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Autoimmunity Reviews 13 (2014) 641–654

Contents lists available at ScienceDirect

Autoimmunity Reviews
journal homepage: www.elsevier.com/locate/autrev

Review

Socioeconomic status. The relationship with health and


autoimmune diseases
Omar-Javier Calixto, Juan-Manuel Anaya ⁎
Center for Autoimmune Diseases Research (CREA), Mederi Hospital Universitario Mayor, Universidad del Rosario, Bogota, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: Socioeconomic status (SES) is a hierarchical social classification associated with different outcomes in health and
Received 1 December 2013 disease. The most important factors influencing SES are income, educational level, occupational class, social class,
Accepted 24 December 2013 and ancestry. These factors are closely related to each other as they present certain dependent interactions. Since
Available online 10 January 2014
there is a need to improve the understanding of the concept of SES and the ways it affects health and disease, we
review herein the tools currently available to evaluate SES and its relationship with health and autoimmune
Keywords:
Socioeconomic status
diseases.
Rheumatoid arthritis © 2014 Elsevier B.V. All rights reserved.
Systemic lupus erythematosus
Sjögren's syndrome
Systemic sclerosis
Type 1 diabetes

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 641
2. What is SES? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 642
3. Measurement tools for SES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 642
4. SES and health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 642
5. SES and ADs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 646
5.1. SES and rheumatoid arthritis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 646
5.2. SES and systemic lupus erythematosus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 647
5.3. SES and multiple sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 647
5.4. SES and type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650
6. Conclusions and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650
Take-home messages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650

1. Introduction
Abbreviations: ACR, American College of Rheumatology; ADs, Autoimmune Diseases;
AIMs, Ancestry Informative Markers; DMARDs, Disease Modifying Anti-Rheumatic There has been a global interest in determining the impact of socio-
Drugs; HAQ, Health Attitude Questionnaire; HbA1C, Glycated hemoglobin; HRQOL,
economic status (SES) on health and disease. The importance of analyzing
Health related Quality of Life; LN, Lupus Nephritis; MS, Multiple Sclerosis; NS-SEC,
National Statistics Socio-Economic Classification; QOL, Quality of Life; RA, Rheumatoid the influence of environmental factors on complex diseases results in
Arthritis; RAI, Rheumatoid Arthritis Index; RF, Rheumatoid Factor; SES, Socioeconomic positive or deleterious effects on overall disease activity indexes, self-
Status; SF-36, Short From-36; SLE, Systemic Lupus Erythematosus; SS, Sjögren's syn- reported health, access to specialized health care and treatment, health
drome; SSc, Systemic Sclerosis; T1D, Type 1 Diabetes; UK, United Kingdom. behavior, and mortality. Since there is a need to improve the understand-
⁎ Corresponding author at: Center for Autoimmune Diseases Research (CREA), School of
Medicine and Health Sciences, Universidad del Rosario, Carrera 24 # 63-C-69, Postal code:
ing of the concept of SES and the ways in which it affects health and
111221 Bogotá, Colombia. Tel.: +57 1 349 9650; fax: +57 1 349 9340. disease, we review herein the tools currently available to evaluate SES
E-mail address: juan.anaya@urosario.edu.co (J.-M. Anaya). as well as the relationship between SES and autoimmune diseases (ADs).

1568-9972/$ – see front matter © 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.autrev.2013.12.002
642 O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654

