Seropositivity of Leptospiral Antibodies and Associated Factors of Leptospirosis in Children at Thaketa Township, Yangon Region

Abstract

Leptospirosis is a neglected zoonotic disease which is considered to be overlooked and under-reported in developing countries. Children, especially school-aged, are known as a risk group for leptospiral infection. Thaketa Township is located near the Bago river and the Pazundaung creek flows through the township. The higher water level during high tide and heavy rainfall, together with poor capacity of drainage system can lead to frequent inundation in some areas of the township increasing the risk of leptospirosis. The problem of leptospiral infection in children in the community is undocumented. This study aimed to detect the estimated prevalence and associated factors of leptospirosis in children at Thaketa Township. It was a cross-sectional study, conducted during the period from September to first week of October, 2019. The study included 409 children (5-16 years old) from 10 selected wards of Thaketa Township. Stratified cluster sampling was used to recruit the children and wards will be regarded as the clusters. Household surveys were conducted and face to face interview to the caregivers and observation of the household environment were done. Leptospiral IgM and IgG were tested on the serum of all children by Enzyme Linked Immunosorbent Assay (ELISA). Seropositivity of leptospiral infection (IgM and/or IgG positivity) was found in 115 children (28.1%, 95% CI: 23.8-32.7). Positive leptospiral IgM antibody was detected in 72 children (17.6%, 95% CI:14.0-21.6) and IgG antibody in 58 children (14.2%, 95% CI: 10.9-17.9). Recent leptospiral infection (positive IgM antibody) was independently associated with female sex (OR 2.8, 95%CI: 1.6-4.8, p <0.001), adolescent age (>10 year) (OR 1.8, 95%CI: 1.1-3.0, p = 0.03), and presence of backyard chickens (OR 2.8, 95%CI: 1.3-6.4, p =0.01). This study highlights that there is a need for a good awareness of leptospirosis and health care providers should consider it as a differential diagnosis in febrile children residing in similar at-risk areas like Thaketa township. It is also important to emphasize on the preventive and control measures of leptospirosis in the community by multidisciplinary approach in One Health perspective.

Introduction

Leptospirosis is a zoonotic disease which is predominantly distributed in tropical regions¹. It is caused by spirochaetes from the genus Leptospira, which has more than 300 serovars³³. According to the report of World Health Organization (WHO) Leptospirosis Epidemiology Reference Group (LERG) in 2015, the annual incidence of this disease is estimated to be 1.03 million cases worldwide². In a study conducted in Karen, Mon, Thai and Bamar subjects from Thailand–Myanmar border, leptospirosis was the second most frequent cause of fever, 17% of 613 adults with febrile illness, in that region³. A study on serum samples from suspected leptospiral cases received at National Health Laboratory, Yangon in 2009 showed 43% of samples were positive for leptospiral IgM⁴. The disease can still be overlooked and underreported in Myanmar because the true incidence of Leptospirosis in human may be much higher than the reported cases; low awareness of the disease, lack of surveillance systems, difficulty in distinguishing clinical signs from those of other diseases and lack of appropriate diagnostic laboratory services are the reasons which can lead to underreporting of the disease^1,5.

A recent study in Myanmar agriculture and sewage workers described that 8.8% of them in North Okkalapa Township in Yangon region and 4.4% of them in Pathein Township in Irrawady region were seropositive for leptospiral IgG⁶. Although leptospirosis is considered as an occupational type disease, any person living in a contaminated environment can be susceptible to the disease⁷. Rodents, livestock and dogs are the main animal reservoirs that excrete the leptospira bacteria in their urine. The excreted leptospira can live in fresh water, damp soil, vegetable and mud for a long time⁸. According to the study from National Health Laboratory in Yangon, leptospiral seropositive cases were detected peaked in July, August and September^4. In the presence of strong rains and floods, human infection can be facilitated in the environment where there is contamination with the urine of infected animals⁹; the organism usually enters the human body via cuts and abrasions in the skin ¹⁰^. Children are known as a risk group for leptospiral infection because of their close contact with the pets and habit of walking or playing bare foot in the puddles of stagnant waters.⁸ Among leptospiral IgM ELISA positive samples detected at National Health Laboratory, 10-19 years age group accounted for the highest detection rate, 26%, and 0-9 years age group accounted for 15% of the seropositivity⁴. School-going age was previously reported as a risk factor for acquiring leptospirosis in children¹⁴.

