities were bias in the study samples. For example, in some studies, subjects
detected across the studies analysed and could not be effec- were recruited from enterprises or factories that offered phys-
tively eliminated even in subgroups. The heterogeneities across ical examinations for employees. These subjects might therefore
countries may have been because of differences in economic have better overall health than the general population. Finally,
or healthcare systems, and income distribution. This paper is few studies explored the association between occupation and
the first attempt, to our knowledge, to include all the specific CKD, or with CKD incidence as an outcome.
determinants of SES and elements of CKD when studying the Most studies on the association between SES and CKD prev-
associations between these two issues. It is in line with the view alence were cross-sectional and not fully adjusted for disease-re-
that association studies should not rely on just one indicator of lated risk factors including access to healthcare (insurance or
routine healthcare visits), and health-related behaviours other
SES, as each one represents a different causal process or pathway
than smoking and alcohol consumption (such as diet, phys-
and they should not be used interchangeably.80 The population
ical activity or sedentary time). The case–control or cohort
in our meta-analysis covered more geographic areas, national
studies often assessed exposure and covariates just once during
income levels and CKD definitions than the previous meta-anal-
follow-up, and did not fully capture the biological mechanism
ysis.5 We also adjusted the results for CKD-related healthcare
governing disease progression. This warrants more explora-
access and health-related behaviours to explore clearer associ-
tion of the changes in comorbid conditions and figures set as
ations and possible mechanisms than socioeconomic indicators
outcomes, and the association between continuous variables.
alone could provide. Our study reflects the global population
(North America, Europe, Asia-Pacific Region, Latin America and
Africa), including regions with different economic and social Conclusion
development levels (developed countries and low-income and Several individual indicators of SES were associated with
middle-income countries). the prevalence and progression of CKD. Lower income was
Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815 277
 Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
associated with prevalence and progression, but the effects of 8 Bruce MA, Beech BM, Crook ED, et al. Association of socioeconomic status
education, occupation and overall status were inconsistent. and CKD among African Americans: the Jackson Heart Study. Am J Kidney Dis
2010;55:1001–8.
Risk estimates differed by national income levels, geographic 9 Plantinga LC. Socio-economic impact in CKD. Nephrol Ther 2013;9:1–7.
locations and adjustment level. Our findings may be useful in 10 Krieger N, Williams DR, Moss NE. Measuring social class in US public health research:
developing more effective CKD prevention programme among concepts, methodologies, and guidelines. Annu Rev Public Health 1997;18:341–78.
socioeconomically disadvantaged populations. 11 Uthman OA, Jadidi E, Moradi T. Socioeconomic position and incidence of gastric
cancer: a systematic review and meta-analysis. J Epidemiol Community Health
2013;67:854–60.
What is already known on this subject 12 Manrique-Garcia E, Sidorchuk A, Hallqvist J, et al. Socioeconomic position and
incidence of acute myocardial infarction: a meta-analysis. J Epidemiol Community
Health 2011;65:301–9.
Individuals with lower socioeconomic status may be more likely
13 Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in
to suffer from chronic kidney disease (CKD). This disease is one epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in
of the major public health concerns of the 21st century because Epidemiology (MOOSE) group. JAMA 2000;283:2008–12.
of its high prevalence, mortality and social cost. Previous studies 14 Wolf G, Busch M, Muller N, et al. Association between socioeconomic status and renal
have obvious limitations including vague and variable definitions function in a population of German patients with diabetic nephropathy treated at a
tertiary centre. Nephrology Dialysis Transplantation 2011;26:4017–23.
of socioeconomic status, because of the multidimensional nature 15 Vart P, Gansevoort RT, Crews DC, et al. Mediators of the association between low
of the concept, and biased results that cannot be generalised socioeconomic status and chronic kidney disease in the United States. Am J Epidemiol
more widely because of country-specific and region-specific 2015;181:385–96.
socioeconomic background. 16 Hossain MP, Palmer D, Goyder E, et al. Association of deprivation with worse
outcomes in chronic kidney disease: findings from a hospital-based cohort in the
United Kingdom. Nephron Clin Pract 2012;120:c59–c70.
17 So BH, Methven S, Hair MD, et al. Socio-economic status influences chronic kidney
What this study adds disease prevalence in primary care: a community-based cross-sectional analysis.
Nephrol Dial Transplant 2015;30:1010–7.
