Trends in snakebite deaths in India from 2000 to 2019 in a nationally representative mortality study

  1. Wilson Suraweera  Is a corresponding author
  2. David Warrell  Is a corresponding author
  3. Romulus Whitaker  Is a corresponding author
  4. Geetha Menon  Is a corresponding author
  5. Rashmi Rodrigues  Is a corresponding author
  6. Sze Hang Fu  Is a corresponding author
  7. Rehana Begum
  8. Prabha Sati
  9. Kapila Piyasena  Is a corresponding author
  10. Mehak Bhatia
  11. Patrick Brown  Is a corresponding author
  12. Prabhat Jha  Is a corresponding author
  1. Centre for Global Health Research, Unity Health Toronto, and Dalla Lana School of Public Health, University of Toronto, Canada
  2. Nuffield Department of Clinical Medicine, University of Oxford, United Kingdom
  3. Centre for Herpetology/Madras Crocodile Bank, Vadanemmeli Village, India
  4. Indian Council of Medical Research, Ansari Nagar, India
  5. Department of Community Health, St. John's Medical College, St. John's National Academy of Health Sciences, India
  6. Department of Statistical Sciences, University of Toronto, Canada
10 figures, 9 tables and 1 additional file

Figures

Spatial distribution of snakebite mortality risk in India for 2004-13.

Note: About 0.33% of the Indian population lived in areas with an absolute risk of 1% or greater of dying from snakebite before age 70 years, and 21% lived in areas with absolute risk of 0.6% or higher. Population estimates used the Gridded Population of the World version 4 for year 2015 (Center for International Earth Science Information Network - CIESIN - Columbia University, 2015). Further details of statistical method and stochastic uncertainties of spatial mortality risk pertaining to these estimates are explained in Appendix 3.

Predicted daily snakebite deaths from analysis of seasonality observed in 2001-2014 (Panel A) and snakebite crude death rates by altitude in meters in 2004-2013 (Panel B).

Notes: The daily snakebite totals are a composite of all study years from 2001 to 2014. The crude death rates by elevation use the RGI’s Sample Registration System population as denominators, and hence are generally lower than the overall rates we apply to the whole of India (using the United Nations death totals, which has the benefit of taking into account undercounts in the SRS data [Menon et al., 2019]). However, the relationship of crude death rates with elevation is unaffected by this procedure.

Characteristics of snakebites from analysis of 88,000 snakebite events in the published literature.
Appendix 1—figure 1
The conceptual overview of role of data sources, input measures and study outcomes.
Appendix 1—figure 2
Observed seasonality of snakebite deaths in study data in 2001-2014.

Note: Proportional snakebite mortality (monthly snakebite deaths to all causes deaths) reported from the 2001 to 2014 rounds of RGI-MDS.

Appendix 2—figure 1
Study selection, inclusion and exclusion details.
Appendix 3—figure 1
Locations of geocoded sampling units from the Sample Registration System (SRS) in 2004–13, excluding sampling units for islands.
Appendix 3—figure 2
Snakebite crude rates in 2004–13.
Appendix 3—figure 3
95% credible intervals of the absolute risks and median absolute risks of snakebite deaths in India, 2004-13.

(a-b) 95% credible interval of the absolute risk estimates, (c) median absolute snakebite risks (from main text Figure 1).

Appendix 3—figure 4
Non-linear effects of year estimated using second order random walk.

Tables

Table 1
Snakebite deaths in the Million Death Study, age-standardized and age-specific mortality rates and risks in India from 2001-2014.
YearStudy deaths from snakebite/all causesStandardized death rate /100,000 (all ages) and age-specific rates /100,000*Snakebite mortality riskEstimated national deaths (000)
All ages0-1415-2930-69
2001199 /418265.35.43.65.90.40%55.0
2002183 /417405.25.23.55.80.39%55.3
2003179 /387985.15.03.45.80.38%55.8
2004190 /373805.04.63.55.70.38%55.6
2005244 /467554.94.83.46.40.40%60.8
2006214 /474715.34.73.26.70.40%62.7
2007225 /485365.34.53.06.40.39%61.0
2008215 /476735.14.22.85.90.36%57.4
2009183 /478734.73.92.65.30.33%53.8
2010200 /457194.33.92.65.00.32%52.4
2011185 /460994.24.02.75.10.33%54.9
2012227 /466354.34.32.85.40.36%59.2
2013214 /453314.64.43.05.80.38%62.3
2014175 /296474.74.23.05.90.37%61.2
2001-20142833 /6114834.84.53.15.80.37%807.5
Plausible range (Lower, Upper)§(4.4, 5.0)(4.1, 4.7)(2.8, 3.2)(5.3, 6.0)(0.34%, 0.38%)(738.2, 833.4)
  1. * Death rates were standardized to the Indian population in census year 2001 to take into account minor changes in the age distribution over time.