In clinical settings, diagnosis of leptospirosis is not often made unless the febrile patient presents with textbook manifestations of Weil’s disease, such as jaundice, renal failure and pulmonary haemorrhage ¹¹. However, the clinical behavior of Leptospirosis had a variety of presentations and it is often difficult to differentiate this infection from other febrile illnesses such as dengue, typhoid, malaria or influenza ¹². Misdiagnosis can be a matter in Myanmar where these infections are endemic; the problem of leptospiral infection in children in the community is absolutely unknown and there is no documented evidence on its incidence or prevalence.

Leptospirosis is reported to be associated with household environmental risk factors such as residence in flood-risk regions with open sewers and proximity to accumulated refuse and rat sightings ¹³. Inadequate garbage management system and water drainage problem in sub-urban townships of Yangon region can create favorable conditions for animal carriers like peri-domestic rodents, which may lead a health risk for leptospirosis in people living there. Thaketa Township is located near the Bago river and the Pazundaung creek flows through the township. The higher water level during high tide and heavy rainfall together with poor capacity of drainage system can lead to frequent flood inundation in some areas of the township. This study aims to detect the estimated prevalence and associated factors of leptospirosis in children at Thaketa Township.

Materials and Methods

It was a cross-sectional analytic study conducted on school-aged children (5-16 years old), residing at Thaketa township. Stratified cluster sampling was used to recruit the children and wards were regarded as the clusters. Firstly, 10 out of 19 wards in Tharketa township were randomly selected after considering two strata of wards, near the river creek and away from the river creek. Therefore, 5 wards near the river/creek (10 North, 10 South, 9, Shu Khin Thar and Setmhu Letmhu wards) and 5 wards away from the river/creek (4 South, 2 South, 3 Yanpyae, Anawmar, 6 wards) were chosen. In each selected ward, at least 40 households were convinently selected from a list of households from the ward administrative office. A total of 409 children were included in the study.

Household survey was conducted for data collection. The caregivers of the selected children were informed about the objective and procedure of the study and signed consent was asked to let their children participate in the study. Assent was taken from children older than 10 years old. Face to face interview to the caregivers according to the questionnaire and observation of the houshold environment were done.

One ml of blood was taken from each child who agreed to participate in the study. ELISA tests for leptospiral IgM and Ig G will be done at Experimental Medicine Research Division, Department of Medical Research by using AccuDiag^TM Leptospira IgM (Sensitivity: 100%, Specificity: 100%) and Ig G ELISA Kits (Sensitivity: 80%, Specificity: 87.5%) (Diagnostic Automation/ Cortez Diagnostics, Inc. USA). The test procedures were done according to the instructions in the ELISA kits. Test results were interpreted as positive if the OD value is >0.5 Units.

The data was subjected to statistical analysis using the SPSS 22 software package. Data was evaluated using descriptive statistics (mean and standard deviation, frequency and percentages as appropriate). Comparison between the proportion of children with and without IgM seropositivity was performed by means of chi-squared test or Fisher’s exact test. The level of significance was set at p ≤ 0.05. Association between IgM leptospiral seropositivity and independent variables was analyzed by logistic regression analysis.

Results

Mean age of children was 9.7 ± 2.6 years. Boys accounted for 53.1% (217/409) and girls for 46.9% (192/409). Seropositivity of leptospiral infection (IgM and/or IgG positivity) was found in 115 children (28.1%, 95% CI: 23.8-32.7). Positive leptospiral IgM antibody was detected in 72 children (17.6%, 95% CI:14.0-21.6) and IgG antibody in 58 children (14.2%, 95% CI: 10.9-17.9). Only 15 (3.7%) had both IgM and IgG positivity.

Fig 1. Seropositivity of Leptospirosis in the selected wards of Thaketa township

Satmhu Letmhu, 4 South, 3 Yanpyae and Anawmar wards have highest leptospiral seropositivity with at least 40% and 10 South ward has lowest leptospiral seropositivity (7.1%).

Fig 2. Environmental and Ecological Characteristics of children in the study

Majority of housesholds, 66%, in the study used tube well water and 3.2% of households used lake water for domestic purpose. More than half, 55.5%, of children had habit of bare-foot walking. Flood on the streets was reported in 52.3% and flood inside house was reported in 40.3%. Rodents were noticed in 83.4% of houses (Fig 2).

