INTRODUCTION
The adverse impact of socioeconomic conditions on health is particularly seen in vector-borne disease like ma- laria, dengue, Japanese encephalitis and congenital dis- eases like tuberculosis, cancer and coronary heart dis- eases1–7. By understanding the socioeconomic conditions of the community, the disease spectrum can be analysed very accurately. Lymphatic filariasis (LF) is a neglected tropical parasitic disease caused by Wuchereria bancrofti, Brugia malayi or B. timori and transmitted by mosqui- toes. Occurrence of this disease is primarily noticed among the low income communities, having poor sanitation facilities and lack of awareness about the disease8–11. The manifestations of filariasis are mostly irreversible, and cause socioeconomic and psychological problems to pa- tients and their families, which lead to impoverishment and poverty12. Few such studies have been carried out on LF that causes considerable economic burden; however, information on the impact of the disease on the factors of
socioeconomics is not properly understood13. Filariasis is a major public-health problem in India and constitutes approximately 45% of the world’s burden, where around 59 million people are infected with the parasites causing LF, of these 19.6 million exhibit filariasis symptoms14. In India, around 250 districts in 20 states/union territo- ries have been declared as filariasis endemic regions15.
In India, the mass drug administration (MDA) programme is being implemented since 2004 in districts where filariasis is endemic which includes 16 districts of Andhra Pradesh. Apart from MDA programme there are various other vector control programmes which are be- ing implemented by government of Andhra Pradesh in these districts. Earlier studies have indicated high inci- dence of filariasis in some villages of Karimnagar, Chittoor, East Godavari and West Godavari districts of Andhra Pradesh16–17. Even after implementation of vari- ous control measures the disease transmission is occur- ring in these regions. Hence, to identify the risk factors for filariasis a prospective, population-based case-con-
Influence of socioeconomic aspects on lymphatic filariasis: A case-control study in Andhra Pradesh, India
Srinivasa Rao Mutheneni
1, Suryanaryana Murty Upadhyayula
1, Sriram Kumaraswamy
1, Madhusudhan Rao Kadiri
1& Balakrishna Nagalla
21Bioinformatics Group, Biology Division, Indian Institute of Chemical Technology (CSIR), Hyderabad; 2 National Institute of Nutrition (ICMR), Hyderabad, Andhra Pradesh, India
ABSTRACT
Background & objectives: Lymphatic filariasis (LF) is a major public health problem in India. The objective of the study was to assess the impact of socioeconomic conditions on LF in Chittoor district of Andhra Pradesh, India.
Methods: A survey was carried out from 2004 to 2007 during which, an epidemiological and socioeconomic data were collected and analysed. The microfilaria (mf) positive samples were taken as cases and matched with control group by sex and age (1:1) for case-control study. Bivariate and multivariate logistic regression was used to identify the potential risk factors for filariasis. Using principal component analysis (PCA), a socioeconomic index was developed and the data/scores were classified into low, medium and high categories.
Results: In total 5,133 blood smears were collected, of which 77 samples were found positive for microfilaria (1.52%). Multivariate analysis showed that the risk of filariasis was higher in groups of people with income
< `1000 per month [OR = 2.752 (95%CI, 0.435–17.429)]; ` 1000–3000 per month [3.079 (0.923–0.275)]; people living in tiled house structure [1.641 (0.534–5.048)], with kutcha (uncemented) drainage system [19.427 (2.985–
126.410)], respondents who did not implemented mosquito avoidance measures [1.737 (0.563–5.358)]; and in people who were not aware about prevention and control of filariasis [1.042 (0.368–2.956)]. PCA showed that respondents with low (41.6%) and medium (33.8%) socioeconomic status are more prone to filariasis (p=0.036).
Interpretation & conclusion: The cross sectional study showed that the population with low and medium socioeconomic status are at higher risk of filariasis. The identified socioeconomic risk factors can be used as a guideline for improving the conditions for effective management of filariasis.