    The probability of dying due to snakebite before reaching age 70 years in the hypothetical absence of other competing causes of death. This was calculated by summing the 5-yearly standardized death rates from ages 0 to 69 years.

  2. Total death estimates at all ages were calculated by applying the MDS sample weighted proportion of deaths from snakebites, using weighted 3-yearly moving average, to the United Nations Population Division death totals.

    § Plausible ranges: The inherent variation in these estimates is not from the underlying demographic estimates but in the determination of primary causes of death. Therefore, we used plausible ranges based on independent cause assignment by two physicians and subsequent agreement on ICD-10 codes (X20 or X29). The lower bound was based on immediate agreement of both physicians and upper bound based on either of two physicians coding snakebite deaths.

Table 2
Estimated snakebite deaths in thousands by age and sex from 2000 to 2019 in India.
Age rangeMale (LL, UL)Female (LL, UL)Both (LL, UL)
0-14 years149 (134, 154)176 (160, 180)325 (294, 334)
15-29 years109 (102, 111)88 (82, 89)197 (184, 199)
30-69 years290 (269, 303)253 (232, 260)543 (501, 564)
70 years or above54 (45, 60)48 (44, 50)102 (89, 110)
All Ages602 (551, 626)565 (518, 578)1,167 (1068, 1204)
  1. Total deaths for 2001-2014 MDS study period were 807,500 (Table 1). Deaths for 2000-2019 were calculated by extrapolating these annual deaths. The extrapolated annual deaths in thousands for outside the study period were 54.0 for 2000, 62.3 for 2015, 62.0 for 2016, 61.4 for 2017, 60.3 for 2018 and 59.8 for 2019.

    Lower limit (LL) and Upper limit (UL) are lower and upper uncertainty bounds for estimates. The major uncertainty in our analyses, however, is not the demographic totals, but the cause of death classification. Hence, the lower bound was based on immediate agreement of both physicians on the ICD-10 code for snakebite and upper bound based on either of two physicians coding as snakebite death.

Table 3
Snakebite death rates by state in India for 2001-2014.
Study deaths in MDSAnnual average standardized death rate /100,000Estimated deaths for 2001-14 (000)
State2001-20042005-20092010-2014Trend
Higher burden states17265.96.16.2557.4
Andhra Pradesh2718.57.35.682.9
Bihar3215.67.68.9101.9
Odisha1917.57.25.940.3
Madhya Pradesh1956.77.76.067.8
Uttar Pradesh3225.25.96.0153.6
Rajasthan1924.96.75.052.1
Gujarat1764.14.85.138.8
Jharkhand584.92.07.120.1
Lower burden states11073.73.12.1249.9
Chhattisgarh426.06.52.516.8
Jammu & Kashmir645.37.00.97.0
Tamil Nadu1766.13.43.042.1
Karnataka1375.63.32.933.0
Maharashtra1474.23.72.656.0
West Bengal1884.13.32.942.7
Punjab672.93.14.014.5
Haryana452.93.31.89.5
Assam272.80.72.17.3
Northeastern states372.30.90.72.4
Kerala431.81.30.56.5
All other states1344.33.93.212.2
All India28335.14.94.5807.5
  1. States are in descending order of annual average death rates for the study period of 2001-2014. We included only the states with populations over 10 million. Andhra Pradesh included Telangana. The Northeastern states include Arunachal Pradesh‚ Manipur‚ Meghalaya‚ Mizoram‚ Nagaland‚ Sikkim and Tripura.

