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      Assessing the Increase of Snakebite Incidence in Relationship to Flooding Events

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          Snakebite envenoming causes up to 138,000 deaths and 400,000 permanently disabled victims worldwide every year. Flooding is one of the many factors that seems to influence the incidence of snakebite. The catastrophic floods from late 2018 in Kerala (India) were widely broadcast and are an example of how flooding events are related to the increased incidence of snakebite. This relationship has been mentioned regularly in scientific and grey literature, but usually quite scarcely in comparison to other topics linked to snakebite. Additionally, web media, mobile communications, and social media have started playing an important role not only in providing access to information on flooding-related snakebite events, but also in snakebite prevention at a larger scale. In order to better understand to what extent the relationship between snakebite incidence and flooding is reported and quantified and appraise the importance of mobile communications and social media in snakebite prevention and management, we performed multiple searches in generic (Google) and specialized (PubMed, Web of Science, Google Scholar) databases. We retrieved 68 scientific articles and 5 reports ranging from 1892 to 2018 mentioning or analyzing flooding and the increased incidence of snakebite. Additionally, we found 68 web media reports linking flooding and snakebite. This review indicates that the increase of snakebite incidence due to flooding has been repeatedly observed all over the world. This phenomenon could be exacerbated because of climate change, which is expected to increase the overall magnitude and frequency of flooding. However, it could also be mitigated by the role the Internet, mobile communications, and social media could play in snakebite prevention and human and animal rescue strategies during flooding.

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          Snakebite envenoming

          Snakebite envenoming is a neglected tropical disease that kills >100,000 people and maims >400,000 people every year. Impoverished populations living in the rural tropics are particularly vulnerable; snakebite envenoming perpetuates the cycle of poverty. Snake venoms are complex mixtures of proteins that exert a wide range of toxic actions. The high variability in snake venom composition is responsible for the various clinical manifestations in envenomings, ranging from local tissue damage to potentially life-threatening systemic effects. Intravenous administration of antivenom is the only specific treatment to counteract envenoming. Analgesics, ventilator support, fluid therapy, haemodialysis and antibiotic therapy are also used. Novel therapeutic alternatives based on recombinant antibody technologies and new toxin inhibitors are being explored. Confronting snakebite envenoming at a global level demands the implementation of an integrated intervention strategy involving the WHO, the research community, antivenom manufacturers, regulatory agencies, national and regional health authorities, professional health organizations, international funding agencies, advocacy groups and civil society institutions.
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            Snakebite Mortality in India: A Nationally Representative Mortality Survey

            Introduction Alexander the Great invaded India in 326 BC, and was greatly impressed by the skill of Indian physicians; especially in the treatment of snakebites [1]. Since then, India has remained notorious for its venomous snakes and the effects of their bites. With its surrounding seas, India is inhabited by more than 60 species of venomous snakes – some of which are abundant and can cause severe envenoming [2]. Spectacled cobra (Naja naja), common krait (Bungarus caeruleus), saw-scaled viper (Echis carinatus) and Russell's viper (Daboia russelii) have long been recognised as the most important, but other species may cause fatal snakebites in particular areas, such as the central Asian cobra (Naja oxiana) in the far north-west, monocellate cobra (N. kaouthia) in the north-east, greater black krait (B. niger) in the far north-east, Wall's and Sind kraits (B. walli and B. sindanus) in the east and west and hump-nosed pit-viper (Hypnale hypnale) in the south-west coast and Western Ghats [2]. Joseph Fayrer of the Indian Medical Service first quantified human snakebite deaths in 1869 for about half of “British India” (including modern Pakistan, Bangladesh and Burma), finding that 11,416 people had died of snakebites [3]. Subsequent estimates of human deaths from snakebite prior to Indian Independence ranged from 7,400 to 20,000 per year [4]–[6]. Government of India hospitals from all but six states reported only 1,364 snakebite deaths in 2008 [7] but this is widely believed to be an under-report as many victims of snakebite choose village-based traditional therapists and most die outside government hospitals. Community-based surveys in some localities have shown much higher annual mortality rates, ranging widely from 16.4 deaths/100,000 in West Bengal [8] to 161/100,000 in the neighbouring Nepal Terai [9]. However, such focal data cannot be extrapolated to provide national or even state totals because of the heterogeneity of snakebite incidence. These uncertainties have resulted in indirect estimates of annual snakebite mortality in India that varied from approximately 1,300 to 50,000 [6], [7], [10]–[13]. To fill this gap in knowledge, we estimated snakebite deaths directly from a large continuing study of mortality in India. Methods Ethics Statement Ethics approval for the Million Deaths Study (MDS) was obtained from the Post Graduate Institute of Medical Research, St. John's Research Institute and St. Michael's Hospital, Toronto, Ontario, Canada [14]–[15]. Most deaths in rural India take place at home without prior attention by any qualified healthcare worker, so most causes are not medically certified [14]–[15]. Other approaches are therefore needed to help determine the probable causes of such deaths. The Registrar General of India (RGI) organises