Key words Case-control; Chittoor; lymphatic filariasis; principal component analysis; socioeconomic index
trol study was conducted in the villages of Chittoor district, Andhra Pradesh. The objectives of this study were to investigate the risk of lymphatic filariasis in associa- tion with socioeconomic characteristics at the level of the individual and to explore whether these factors are inde- pendent or whether they are linked; and to estimate the relative contribution of each factor to the burden of filari- asis. This study would help the health authorities to un- derstand the factors associated with filariasis in these ar- eas for better planning and intervention to control the disease.
MATERIAL & METHODS
Chittoor district lies between the coordinates, 12°37'–
14°8' N and 78°3'–79°55' E and is located on the south- ern part of Andhra Pradesh (Fig. 1). Most of the popula- tion in this district depends on agriculture and farming activities for livelihood. Chittoor district is known to be endemic for lymphatic filariasis, where single dose of di- ethylcarbamazine (DEC), albendazole or both was dis- tributed during annual mass drug administration programme, but still filarial cases exist.
The epidemiological and socioeconomic data col- lected from 30 villages of Chittoor district of Andhra Pradesh were used for case-control study during the year 2004 to 2007. The cases were diagnosed by using finger
prick method and identified as individuals infected with microfilaria (mf). For this, 20 μl of blood sample was collected randomly from individuals of selected house- holds in a village between 2000 and 2300 hrs. Approxi- mately, 200 blood smears were collected from each vil- lage and stained with JSB (Jaswant-Singh-Bhattacherji) stain and then checked for microfilaria (mf) under micro- scope. During the study period, 77 positive cases were found from the study area. A case-controlled study was carried out with 77 infected persons comprising 40 males and 37 females. Similarly, controls of same age and sex corresponding to positive cases were selected from 30 villages of Chittoor district. The controls were carefully selected individuals with no history of either acute or chronic filariasis symptoms.
Apart from epidemiological survey, data on demo- graphic and socioeconomic aspects were also collected from each respondent through structured questionnaire.
The information on family characteristics with a possible influence on filariasis occurrence like sex, age, use of mosquito avoidance measures, number of children in a family, place of residence, monthly income, house struc- ture, education and occupation details, awareness on fi- lariasis, vector breeding habitats and participation in MDA were collected by interviewing each head of the family or from another member of the family. In this case-con- trol study, we compared demographic and health infor-
Fig. 1: Map showing the study areas in Chittoor district of Andhra Pradesh, India.
mation of microfilaria case group with that of controls groups (Table 1).
Ethical issues: The study was approved by the Ethi- cal Committee which was constituted by CSIR-Indian Institute of Chemical Technology, affiliated to Ministry of Science and Technology, Govt. of India. This epide- miological survey was overall supervised by the con- cerned health officials of Chittoor district, Government of Andhra Pradesh. Besides this, written consent of each
individual (parents/guardians in case of minors) was also obtained, who participated in this survey.
Statistical analysis: The data was analyzed with SPSS version 15.0. The Pearson’s chi-square test was performed to determine significant association between socioeco- nomic variables and case-controls. Bivariate and multi- variate logistic regression was used to calculate odds ra- tio and their 95% confidence intervals (CI) to assess the association of the variable with filariasis. We used bi- variate analysis to identify predictors for filariasis before multivariate analysis. To know the risk factors of filari- asis such as occupation, education, house structure, breed- ing habitats, drainage system and respondents who par- ticipated in MDA programme, the data were subjected to multivariate analysis to assess possible predictor variables for disease occurrence. Principal component analysis (PCA) was carried out to estimate a relative household socioeconomic index from a combination of various so- cioeconomic factors and income. Level of significance was considered as 0.05.
Measurement of the socioeconomic index: Principal component analysis was done using SPSS Version 15.0 to estimate the socioeconomic index from a combination of household and asset variables18. The household socio- economic position was defined as the complex of social and economic factors that influences in what position in- dividuals and groups hold within the structure of soci- ety19. Socioeconomic and disease related information in- cludes occupation, age groups, education details, monthly income, house structures, drainage system, mosquito breeding habitats and participation in MDA programme.