Table 4
Government hospital reports of snakebites and deaths, compared to MDS death totals by state for 2003-2015.
Government reporting*MDS estimates
StateNo. of bites (000)No. of deaths (000)% died in hospitalTotal no. of deaths (000)No. died in hospital (000)% Government coverage
(1)(2)(3)(4)(5)(6)=(4)*(5)(7)=(3)/(6)
Higher burden states530.06.919%539.694.67%
 Andhra Pradesh251.31.416%74.111.612%
 Bihar20.90.116%105.417.01%
 Odisha76.21.829%36.910.917%
 Madhya Pradesh28.31.122%64.414.18%
 Uttar Pradesh27.80.613%150.720.23%
 Rajasthan71.31.016%49.67.813%
 Gujarat45.70.827%38.610.57%
 Jharkhand8.50.112%20.02.56%
Percentage to national41%45%71%61%
Lower burden states772.28.628%219.859.614%
 Chhattisgarh16.70.317%14.32.413%
 Jammu & Kashmir18.40.026%5.91.52%
 Tamil Nadu106.60.528%36.010.05%
 Karnataka89.21.621%28.16.026%
 Maharashtra178.71.225%49.012.510%
 West Bengal208.93.441%38.915.922%
 Punjab9.10.210%14.21.413%
 Haryana14.30.116%8.51.311%
 Assam3.60.132%6.62.13%
 Northeastern states11.10.125%1.80.411%
 Kerala37.90.227%5.23.56%
 All other states77.80.824%11.12.732%
Percentage to national59%55%29%39%
India1302.215.522%759.4154.210%
  1. * Government statistics are as published by the Ministry of Health and Family Welfare, Government of India (Government of India, 2015).

    Higher burden states are those where the snakebite death rate at all ages is above 5/100,000 deaths for the entire study period of 2001-14 as listed in Table 3. In cases of number less than 100 deaths, they are listed as 0.0 in thousands.

Appendix 1—table 1
Snakebite deaths in the present study and mortality estimates by age and gender in 2000-2014.
Age group/Year200120022003200420052006200720082009201020112012201320142001-14
All ages
Study deaths*
Total1991831791902442142252151832001852272141752833
Male12010610311013012311511992115981301131051579
Female79777680114911109691858797101701254
Rural1901771721742232072072051721831702102061562652
Urban96716217181011171517819181
In hospital4046403248374957523836505252629
Out of hospital1591371391581961771761581311621491771621232204
Estimated deaths (000)
Total55.055.355.855.660.862.761.057.453.852.454.959.262.361.2807.5
Male29.529.429.528.731.432.431.529.527.626.928.230.632.131.1418.5
Female25.525.926.326.929.430.329.527.926.225.626.628.630.230.1389.0
Standardized death rate
Male5.45.25.24.95.35.45.14.74.34.24.34.54.74.54.8
Female4.94.94.94.95.25.35.04.74.34.24.44.64.94.84.8
Probability of dying (%) §
Male0.400.400.390.370.410.420.400.360.330.310.320.340.360.350.37
Female0.370.370.380.380.390.390.370.350.340.340.360.380.400.400.37
Children age under 15 years
Study deaths
Male4533243835393241242728252212425
Female2920153040273325262925312814372
Estimated deaths (000)
Male10.810.410.08.79.29.39.18.57.87.37.06.76.35.4116.4
Female7.98.38.78.58.68.47.87.37.07.38.29.310.110.1117.8
Age-specific death rate
Male5.65.45.14.44.74.74.64.33.93.73.53.43.22.84.2
Female4.54.75.04.84.94.74.44.13.94.14.65.35.85.84.8
Ages 15-29 years
Study deaths
Male2230283132222620172623303218357
Female1924191022192118211820211912263
Estimated deaths (000)
Male5.65.75.76.06.25.95.34.64.03.94.55.46.36.575.5
Female4.84.84.85.14.64.44.44.64.84.94.84.54.13.864.4
Age-specific death rate
Male3.73.63.63.73.73.53.12.62.32.22.53.03.43.63.2
Female3.43.33.33.43.02.82.82.93.03.02.92.72.52.32.9
Ages 30-69 years
Study deaths
Male4938453856555448444640655365696
Female2832353540395147373435394935536
Estimated deaths (000)
Male11.611.812.012.014.315.415.214.213.112.513.114.616.217.0193.0
Female10.710.911.111.412.813.513.212.411.611.311.812.813.814.0171.2
Age-specific death rate
Male6.05.95.95.76.67.06.76.15.55.15.35.76.16.36.0
Female5.85.75.75.66.26.46.15.65.14.84.95.25.45.45.6
Age 70 years or above)
Study deaths
Male456377310716710610101
Female31751265674765983
  1. Notes:

    * Study deaths were from 2001 to 2014 MDS study rounds.