the Sample Registration System (SRS), which monitors all births and deaths in a nationally representative selection of 1.1 million homes throughout all 28 states and seven union territories of India. India was divided into approximately one million areas for the 1991 census, each with about 1,000 inhabitants. In 1993, the RGI randomly selected 6,671 of these areas to be represented in the SRS. Household characteristics were recorded and then enumerated twice yearly thereafter, documenting new births and deaths, but not the causes of death [16]. Since 2002, one of 800 non-medical field staff (trained by the RGI in appropriate fieldwork methods) visited each SRS area every six months to record a written narrative (in the local language) for each death from families or other reliable informants. In addition to the narratives, answers to standard questions about the deaths were also recorded in the field report. Fieldwork quality control methods were used routinely, including random re-sampling by teams reporting directly to the study investigators [14], [15]. This survey is part of the MDS, which seeks to assign causes to all deaths in SRS areas for the period between 2001–14 [14]–[16], [17]–[19]. These field reports, or ‘verbal autopsies’, were emailed randomly (based on the language of the narrative) to at least two of 130 collaborating physicians trained in disease coding. Physicians worked independently to assess the probable underlying cause of death, assigning each case a three-character International Classification of Diseases (ICD; 10th revision) code [20]. Any differences between the two coders were resolved by anonymous reconciliation between them (asking each to reconsider) or, for persisting differences, adjudication by a third physician (3% or 15/562 of snakebite deaths, and 18% or 22,845/122,848 of all deaths). The physician coders' training and their written guidelines (available online [21]) instructed them to use their best medical judgement to determine the most probable cause of death. Field reports could not be collected on 12% of the identified deaths due to migration or change of residence. As these missing deaths were mostly random, a systematic misclassification in cause of death was unlikely. We used logistic regression to quantify the odds of snakebite versus other deaths for gender, state, religion, education, occupation, place of death and season. Risk is measured compared to the reference group of lowest risk for each variable. Climate data on rainfall and temperature were obtained for each state from the India Meteorological Department [22]–[23]. The proportion of cause specific deaths in each age category was weighted by the inverse probability of household selection within rural and urban sub divisions of each state, to account for the sampling design [16]. Using methods described earlier [14]–[15], [17]–[19], the resulting proportion of deaths from each cause was applied to the United Nations (UN) population division estimates of deaths in India in 2005 [24] (9.8 million, upper and lower limits 9.4–10.3 million) to generate cause- specific death totals and rates. The UN totals (which undergo independent demographic review [24]) were used because the SRS underestimates adult mortality rates by about 10% [25]–[26]. The UN totals are not affected by the 12% of the SRS-enumerated deaths that were unavailable for interview in our survey. Totals for 2005 were used because they: (i) were most complete; (ii) could be compared to the available Indian Census projections for 2006; and (iii) captured information prior to the implementation of a new national health program in rural areas [27]. However, applying the 2001–03 proportions to the 2005 total deaths did not introduce major biases since there was little change in the yearly distribution in snakebite deaths in our survey, or in the annual number of deaths reported from snakebites in routine national hospital surveillance data between 2003 and 2008 [7]. Results Snakebite deaths in study and nationally Of the 643 deaths coded by physicians as ICD-10 codes X20–X29 (contact with venomous animals and plants), 523 (81%) were coded as X20 (venomous snakes) and review of these yielded no misclassified causes. Central re-examination of the symptoms and key words found 39 of 45 deaths coded as X27 (animals) and X29 (uncertain) to be snakebite deaths. We excluded 75 deaths coded as X21–X25 (various arthropods), X26 (marine organisms) and X28 (plants). Among all 122,848 deaths, 2,179 of the deaths that were randomly chosen to be re-interviewed by independent teams were eventually matched to the identical houses and individuals of the MDS. Of the 2,179 re-sampled deaths, 9 were coded as snakebites, and 7 of these were found in the MDS. Thus, the sensitivity and specificity of the SRS field survey, assuming the re-sample deaths are the standard comparison, was 78% (7/9) and 100% (2,170/2,170), respectively. A total of 562 of the 122,848 deaths (0.47% weighted by sampling probability or 0.46% unweighted) were from snakebites (Table 1). Almost all snakebite deaths (544 or 97%) were in rural areas. More men (330, 59%) than women (232, 41%) died from snakebites (overall ratio of 1.4 to 1). The proportion of all deaths from snakebites was highest at ages 5–14 years. Only 23% (127/562) of the deaths occurred in a hospital or other healthcare facility. 