Socioeconomic index was derived after performing the PCA by including all socioeconomic variables. Informa- tion on socioeconomic variables was used to generate eigen values (weights) by PCA using varimax rotation method;
the higher eigen value of a variable, means its stronger as- sociation with a high socioeconomic status20. The PCA analysis showed that the first five factors had shown 82%
of cumulative variance. These weights were used to create a socioeconomic index in the study area. Based on the weights the data were grouped according to socioeconomic status into three categories, low, medium and high.
RESULTS
During the survey 5133 blood samples were collected from 931 households, of which 77 (1.52%) sera samples were found to be positive for mf. For a case-controlled study (cases : controls; 1:1), equal number of non-infected respondents to that of mf positive cases were included as control. The details of various socioeconomic character-
Table 1. Demographic and socioeconomic characters of cases and controls
Variables/Categories Cases Controls χ2 p-value (n = 77) (n = 77)
Age/group (yr)
6–10 2 (2.6) 2 (2.6) 0 1
11–17 5 (6.5) 5 (6.5)
18–25 14 (18.2) 14 (18.2)
26–40 25 (32.5) 25 (32.5)
41–60 24 (31.2) 24 (31.2)
>61 7 (9.1) 7 (9.1)
Gender
Male 40 (51.9) 40 (51.9) 0 1
Female 37 (48.1) 37 (48.1)
Occupation
Agriculture 38 (49.4) 19 (24.7) 23.512 <0.001 Labourers 13 (16.9) 13 (16.9)
Business and employees 17 (22.1) 10 (13)
Others 9 (11.7) 35 (45.5)
Education
Undergraduate 58 (75.3) 44 (57.1) 5.691 0.017
Graduate 19 (24.7) 33 (42.9)
Income (`)
<1000 10 (13) 4 (5.2) 2.905 0.234
1000–3000 51 (66.2) 57 (74)
>3000 16 (20.8) 16 (20.8)
House structure
Hut 23 (29.9) 16 (20.8) 9.644 0.008
Tiled 30 (39) 18 (23.4)
RCC 24 (31.2) 43 (55.8)
Breeding habitats
Cess pit and cess pool 30 (39) 47 (61) 13.534 0.001 Open drainage 16 (20.8) 19 (24.7)
No, breeding habitats 31 (40.3) 11 (14.3) Drainage system
Kutcha 35 (45.5) 20 (26) 6.364 0.012
Pucca 42 (54.5) 57 (74)
Mosquito avoidance
Yes 28 (36.4) 37 (48.1) 2.156 0.142
No 49 (63.6) 40 (51.9)
Participation in MDA programme
Yes 26 (33.8) 11 (14.3) 8.004 0.005
No 51 (66.2) 66 (85.7)
Filaria awareness
Yes 29 (37.7) 37 (48.1) 1.697 0.193
No 48 (62.3) 40 (51.9)
Figures in parentheses indicate percentages.
istics of both the cases and control respondents are given in Table 1. The disease rate was high among 26 to 40 and 41–60 yr age group. While, comparing the rate of filari- asis among male and female respondents, it was found that, higher numbers of cases were reported in males than in female respondents, although the difference was not statistically significant. Analyses of the socioeconomic data of the respondents, revealed that the disease preva- lence is strongly associated with the nature of occupation (p = 0.001), education (p = 0.017), type of house struc- ture (p = 0.008), breeding habitats (p = 0.001), drainage system (p = 0.012) and participation in MDA programme (p = 0.005) (Table 1).