This study is a first effort to quantitatively evaluate associations 18 Merkin SS, Coresh J, Diez Roux AV, et al. Area socioeconomic status and progressive
CKD: the Atherosclerosis Risk in Communities (ARIC) Study. Am J Kidney Dis
between CKD and key indicators of socioeconomic status,
2005;46:203–13.
including income, educational attainment, occupation and a 19 Merkin SS, Diez Roux AV, Coresh J, et al. Individual and neighborhood socioeconomic
comprehensive index. Subgroup and sensitivity analyses were status and progressive chronic kidney disease in an elderly population: The
used to explore how associations were affected by other factors, Cardiovascular Health Study. Soc Sci Med 2007;65:809–21.
including study locations and times, adjustment for other 20 Ward MM. Socioeconomic status and the incidence of ESRD. Am J Kidney Dis
2008;51:563–72.
factors and national economic background. These may help in 21 Agency for Healthcare Research and Quality, US Department of Health and Human
developing more effective kidney disease prevention programme Services. 2010 National healthcare quality and disparities reports. Rockville, MD:
for disadvantaged populations. Agency for Healthcare Research and Quality, 2011.
22 Agardh E, Allebeck P, Hallqvist J, et al. Type 2 diabetes incidence and socio-
economic position: a systematic review and meta-analysis. Int J Epidemiol
Contributors XZ and JL conceived the study. JL and ST extracted the data. XZ, 2011;40:804–18.
JL and HGH analysed the results and drafted the manuscript. HGH and YL assisted 23 Akrawi DS, Li X, Sundquist J, et al. End stage renal disease risk and neighbourhood
with the statistical analyses and edited the manuscript. YL and PF refined the deprivation: a nationwide cohort study in Sweden. Eur J Intern Med 2014;25:853–9.
study design and contributed to supervision. Each author contributed important 24 Al-Qaoud TM, Nitsch D, Wells J, et al. Socioeconomic status and reduced kidney
intellectual content during the manuscript drafting or revision and accepts function in the Whitehall II Study: role of obesity and metabolic syndrome. Am J
accountability for the overall work by ensuring that questions pertaining to the Kidney Dis 2011;58:389–97.
accuracy or integrity of any portion of the work are appropriately investigated and 25 Fored CM, Ejerblad E, Fryzek JP, et al. Socio-economic status and chronic renal
resolved. failure: a population-based case-control study in Sweden. Nephrol Dial Transplant
2003;18:82–8.
Funding This work was partially supported by the international cooperation project 26 Tohidi M, Hasheminia M, Mohebi R, et al. Incidence of chronic kidney disease and
(2016HH0069) funded by the Science and Technology Department of Sichuan its risk factors, results of over 10 year follow up in an Iranian cohort. PLoS One
Province, China. 2012;7:e45304.
Competing interests None declared. 27 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials
1986;7:177–88.
Provenance and peer review Not commissioned; externally peer reviewed.
28 Blettner M, Sauerbrei W, Schlehofer B, et al. Traditional reviews, meta-analyses and
© Article author(s) (or their employer(s) unless otherwise stated in the text of the pooled analyses in epidemiology. Int J Epidemiol 1999;28:1–9.
article) 2018. All rights reserved. No commercial use is permitted unless otherwise 29 Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med
expressly granted. 2002;21:1539–58.
30 Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses.
BMJ 2003;327:557–60.
References 31 Normand SL. Meta-analysis: formulating, evaluating, combining, and reporting. Stat
1 Hallan SI, Coresh J, Astor BC, et al. International comparison of the relationship Med 1999;18:321–59.
of chronic kidney disease prevalence and ESRD risk. J Am Soc Nephrol 32 Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a
2006;17:2275–84. simple, graphical test. BMJ 1997;315:629–34.
2 Zhang L, Wang F, Wang L, et al. Prevalence of chronic kidney disease in China: a cross- 33 Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for
sectional survey. Lancet 2012;379:815–22. publication bias. Biometrics 1994;50:1088–101.
3 Coresh J, Selvin E, Stevens LA, et al. Prevalence of chronic kidney disease in the 34 Seck SM, Doupa D, Gueye L, et al. Prevalence of chronic kidney disease and
United States. JAMA 2007;298:2038–47. associated factors in senegalese populations: a community-based study in saint-louis.
4 Lee S, Lee S, Harada K, et al. Relationship between chronic kidney disease with Nephrourol Mon 2014;6.
diabetes or hypertension and frailty in community-dwelling Japanese older adults. 35 Flessner MF, Wyatt SB, Akylbekova EL, et al. Prevalence and awareness of CKD among
Geriatr Gerontol Int 2016;57. African Americans: the Jackson Heart Study. Am J Kidney Dis 2009;53:238–47.
5 Vart P, Gansevoort RT, Joosten MM, et al. Socioeconomic disparities in chronic kidney 36 Crews DC, Charles RF, Evans MK, et al. Poverty, race, and CKD in a racially and
disease: a systematic review and meta-analysis. Am J Prev Med 2015;48:580–92. socioeconomically diverse urban population. Am J Kidney Dis 2010;55:992–1000.