2. What is SES? any insurance [22], and those who do not have health insurance are
not receiving the care they may require [31].
SES was defined by Mueller and Parcel in 1981 as “the relative posi- A report from two different cohorts, one from France and one from
tion of a family or individual in a hierarchical social structure based on the United Kingdom (UK) [36,37], found that psychosocial work charac-
their access to or control over wealth, prestige and power” [1]. More teristics were a determinant of health when they were compared to
recently, SES has been also defined as “a broad concept that refers to the type of employment and self-reported health. However, this was
the placement of persons, families, households, and census tracts or greater in the UK cohort than in the French one, a finding that may
other aggregates with respect to the capacity to create or consume reflect cultural differences in the subjective perception of health
goods that are valued in our society” [2]. Others defined SES as an [36,37]. Data from a cohort in the US showed similar results [5].
individual or group's position within a hierarchical social structure, Marmot has established 10 major social determinants of health with
which is measured by variables such as education, occupation, income, respect to cardiovascular disease, a common chronic condition: social
wealth and place of residence [3,4], and these resources may enable gradient, unemployment, stress, social support, early life, addiction,
people to achieve certain goals (e.g., health) [5]. social exclusion, food, work, and transportation [18]. An analysis of
For centuries there has been a belief that poor living and working disparities in health is difficult to assess even in developed countries.
conditions are associated with shorter lives [6]. In the 19th century, In the US, there are millions of individuals who do not have health insur-
the most important improvements in health were caused by changes ance, and in places such as the UK or Sweden, it is difficult to evaluate
in nutritional and environmental conditions [7], but the problem of the impact of lack of medical care [38].
those with fewer resources having worse health outcomes for a number A report from Singapore showed that a prevalence of health-
of different causes persisted [3]. damaging behaviors (i.e., no physical activity, daily smoking, and regu-
Geographical differences are associated with the characteristics of a lar alcohol consumption) was consistently highest among men and
place, the influence of local cultures, scarcity of resources, and lack of women who had elementary or no education [39]. High SES could be as-
mobility as major determinants [8,9]. In certain areas, life expectancies sociated with better health, but it could only influence men because
increase and, in other areas, they fail to improve due to unacceptable women practice healthier behaviors [40]. Other studies have shown
disparities in health that are caused by global inequities in wealth that each year of education is associated with a lower probability of
[10–14]. smoking [41,42]. Results from a UK cohort found that educational
The impact of SES on health is increasing as it has important reper- achievement had a major impact in early adulthood. This effect was
cussions on local and international public policies [15]. The relationship not marked among women after they finished formal schooling, got
between a lower SES and higher incidence and prevalence of health older, [43] and started smoking [44]. Thus, education acts as a predictor
problems, disease, and death is present all around the world [16]. for attitudes and values shaping health-related behavior [45,46]. In the
The reason for governments to be interested in health inequity US, smoking rates among the better educated were one-third the rate
policies is to take action with respect to them and close the gap for the less educated, and obesity rates were reduced among the better
[17–20]. This is a topic that has been discussed at several World Health educated for each additional schooling year [41]. In the Netherlands, the
Organization meetings since Brock Chisholm, as first Director General, lower educated [47,48] and manual workers [47] were associated with a
postulated the death rate in tuberculosis as a sensitive index of the higher presentation of myocardial infarction.
state of public health and economic and social well-being in a commu- The most important factors reported to influence SES are income,
nity [21]. Growing socioeconomic disparity is a global concern as it educational level, occupational class, social class, and ancestry. These
could affect population health. Health disparities have grown geometri- factors are closely related to each other as they present certain interde-
cally over the past 20 years [22]. Policy initiatives have included rural pendent interactions (Fig. 1).
employment, food security, universal health care, social security for
informal workers, education, housing, and rights of tribal and forest 3. Measurement tools for SES
dwellers [17]. Nevertheless, research on how social changes in a
population are reflected in health and disease is scarce [23,24]. Although there have been extensive research revealing socioeco-
Health disparities frequently refer to disparities in health care in- nomic health inequalities across different societies, analysis and
cluding different access to screening and treatment options, or unequal measurement of SES are not an easy endeavor. Most health studies
availability of culturally or linguistically knowledgeable and sensitive that consider SES usually include only a single socioeconomic variable
health personnel [22,25]. The most common study design involved a measured during a single period and level [49]. There is less evidence
comparison of health status or mortality for individuals whose individ- about multiple risk exposure across different levels of SES. Measure-
ual or household income fell below the US federal poverty line com- ment tools for SES vary greatly and their use also varies from country
pared to those who were above this line [22,26]. Developments in to country. They include everything from single measurement tools to
health measurement instruments including everything from gathering complex questionnaires, which are used to extract variables in an
data by census to national health surveys have improved the way this attempt to classify a population. A deeper understanding of the SES
research is handled [27,28]. health gradient can be achieved by studying individual-level variables
The effects of severe poverty on health could be directly associated such as education, income, and occupational status. Others are influ-
with the effects of poor nutrition or unsanitary living conditions, but enced by social level. These are depression, hostility, sense of control
there is little information on the effects of SES at other levels of the social and health behaviors, and these depend on one's residential neighbor-
hierarchy [29]. A great variety of factors may account for the health hood, community, and work environment [28,29,33,50]. Although
effects of a low SES including exposure to environmental toxins, air socioeconomic data are not usually used in vital national statistics,
and water pollution, ambient noise, employment in jobs that have a they can provide outstanding information on attributable morbidity or
high risk of injury or disability, lack of health insurance or access to death rate among people sharing certain characteristics [6]. Table 1
high quality and preventative health care, poor nutrition as well as discloses tools that are the most widely used to measure SES and its
adverse health behaviors such as smoking, excessive alcohol intake, relationship with health.
sleeping patterns, and physical inactivity [16,30–33]. This highlights
the inverse relationship between income and overall mortality [34], 4. SES and health
and between income and population health [35].
It has been widely reported that in countries where there is a lack of The aspects related to SES that are curtailed over the course of life
universal coverage, the population with lower incomes does not have can be divided into two groups. The first is the physical environment,
O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654 643

Fig. 1. Most relevant associations of socioeconomic status with health outcome. The analysis of socioeconomic status (SES) can integrate a general view of the individual, household, and
community. All of these are influenced by ancestry, ethnicity, poverty, allostatic load, environment, access to health care, social networks, and lifestyles. This results in positive or negative
effects in the development and prognosis of acute or chronic diseases.