  2. Estimated deaths were adjusted to United Nations Population Prospects estimated India deaths (United Nations, 2019).

    Annual death rates per 100,000 were standardized to 2001 census year population.

  3. § The probability of dying from snakebite before age 70 years in the hypothetical absence of other causes.

    Annual deaths above age 70 years were too few to quantify for death rates or totals, but total death estimates for the whole study period in thousands were 33.5 for males and 35.6 for females.

Appendix 1—table 2
Expected snakebite prevalence in 2015.
In- hospital case-fatality rate/100 bitesOut-of-hospital to in-hospital hypothetical ratio
K = I(h')/I(h)
Hypothetical % who sought hospital treatment 1/(k+1)Expected no. of snakebites in 000No. of envenomations in 000No. of dry bites in 000
In-hospitalOut-of- hospitalTotal
(1)(2)(3)(4)(5)(6)(7)(8)
3.21.540%442.2663.41,105.6773.9331.7
3.22.033%442.2884.51,326.7928.7398.0
3.23.025%442.21326.81,769.01238.3530.7
  1. Notes:

    1. We calculated in-hospital case-fatality rates (CFR) (Column 1) from a regression analysis of 66 relevant studies in the systematic literature review (Appendix 2—table 1). We excluded the Government’s annual health statistics reporting from public hospitals as case-fatality rates calculated from these data were implausibly low and inconsistent. We used an ordinary least square regression to calculate the combined CFR, treating the number of snakebite deaths as the outcome variable and snakebite prevalence as the explanatory variable while excluding outliers. The in-hospital snakebite case-fatality rate (per 100 bites) is:

  2. CFR(h)=D(h)I(h)100(1)

    where D(h) represents the number of in-hospital snakebite deaths and I(h) represents the in-hospital snakebite prevalence. The CFR was 3.2% and 95% CI were (2.5, 3.8) (Appendix 2—table 1).

  3. 2. The MDS study estimates 62,300 snakebite deaths in 2015, of which 22.7% or 14,200 died in hospitals. Inverting formula 1 with the CFR of 3.2 to solve for I(h) yields 442,200 in-hospital snakebite prevalence in 2015 (Column 4).

    3. To estimate out-of-hospital prevalence of snakebites (Column 5), we used a hypothetical relationship between in-hospital and out-of-hospital prevalence. If the out-of-hospital to in-hospital prevalence proportion is ‘K’, then we can express the out-of-hospital snakebite prevalence I(h’) as:

  4. I(h)=KI(h)(2)

    K is an unknown parameter but can also be expressed by 1/(k+1) to represent the proportion of prevalent snakebite cases that would have sought in-hospital treatment. Given the estimated I(h), we determined I(h’) by varying the K values. We applied 1.5, 2.0, and 3.0 as plausible K values (Column 2), corresponding to 40%, 33.3% and 25% of cases who sought treatment (Column 3).

  5. 4. The sum of I(h) and I(h’) or Columns 4 and 5 is the national snakebite prevalence (Column 6).

    5. Among 44 studies, an average of 70% of patients received antivenom after a diagnosis of systematic envenomation (Appendix 2—table 1). We applied this percentage to obtain the expected number of envenomations in India (Column 7). The remainder were “dry bites” without envenomation (Column 8).

Appendix 2—table 1
Case-fatality and summary of public health related snakebite characteristics.

(Summary of 78 snakebite studies from 2000 to 2019 included in the systematic review).