Table (1). Factors associated with Recent Leptospiral Infection

Age >10 years, female and having chickens in backyards were independently associated with IgM seropositivity.

Discussion

Myanmar is one of the regions in South East Asia, where there is very limited data for leptospirosis in human. This study fills the knowledge gap on epidemiology of leptospirosis in children at a suburban area of Yangon region.

A previous seroprevalence study conducted among healthy agricultural and sewage workers in North Okkalapa township, Yangon region and Pathein township, Ayeyarwaddy region showed the IgG seroprevalence of 8.8% and 4.4% respectively. The proprtion of IgG seropositivity in school age children in this study was higher than that of agricultural and sewage workers, which indicates that school age children in a sub-urban township, were frequently exposed to leptospirosis. High rates of seropositivity among healthy children in urban poor community in Malaysia was previously reported; 15.4% IgM positivity among under 12 years age group (n=13) and 13.3% IgG positivity with 40% IgM positivity among 13-17 years age group (n=15). The proportion of IgG positivity in this study was also slightly higher and comparable to 12.8% (n=963) IgG seroprevalence of 7-14 years old Vietnamese children ^14.

In this study, the proportion of recent leptospiral infections (positive IgM) was slightly higher than those of past infection (positive IgG alone), 17.6% vs 14.2%. One of the reasons may be due to the time of sample collection, September to early October, which was purposively chosen to meet higher number of recent infections based on the report of National Health laboratory, which described that IgM seroprevalence in suspected leptospirosis cases were highest in July, August and September. Since the majority of IgM seropositive cases in this study had negative IgG antibody, these children seemed to have recent primary infection. However, the response upon reinfections such as augmented IgM production by repeated infection and declining IgG antibody may mimic the seroconversion of primary infection. Antibody response in leptospirosis was suggested to be different from classical IgM and IgG pattern of other human infections. It was reported that all patients develop IgM antibodies after leptospiral infection and persist in blood for about 6 months or longer ¹⁵. On the other hand, IgG levels were reported to be variable from non-detectable or positive for a short time or several years³⁰. According to some studies, 10-12.5% of patients do not develop IgG antibody after infection ^15,16..

In this study, both of children who had jaundice within the previous 6 months had positive leptospiral IgM. However, any signs and symptoms suggestive of leptospirosis were not associated with IgM seropositivity. Inability to distinguish the mild and subclinical case of leptospirosis from other endemic febrile diseases and inadequate laboratory facility can lead to underestimation of the burden of leptospirosis.

In Myanmar, only 60 cases of leptospirosis were reported in 2017. Seroprevalence of leptospirosis in chidren at Thaketa township in this study was 28%; however, no child with positive serology had been diagnosed as leptospirosis by a doctor. It reflects that awareness and suspicion for leptospirosis is low among healthcare providers. In an endemic country like Myanmar, it is important to have suspicion of leptospirosis in patients with febrile illness because early antibiotic therapy is associated with lower risk of severe disease ³⁷. However, inappropriate dispensing of antibiotics by some drug retailers without prescription or irrational prescription of antibiotics in cases of fever by some clinicians might be a factor which mask the clinical leptospirosis cases. The inconsistency between the high seroprevalence and low report of morbidity was also found in Thailand; the reported morbidity of leptospirosis in some regions was less than 3 cases per 100,000 person-years although the seroprevalence of leptospiral antibody in the population was more than 40% ³⁶. A survey in Brazil estimated that only 1 out of 191 leptospiral infections lead to clinical leptospirosis ¹⁷. Further research are needed to determine whether repeated leptospiral infections by non-virulent strains can produce protective immunity against virulent strains as in vaccination or repeated infections can cause immune enhancement leading more severe disease ¹⁴.

Many studies described that male were prone to have leptospiral infection because of their occupation ^18-21. Thai et al reported that seroprevalence among boys was higher than that of girls in a rural region of Vietnam. They suggested that boys may have higher exposure of leptospiral infection because they help in agricultural work of fathers ¹⁴. Contrast to these findings, girls were independently associated with leptospirosis in this study. Girls, who used to help household work in the environment with poor sanitation may prone to contact more leptospiral infection. There are also some studies in adults which reported the significant association between female sex and leptospirosis ^21-24. Some studies suggested that seroprevalence rates in man and women also depend on the specific leptospiral serovars ^25,26 the fact that this study could not assessed.