which includes exposure to pathogens, carcinogens and other environ- Educational attainment affects occupational class, which in turn
mental hazards. The second is the social environment, including contributes to income, and these differences in earnings could affect
interpersonal vulnerability, violence, difficulty in getting access to social health [41,45]. Both income and education can influence the etiology
support, psychological development, affection, and finally, health of many health outcomes partly due to material resources [49,61].
behavior [26,29]. The main health exposures related to SES are cigarette In a European cohort, there was an association between high
smoking, alcohol consumption, physical inactivity, depression, hostility, educational level and lower prevalence of chronic conditions such as
and psychological stress [23,29]. dyslipidemia, hypertension, insulin-dependent diabetes, hyperurice-
The notion that societal conditions and social environment influence mia, myocardial infarction, stroke, cancer [62] and low back pain [63].
states of health and disease has been reported broadly [51]. People Even when life expectancies in the European region are analyzed,
higher up on the social economic scale may have significant opportuni- people with a university degree have longer life spans compared to
ties more frequently to influence the events affecting their lives by those with lower secondary education [64]. Education is a factor that
modifying multiple variables involved in health determinants has an impact on high income and better lifestyles [54].
[18,22,29,33,38]. One example would be receiving treatment in larger, In a study of social status inconsistency, an association between low
better, or more specialized hospitals as well as receiving medication educational level and high occupational level resulted in higher
for secondary prevention more often [18]. incidence of cardiovascular disease [65]. A causal relationship between
SES influences mortality and morbidity rates in almost every disease education and mortality has been also pointed out [66].
[14,29,38,52,53]. The relationship between prevalence of chronic An association between higher educational attainment and
diseases and SES shows a linear gradient [26]. There is a strong and better health status has been repeatedly reported in the literature,
consistent SES influence on cardiovascular disease, coronary heart and the potential causal mechanisms linking schooling and income
disease, obesity, diabetes, metabolic syndrome, arthritis, tuberculosis, to health were recently reviewed by Kawachi et al. [67], who highlight-
chronic respiratory disease, gastrointestinal disease, and adverse birth ed that schooling is causally related to improvements in health
outcomes as well as on accidental and violent deaths [16,22,26,54,55]. outcomes and that raising the incomes of the poor leads to improve-
Social relationships affect the association between SES and health ment in their health outcomes. Nevertheless, according to authors,
across age [33,56]. Even though there is a gradient established for “some issues still remain unanswered, for example, what type of educa-
different ages, the greatest impact of SES on health is during adulthood tion matters for health, or whether there is a difference between
(age 40–65) [3,22]. Older, lower SES adults are more vulnerable to the health impacts of temporary income shocks versus changes in
health problems [56]. However, disparities tend to narrow after the long-term income” [67].
age of 65 [3,22]. Income constantly changes over one's lifetime and there is also an
Encouraging policies that improve the economic status of low SES important transition phase between childhood and adulthood. Howev-
populations (i.e., poverty reduction), leads to a tighter distribution of in- er, the time period of life in which socioeconomic gradients influence
come in society [57,58]. In Sweden, a two-fold rise in poor self-rated health remains unclear [19,43,54,68,69]. The influence of parental SES
health based on economic hardships was reported [52] while, in may be correlated to children's access to educational opportunities
Japan, the same results were observed from low income level individ- and to higher status, but it is unclear if it really influences health in
uals [59]. Noteworthy, perceptions of SES may differ across populations adulthood [70,71]. Parental low educational level has been associated
regardless of income level [53,60]. with a higher risk of diarrhea [72], and earlier asthma presentation
644
Table 1
Most widely tools used to measure SES and its relationship with health.

Method Characteristics Strengths Limitations References

Income Quantitative variable grouped by categories. The Gini Allows access to material goods and services. Age dependent, casual relation is limited by [1,37,67,172]