Socioeconomic index
The number of factors which showed eigen values
>1 were identified and used in this study. The I principal component factor showed an eigen value of 2.150 and accounted for 23.885% variance, followed by II factor:
1.624 (18.040% variance), III factor: 1.398 (15.532% vari- ance), IV factor: 1.247 (13.854% variance), and V factor: 1.047 (11.633% variance). The five factors con- tributed nearly 83% of total variance of the variables in- cluded in the PCA (Table 2). The socioeconomic vari- ables strongly associated with filariasis in I factor were education, house structure and drainage; whereas in II factor the variables were mosquito avoidance and breed- ing habitats; in III factor, participation in MDA programmes; in IV factor, filariasis awareness and mos- quito avoidance; and while in V factor, income was found to be strongly associated with filariasis (Table 3). For fur- ther analysis, the socioeconomic scores were classified in three categories: low, medium and high. The socio- economic index (Table 4) showed that the majority of the filarial cases were reported among the low (n=32, 41%) and medium socioeconomic groups (n=26, 33.8%), when compared with high socioeconomic group (n=19, 24.7%),
Table 2. Eigen values of various socioeconomic factors analysed through principal component analysis
Component Eigen values % of variance Cumulative %
Factor-I 2.150 23.885 23.885
Factor-II 1.624 18.040 41.924
Factor-III 1.398 15.532 57.457
Factor-IV 1.247 13.854 71.311
Factor-V 1.047 11.633 82.944
Factor-VI 0.629 6.984 89.928
Factor-VII 0.462 5.132 95.060
Factor-VIII 0.298 3.316 98.376
Factor-IX 0.146 1.624 100
Table 3. Varimax rotation component matrix of socioeconomic variables analysed principal component analysis Characteristics Principal components
I II III IV V
Occupation 0.072 0.202 – 0.138 – 0.170 – 0.877 Education 0.507 – 0.188 – 0.708 0.097 0.172 House structure 0.897 – 0.112 – 0.025 0.105 – 0.012
Income 0.241 0.448 – 0.194 – 0.178 0.628
Breeding habits 0.023 0.867 0.059 – 0.136 – 0.117
Drainage 0.862 0.325 0.131 0.155 0.050
Mosquito avoidance 0.037 0.614 0.102 0.615 0.169 Filariasis awareness 0.009 – 0.165 – 0.089 0.889 0.014 Participation in MDA 0.255 – 0.024 0.910 – 0.007 0.137
programme
Table 4. Filariasis incidence in different socioeconomic groups of Chittoor district, Andhra Pradesh
Index Cases Controls χ2 p-value
Low 32 (41.6) 19 (24.7) 6.627 0.036
Medium 26 (33.8) 26 (33.8)
High 19 (24.7) 32 (41.6)
Figures in parentheses indicate percentages.
and the distribution among the socioeconomic groups was statistically significant (p=0.036).
Risk factors for prevalence of filariasis
In bivariate analysis, factors like no breeding habi- tats in and around the house (OR 4.279, p = 0.001), kutcha drainage system (OR 2.375, p = 0.012), hut structured house (OR 2.576, p = 0.022) and tiled house structures (OR 2.375, p = 0.005) showed statistically significant risk for filariasis (Table 5).
As bivariate analysis did not reveal much satisfac- tory information on the type of risk factors associated with filariasis occurrence, we carried out multivariate analysis to find out the predictors of filariasis by adjust- ing other socioeconomic factors (Table 6). The middle level income [category (`1000–3000), (OR=3.079, p=0.067)] and the presence of kutcha drainage system (OR=19.427, p=0.002) were found as significant risk fac- tors for filariasis. The respondents living in tiled house structure (OR=1.641) were observed as prevalent for filariasis diseases (Table 6). The factors like tiled houses and kutcha drainage system persisted even after adjusting the various socioeconomic variables in multi- variate analysis. Besides these, the study also revealed that mosquito avoidance measures (OR=1.042), disease awareness (OR=1.737) are prevalent risk factors for filariasis (Table 6).
this region, even after implementation of drug administra- tion programmes. Hence, it was assumed that, occurrence of filariasis in this region might be due to many intrinsic factors like lack of disease awareness, non-implementation of mosquito avoidance measures, low income, ample vec- tor breeding habitats and non-participation in mass drug administration. Hence, a cross-sectional study was under- taken to understand the influence of these socioeconomic factors on filariasis and its prevalence in the region.