6 Schäfer I, Hansen H, Schön G, et al. The influence of age, gender and socio-economic 37 Choi AI, Weekley CC, Chen SC, et al. Association of educational attainment with
status on multimorbidity patterns in primary care. First results from the multicare chronic disease and mortality: the Kidney Early Evaluation Program (KEEP). Am J
cohort study. BMC Health Serv Res 2012;12:89. Kidney Dis 2011;58:228–34.
7 Crews DC, Gutiérrez OM, Fedewa SA, et al. Low income, community poverty and risk 38 Fisher MA, Taylor GW, Shelton BJ, et al. Periodontal disease and other nontraditional
of end stage renal disease. BMC Nephrol 2014;15. risk factors for CKD. Am J Kidney Dis 2008;51:45–52.

278 Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815

 Chronic kidney disease

J Epidemiol Community Health: first published as 10.1136/jech-2017-209815 on 2 February 2018. Downloaded from http://jech.bmj.com/ on July 19, 2024 by guest. Protected by copyright.
39 Kim TH, Lee MJ, Yoo KB, et al. Association of demographic and socioeconomic 60 Couchoud C, Guihenneuc C, Bayer F, et al. Medical practice patterns and socio-
factors with risk factors for chronic kidney disease. J Prev Med Public Health economic factors may explain geographical variation of end-stage renal disease
2015;48:170–7. incidence. Nephrol Dial Transplant 2012;27:2312–22.
40 Lin MY, Chiu YW, Lee CH, et al. Factors associated with CKD in the elderly and 61 Klag MJ, Whelton PK, Randall BL, et al. End-stage renal disease in African-American
nonelderly population. Clin J Am Soc Nephrol 2013;8:33–40. and white men. 16-year MRFIT findings. JAMA 1997;277:1293–8.
41 Liu Q, Li Z, Wang H, et al. High prevalence and associated risk factors for impaired 62 Lipworth L, Mumma MT, Cavanaugh KL, et al. Incidence and predictors of end stage
renal function and urinary abnormalities in a rural adult population from southern renal disease among low-income blacks and whites. PLoS One 2012;7:e48407.
China. PLoS One 2012;7:e47100. 63 Perneger TV, Whelton PK, Klag MJ. Race and end-stage renal disease. Socioeconomic
42 Seck SM, Doupa D, Guéye L, et al. Chronic kidney disease epidemiology in northern status and access to health care as mediating factors. Arch Intern Med
Senegal: a cross-sectional study. Iran J Kidney Dis 2014;8:286–91. 1995;155:1201–8.
43 White SL, McGeechan K, Jones M, et al. Socioeconomic disadvantage and 64 Tsai SY, Tseng HF, Tan HF, et al. End-stage renal disease in Taiwan: a case-control
kidney disease in the United States, Australia, and Thailand. Am J Public Health study. J Epidemiol 2009;19:169–76.
2008;98:1306–13. 65 Young EW, Mauger EA, Jiang KH, et al. Socioeconomic status and end-stage renal
44 Xue L, Lou Y, Feng X, et al. Prevalence of chronic kidney disease and associated disease in the United States. Kidney Int 1994;45:907–11.
factors among the Chinese population in Taian, China. BMC Nephrol 2014;15:205. 66 Young BA, Katz R, Boulware LE, et al. Risk factors for rapid kidney function
45 Hsieh CF, Huang SL, Chen CL, et al. Increased risk of chronic kidney disease decline among African Americans: the Jackson Heart Study (JHS). Am J Kidney Dis
among users of non-prescribed Chinese herbal medicine in Taiwan. Prev Med 2016;68:229–39.
2012;55:155–9. 67 Mavridis D, Salanti G. How to assess publication bias: funnel plot, trim-and-fill method
46 Su SL, Lin C, Kao S, et al. Risk factors and their interaction on chronic kidney disease: and selection models. Evid Based Ment Health 2014;17:30.
a multi-centre case control study in Taiwan. BMC Nephrol 2015;16:83. 68 Garland JS. Elevated body mass index as a risk factor for chronic kidney disease:
47 Barreto SM, Ladeira RM, Duncan BB, et al. Chronic kidney disease among adult current perspectives. Diabetes Metab Syndr Obes 2014;7:347.
participants of the ELSA-Brasil cohort: association with race and socioeconomic 69 Eikemo TA, Bambra C, Joyce K, et al. Welfare state regimes and income-related
position. J Epidemiol Community Health 2016;70:380–9. health inequalities: a comparison of 23 European countries. Eur J Public Health
48 Chudek J, Wieczorowska-Tobis K, Zejda J, et al. The prevalence of chronic kidney 2008;18:593–9.
disease and its relation to socioeconomic conditions in an elderly Polish population: 70 Stephan D, Gaertner S, Cordeanu EM. A critical appraisal of the guidelines from
results from the national population-based study PolSenior. Nephrology Dialysis France, the UK, Europe and the USA for the management of hypertension in adults.
