Risk factors for acute scrub typhus infection among housewives – A subgroup analysis of pooled community-based serosurvey in Gorakhpur, India

Sir,

Scrub typhus is an acute febrile illness caused by Orientia tsutsugamushi and is commonly reported as the causative aetiology among febrile hospitalized patients from different parts of India. Acute meningoencephalitis is one of the complications associated with scrub typhus1. There is well documented evidence of scrub typhus aetiology in acute encephalitis syndrome (AES) cases reported from Gorakhpur district, Uttar Pradesh, occurring predominantly during the monsoon season as an endemic disease in all age groups, with mortality being observed primarily in the paediatric population2.

The previous community serosurveys conducted by our group during both lean (April-May 2016: Phase 1) and epidemic periods (October-November 2016: Phase 2) of AES outbreaks in Gorakhpur revealed O. tsutsugamushi seroprevalence ranging from 50.6 to 70.8 per cent for IgG and 3.4 to 4.4 per cent for IgM antibodies, respectively2. These individual serosurveys identified the risk factors associated with IgG-positive cases (endemic infection). Identification of risk factors for community-based acute scrub typhus cases will be helpful to identify individuals who are likely to progress or manifest with complications3 and plan appropriate preventive strategies. The present subgroup analysis was thus carried out with the objective of determining the risk factors associated with acute scrub typhus cases by pooling data of IgM-positive cases from both the serosurveys.

This study was carried by the division of Epidemiology & division of Microbiology, ICMR-National AIDS Research Institute, Pune, Maharashtra, India, after approval from the Institutes Ethics Committee. A written informed consent was taken from all the study participants.

Detailed methodology of the serosurvey is described previously2. Except for the timing of the surveys, the methodology and sampling techniques used were similar in both the surveys. These surveys were conducted across different villages of Gorakhpur district reporting recent AES cases with an undiagnosed aetiology. A total of 1991 individuals participated in these surveys (1085 in Phase 1 and 906 in Phase 2). The two datasets were pooled together with an additional indicator variable as Phase (i.e. Phase 1 for lean period and Phase 2 for epidemic period) as shown in Figure A and B.

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Figure

(A) Bar graph showing data structure and socioeconomic characteristics of acute scrub typhus cases (IgM-positive) in pooled data. Numbers on the bars represent population size. (B) Representation of pooled data and subgroup of housewives.

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Data analysis was carried out using SPSS 15.0 (IBM Corp, Armonk, NY, USA). The sociodemographic composition of the population during both phases of the survey was similar with regard to age (P=0.35), gender (P=0.37) and literacy (P=0.13).

Acute scrub typhus cases were estimated from the pooled data and the risk factors were analyzed. Thus, a total of 84 [Phase 1=44 (4.1%) and Phase 2=40 (4.4%)] acute scrub typhus cases were available for analysis. A case-control analysis was carried out after associated risk factors were identified through univariable analysis of pooled data.

The overall IgM positivity or acute scrub typhus cases in the pooled data was 4.2 per cent (84/1991). Of these, 32.1 per cent were in the age group of 6-15 yr, 24.4 per cent in 16-25 yr and 46.4 per cent were 25 yr and above. Of the 84 cases, 51 (60.7%) were females, 53 (66.3%) were literate and 27 (32.5%) were housewives. Logistic regression showed that housewives [odds ratio (OR): 1.90, 95% confidence interval (CI): (1.052, 3.437), P=0.033] and older people [OR: 1.014, 95% CI: (1.001, 1.027), P=0.037] were significantly associated with acute scrub typhus infection.