10.1371/journal.pntd.0001018.t001 Table 1 Snakebite deaths in the present study, 2001–03 and estimated national totals, by age. Study deaths 2001–03 All India estimates 2005 Numbers attributed Proportion snakebite deaths per 1,000* Died in health facility Rural area All causes deaths/population (million): UN estimates † Snakebite deaths in thousands Death rate per 100,000 Age in years Male/Female Snakebite/all causes National Rural 0–4 29/23 52/23,630 2.1 8 52 2.3/128 5.0 3.9 4.9 5–14 73/41 114/3,881 28.5 24 111 0.3/246 9.7 4.0 5.1 15–29 80/62 142/9,121 15.9 31 134 0.7/313 11.0 3.5 4.7 30–44 60/44 104/10,872 9.4 30 102 0.9/222 8.3 3.8 5.3 45–59 52/27 79/18,133 4.6 22 73 1.5/142 6.8 4.8 6.2 60–69 21/24 45/21,136 2.2 6 44 1.5/49 3.3 6.6 8.7 70+ 15/11 26/36,075 0.7 6 28 2.6/30 1.8 6.2 8.0 All ages 330/232 562/122,848 4.7 127 (23%) 544 (97%) 9.8/1,130 45.9 4.1 5.4 (99% CI ) (40.9, 50.9) (3.6, 4.5) (4.8,6.0) The overall study death total of 122,848 includes 8.7% senility, unspecified or ill defined deaths, which were not assigned to any specific disease categories. *Proportional snakebite mortality per 1,000 after applying sample weights to adjust urban-rural probability of selection. †: United Nations 2005 estimates for India. Expressed as national totals, snakebites caused 45,900 deaths in India in 2005 (99% CI 40,900 to 50,900). The age-standardised death rate per 100,000 population per year was 4.1 (99% CI 3.6–4.5) nationally and was 5.4 (99% CI 4.8–6.0) in rural areas. Risk factors and seasonality Figure 1 shows the odds ratios for snakebite deaths versus other deaths, adjusted for age, gender, and for high prevalence states (13 states with age-standardised snakebite death rates greater than 3 per 100,000) versus other states. The risks of snakebite deaths were significantly increased among Hindus and farmers/labourers, deaths occurring outside home, and during the monsoon months of June to September (Figures 1 and 2). In contrast, gender and education were not significantly associated with risk of snakebite death. About 5,000–7,000 snakebite deaths per month occurred during the monsoon period, compared to less than 2,000 deaths in the winter months. Monthly numbers of snakebite deaths correlated with rainfall (R = 0.93, p<.0001) and mean minimum temperature (R = 0.80, p = 0.0017), but not with mean maximum temperature (R = 0.35, p = 0.2585; Figure 2). 10.1371/journal.pntd.0001018.g001 Figure 1 Selected risk factors for snakebite mortality in India (study deaths 2001–03). Odds ratio after adjusting for age, gender and states with a high prevalence of snakebite deaths (see definition in Table 2). Occupation ‘Other’ includes students and house wives. 10.1371/journal.pntd.0001018.g002 Figure 2 Seasonality pattern of snakebite mortality and rainfall in states with high prevalence of snakebite deaths (2001–03). Rainfall amount (mm) is cumulative daily rainfall for the past 24 hours measured by the India Meteorological Department [22], [23]. Maximum and minimum temperatures are also measured daily and presented as monthly averages across the 13 snakebite high prevalence states. Pearson correlation coefficients between snakebite mortality and weather were: (i) rainfall; 0.93 (p<0.0001); (ii) minimum temperature: 0.80 (p = 0.0017); (iii) maximum temperature: 0.35 (p = 0.2585). State mortality patterns Annual age-standardised mortality rates per 100,000 from snakebite varied between states, from 3.0 (Maharashtra) to 6.2 (Andhra Pradesh) in the 13 states with highest prevalence (average 4.5) compared to 1.8 in the rest of the country (Table 2; Figure 3). Total deaths were highest in Uttar Pradesh (8,700), Andhra Pradesh (5,200), and Bihar (4,500). The age and gender of snakebite deaths also varied by region, although these differences were not significant due to the small numbers of snakebite deaths in each state. Deaths at ages 5–14 years were prominent in the states of Jharkhand and Orissa, whereas deaths at older ages were prominent in Andhra Pradesh, Bihar, Madhya Pradesh, and Uttar Pradesh (data not shown). In Bihar, Madhya Pradesh, Maharashtra and Uttar Pradesh, female deaths exceeded male deaths (Table 2). 10.1371/journal.pntd.0001018.g003 Figure 3 Estimated deaths and standardized death rates in states with high prevalence of snakebite deaths, 2005. Death rates are standardised to 2005 UN population estimates for India [24]. The vertical bars represent the state wise estimated deaths (in thousands). Total snakebite deaths for the 13 states with high-prevalence of snakebite death are 42,800 or 93% of the national total (these states have about 85% of the total estimated population of India). States where the snakebite death rate was below 3/100,000 or where populations are less than 10 million are not shown. The states with high-prevalence of snakebite deaths are: AP-Andhra Pradesh, BR-Bihar, CG-Chhattisgarh, GJ-Gujarat, JH-Jharkhand, KA-Karnataka, MP Madhya Pradesh, MH-Maharashtra, OR-Orissa, RJ- Rajasthan, TN-Tamil Nadu, UP-Uttar Pradesh, WB-West Bengal. 10.1371/journal.pntd.0001018.t002 Table 2 Estimated snakebite deaths in the Indian states with a high prevalence of snakebite deaths, 2005. Study deaths 2001–03 Estimated state and national deaths 2005 State Snakebite/all causes Male/female Died outside health facility Proportional mortality/1,000 Snakebites deaths in thousands Death rate per 100,000 States with high-prevalence of snakebite deaths * Andhra Pradesh 45/5,831 31/14 42 7.4 5.2 6.2 Madhya Pradesh 41/7,257 20/21 31 5.7 4.0 5.9 Orissa 37/7,364 22/15 26 5.2 2.2 5.6 Jharkhand 12/2,179 8/4 12 5.8 1.5 4.9 Bihar 50/9,824 21/29 45 5.8 4.5 4.9 Tamil Nadu 38/6,316 26/12 28 5.1 3.1 4.7 Uttar Pradesh 78/15,403 36/42 72 4.8 8.7 4.6 Chhattisgarh 13/2,328 6/7 11 4.6 1.0 4.4 Karnataka 41/6,961 32/9 32 5.0 2.4 4.2 West Bengal 40/8,330 24/16 20 4.7 3.0 3.5 Gujarat 28/6,151 20/8 20 4.1 1.9 3.5 Rajasthan 29/6,769 18/11 24 4.2 2.1 3.3 Maharashtra 28/6,274 9/19 18 3.9 3.2 3.0 Sub total 480/90,987 273/207 381 5.1 42.8 4.5 Remaining states 82/31,861 57/25 54 2.2 3.1 1.8 All India 562/122,848 330/232 435 4.7 45.9 4.1 (99% CI) (40.9, 50.9) (3.6, 4.5) States are listed in descending order of death rates. Death rates are standardised to 2005 UN national estimates for India. *States with a high-prevalence of snakebite deaths are defined as those with more than 10 million people where the annual snakebite death rate exceeds 3 per 100,000 population. Discussion Snakebite remains an important cause of accidental death in modern India, and its public health importance has been systematically underestimated. The estimated total of 45,900 (95% CI 40,900–50,900) national snakebite deaths in 2005 constitutes about 5% of all injury deaths and nearly 0.5% of all deaths in India. It is more than 30-fold higher than the number declared from official hospital returns [7]. The underreporting of snake bite deaths has a number of possible causes. Most importantly, it is well known that many patients are treated and die outside health facilities – especially in rural areas. Thus rural diseases, be they acute fever deaths from malaria and other infections [19] or bites from