Socioeconomic status and organ damage in Mexican systemic lupus erythematosus women

Abstract

The objective of this cross-sectional study was to determine relationships between socioeconomic status and organ damage in Mexican systemic lupus erythematosus (SLE) patients. Demographic and clinical variables were assessed. Socioeconomic status was evaluated using the Graffar method and monthly household income. Lupus activity and organ damage were measured using the SLE disease activity scale, validated for the Mexican population (Mex-SLEDAI), and the Systemic Lupus International Collaborating Clinics/American College of Rheumatology (SLICC/ACR) scale. The 143 Mexican female SLE patients included (mean age 40.1 ± 8.9 years, mean disease duration 8.9 ± 6.3 years) had a mean monthly household income of $ 407.2 ± 326.5. According to the Graffar index, 18.9%, 52.5%, and 28.7% had high/medium-high, medium, and medium-low/low socioeconomic status, respectively. Organ damage was observed in 61 patients (42.7%). Patients with organ damage had lower monthly household incomes ($241.4 ± 152.4 vs. $354.8 ± 288.3) and were more frequently unemployed (57.3% vs. 35.3%; p = 0.01) than those without. Low monthly income was not associated with lupus activity or self-reported health status. In the adjusted multivariate analysis, low monthly income ( < $300) was associated with organ damage. In conclusion, low income may be associated with organ damage in Mexican SLE patients.

Keywords

Systemic lupus erythematosus socioeconomic status organ damage lupus activity

Introduction

Systemic lupus erythematosus (SLE) is an autoimmune disease noted for the heterogeneity of manifestations and outcomes. Although advances in disease management in recent decades have improved the prognosis of SLE patients, recent studies indicate that risk of mortality is twice that of the general population,¹ and the disease burden remains very high.

There are many reports on the associations between socioeconomic status and chronic disease outcomes that show greater morbidity and mortality in people with lower socioeconomic status. Numerous studies have explored these associations in SLE outcomes, including disease activity,^2–4 organ damage,^4–7 lupus nephritis,^8–13 hospitalization,¹² and mortality.^14–17 Most studies have found worse outcomes in people with lower socioeconomic status, which is a complex concept compromising two distinct aspects: first, resources such as education, income and wealth, and second, status or rank in a hierarchical society. Direct measurement of socioeconomic status is difficult and surrogate markers are often used.

In developing countries, SLE has been associated with unfavorable outcomes, including disease activity, damage accrual, work disability and mortality.¹⁸ Low socioeconomic status and lack of access to healthcare, especially in medically underserved communities, may be responsible for many of the disparities observed. Most clinical studies on the socioeconomic status and SLE have been conducted in developed countries, and transposition of the results to emerging countries is not always possible and meaningful. According to the International Monetary Fund World Economic Outlook Report, April 2014 and World Bank data, Mexico, with a population of 122 million, is considered a developing economy.¹⁹ Although Puebla is considered one of Mexico’s most industrialized states,²⁰ the United Nations has ranked the state as the seventh most underdeveloped in the country.²¹ The objective of this study was to determine the relationship between socioeconomic status and organ damage in patients with SLE.

Methods

Study population

SLE patients were recruited from Hospital Regional No, 36, IMSS, Puebla, between January 2012 and January 2013. SLE patients were consecutively invited to participate in a single-center cross-sectional study. The hospital is a public institution that treats patients from throughout Puebla state. Patients have full public health coverage and no private health insurance. All patients, who were aged ≥18 years, fulfilled the 1997 American College of Rheumatology (ACR) revised criteria for the classification of SLE.²² Exclusion criteria were major cognitive deficits that would preclude questionnaire completion. This study was approved by the Hospital Ethics Committee, and written informed consent was obtained from all participants. Participants consented to complete a battery of questionnaires, which included a demographics form evaluating ethnicity, gender, age, marital status, current working status (paid employment or not), income and education; the LupusQoL instrument; the Graffar scale; and a medical history and examination by the treating physician to obtain a standard index of activity and organ damage. Ethnicity was determined by questions on the place of birth, and the place of birth of parents and grandparents.²³

Measurement of clinical variables

The primary dependent variables in the analysis were measurement of SLE activity, cumulative organ damage, and health-related quality of life.

SLE disease activity was assessed by physical examination and laboratory testing and was scored using the SLE Disease Activity Index, translated into Spanish and validated for the Mexican population (Mex-SLEDAI).²⁴ The Mex-SLEDAI was reduced from the original SLEDAI to the 10 main clinically-defined variables and does not include immunological tests, making it less expensive to administer. It provides a global score that ranges from 0 to 24 (greater activity). Active disease was defined as Mex-SLEDAI ≥ 4.