O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654


coefficient is sometimes used. methodological flaws.
Wealth Household or individual. Results are based on inherited Reflects the ability to meet emergencies or to absorb Difficult to calculate because of the multiple factors that [1,12,58,173]
wealth or savings. economic shock. Could be presented as the remains of contribute to its assessment. It changes over time.
deficits from previous income.
Education Years of educational attainment, credentials earned. Easy to measure. Excludes few members of the population. Economic returns may differ significantly across racial/ [1,2,56,174]
Less likely to be influenced by disease in adulthood than ethnic and gender groups. SES does not rise consistently
income and occupation. Higher levels of education are with increases in years of education.
usually predictive of better jobs, housing, neighborhoods,
working conditions and higher incomes.
Occupation Classification of work based on manual vs. non-manual Major structural link between education and income. Measurement may be influenced by variation in [1,83]
labor or occupational classes. Provides a measure of environmental and working education, income and prestige. Lacks of accuracy.
conditions. Assesses benefits and hazards related to job. Homemakers and retirees are difficult to classify.
Health insurance status Classifies people in private or public health care Informs about health care access. Influenced by the quality of service. [141,175–177]
Marital status Classifies people into married, unmarried, widow, and Informs primary close social status, and informs about Does not directly correlate with other SES variables. Low [175,177]
divorced. possible additional incomes accuracy.
Wright Singelmann class structure Classifies classes according to decision-making power, One of the first population analysis used. Does not include information on other members of the [178–180]
supervisory power, or work autonomy. household.
Registrar General's measure of Assesses explanatory variables by assigning scores from 1 Useful in the initial assessment of coronary heart disease. Does not include self-employment. Less accurate for the [3,44,81,181–183]
social class to 6 (i.e., professionals to unskilled manual workers). assessment of SES than income and other measurements,
and varies depending on ethnicity.
National Statistics Socio-Economic Based on employment relations and conditions. Assesses the relationship between social working class and Does not properly assess non-working population, [76,81,82,184–187]
Classification (NS-SEC) health outcomes including ethnicity. Highly associated with unemployment, handicaps, or housewives.
self-assessed health.
Occupational prestige scale Design for National Opinion Research Center. Range from 0 Assesses social hierarchy based on social level of Does not change according to other variables. [188]
to 100 points. employment.
Townsend index Consists of data on percentages of crowding, Simple census-based index of material deprivation Does not account for differences in rural and urban [172,189,190]
unemployment, lack of car ownership, and renters. calculated by the combination of four census variables. measurement of SES
Nam Socio-Economic Status score Employs occupation, education and income as indicators in Widely used in the US. Modified on repeated occasions. [183,189]
a composite index of social position.
Erikson–Goldthorpe class schema Eleven classes are defined according to labor market Combines trust, confidence and autonomy indicators. Few significant associations with health outcomes. [2,76,181,182,189,
condition characteristics (i.e., employment, degree of 191]
occupational security and promotion prospects).
Cambridge scale Hierarchical measurement of social distance between Strong association with smoking, behavior and social Based more on social interactions than individual [76,181,182,184,189,
occupations. Six categories are established. support. Represents a better measurement of social perceptions. 192]
inequities.
McClements equivalence scale Household total income is classified into sextiles. Most direct measurement of material and economic Based only in income. [185,193]
circumstances. Other equivalence scales may produce lower
estimates of inequality and poverty.
Carstairs score Measures the level of social deprivation based on four Based on income and occupational status. Does not involve other members of household in the [194–196]
variables: male unemployment, social class of the head of score evaluation.
household, overcrowding, and access to a car.
Swedish socio-economic classifica- Classifies occupation as manual workers, non-manual Reports classification based in Nordic occupational Do not assess retired status, unemployed, housewives, [197,198]
tion (SEI) employees, and employers. classification. and students.
New Zealand Index of Deprivation Uses household census data and includes nine aspects of Establishes a regional analysis for SES in a scale according to Do not provide individual information. Lack of replication [167]
material and social deprivation to divide New Zealand into residential address. in other countries.
tenths (scored from 1 to 10)
Graffar scale Measures educational level of head of household, Addresses interest in housing characteristics such as Information based only on the head of household. [199,200]
occupational status, and housing characteristics. property, house type, water supply, disposal management
and house assets.
Index of relative socioeconomic Based on Australian census data. Provides a summary of Indigenous descent, unemployed, and relatively unskilled Do not provide individual information. Lack of replication [201]
disadvantage SES measurement at a geographical area occupations are variables included. in other countries.
Critério de Classificação Econômica Based on educational level of head of household, and It implements a score addressing 8 classes according an Does not include information on other members of the [202]
Brasil number of possessed items. approximation to household's income. household. Lack of replication in other countries.
Winkler index Ranged from 3 to 21 points. Categorized as low (3–8), Graduation, school and professional education, academic Information based only on the head of household. [169]
moderate (9–14), and high (15–21) training, profession, and income are the main variables.
Duncan Socioeconomic status Three household characteristics are evaluated: number of Includes subjective information related to household Assumes that all SES variables are represented by the [74,183]
index assets, number of people sleeping in the same room and a situation. household ability to maintain the same living standards.
subjective assessment of the family's material situation.
Census Zip code-based Data from US national census are used to define areas with Used in big studies gathering population. Information is not based on individuals. Only used in US. [203]
similar SES characteristics.
Socioeconomic stratification Measurement by housing characteristics. Results given in Provides easily documented data. Reported in public services Information is not based on individuals. Data do not vary [111,131,204,205]

O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654


block units from an average taken of buildings within a classification. over time. Does not provide ownership status.
single block.
SES Index of Agency for Healthcare Based on unemployment, number of people below line of Provides an analysis integrating multiple SES variables. Does not provide individual characteristics. [206]
Research and Quality poverty, median income, property values, low education,
high education and crowded households in block analysis.
Index of Multiple Deprivation Data relating to 10 domains and subdomains: income, Assesses an integrated questionnaire with multiple SES Does not provide individual data. [207]
employment, health, child education, adult education, variables.
crime, barriers to housing, barriers to services, indoor
environment, and outdoor environment.
Subjective SES (MacArthur ladder Analog scale. Asks individuals to place themselves on one Perception shows significant associations with health Accuracy is low. [37,67]
measure) of the rungs of a 10-rung ladder where the top represents outcomes.
the most education, money or prestige and the bottom
those with the least of these.
Wealth Questionnaire Four variables are measured: duration of living standards Allows multiple ranges in every variable. Adapted from Variables are not aggregated into a score but examined [6,208,209]
after hypothetical income is lost, description of food eaten Women's Health Initiative study. individually.
over the last year, family patrimony, and familial debts.
Index of Social Position (ISP) Based on place of residence and head of household Variables are used as a whole allowing a better SES Does not include other household member in the [16,93,183,210–212]
characteristics. Categorized into 5 different classes. measurement. measurement.
Poverty income ratio (PIR) Index of household income relative to the federally defined A governmental measure providing general information. Varies depending on level of poverty reported by each [89]
poverty level. country.
Childhood SES Based on parental occupation status. Family income during childhood is a significant predictor of Changes according to external variables and across ages. [37,67,71]
adult health.
Neighborhood SES Based on the proportion of total household gross income Assesses the impact of community risk factors. Based on census data. Does not establish individual [34,103,104,213,214]
earned by the poorer 50% of the households in the area. information.
Aggregate measurements of individual data.