During both the surveys, IgG antibody positivity was significantly higher among women (lean period 61%; epidemic period 78%), especially housewives (lean period 74%; epidemic period 89%). There is evidence with regard to the development of autoimmune disorders among females after three years of scrub typhus infection3. It was observed that being housewife was significantly associated with acute scrub typhus infection. Housewife is defined as a female, ‘who did not work at a job or business’ and that they were ‘taking care of house or family’4. To determine whether any targeted intervention/prevention could be advocated for housewives, we further explored the risk factors among them by case-control analysis. A subgroup analysis for housewives with age-matched controls using conditional logistic regression model was therefore conducted, where cases (n=27) and controls (n=108) were selected in 1:4 ratio. IgM-positive housewives in both the surveys were considered as cases and IgM-negative as controls. Sociodemographic variables (literacy, occupation), socioeconomic variables (house type, source of drinking water, toilet facility and presence of cattle shed near to home) and hygiene characteristics (wearing shoes during outdoor activity, taking bath after work, daily bathing with soap, changing clothes daily, head and body louse infestation and contact with bushes) were included in the subgroup analysis.

The scrub typhus IgG antibody positivity among both cases and controls was comparable (14.8 vs. 11.1%, P=0.69). The subgroup case-control analysis among housewives revealed that not changing clothes daily [OR: 6.2, 95% CI (2.07, 18.50), P=0.001] was the only factor that was significantly associated with acute infection among them.

Although risk factors associated with scrub typhus have been reported previously, majority of the studies were hospital-based1,5. However, the scenario of acute scrub typhus infection at the community level is largely not understood. Our earlier study highlighted that majority of the scrub typhus cases went undetected in the community (54%)2. This subgroup analysis was attempted to assess the predictors of acute scrub typhus infection from community-based settings. Two community-based serosurveys were conducted covering around 2000 participants; however, number of cases with acute infection in each survey was not adequate to determine the associated risk factors. The development of AES as a consequence of scrub typhus may be a tip of an iceberg, and therefore, acute infections at the grass-root level need to be studied further. Identification of risk factors for acute cases will be helpful for primary physicians to identify cases who are likely to progress or manifest with complications3.

We identified being housewife and older age group as the risk factors associated with acute scrub typhus infection. These factors were also associated with IgG positivity as determined by us previously2.

In our analysis, not changing clothes daily was the significant risk factor associated with acute infection among housewives. Scrub typhus is an arthropod borne infection transmitted through larval stage of trombiculid mites of the genus Leptotrombidium. These larvae commonly referred as chiggers attach to the clothes and subsequently infect the human host, especially if they do not change their clothes once they return from work6-9. Housewives remain involved in various activities, which could lead to exposure to scrub typhus infection such as animal rearing and kitchen gardening. However, changing clothes after work might not be a practice followed by them as they are staying in house throughout the day, compared to other household members involved in occupations with outdoor travel. It is well documented that the squatting position adopted by women while working on the farm, cooking in courtyard and defecating in the bushes expose them to potential scrub typhus infection7. Although not changing clothes daily was observed as an associated risk factor for IgM positivity among housewives, it has its strong roots pertaining to social issues such as gender inequality, position of women in households and poverty which needs women’s empowerment. Furthermore, in rural areas, open air defecation in bushes is common, due to inadequate access of sanitary latrine facility exposing them to risk of acquiring infection10. Lack of hygiene while performing these activities make them more susceptible for acute rickettsial infection2,5.

Our analysis had several limitations such as the findings were based on data collected in the year 2016-2017. Occurrence scrub typhus cases increased in the following years11. Although there are improvements in socioeconomic parameters in the last five years in terms of poverty reduction, improvement in sanitation and access to safe drinking water across the State of Uttar Pradesh, in Gorakhpur district, the situation remained suboptimal as far as the attainment of Sustainable Development Goals (SDGs) were concerned against district targets and also in comparison with the other districts12. Thus, regular surveillance for scrub typhus in the district of Gorakhpur is necessary to understand the trend of infection and potential risk factors to plan appropriate preventive strategies.

In conclusion, through this subgroup analysis based on the pooled data, we have identified the risk factors associated with acute IgM positivity in community setting, which may help identify acute scrub typhus cases who are likely to progress or manifest with complications3. Preventing the transmission of various diseases is one of the sustainable development goals (SDG 3.3). Awareness programme among housewives who could be at risk of acquiring scrub typhus infection can be arranged with the help of accredited social health activists (ASHA) workers, peer educators and self-help groups. Improvement in sanitation, socioeconomic conditions and women empowerment remain as key factors for prevention of O. tsutsugamushi infection.