The Systemic Lupus Index Collaborating Clinic/American College of Rheumatology (SLICC/ACR) damage index (DI) for SLE was also scored at study entry.²⁵ This index measures the accumulated organ damage due to the disease, the complications of therapy, and concurrent illness such as cancer from the onset of SLE and includes descriptors in 12 organ systems. Organ damage is considered only if present for at least 6 months. Total scores range from 0 (no damage) to 46 (maximum damage). Patients were categorized into two groups according to the cumulative systemic damage index (SDI) as SDI ≥ 1 (with damage) and SDI = 0 (without damage).

The LupusQoL questionnaire was used to assess patient self-reported health status. It contains 34 items across eight domains defined by patients as important. The questionnaire is copyrighted jointly to the University of Central Lancashire and East Lancashire Hospitals NHS trust. The LupusQoL has good internal consistency, good test-retest reliability, good concurrent validity with comparable domains of the SF-36 and discriminating validity for different levels of disease activity. It contains eight domains: physical health, emotional health, body image, pain, planning, fatigue, intimate relationships, and burden to others, and typically requires <10 minutes to complete. Scoring and transformation takes about 5 minutes. Each question is evaluated using a five-point Likert response, where 0 = all of the time, 1 = most of the time, 2 = a good bit of the time, 3 = occasionally, and 4 = never. Scores for each of the eight domains range from 0 (worst health status) to 100 (best health status).²⁶

Socioeconomic status was evaluated using the validated Graffar scale,²⁷ which has been used in Latin America and employed to evaluate socioeconomic status in SLE patients.^28,29 The Graffar scale takes into account five variables: parental occupation, parental level of education, main source of income, housing, and neighborhood quality. Each variable has five categories with independent and progressive scores. A final score classifies subjects in five categories: high, medium-high, medium, medium-low, and low.

The variable of interest, place of residency, was categorized as urban (≥10,000 inhabitants) and rural (<10,000 inhabitants). Monthly household income was grouped into 3 categories: <$300 US, $300 to ≤$700 and ≥$701.

Statistical analysis

Descriptive data were expressed as means ± SD for continuous variables and frequencies for categorical variables. Comparisons between groups were assessed using the Student’s t test for normally distributed variables and the Mann–Whitney U test for non-normally distributed variables. Categorical variables were analyzed using the chi-squared test. Spearman’s correlation coefficient was used to analyze the relationship between chronic damage and monthly household income and education level. Multivariable logistic regression models were used to analyze the influence of socioeconomic status variables on organ damage in SLE patients. All results are presented as odds ratios (ORs) with their corresponding 95% confidence intervals (CIs). All statistical tests were two-sided with a level of significance of 5%. The statistical package for SPSS 21 (Chicago, IL, USA) was used for all data management and analyses.

Results

A total of 143 female SLE patients were included, with a mean age at study entry of 40.1 ± 8.9 years and a mean disease duration of 8.9 ± 6.3 years (median 7.0 years; range 1–31 years): 98.5% were living in urban areas and 1.5% in rural areas. The median education level was 11.5 ± 4.2 years. No patient was illiterate. Seventy-nine (55.2%) patients were in paid employment. The mean monthly household income was $407.2 ± 326.5: 48.3% had household incomes <$300 and 13.3% ≥ $700. Table 1 shows the main sociodemographic and clinical variables. Only 39 (27.3%) patients had active disease (Mex-SLEDAI ≥ 4) with mild levels of disease activity at the evaluation, with a mean (± SD) of 2.4 ± 3.0. The mean self-reported health status was 68.1 ± 22.2 on the LupusQoL scale.

Table 1

Sociodemographic and disease characteristics in SLE patients

Variable	SLE patients, n = 143
Age, mean ± SD, years	40.1 ± 11
Education, mean ± SD, years	11.5 ± 4.2
Marital status, married, living together, n %	84 (58.7)
Unemployed, n (%)	61 (42.7)
Socioeconomic status,^a n (%) High/medium-high Medium Medium-low/low	27 (18.9) 75 (52.4) 41 (28.7)
LupusQoL, mean ± SD, range 0–100	68.1 ± 22.2
Disease duration, mean ± SD, years	8.9 ± 6.3
Mex-SLEDAI, mean ± SD, score	2.4 ± 3.0
SLICC, mean ± SD score	1.4 ± 0.5
Glucocorticoid (doses), media ± SD, mg/d	11.9 ± 8.0

SD: standard deviation; Mex-SLEDAI: Mexican Systemic Lupus Erythematosus Disease Activity Index; SLICC: Systemic Lupus International Collaborating Clinics/Damage Index.

According to Graffar scale.