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646 O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654

[73]. However, variables of parental SES such as educational level can be Education may be a poor indicator of SES in studies of the elderly and
questionable due to its inconsistency [74]. varies depending on ethnicity [98], which is an important determinant
Scharown-Lee et al. [54] found that education among different of health perception [99]. Although it is difficult to disentangle the
ethnic groups had an inverse association with obesity, where SES can relationship between genetics and social factors in their contributions
motivate and encourage positive health related behaviors [16]. In a to health and disease risk [100], higher SES in Latin America is character-
study done on the US population [68], there was a significant association ized by lower levels of Native American ancestry [101].
between acute diseases and poverty conditions in the younger popula- SES is both complex and dynamic. That is, not only can individuals
tion. Mackenbach et al. [75] showed that mortality inequalities, based move up or down the social ladder, but also the definitions of, and rela-
on low educational levels and occupational classes, tended to increase tionships between social classes can also change over time. Thus, the
in Europe. However, this does not always imply a relationship between analysis of SES data should be done at different levels. The study of
health and the occupational hierarchy [76]. health at certain times in a person's life needs to be done not only on
The Whitehall study showed significant increases in relative risks of the individual level but also on the household and, ideally, the neighbor-
mortality over 10 years in the population at the lowest employment hood levels [6,18,102,103]. Moreover, analyses of individual risks may
level [22,29,77]. The Whitehall II study presented consistent evidence not provide the right kind of information as a result of the atomistic
of an inverse relationship between the level of employment and self- fallacy (i.e., inferring individual behavior from aggregate data) [7].
rated health [78–80]. Similar results were reported using National Therefore, caution should be exercised in making inferences for a
Statistics Socio-Economic Classification (NS-SEC) in the UK [81,82]. population based on observed relationships at the individual level.
Some measurements of occupational status may lack of accuracy The place of residence is strongly related to social position and
since they are recorded as a dichotomous variable (i.e., manual and ethnicity. Neighborhoods or residential areas have emerged as poten-
non-manual workers) [49]. The assessment of working conditions is tially relevant contexts because they possess both physical and social at-
becoming difficult as nonstandard work arrangements and unskilled tributes which could plausibly affect individual health [104]. This is due
labor become increasingly common. This is related to the health impact to the fact that the neighborhood characteristics reflect SES, culture,
of job insecurity, high work strain, limited control at the place of work, physical environment, and access to facilities. This will affect whether
repetitive work, exposure to uncomfortable conditions, contract work, or not people are exposed to risk situations [6,31,103,104].
self-employment, and increasing underemployment as important new Residence in a deprived or fragmented neighborhood is associated
factors to be measured [16,83]. Nevertheless, occupational status is a with poorer mental health apart from personal economic status [105].
better long term indicator than income [84]. Hypertension rates in It also influences mortality rates even when controlling for individual
blue-collar (production) and white-collar (supervisors and administra- SES [29,106]. Environments dominated by easy access to tobacco prod-
tive) workers found elevated hypertension risks in the former [83]. ucts and alcohol, fast food outlets, scarcity of affordable and appealing
Blue-collar workers also showed elevated psychophysiological stress fresh fruit and vegetables, and unsafe, uninviting community conditions
levels [85]. that restrict physical activity increase the odds against good health
Under the influence of economic stress, low job satisfaction, unem- [22,107]. Segregation of poor communities increases as a result of the
ployment or the threat of unemployment, and lack of influence and con- concentration of the low income population in deprived neighborhoods
trol over his life, the individual is more likely to adopt a passive lifestyle [106,108–111]. Nevertheless, there are cities where the impact of socio
[85]. The aforementioned characteristics influence the appearance of economic features does not influence health [106]. Results from a study
unhealthy behaviors and depression symptoms [85,86]. done on a Scottish population did not support the theory that lower SES
Social class, referred as social groups arising from interdependent influences regular physical activity or a sedentary behavior [112]. Fur-
economic relationships among people, was considered to be the result thermore, a neighborhood analysis from Syria disclosed no significant
of resource-based and prestige-based measurements of access to and SES association in spite of the fact that it is considered a developing
consumption of goods, occupational prestige, and educational level country. [113].
[6]. People born into a lower social class grow up in an environment The presence of social capital can boost self-esteem, provide social
which is in many respects less stimulating intellectually and emotional- support, help people to get access to better resources, and act as a buffer
ly than people born into a higher social class [87]. A low social class is for stressful events [22,114]. Other social factors include trust, civic par-
linked to the activity of the two main biological stress pathways: the ticipation, reciprocity and optimism, and norms facilitating cooperation
sympatho-adreno-medullary axis and the hypothalamic-pituitary- for mutual benefit [51,61,114]. These factors are evident in studies that
adrenal axis [31,38,85]. When this stress persists, it becomes chronic analyze social trust on the national level and correlate it with positive
and induces an allostatic load, a cumulative physiological consequence association with self-rated health [51]. In addition, results from a gener-
of chronic exposure to fluctuating or heightened neural or neuroendo- al social survey in the US showed residents who believed that people
crine responses that results from repeated stress. This involves past could be trusted had a lower age-adjusted rate of death from all causes
stressful experiences and changes in lifestyle associated with chronic [114]. Generally, stronger social ties have been linked to lower mortali-
stress [88–90]. The allostatic load modifies risks for a range of health ty, and higher participation in social activities is related to better mental
problems including metabolic syndrome, obesity, hypertension, diabe- and physical health [114].
tes mellitus type 2, lipid imbalance, atherosclerosis, accelerated brain In Fig. 2, a summary of contrasting characteristics associated with
aging, hippocampal atrophy, cognitive impairment, loss of bone mineral higher or lower SES in the general population is presented.
density, sarcopenia, and immune dysfunction [89,91,92]. The allostatic
load is elevated in those of low SES as compared to those of high SES 5. SES and ADs
[88–90]. Another interesting fact is the influence of social classes on
quality of mental illness treatment [93,94]. Table 2 summarizes the relationship between SES and some
Other factors such as race and ethnicity can also influence health common ADs according to different countries results.
[95]. Ethnicity is closely related to those socio-demographic variables
that constitute common measures of SES, and it can be argued that 5.1. SES and rheumatoid arthritis
social inequalities such as discrimination and prejudice typically
linked to minority status can be associated with lower SES groups A large number of economic evaluations have been done in recent
[31,54,84,96]. The confusion between SES and racial disparities is a years to assess the burden of rheumatoid arthritis (RA) for patients,
function of the wider distribution of risky health behavior among healthcare providers, and society in general [115]. Different studies of
lower class people [97]. diverse populations, reported an RA risk reduction as the educational
O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654 647