Table 5. Bivariable analysis of association between socioeconomic conditions and filaria risk in Chittoor district of Andhra Pradesh Variables/Categories Bivariate analysis p-value
OR (95% CI) Age group (yr)
≤ 25 Reference
26–40 1 (0.440–2.272) 1
41–60 1 (0.437–2.289) 1
≥ 61 1 (0.298–3.353) 1
Gender
Male Reference
Flemale 1.053 (0.560–1.983) 0.872
Occupation
Agriculture 1.176 (0.452–3.059) 0.739
Labourers 0.588 (0.197–1.760) 0.343
Others 0.151 (0.052–0.441) 0.001*
Business and employee Reference Education
Undergraduates 2.289 (1.152–4.551) 0.018*
Graduate Reference
Income (`)
<1000 2.50 (0.648–9.651) 0.184
1000–3000 0.895 (0.406–1.970) 0.782
>3000 Reference
House structure
Hut 2.576 (1.145–5.791) 0.022*
Tiled 2.986 (1.384–6.441) 0.005*
RCC Reference
Breeding habitats
Cess pit 0.759 (0.175–3.297) 0.713
No breeding habitats 4.279 (1.844–9.934) 0.001*
Open drainage 1.279 (0.561–2.914) 0.558
Cess pool Reference
Drainage system
Kutcha 2.375 (1.205–4.682) 0.012*
Pucca Reference
Mosquito avoidance
Yes Reference
No 1.619 (0.850–3.084) 0.143
Participation in MDA programme
Yes Reference
No 0.327 (0.148–0.723) 0.006*
Filariasis awareness
Yes Reference
No 1.531 (0.806–2.910) 0.194
*p<0.05.
Table 6. Multivariate analysis of association between socioeconomic conditions and filaria risk in Chittoor
district of Andhra Pradesh
Variables/Categories Multivariate analysis p-value OR (95% CI)
Age group (yr)
≤ 25 Reference
≥ 26 0.521 (0.198–1.371) 0.187
Gender
Male Reference
Female 0.799 (0.340–1.877) 0.606
Occupation
Agriculture 0.583 (0.077–4.406) 0.601
Labourers 0.245 (0.026–2.329) 0.221
Others 0.100 (0.013–0.0780) 0.028
Business and employee Reference Education
Undergraduates 0.766 (0.123–4.763) 0.775
Graduate Reference
Income (`)
<1000 2.752 (0.435–17.429) 0.282
1000–3000 3.079 (0.923–10.275) 0.067
>3000 Reference
House structure
Hut 0.677 (0.156–2.946) 0.603
Tiled 1.641 (0.534–5.048) 0.387
RCC Reference
Breeding habitats
Cess pit and Cess pool 0.111 (0.021–0.586) 0.010 No breeding habitats 1.718 (0.267–11.039) 0.569
Open drainage Reference
Drainage system
Kutcha 19.427 (2.985–126.410) 0.002
Pucca Reference
Mosquito avoidance
Yes Reference
No 1.737 (0.563–5.358) 0.336
Participated in MDA programme
Yes Reference No
0.107 (0.021–0.542) 0.007
Filariasis awareness
Yes Reference
No 1.042 (0.368–2.956) 0.938
DISCUSSION & CONCLUSION
Based on the reports of health department, Govt. of Andhra Pradesh it is understood that, Chittoor district is covered under mass drug administration of diethylcar- bamazine (DEC) (6 mg/kg body weight), albendazole (400 mg) or both due to high endemicity of filariasis. The results from our study indicate that filariasis is endemic in
To identify socioeconomic risk factors for filariasis a case-control study was carried out by considering MF positive samples as case group and samples negative for mf as control group. Higher numbers of mf cases were found in males than in females particularly in the age groups of 26 to 40 followed by 41–60 yr. When age and genders were considered for determining the susceptibil- ity to filariasis, it was observed that, these factors were not significantly associated with filariasis indicating that filariasis can occur to both genders irrespective of age.