In this study, older children, who were adolescents, are also independently associated with leptospirosis. In the serum samples of febrile patients tested in NHL, adolescents group had the highest detection rate for leptospiral IgM. This finding agreed with Thai et al which showed that the seroprevalence of leptospirosis significantly increased with 1.47% per year in children¹⁵. The continuous exposure of the bacteria in the endemic region may lead to age dependent increase in leptospiral seropositivity²⁷.

Infected peridomestic animals are a well-known source of leptospiral transmission to human. Having backyard chickens was independently associated with IgM seropositivity. The spread of chicken feeds around the house may attract the more rodents and might lead the environment loading with leptospiral bacteria. Although more than 80% of the children in this study reported that they saw rodents in their houses, the questionnaire could not assess the quantity of rodents in each house. There was no association between leptospiral antibody and having cats, dogs, rodents and pigs at domestic area in this study, which was concordant with Thai et al study. However, it was discordant with Espinosa et al study, in which allowing dogs inside the house was associated with Leptospira in blood ²⁸. Absence of the association between the pets and leptospirosis in this study may be the low sensitivity of the questionnaire which could not determine the intimacy between children and their pets.

In this study, the factors associated with recent leptospiral infection (positive IgM) were determined instead of total seropositivity because the sensitivity and specificity of IgM ELISA were significantly better than that of IgG assays ²⁹. In ELISA test, IgM has low affinity and IgG has high affinity to be captured by antigens ³⁰. Therefore, non-specific IgG can be reflected as a false positive result, which is not shown for non-specific IgM. Therefore, non-specific IgG in other febrile illnesses such as Epstein-Barr virus infection, viral hepatitis, and cytomegalovirus infection may cause false positive result for leptospiral IgG antibody ³². One of the limitations of this study was that these infections could not be excluded in the serum of children and leptospirosis could not be confirmed by gold standard Microscopic agglutination test (MAT).

The ELISA kit used in this study is based on Leptospira biflexa antigen, which detects antibodies against a wide range of virulent leptospires ¹⁵. However, it can also detect low pathogenic leptospires because there can be cross-reactions between different leptospiral serovars. In Myanmar, serovar pomona, icterohaemorrhagiae, grippotyphosa and sejroe were reported to be deteted in urine cultures of cattles ³¹. Serogroups maintained by the animal population in a region usually reflect the human leptospiral infections ^34,35. Local serovars of endemic leptospiral strain are needed to know for vaccine development for that region because current bacterin vaccines elicit immunity restricted to serovars with related agglutinating LPS antigens. Studies should be conducted to find out the currently circulating leptospiral serovars in both human and animals in Myanmar.

In this study, many children from squatters living in unhygienic places were involved. Overcrowding, poverty, poor sanitation and inadequate waste management in people especially among squatters might contribute the high seroprevalence of leptospirosis in some wards of this township. Flood inside house was reported in 40.3% and flood on street was reported in 52.3%, which reflect the need for proper drainage system in this township. More than 80% of houses in the study reported to have rodents, indicating the need for improved garbage management system and rodent control measures in the community.

Conclusion

This study highlights a need for awareness of leptospirosis in the community. Healthcare providers should consider leptospirosis as a differential diagnosis in febrile children residing in similar at-risk areas like Thaketa township. Health authorities should promote surveillance and facilities for case detection in both human and animal infections. As risk factors of leptospirosis include human, animal and environmental factors, it is important to emphasize on the preventive and control measures of leptospirosis in the community by multidisciplinary approach in One Health perspective.

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Author Information

Win Lai May¹, Aye Aye Win², Myo Myo Mon³, Nway Htike Maw⁴, Han Win⁵

MBBS, MMedSc (Paediatrics), PhD(Clinical Tropical Medicine), DipRMRE, Department of Medical Research
MBBS, MMedSc (Pathology), PhD(Pathology), Department of Medical Research
MBBS, MPH, PhD (Epidemiology), Department of Medical Research
MBBS, MMedSc (Physiology)
MBBS, MMedSc(Paediatrics), MRCPCH, Department of Paediatrics, University of Medicine 2