Fig. 2. Contrasting characteristics associated with socioeconomic status (SES). There are multiple variables affected by SES. Here we listed some of the most recognized. They are repre-
sented by arrows pointing up or down depending on whether the characteristics referred to higher or lower SES. *non-Caucasian includes ancestry populations that are Amerindian,
African, Asian, and Islander.

and income level rose [116–119]. An inverse relationship between the 5.2. SES and systemic lupus erythematosus
mortality rate and years of education has been reported. Eleven years
of education or less correlate with a two-fold increase in poor prognoses Systemic lupus erythematosus (SLE) tends to present earlier and
[120]. Thus, in RA, the lower the patient's educational level, the greater is often associated with worse outcomes in people of Hispanic, Asian
the chance of mortality and the lower the functional capacity is [29,121]. or African ancestry than in Caucasians. This may be related in part to
Residential location in deprived areas could also bring about the same overall poor SES including less structured families, fewer years of formal
outcomes [122]. However, a study of a Chilean population showed education, occupational status, household income, higher poverty, and
that a low educational level was not associated with severity of inadequate health insurance [139–148]. Results showing evidence of
RA [123]. Furthermore, a low educational level was associated with genetic influence alone are also reported [149].
rheumatoid factor positivity [121]. The relationship between ancestry and SES in SLE patients was
According to self-assessment, health quality is typically low in evaluated recently. An association between Amerindian ancestry and a
patients with RA who are older, female, less educated, obese, unem- low SES, which also influenced important clinical differences that
ployed, and less affluent than other groups [124-128]. Patients with depended on genetic ancestry, was observed [146]. Note that ethnic
a low SES may present with worse disease activity, physical health, self-identification is culturally and biologically complex and is not
mental health, and quality of life (QOL) than patients with a high correlated with ancestry, which should be no longer evaluated by ques-
SES [129–131]. tionnaire but rather by the use of ancestry information markers (AIMs)
Many patients with RA are unable to work due to low functional at the molecular level [150,151].
capacity and thus become dependent on the state for their health The costs of SLE can be different depending on the health care
services and social welfare support [123,132–134]. Individuals with a system. The impact of indirect costs is influenced by poor physical or
low income and those living in low SES neighborhoods received mental health, low social support, low educational level, unemploy-
fewer disease-modifying anti-rheumatic drugs (DMARDs) [36,135]. ment, and high disease activity [152].
There is evidence that African Americans with RA who went to non- Clusters of SLE patients with elevated mortality reported greater
rheumatologists did not receive DMARD therapy in 30% of the levels of poverty [140,153,154]. The incidence of end stage renal disease
cases [136] or got sub-optimal treatment [137]. in poverty-stricken areas also suggested a relationship with poor access
Increased Health Assessment Questionnaire scores and low SES to health care [155–158].
are associated with depression in patients with RA. As stated by
Margaretten et al. [138], “at every level of functioning, persons from 5.3. SES and multiple sclerosis
a lower SES may not have the support and coping skills to perform
as well as those from a higher SES, leading to even higher rates of Multiple sclerosis (MS) in the African American population has been
depression”. reported to start at a younger age than Caucasians or Hispanics.
648
Table 2
Results from diverse measure of SES in ADs.