snakes or mammals (rabies; [28]), are underestimated by routine hospital data. Moreover, even hospital deaths may be missed or not reported as official government returns vary in their reliability, as shown from a study of snakebites in Sri Lanka [29]. The true burden of mortality from snakebite revealed by our study is similar in magnitude to that of some higher profile infectious diseases; for example, there is one snakebite death for every two AIDS deaths in India [18]. Consequently, snakebite control programmes should be prioritised to a level commensurate with this burden. Our data suggest underestimation in recent global estimates of mortality from snakebite deaths [10]: the upper bounds of recent annual estimates were 94,000 deaths globally and 15,000 deaths in India. This total for India is only about one-third of the snake bite deaths detected in our study. The incidence of snakebite deaths per 100,000 population per year in a recent community-based study in Bangladesh was similar to ours [30], suggesting that much of South Asia might have thousands more snakebite deaths than is currently assumed. Considering the widely accepted gross underestimation of snakebite deaths in Africa [11], it seems highly probable that well over 100,000 people die of snakebite in the world each year. A minimal number of non-fatal snakebites in India may be estimated with far less certainty. Indian data from routine public sector hospitals [7] are clearly under-reports of deaths (recording only 1 in 5 of the deaths we estimated to have occurred in hospital). Nonetheless, the ratio of non-fatal bites (about 140,000) to fatal bites (about 2,200) in these hospital data from 2003–08 (about 64∶1) is informative of the relative burden of bites to deaths. Very crudely, even if we halve the fatal/nonfatal bite ratio to 32, this would suggest at least 1.4 million non-fatal bites corresponding to the 45,000 fatal bites. The actual number of non-fatal bites in India may well be far higher, as the community-based study in Bangladesh found about 100 non-fatal bites for each death [30]. Our study has limitations; notably the misclassification of snakebite deaths. However, snakebites are dramatic, distinctive and memorable events for the victim's family and neighbours, making them more easily recognizable by verbal autopsy. We observed a reasonably high sensitivity and specificity when compared to re-sampled deaths. Confusion with arthropod bites and stings is unlikely because of the different circumstances, size and behaviour of the causative animal and the course of envenoming. For example, most deaths from hymenoptera stings result from rapidly evolving anaphylaxis. Kraits (important agents of snakebite death in South Asia) may unobtrusively envenom sleeping victims, who may die after developing severe abdominal pain, descending paralysis, respiratory failure and convulsions [31]. Such deaths might not be associated with snakebite at all. These examples suggest possible underestimation of deaths in our data. Since the numbers of deaths observed in each state were small, the estimated totals for each state are uncertain. However, the state distribution is broadly consistent with that reported by the RGI survey of deaths in selected rural areas in the 1990s [32]. The marked geographic variation across states in our study is similar to that in a country-wide survey conducted during the period 1941–45, which identified Bengal, Bihar, Tamil Nadu, Uttar Pradesh, Madhya Pradesh, Maharashtra and Orissa as having the highest death rates from snakebite [6]. Moreover, despite the obvious underestimates in hospitalised data [7], their geographical distribution of bites and deaths were similar to what we observed from household reports of deaths. The marked differences in snakebite mortality between states of India may be attributable to variations in human, snake and prey populations, and in local attitudes [8] and health services. The 13 states with the highest snakebite mortality are inhabited by the four most common deadly venomous snakes: Naja naja, Bungarus caeruleus, Echis carinatus and Daboia russelii. With the exception of E. carinatus, which favours open wasteland, these are widely distributed species of the plains and low hills where most Indians live. While some species can inhabit altitudes of up to 2,700 metres [2], this is exceptional and higher mountainous regions have considerably lower death rates. As found in an earlier study [33], the peak age group of snakebite deaths is 15–29 years (25% or 142/562). However, the relative risk of dying from snakebite versus another cause was greater at ages 5–14 years. The peak age range and gender associated with snakebite mortality varied between states, perhaps reflecting differences in the relative numbers of children and women involved in agricultural work [34]–[35]. The slight excess among Hindus may reflect more tolerance of snakes and greater use of traditional treatments [2]. Snakebites and snakebite fatalities peak during the monsoon season in India [33], [36] and worldwide [10], probably reflecting agricultural activity, flooding, increased snake activity, and abundance of their natural prey. Only 23% of the snakebite deaths identified in our survey occurred in hospital, consistent with an earlier study from five states [33]. This emphasises three points: (i) hospital-based data reflect poorly the national burden of fatal snakebites; (ii) inadequacy of current treatment of snakebite in India; and (iii) vulnerability of snakebite victims outside hospital. Practicable solutions include strengthening surveillance to allow a more accurate perception of the magnitude of the problem, improving community education to reduce the incidence of snakebites and speed up the transfer of bitten patients to medical care, improving the training of medical staff at all levels of the health service (including implementation of the new WHO guidelines [12]), and deployment of appropriate antivenoms and other interventional tools where they are needed in rural health facilities to decrease case fatality [36]–[38]. In addition, phylogenetic and venom studies are needed to ensure appropriate design of antivenoms to cover the species responsible for serious envenoming.