Higher number of filarial cases was reported among the persons engaged in agriculture than in other occupations (e.g. labourers, business, employees etc.). This might be due to the reason that they spend more time in the fields and sometimes even sleep in the farming places, hence, have more chances of getting exposed to mosquito bites.
The results of the study showed that, majority of the fi- larial cases were found among the undergraduates popu- lace than the graduate respondents. Awareness about the disease and its management strategies has great impact on the overall reduction of disease. The populace having poor knowledge on disease and its management activi- ties is one of the risk factor for filariasis in rural areas of Andhra Pradesh9. Similar reports have been observed from Philippines and Tanzania21–22.
In income category, the high numbers of microfila- raemia cases were recorded in middle income (`1000 to 3000 per month) respondents as they generally spend more time in the agricultural fields due to their occupation and hence have high chance of exposure to infected mosqui- toes. From the study, it was found that the type of house structure was significantly associated (p=0.008) with the prevalence of filariasis. Higher number of microfilaraemia cases was recorded from tiled house than the hut and re- inforced cement concrete (RCC) houses. The mosquito breeding habitats were found to be significantly associ- ated with filarial cases (p=0.001). The breeding habitats like cess pit, cess pool and open drainage help to increase the vector density and there is a higher risk of transmis- sion of filariasis. Similar type of reports suggests that cesspit and cess pools favour proliferation of the filari- asis vector Culex quinquefasciatus23.
In filaria endemic regions, lack of awareness about disease and non-participation in mass drug administra- tion programs could enhance transmission of the disease.
Awareness on preventive measures to avoid mosquito bites promotes use of bed nets, repellents, coils, etc. In Tamil Nadu, south India only ~20% of people know that filariasis is caused by mosquitoes24. In this study, it was observed that about 63.6% of the case respondents had not implemented any such control measures to avoid
mosquito bites which might be a major reason for high occurrence of filariasis among them. Higher number of filaria infections was observed among the case respon- dents who were not aware about filariasis (62.3%) and those who did not participated in MDA programmes (66.2%; p=0.005).
Although, lymphatic filariasis is not a fatal disease, the development of lymphoedema of lower limb in both men and woman and hydrocele in men is a burden to the infected patients. Patients with chronic manifesta- tions of filariasis often confine them to their homes, which subsequently leads to loss of work and income and in turn they become burden to their families. Such types of patients become carriers for further transmission of disease within the family as well as to those living nearby.
Analysis of various socioeconomic parameters on occurrence of filariasis indicated that, the disease preva- lence was higher among the respondents with low-socio- economic status and educational background, who gen- erally resides near mosquito breeding habitats like cess pit and cess pools which are important risk factors. Apart from these, lesser or no implementation of mosquito avoidance measures as well as not participating in the regular MDA programmes increase the chance of occur- rence of filariasis in the endemic area of Chittoor district of Andhra Pradesh. Hence, it is essential to uplift the so- cioeconomic conditions by providing better facilities like clean environment, alternate income sources, affordable education and frequent visits of health officials to moni- tor the disease transmission which might be helpful in reducing the filariasis burden in endemic areas.
ACKNOWLEDGEMENTS
The authors are grateful to the Director, Indian Insti- tute of Chemical Technology (CSIR) for his encourage- ment and support. The authors are thankful to Ministry of Communication and Information Technology (MC &
IT), Govt. of India for sponsoring the project.
Conflict of interest
The authors declare no conflict of interest.
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Correspondence to: Dr U. Suryanarayana Murty, Chief Scientist, Head, Biology Division, Indian Institute of Chemical Technology (CSIR), Tarnaka, Hyderabad–500 007, Andhra Pradesh, India.
E-mail: murty_usn@yahoo.com
Received: 10 March 2016 Accepted in revised form: 28 June 2016