Organ damage (SDI score > 0) was observed in 61 patients (42.7%). The mean SDI score was 1.4 ± 0.5. Organ damage occurred most frequently in the musculoskeletal system (62 patients; 43.3%), the renal system (25 patients; 17.4%), and the neuropsychiatric system (15 patients; 10.4%). Patients with organ damage had a non-significant higher daily prednisone dose than patients without organ damage (12.2 ± 8.7 vs. 11.6 ± 7.7 mg/day; p = 0.68) and less frequent use of azathioprine and methotrexate (9.6% vs. 28.0%; p = 0.40 and 8.7% vs. 9.3%; p = 0.58, respectively). Antimalarial use did not differ significantly between the groups.

Although the socioeconomic status was not associated with organ damage measured by the SLICC (p = 0.52), on the Graffar scale patients with organ damage had a non-significantly lower mean monthly household income ($241.4 ± 152.4 vs. $354.8 ± 288.3; p = 0.08), a significantly-higher frequency of a monthly household income <$ 300 (60.7% vs. 39.0 %; p = 0.01), and were more frequently unemployed (57.3% vs. 35.3%; p = 0.01) than patients without organ damage. There were slight negative correlations between monthly household income and educational levels and chronic damage (r = −0.23; p = 0.002 and r = −0.23; p = 0.006). However, we found no association between socioeconomic status variables (Graffar scale, household income, unemployed status and educational level) and lupus activity measured by Mex-SLEDAI or the self-reported health status measured by the LupusQoL questionnaire. Table 2 shows the sociodemographic and clinical variables of patients with and without organ damage.

Table 2

Sociodemographic and clinical variables of SLE patients categorized by cumulative disease damage index (SDI)

	Group with disease damage (SDI ≥ 1) n = 61	Group without disease damage (SDI = 0) n = 82	p
Age, mean ± SD, years	43.5 ± 12.8	37.6 ± 10.5	0.05
Education, mean ± SD, years	10.6 ± 3.7	12.2 ± 4.4	0.27
Marital status, married, living together, n %	34 (61)	50 (60.9)	0.32
Unemployed, n (%)	35 (57.3)	26 (35.3)	0.01
Socioeconomic status, n (%) High/medium-high Medium Medium-low/low	10 (16.4) 31 (50.8) 20 (32.8)	17 (20.7) 44 (53.7) 21 (25.6)	0.52
Income monthly, media ± SD, US $	241.4 ± 152.4	354.8 ± 288.3	0.08
Household income, n (%) <$300 $300 to ≤$700 >$701	37 (60.7) 20 (32.8) 4 (6.5)	32 (39.0) 35 (42.7) 15 (18.3)	0.01
LupusQoL, mean ± SD, range 0–100	64.6 ± 22.5	70.9 ± 21.6	0.08
Disease duration, mean ± SD, years	10.6 ± 6.6	7.6 ± 5.7	0.11
Mex-SLEDAI, mean ± SD, score	2.1 ± 2.6	3.2 ± 3.3	0.11
Glucocorticoid (doses), media ± SD, mg/d	12.2 ± 8.7	11.6 ± 7.7	0.96

SD: standard deviation; Mex-SLEDAI: Mexican Systemic Lupus Erythematosus Disease Activity Index; SDI: Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index.

After adjusting for possible confounding factors using multivariable logistic regression models, only a lower household income (<$ 300) was strongly associated with organ damage (SDI ≥ 1) (OR 4.6, 95% CI 1.3–16.1).

Discussion

We studied the relationship between socioeconomic status and SLE variables in Mexican patients with SLE. Monthly household income was associated with organ damage but not with lupus activity or self-reported health status.

Major determinants of geographical differences are the characteristics of a place, the influence of local cultures, the scarcity of resources, and lack of mobility.³⁰ In certain areas, life expectancies increase and in others they fail to improve due to unacceptable disparities in health caused by global inequities in wealth.^31,32 The impact of socioeconomic status on health is increasing as it has important repercussions on local and international public policies. There is a relationship between lower socioeconomic status and a higher incidence and prevalence of health problems, disease, and death worldwide.³³ Tools for the measurement of socioeconomic status vary greatly, as does their use between countries, and may include everything from single measurement tools to complex questionnaires, which are used to extract variables in an attempt to classify a population.³⁴

Non-Caucasian populations have a higher overall occurrence of SLE, and less-favorable outcomes in terms of worse survival rates.¹⁷ This has been clearly documented for African Americans in the US, and is beginning to be recognized among other ethnic minorities (e.g. Hispanics) living in the US or their country of origin.^2,12,35