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              Annual Incidence of Snake Bite in Rural Bangladesh

              Introduction Snake bite particularly in the rural tropics is a major cause of mortality and morbidity, and it has a significant impact on human health and economy through treatment related expenditure and loss of productivity [1]. Snake bite is the single most important cause of envenoming worldwide and results in substantial mortality in many parts of Africa, Asia, and the Americas [2]. Snake bite is significantly neglected as a public health problem in the world as evidenced by the lack of available incidence data from most of the rural tropics where snake bites occur frequently. Global snakebites (envenomings) incidence has been estimated as 500,000 and mortality between 30000–40000 per year [3]. Chippaiux estimated that venomous snakes cause 5.4 million bites, approximately 2.5 million envenomings and over 125,000 deaths worldwide annually [4]. White estimated more than three million bites per year resulting in more than 150,000 deaths [5]. Details of the methods used to estimate these numbers have not been clearly described. More recently Anuradhani et al reported that, globally at least 421,000 envenomings occur annually, but this may be as high as 1,841,000 [6]. According to this estimate, the highest numbers of envenomings are estimated for South Asia (121,000) followed by South East Asia (111,000), and East Sub-Saharan Africa (43000). Global estimates of snakebite envenomings and deaths seem to be more accurate than previous estimates due to improved study methodology. However, this data may be inaccurate because of assumptions used in the calculations, lack of information relating to snake bites and related deaths in rural tropics. It is likely that the true numbers of these events may be substantially different from the estimates presented in this report. The true incidence of snake bite in rural Bangladesh is largely unknown. Previously, an incidence of 4.3 snake bites per 100,000 populations was reported with approximately 2000 deaths occurring annually in Bangladesh [7]. This estimate is based on data from a small study. During 1988–89, a small survey was conducted in 50 Upazillas (sub-districts) of Bangladesh that recorded 764 episodes of snakebite, of which 168 (22%) died [8]. Due to methodological limitations, these estimates are unlikely to be representative of the whole country population. According to Faiz, 1666 snake bite victims attended to the Chittagong Medical College Hospital (CMCH) for treatment between 1993 and 2003. Among those victims, 28.5% were bitten by poisonous snakes and only eight (0.5%) died [1]. In this context, this cross-sectional survey was carried out to determine the annual incidence density of snake bite in rural Bangladesh. In addition, the study also developed an epidemiologic profile of snake bites that includes age and sex specific incidence of snake bites, consequence of snake bite, treatment seeking behaviour of the patients, seasonal trend, and geographical distribution of snake bites in the context of rural Bangladesh. The study was conducted during February to June 2009 in Bangladesh. Methods Ethics statement This study was conducted according to the principles expressed in the Declaration of Helsinki. The study was approved by the Human Research Ethics Approval Committee, The University of Newcastle and the Bangladesh Medical Research Council (BMRC). Informed written consent was obtained from head or in his/her absence from any adult member of each selected household. Study population Bangladesh is divided into six administrative divisions. We undertook a multistage cluster sample of households within each administrative division. Firstly, all six administrative divisions were selected. Afterwards, four districts from each selected division, two upazilas from each selected district, two unions from each selected upazila and two blocks from each selected union were randomly selected. At present, the block is the lowest administrative unit in both Urban and rural areas in Bangladesh. The number of households required per block per division was selected based on probability proportionate to size of the total population. In absence of any sampling frame of households at the block level, we arbitrarily divided each block into four quarters. We then scatteredly identified one-fourth of the required households from each quarter of the block. After selection of the households, interviewers visited all these households and explained the study to the head or in his/her absence any adult member of the household. After obtaining the respondent's written consent, information was collected on socio-demographics, snake bites and their consequences, and treatment seeking behavior following snake bites from the respondent. The respondent answered for every member who spent any part of the past year in the selected household. All information was collected using an interviewer administered pre-tested partially close ended questionnaire through face to face interview. Frequency of snake bite(s) on each member and their length of stay in months in that house during past 12 months were collected from the respondents. Later on, person-time was converted from person-month to person-years to calculate annual incidence density of snake bites in rural Bangladesh. Statistical analysis We estimated the incidence density, and 95% poisson confidence interval of snake bite by using the number of episodes of snake bites as the numerator and person years of stay in the surveyed house as the denominator. Incidence density was adjusted for the design effect of the survey by using “svy” command in STATA. Since there was no non-response in our survey, only design-based weights computed as the inverse of each observational unit's probability of selection at each stage of sampling were used to obtain unbiased estimates of population rates[9]. The chi squared statistic was calculated to compare incidence rates among categories of age, occupation and other variables. We also used this incidence density to estimate the total number of episodes of snake bite per year in rural Bangladesh. We calculated the total number of snake bite victims and related deaths by extrapolating the proportion of snake bite and related death