AD Country Year N SES measurement method Results Reference

SLE China 2013 170 Educational level, income, employment status. SES was significant correlated to disease activity, anxiety, and depression. [215]
Latin America 2012 1426 Graffar scale. Rural residency was associated with mestizo ethnicity, low SES, and renal disease occurrence. [216]
United Kingdom 2000 201 Occupational and household facilities. There was no association between SES and LN in Afro-Caribbean patients. [217]
United States 2013 34,349 Census Zip code-based. The association of county-level SES and LN prevalence was assessed. LN prevalence was higher in [218]
deprived areas.
2013 4214 Census Zip code-based, employment status, educational level. African Americans recipients with LN with lowest income had a significantly increased risk. [219]
2012 1752 Educational level and income. Low SES in Caucasians increases the risk of cardiovascular disease. [220]
2012 1129 Educational level, household income and neighborhood SES. European genetic ancestry was associated with a lower risk of LN, regardless of SES. [149]
2010 775 US Census, including educational level and neighborhood SES. The number of physician visits for SLE decreases according to low SES. [221]
2010 211 Educational level and census Zip code-based. SES was associated to HRQOL, independent of regional or individual SES measurement method. [143]
2010 702 Census Zip code-based. Inconclusive results were found about the effect of SES on ESRD. [203]
2008 957 Educational level, household income, poverty status and neighborhood Individual SES was associated with physical and mental health outcomes. Low neighborhood SES [222]

O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654


SES. contributed independently to high levels of depressive symptoms.
2007 867 Educational level and income health insurance status. Low income was associated to lower likelihood to report visits to rheumatologist, and health care [223]
access.
2007 459 Educational level, income, health insurance and marital status, and Association of SES; poverty is an important factor associated with ethnicity according disease [141]
housing. activity.
2006 459 SES according federal US guidelines adjusted for the number of Association of SES with presence of LN in a multi ethnic cohort. Admixture separately explained a [158]
inhabitants in the household. much larger proportion of the ethnicity explained variance that SES. Together, they explained the
majority of ethnicity related variability.
2004 202 Wealth Questionnaire and traditional values of SES. Wealth, per se, did not appear to have an additional predictive value over the traditional measures of [208]
SES in SLE disease activity.
2004 4779 Educational level. In Whites high educational level correlates with low mortality rates, but not in minorities [224]
(i.e., African-American, Asia or Pacific Islander.
2003 128 US Census, neighborhood SES Poverty is an important risk factor for progression of proliferative LN, independent of race/ethnicity. [225]
2001 200 Educational level, income, occupational prestige scale. Social support is particularly beneficial for those possessing social, economic and health advantages. [188]
2001 11,102 US Census Bureau. Geographical patterns of SES status were related to the variation of SLE mortality across US. [154]
Hispanics disclosed higher rates of mortality.
1999 67 Income, educational level, housing facilities, and US Census Bureau. Association between low SES and acculturation was found, but also with less disease activity at [226]
enrollment.
RA China 2011 353 Employment status. RA patients reported a lower rate of labor force participation than control group. [227]
2011 144 Educational level. Older age, lower education level and functional disability independently predicted high indirect [228]
costs.
Colombia 2003 79 Socioeconomic stratification. SES was not associated with disease activity. [131]
Denmark 2006 515 Educational level in year and grading, childhood SES, and subjective Low educational level was associated with the risk of developing RA (mainly rheumatoid factor [229]
SES. positive).
Korea 2012 17,311 Educational level, household income, individual income, and Women with RA had a significant lower employment rate compared population without RA. [230]
occupational status.
Latin America 2012 1093 Graffar scale. Patient disease activity indexes were significantly worse in those with low/low-middle SES, in very [200]
early disease.
Morocco 2012 100 Income. Low SES patients had lower scores on SF-36, and decreased educational level. [231]
2006 100 Marital status, educational level, occupational status, income, health Increased affection was associated with low SES and problems with health care services. [133]
insurance status.
Netherland 2003 878 Educational level. Low SES patients have worse outcomes as; disease activity, physical health, mental health. However [129]
these differences decreased over time.
Sweden 2012 1460 Occupation and immigrant status. RF positivity and occupational class referred as other were independently associated with poorer [232]
prognosis.
2011 290 Swedish socio-economic classification. Low SES and smoking were independent risk factors for RA. [198]
2008 28,339 Educational level. RA was associated with low childhood SES sustained into adulthood. [233]
2005 930 Educational level and occupation. There was an association between high SES and lower risk for RA. [121]
United Kingdom 2013 421 Carstairs score. SES had no significant effect in the analysis of height and disease activity. [234]
2012 25,455 Social class and educational level. Higher social class or degree education was associated with reduced risk of inflammatory [235]
polyarthritis.
2012 6298 Townsend index. Area-level socio-economic deprivation was a significant risk factor for RF positivity. [236]
2012 553 Index of Multiple Deprivation. There was an association of low SES and poor outcomes; HAQ, but it was not significant including [237]
RAI into analysis, as a factor associated in SES influence.
2009 1393 Index of multiple deprivation and social class. Within the lowest social class, there was poorer outcome in patients from increasingly more [238]
deprived areas.
2005 466 Townsend index. Increasing social deprivation was associated to higher disease activity, higher pain, poorer physical [190]
function; poorer emotional aspects of mental health, and lower quality of life were found at baseline.
United States 2013 50,884 Childhood SES and educational level. Low childhood SES and adult education were associated to RA. [239]
2013 1100 Income, educational level, health insurance status. Patients presented cost-related medication non-adherence and spending less on basic needs to [240]
afford medication associated to educational level and low income.
2011 93,143 Census Zip code-based. Low personal income and those living in low SES neighborhoods had reduced DMARD receipt. [135]
2010 696 Educational level, household income, occupation status, home Individual's perception of neighborhood environment characteristics is predictive of health [241]
ownership, and neighborhood SES. outcomes among adults.
T1D Australia 2006 1143 Index of Relative Socioeconomic Disadvantage. A higher incidence of T1D was presented in high SES, especially in urban area. [201]
Bosnia and 2013 65 Parental educational level, employment status and Hollingshead index Low and middle SES in families with children with T1D was associated to low QOL. [242]
Herzegovina of social position.
Brazil 2012 3591 Critério de Classificação Econômica Brasil Low or very low SES was found in up to 87% of the studied patients. [243]
2011 71 Critério de Classificação Econômica Brasil The low educational level of the caregivers influenced the inadequate glycemic control. [244]
Germany 2011 296 Winkler index. Presence of low SES correlates with low metabolic control and increase of HbA1C levels. [169]
Greece 2008 127 Parental educational level, occupation and social class. Middle and upper social classes had a protective effect on T1D presentation. [245]