The lupus outcome study (LOS) evaluated whether there are disparities in assessments of interactions with health care providers and health plans, and whether these interactions affect the technical quality of SLE care. Ratings in the lowest quartile on all dimensions of interactions with providers and the health care system were associated with lower technical quality of care, potentially resulting in poorer SLE outcomes.³⁶

We found no relationship between socioeconomic status, assessed using the Graffar scale, and organ damage in SLE patients. In contrast, a multiethnic Latin American cohort study showed that socioeconomic factors, including the Graffar scale, are important mediators of less favorable outcomes in patients with SLE.^29,37 A possible explanation for this disparity might be that the Graffar scale measures educational level, which was higher than the Mexican national average (8.6 years) according to the Mexican National Institute of Statistics, Geography and Informatics.³⁸

In our cohort, damage occurred in at least 1 item of the SDI in 42.7% of patients, a rate similar to those reported in other studies including large proportions of minorities.⁵ We found an association between household income and organ damage, similar to the results found by Sutcliffe et al., in an analysis of 184 patients with SLE, who observed that end-organ damage was greater in patients of non-Caucasian race with low socioeconomic status.⁷ Similar finding were reporting in 132 whites and African American SLE patients with early disease damage: African American ethnicity and lower household income were independently associated with disease damage (39). In contrast, Rivest et al. and Esdaile et al. found no relationship between socioeconomic status and organ damage.^6,40

In the bivariate analysis, educational level was weakly correlated with organ damage, as found by other studies.^7,41 However, this association disappeared in the multivariate analysis. This could be due to various factors, including a lack of statistical power.

Unemployment was 42.7% in our SLE patients almost 9 years after disease onset, a much higher rate than in the Mexican general population (4.5%) during the study period.³⁸ Other studies have reported comparable figures in SLE patients.⁴²

We found no relationship between socioeconomic status and SLE disease activity. Alarcon et al. evaluated a multiethnic cohort and found that wealth per se had no impact on disease activity.² Reveille et al. found that genetic and ethnic factors appear to be more important than socioeconomic determinants in influencing disease activity and some organ manifestations at disease onset.⁴³ In contrast, less education and lower income were associated with greater disease activity in a telephone survey of 957 patients with confirmed diagnosis of SLE.⁴⁴ Recently, a Chinese study found significant correlations between socioeconomic status, disease activity and anxiety/depression in SLE patients.⁴⁵ A review by Calixto et al. examined the influence of socioeconomic status on autoimmune diseases. However, the majority of studies linking socioeconomic status with health are cross-sectional, which reduces the level of evidence.³⁴

Our study had some potential limitations and biases. First, in an observational study such as ours, some caution is required in interpreting the results. Non-random sampling of subjects may have led to selection bias. The cross-sectional nature of the study did not allow consideration of changes over time in lupus activity and socioeconomic variables such as household income, making it difficult to show a cause-effect relationship between socioeconomic status and lupus outcomes. Secondly, we analyzed household income variables: however, social scientists have emphasized that income per household might not be an accurate indicator of socioeconomic status because, even within individuals falling below the poverty line, there are distinct levels of wealth or lack of wealth.⁴⁶ Even so, this measure may provide sensitive information. Income levels have been used in several epidemiological studies of SLE patients.^2,5,38,47 Thirdly, most of our participants had low levels of lupus activity, and therefore our findings should not be applied to patients with severe SLE. Fourthly, although our patients were defined as mestizo ethnicity, this was only a visual and subjective estimation of the patient’s ancestry. Since Amerindian genetic ancestry has been correlated with lower socioeconomic status,⁴⁸ it would have been interesting to have analyzed genetic ancestry in our study. Finally, in developing countries, SLE has been associated with several unfavorable outcomes. Poor socioeconomic status and lack of access to healthcare, especially in medically-underserved communities, may explain these outcomes. However, in the present study, all patients had health insurance, but chronic damage was observed in patients with lower incomes. This suggests that factors not measured in our study, such as poor treatment adherence, delays in diagnosing SLE in some patients or infectious complications, may have contributed to organ damage.¹⁸ Longitudinal and observational prospective studies and registries may help to identify the influence of socioeconomic status on poor SLE results in developing countries.

This study provides additional evidence that socioeconomic status plays a role in organ damage in Mexican SLE patients. Monthly household income was strongly associated with organ damage measured by the SDI, independently of other variables. Further studies of the effect of income, other measures of socioeconomic status, and ethnicity, on total damage and specific types of damage seen in Latin American SLE patients are required to identify high-risk groups.

Footnotes

Acknowledgments

The authors would like to thank all patients who participated in this study for their patience and understanding. We would like to thank David Buss for his valuable guidance and advice during this project.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest statement

The authors have no conflicts of interest to declare.

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