from this study on the total population of rural Bangladesh (BBS 2001).To determine any correlation of snake bite with rain fall and temperature we plotted monthly rate of snake bite against mean monthly rainfall and temperature. All statistical analyses were carried out using Stata version 10.1 [10]. A sample size of 16500 is sufficient to demonstrate an annual incidence of 50 per 100,000 with a 95% confidence interval of ±20 per 100,000. Considering the non-compliance and non-response, an extra ∼10% of the participants were included. Therefore, 3993 households were approached. Results We collected information on 18857 individuals from 3993 households. A sample of 1287, 975, 678, 272, 285 and 496 households were selected from Dhaka, Rajshahi, Chittagong, Barisal, Sylhet and Khulna division, respectively. The total population for Dhaka, Rajshahi, Chittagong, Barisal, Sylhet and Khulna divisions are 39,044,716; 30,201,873; 24,290,384; 8,173,718; 7,939,343; 14,705,223; respectively [11] (BBS 2001). The main characteristics of the participants are given in Table 1. 10.1371/journal.pntd.0000860.t001 Table 1 Characteristics of the study population* (n = 18,857). Variable Frequency (%) Sex * Male 9773 (52) Female 9075 (48) Age (years); mean ± SD 26.75±18.87 Age category (years) ** 0–10 4619 (25) 11–20 4032 (21) 21–30 3520 (19) 31–40 2614 (14) 41–50 1925 (10) 51> 2142 (11) Religion ** Muslim 16854 (89) Hindu 1728 (9) Christian 38 (1) Buddhist 232 (1) Occupation ** Service 1026 (5) Farmer 2178 (12) Student 4546 (24) Housewife 4766 (25) Business 1200 (6) Day laborer 1279 (7) Others 3857 (21) Number of participants per division Barisal 1277 (7) Chittagong 3602 (19) Dhaka 5983 (32) Khulna 2164 (11) Rajshahi 4272 (23) Sylhet 1559 (8) Years of schooling None 6824 (36) 1–5 6258 (33) >5 5775 (31) Total household monthly income (taka) 7000 Tk 4252 (23) Marital status Married 9453 (50) Unmarried 8825 (47) Others 579 (3) *Missing data = 9, **Missing data = 5. There were 98 snake bites reported overall, and only one person died of the snake bite. The incidence of snake bite episode was 623.4 (95% CI 513.4–789.2) bites per 100,000 person years. The highest incidence was found for Barisal division (2667.7) and the lowest for Sylhet division (321.6). The between division rates were significantly heterogeneous (Table 2). Eight percent of the snake bite victims are bitten more than once in a year, therefore the total number of snake bite episodes exceeds the number of snake bite victims. 10.1371/journal.pntd.0000860.t002 Table 2 Distribution of snake bite by division. Division Number of snake bites Annual incidence per 100000 person-years* (95% CI) Dhaka 22 440 (285–649.9) Chittagong 9 397.8 (211.8–680.3) Barisal 22 2667.7 (1787.2–3829.5) Khulna 20 936.2 (571.9–1445.6) Sylhet 5 321.6 (104.4–750.2) Rajshahi 20 472.7 (288–680.3) Over all 98 623.4 (513.4–789.2) *: Weighted estimates have been used; P 51) is similar (23%) to that in the young age group of 11–20 years (22%). However, the annual incidence is nearly double (1063 per 100,000) in the old age group because of the small proportion of people at risk under this category (Table 3). Similarly, both of the youngest age group (0–10 years) and the age group of 41–50 account for the 11% of snake bite victims, but the annual incidence in the youngest group (248 per 100,000) is less than half of the other group due to due to the large population at risk in the youngest group. 10.1371/journal.pntd.0000860.t003 Table 3 Distribution of 98 snake bite by age group. Age-group Frequency of victims Percent of victims Annual incidence per 100,000* 0–10 11 11 248 (101–394) 11–20 21 22 544 (312–776) 21–30 18 18 531 (286–776) 31–40 15 15 594 (294–814) 41–50 11 11 587 (241–934) >51 22 23 1063 (621–1506) *adjusted for sampling design. Analysis by sex reveals that snake bites are similarly distributed among males (52%) and females (female 48%), the annual incidence density is also similar for males and females(698, 95% CI 538.8–889.6) than females (543.5, 95% CI 399.4–722.7) (not shown in analysis). Housewives made up the highest category of snake bite victims (30%) with the smallest percentage occurring in day laborers (8%) (Table 4). 10.1371/journal.pntd.0000860.t004 Table 4 Distribution of 98 snakebite (percent) by occupation, place of bite and activities during the bite. Occupation Frequency (%) Place of bite Frequency (%) Activities during the bite Frequency (%) Housewife 29 (30) Water 26 (27) Lying/sleeping 15 (15) Student 20 (21) Field 24 (24) Walking 28 (29) Farmer 19 (19) Road side 22 (23) Working in field 18 (18) Businessman 11 (11) Inside home 12 (12) Fishing 14 (14) Day laborers 8 (8) Home premises 11 (11) others 23 (24) Others 11 (11) Others 3 (3) A relatively high proportion of snake bite episodes happened during night times (36%), whereas morning and afternoon account for same proportion (32%) close to a third in each category. Housewives receive more bites (40%) at night where as farmers receive more bites (71%) during day time. Bites that occur at night are more frequent at home or on the road side (59%) (not shown in analysis).This is perhaps related to krait being an important snake in Bangladesh, and would explain the increased proportion of housewife victims as well. Most of the snake bites occurs in water (27%) followed by the field (24%). Home premises and inside the home account for similar proportion of bites (11% and 12% respectively) (Table 4). As expected, the majority of snake bites occurred on the feet (71%), followed by the hand (27%) and other parts of the body (2%) (not shown in analysis). Although highest proportion of snake bite occurs in water (27%), fishing accounts for the lowest proportion (14%) of all activities (Table 4). This may be because during monsoon season, many people travel by boat as the roads are often submerged under water. The distribution of monthly snake bites, rainfall and temperature data are presented in Figure 1. The month of October (22%) and July (15%) account for the highest proportion of bite episodes. There is also an increase in snake bites in the month of December as harvesting activities increase during this month. Although scatter plot of monthly snake bite rate and mean rainfall and temperature did not show any evidence of linear relationship. 