O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654


Italy 2013 414 Parental educational level and crowding index. Crowding houses conferred and 3-fold greater risk of having T1D up to 3 years of age, and low [246]
parental educational level had a protective effect in the group of 4–14 years.
Malaysia 2000 926 Income and educational level. Household income was an important determinant of glycemic control in T1D. [247]
New Zealand 2008 555 New Zealand Index of Deprivation. Presence of low SES correlates with low metabolic control and increase of HbA1C levels. [167]
United States 2013 167 Health insurance status as indirect measure. Patients covered with Medicaid presented higher risk to present diabetic ketoacidosis. [248]
2012 1502 Income, educational level, poverty index ratio. Higher risks of T1D incidence were found in higher median income, higher housing value and no [249]
poverty designation.
2012 349 Hollingshead index of social position. Reported ethnic differences in HbA1C and disease care behaviors, better explained by SES. [250]
2011 505 Educational level, occupational status, and neighborhood SES. Neighborhood characteristics related to greater affluence, occupation, and education are associated [166]
with higher T1D risk.
2011 317 Household income, educational level and Hollingshead index of social Lower SES in T1D is a robust predictor for diabetes complications. [251]
position.
2011 317 Household income, educational level and Hollingshead index of social Baseline education level predicted all-cause mortality in T1D population. [212]
position.
2006 222 Index of social position. Poor glycemic control in pediatric T1D is associated with lower SES and depression. [252]
2003 184 Parental educational level, Income, health insurance status, marital Hispanic youths with T1D may be at greater risk for poor glycemic control because their low SES. [253]
status
MS Canada 2009 5458 Educational level, Income, health insurance status, marital status, and Low SES was associated with a minor report of smoking habit in MS patients. [175]
region of residence.
2009 8983 Educational level, Income, health insurance status, marital status, and Lower SES was associated with a higher frequency of adverse health behaviors accounting for other [254]
region of residence. demographic factors.
2008 8983 Educational level, Income, health insurance status, marital status, and Lower SES was associated with a higher presence of comorbidity. [177]
region of residence.
Denmark 2013 2205 Parental educational level and household income. Children whose mothers had a secondary or higher level of education reduced risks of MS. [255]
Iran 2010 174 Educational level, Income, occupation, marital status. SES groups showed no significant correlation with other factors related to education needs. [256]
Lebanon 2013 201 Educational level, employment status, region of residence, and QOL is determined by social support, living area, depression, educational level, employment, fatigue [257]
household integrant. and religiosity.
Sweden 2008 5231 Educational level. Increment of educational level was associated with slightly low risk for hospitalization. [258]
SS Morocco 2012 57 Income and educational level. Low SES and educational level altered fatigue level and QOL. [259]
Netherlands 2009 135 Education level and employment status. High level of education was associated to employment in SS. [260]
SSc Canada 2013 1145 Educational level. Educational level did not show significant differences in survival, as poor outcomes. [261]
France 2010 87 Employment status and income. Decreased income was associated with receiving a disability pension. [262]
Serbia 2010 35 Employment status. Symptoms of depression were associated with economic variables. [263]

ACR, American College of Rheumatology: ADs, Autoimmune Diseases: Disease Modifying Anti-Rheumatic Drugs, DMARDs: HAQ, Health Attitude Questionnaire: HbA1C, Glycated hemoglobin: HRQOL, Health related Quality of Life: LN, Lupus
Nephritis: MS, Multiple Sclerosis: QOL, Quality of Life: RA, Rheumatoid Arthritis: SES, Socioeconomic Status: SF-36, Short From-36: SLE, Systemic Lupus Erythematosus: SS, Sjögren's syndrome: SSc, Systemic Sclerosis: RAI, Rheumatoid Arthritis
Index: RF, Rheumatoid Factor: T1D, Type 1 Diabetes.

649
650 O.-J. Calixto, J.-M. Anaya / Autoimmunity Reviews 13 (2014) 641–654

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