Transplantation 2014;29:1073–82. Arch Cardiovasc Dis 2015;108(8-9):453–9.
49 Fraser SD, Roderick PJ, Aitken G, et al. Chronic kidney disease, albuminuria and 71 Basu S, Hassenplug JC. Patient access to medical devices-a comparison of U.S. and
socioeconomic status in the health surveys for England 2009 and 2010. J Public European review processes. N Engl J Med 2012;367:485–8.
Health 2014;36:577–86. 72 Feinglass J, Lin S, Thompson J, et al. Baseline health, socioeconomic status, and
50 Guessous I, Ponte B, Marques-Vidal P, et al. Clinical and biological determinants 10-year mortality among older middle-aged Americans: findings from the health and
of kidney outcomes in a population-based cohort study. Kidney Blood Press Res retirement study, 1992 2002. J Gerontol B Psychol Sci Soc Sci 2007;62:S209–S217.
2014;39:74–85. 73 Lantz PM, Golberstein E, House JS, et al. Socioeconomic and behavioral risk factors
51 Suarez JJ, Isakova T, Anderson CA, et al. Food access, chronic kidney disease, and for mortality in a national 19-year prospective study of U.S. adults. Soc Sci Med
hypertension in the U.S. Am J Prev Med 2015;49:912–20. 2010;70:1558–66.
52 Vart P, Gansevoort RT, Coresh J, et al. Socioeconomic measures and CKD in the United 74 Rask K, O’Malley E, Druss B, et al. Impact of socioeconomic, behavioral and clinical
States and The Netherlands. Clin J Am Soc Nephrol 2013;8:1685–93. risk factors on mortality. J Public Health 2009;31:231–8.
53 Amato D, Alvarez-Aguilar C, Castaneda-Limones R, et al. Prevalence of chronic 75 Cutler DM, Lleras-Muney A. Education and health: evaluating theories and evidence.
kidney disease in an urban Mexican population. Kidney Int In: Schoeni RF, House JS, Kaplan GA, eds. Making Americans healthier: social and
2005;68(SUPPL. 97):S11–S17. economic policy as health policy. russell sage foundation, 2008:29–59. p..
54 Drey N, Roderick P, Mullee M, et al. A population-based study of the incidence and 76 Hiltunen LA. Are there associations between socio-economic status and known
outcomes of diagnosed chronic kidney disease. Am J Kidney Dis 2003;42:677–84. diabetes in an elderly finnish population? Cent Eur J Public Health 2005;13:187–90.
55 Shoham DA, Vupputuri S, Kaufman JS, et al. Kidney disease and the cumulative 77 Morikawa Y, Nakagawa H, Miura K, et al. Effect of shift work on body mass index and
burden of life course socioeconomic conditions: the Atherosclerosis Risk in metabolic parameters. Scand J Work Environ Health 2007;33:45–50.
Communities (ARIC) study. Soc Sci Med 2008;67:1311–20. 78 Vasan RS, Larson MG, Leip EP, et al. Assessment of frequency of progression to
56 Martins D, Tareen N, Zadshir A, et al. The association of poverty with the prevalence hypertension in non-hypertensive participants in the framingham heart study: a cohort
of albuminuria: data from the Third National Health and Nutrition Examination Survey study. Lancet 2001;358:1682–6.
(NHANES III). Am J Kidney Dis 2006;47:965–71. 79 Fitzpatrick R. Social status and mortality. Ann Intern Med 2001;134:1001–3.
57 Tamrat R, Peralta CA, Tajuddin SM, et al. Apolipoprotein L1, income and early kidney 80 Geyer S, Hemström O, Peter R, et al. Education, income, and occupational class cannot
damage. BMC Nephrol 2015;16:14. be used interchangeably in social epidemiology. Empirical evidence against a common
58 Hsu CY, Iribarren C, McCulloch CE, et al. Risk factors for end-stage renal disease: 25- practice. J Epidemiol Community Health 2006;60:804–10.
year follow-up. Arch Intern Med 2009;169:342–50. 81 Singh NP, Ingle GK, Saini VK, et al. Prevalence of low glomerular filtration rate,
59 Brancati FL, Whittle JC, Whelton PK, et al. The excess incidence of diabetic end-stage proteinuria and associated risk factors in North India using cockcroft-gault and
renal disease among blacks. A population-based study of potential explanatory modification of diet in renal disease equation: an observational, cross-sectional study.
factors. JAMA 1992;268:3079–84. BMC Nephrol 2009;10:4.

Zeng X, et al. J Epidemiol Community Health 2018;72:270–279. doi:10.1136/jech-2017-209815 279