10.1371/journal.pntd.0000860.g001 Figure 1 Distribution of snake bites, temperature and rain by month. After recognizing a snake bite episode the victims received different combination of management strategies. The distribution of post snake bite management options are shown in Table 5. Since most of the victims received more than one form of management, the total percentage is great than 100%. The most prevalent management is recitation of mantras by the snake charmers (60%) or ‘ozhas’. Potentially harmful approaches such as making multiple incisions around the bite site, incorrect application techniques in tourniquets (e.g. wrong pressure), sucking blood orally from the multiple cuts are practiced in an alarmingly high proportion of cases. In only 31% of snake bites the bitten parts of the body were kept immobile, which is likely to be clinically beneficial to limit systemic spread of venom. 10.1371/journal.pntd.0000860.t005 Table 5 Distribution of treatments received by the 98 snake bite victims. Type of treatment Frequency of victims Percent of victims 1 tourniquet was given 37 39 >1 tourniquets were given 26 27 Kept immobile 30 31 Sucked blood orally 10 11 Multiple cuts around the bite site 41 43 Utters mantras 57 60 Forced vomiting 17 18 Snake charmers were the first contact following a snake bit for 86% of the victims, with 6% contacting traditional village doctors, only 3% contacting a registered physician or a nearby hospital and the remaining 5% contacting other sources such as directly going to a drug store (not shown in analysis). This information is consistent with Table 5 that almost all the treatments were offered by the traditional healers, i.e., ozhas or snake charmers. Discussion We have assessed the risk of snake bite in rural Bangladesh. The findings suggest that an annual incidence density of snake bite is 623.4 per 100,000 person-years, which may be as high as 789.2 per 100,000 person-years. According to the study findings an estimated 710,159 episodes of snake bites occur annually in rural Bangladesh. An estimated 589,919 individuals are bitten by snakes and 6041 die from snake bites every year in rural Bangladesh. This incidence is much higher than the previously estimated incidence. The highest incidence was observed in southwestern coastal Barisal division followed by Khulna division. The highest incidence was also found in Barisal division previously [7]. This high rate of Barisal division could be attributed to its geographical location and natural environmental condition. In this study, the majority of the snake bite victims are of a younger age and this reflects that an active population is at higher risk of snake bites. Similar observations were reported from Nepal, Malaysia and a previous study in Bangladesh [7], [8], [12], [13], [14], [15]. This information has important public health implications that despite of the comparatively low incidence the youngest age group should be given priority in directing any intervention for snake bite. Our study found a similar ratio of male and female snake bite victims. Male preponderance was observed from a few studies, largely due to bites in paddy fields although male to female ratio varied in these studies [7], [8], [12], [16], [17], [18]. Our study finding on the male female ratio differs from other studies. This difference may partly be explained as this is a community based study compared to most of the reported hospital based studies and therefore more likely to be representative of the total population exposed. Males may have higher hospitalization rates than females in developing countries. Moreover, women receive more bites at home and during night time. This may be due to the presence of krait at the home premises. Krait is usually nocturnal. It lives close to the human dwellings and hides in holes, woods or homestead gardens. At night, especially at the height of the monsoon season, kraits enter into human dwellings, presumably in hunt of their natural prey that includes small snakes, amphibians, rodents, and geckos, which are abundant in rural homes [19], [20], [21]. In many areas of Bangladesh, women are also involved in agricultural activities at the field with the males. In our study, we found that the highest number of snake bites occurs during the monsoon season from June to October. This is probably because most of the agricultural activities take place during this season. Furthermore, there is increased snake activity during this period in the hot weather and monsoon's rain. These changed conditions are likely to force snakes to come out of their shelters and seek refuge in comparatively high and dry places. This may be partially responsible for increased risk of snake bite during the monsoon season. Similar findings were reported from other studies.[7], [8], [12], [22], [23]. An increase of snake bite in December was also observed. This is likely due to increased agricultural activities in this month. Our data did not suggest any relationship between monthly snake bites, temperature and rainfall. Even if there is any relationship between snake bites, temperature, and rainfall, often it is difficult to determine exactly what the relationship is, particularly if there are two things that are driving the effect, e.g. rainfall and temperature or rainfall and harvesting. Biting occurs mostly when individuals are at work, engaging in activities such as cultivation, fishing, plantation, wood collection, or tending crops or gardens. However, bites are fairly common when the victims are walking or sleeping. In this study, 51% of victims received their snake bite while working either in the agricultural field or in water. Twenty three percent had snake bites while staying at home. Most of the houses in Bangladesh are not brick and the snakes sometimes live in the holes of the muddy floors. Moreover, most of the houses in rural areas of the country have homestead bush, which offers normal habitats for snakes. As a result, events of snake bites are also common when people are at home. To go to the toilet and for other domestic purposes, people often come out of their houses and become victims. Village people store grains, including paddy, in their bedroom, which also provides shelter to the snakes, therefore increasing the risk of snake bite. Similar observations were also reported from a previous study in Bangladesh [7]. The majority of the victims (71%) received snake bites in lower extremities. This may be because most of the time the snakes were trodden upon by the victims. Bites at the agricultural fields are also more likely to occur on the lower limbs. Cobras are common sources of daytime bites in Bangladesh. Similar findings were reported from Nepal, Bangladesh, Malaysia and Hong Kong [7], [8], [12], [13], [14], [24], [25]. Although Plowman and co-workers reported that two-thirds of the snake bite cases occurred in the upper limb [26], in our study, 27% victims received snakebites at their upper limbs. Many of the bites just occurred while lying on the ground in bed. Bites in the upper limbs or head and neck region may occur during sleep on ground as kraits often enter human dwelling at night in search of food. Similar observations were made in Nepal earlier [12], [27]. Bites in the head and neck region may also occur by the green pit viper which was also found in earlier studies in Chittagong area [1]. Seventy five percent of the victims received any form of management within two hours of the snake bite. Eighty six percent of the victims go to a snake charmer first to seek treatment, only three percent go to a medical doctor or hospital directly after the bite. Later on, 10% victims visit a medical doctor or hospital. He majority of the rural people do not want to go to a doctor following snake bites. The reasons for this require thorough evaluation but may include lack of awareness of the efficacy of medical treatment with antivenins, lack of availability of snake antivenins in the public hospital, lack of transport facilities and inability to afford transportation. Similar observations were made in the past studies conducted in Nepal [12], [18], [27]. Intravenous snake antivenin is the most effective treatment for envenoming by snakes [28]. Our study observed that snake charmers practice many unhygienic measures such as multiple incisions, tight tourniquet around the bite mark, sucking of blood from the bite wound to manage the snake bite. Therefore, these snake charmers should be trained on as a priority, so that they can stop their risky practices, perhaps be trained to apply tourniquets correctly and immediately refer the patients to the nearest health facilities. Snake antivenin should be made available in the public hospitals free of cost, particularly in the remote rural areas. To the best of our knowledge, this is the largest community based study so far that has been conducted to the determine incidence of snake bites in any country in the world. The main strength of this study is its epidemiological approach which was followed rigorously at each stage of the study. Limitations of this cross-sectional study involve the methods that were used for sampling at the block level. Because the survey involved remote rural areas and because no list of households exists in those areas, a perfectly random sample could not be obtained. However, there is no reason to believe that the adopted sampling strategy would have resulted in a non-representative study population. We collected information from the respondents on snakebite which occurred during the previous twelve months. Although recollecting information from the past, recall error is unlikely to occur because the victim or the household members are less likely to forget an important event such as snakebite. Households that were fully vacant during interview team's visit were excluded from the survey. We did not record the actual number of vacant houses. However, only a very few households were totally vacant during the household survey. In this survey, we observed only one death out of 98 snakebites; this may reflect the nature of snake bites in Bangladesh, the majority of which are non-venomous. This study reported that only one person died of the snake bite. Based on this single death, we estimated the number of snakebite related deaths i.e., 6041 in rural Bangladesh. Although this single death may not be statistically stable to estimate total snake bite related deaths, the estimated number of deaths seem reasonable. The estimated number of deaths is also likely to be representative because of this large population based representative survey. We only collected information on annual incidence of snake bites in rural Bangladesh in this study. Future studies could investigate snakebites which occurred throughout the life of study participants, although recall bias is likely to increase with increasing time since the event. The study findings would be useful for planning and formulating strategies and specific interventions to combat snake bite related health problems in Bangladesh. Poor access to health services increases the risk of morbidity and mortality attributable to snake bites. Scarcity of supply of snake antivenin is a major factor which needs to be addressed by local production. Snake bite related deaths are preventable. Supporting Information Checklist S1 STROBE checklist. (0.08 MB DOC) Click here for additional data file.
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                Author and article information

                Journal
                Journal of Environmental and Public Health
                Journal of Environmental and Public Health
                Hindawi Limited
                1687-9805
                1687-9813
                May 18 2020
                May 18 2020
                : 2020
                : 1-9
                Affiliations
                [1 ]Institute of Global Health, Department of Community Health and Medicine, Faculty of Medicine, University of Geneva, 1202 Geneva, Switzerland
                [2 ]Institute for Environmental Sciences, University of Geneva, 1205 Geneva, Switzerland
                [3 ]Department of Biological Sciences, Florida Gulf Coast University, Ft Myers, FL 33965, USA
                [4 ]Division of Tropical and Humanitarian Medicine, Geneva University Hospitals, 1206 Geneva, Switzerland
                [5 ]Médecins Sans Frontières–Doctors Without Borders, 1211 Geneva, Switzerland
                Article
                10.1155/2020/6135149
                85ca4315-7777-4584-908b-06f02b9a7357
                © 2020

                http://creativecommons.org/licenses/by/4.0/

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