Source of study
VariableAutopsyCommunity surveyEMSHospitalAll studies combinedVariable range **
Summary of study outcomes
 No. of studies7416678
 No. of snake bites193814052750956738 87590
 No. of snake bite deaths1938131359901 3329
Case-fatality (per 100 bites)*
 Crude estimaten.a.9.31.31.63.8(1.3, 9.3)
 Regression estimaten.a.12.21.23.2
Summary characteristics of snakebites (n = no. of studies)
Age (in years) (n = 43)
 <1514%10%11%11%11.1%(9.6, 13.8)
 15–2924%30%30%32%30.4%(24.0, 32.0)
 30–6960%58%57%55%56.5%(54.6, 59.8)
 70+2%2%2%2%1.9%(1.7, 2.4)
Sex (n = 66)
 Male70%62%56%61%58.5%(56.0, 70.2)
 Female30%38%44%39%41.5%(29.8, 44.0)
Season (n = 19)
 Summer (March-May)18%n.a.19%17%19.1%(17.3, 19.5)
 Monsoon (Jun-Sep)51%n.a.47%53%47.9%(46.8, 52.8)
 Post Monsoon (Oct-Dec)21%n.a.25%21%24.1%(21.1, 24.9)
 Winter (Jan-Feb)10%n.a.9%8.8%8.9%(8.8, 9.5)
Place bite happened (n = 16)
 Indoor37%16%n.a.38%36.4%(15.9, 38.0)
 Outdoor63%84%n.a.62%63.6%(62.0, 84.1)
Body location (n = 40)
 Lower extremity66%82%n.a.77%76.7%(66.3, 81.9)
 Upper extremity31%16%n.a.21%21.2%(16.2, 30.9)
 Head, neck or trunk3%2%n.a.2%2.1%(1.9, 2.8)
Snake species identified (n = 33)
 Russell's viper71%n.a.n.a.42%43.2%(42.2, 71.0)
 Krait9%n.a.n.a.18%17.7%(9.0, 18.0)
 Cobra14%n.a.n.a.12%11.7%(11.6, 14)
 Hump nose vipern.a.n.a.n.a.4%4.0%(4.2, 4.2)
 Saw-scaled vipern.a.n.a.n.a.2%1.7%(1.8, 1.8)
 Water snaken.a.n.a.n.a.0.4%0.3%(0.4, 0.4)
 Unknown6%n.a.n.a.22%21.3%(6.1, 21.9)
Time of the bite (n = 18)
 12am-6am6%n.a.13%23%13.6%(5.6, 22.8)
 6am-Noon35%n.a.28%23%27.4%(23.3, 35.2)
 Noon-6pm39%n.a.29%25%28.9%(24.9, 38.9)
 6pm-12am20%n.a.30%29%30.1%(20.4, 30.2)
Hours to treatment (n = 19)††
 <6 hrn.a.n.a.100% 66%65.9%(23.6, 100)
 6–12 hrn.a.n.a.0%18%17.9%(2.7, 36.3)
 12–24 hrn.a.n.a.0%10%9.8%(4.1, 33.3)
 >24 hrn.a.n.a.0%6%6.4%(0.7, 31.9)
Number treated with antivenom (n = 44)§ ††
 Treatedn.a.n.a.n.a.70%69.7%(13.3, 100)
Survived by antivenom (n = 19)¶ ††
 Failedn.a.n.a.n.a.6%5.6%(0, 34.6)
 Survivedn.a.n.a.n.a.94%94.4%(65.4, 100)
  1. Notes:

    * Crude case fatality rates are the aggregated number of deaths divided by snakebites. Case-fatality regression estimate was calculated after refining the row data for outliers. After careful assessment of all 66 hospital studies, only 11727 snakebite events followed by 487 deaths from 44 studies were considered for regression estimate (3.17, 95% Cl (2.54, 3.79)).

  2. EMS - ‘108 call’ GVK Emergency Ambulance Services in India (Gimkala et al., 2016). EMS data is for 2014 covering 12 states in India (Andhra Pradesh, Chhattisgarh, Dadra and Nagar Haveli, Daman and Diu, Goa, Gujarat, Himachal Pradesh, Karnataka, Meghalaya, Tamil Nadu, Telangana, Uttarakhand). Out of 359 EMS deaths, 168 died before reaching hospital and the remainder died after 48 hr follow up in hospitals.

    Time from EMS service call to transport to hospital.

  3. § Patients who received antivenom at hospital after diagnosis of systematic envenoming.

    Survived by antivenom was calculated by dividing the deaths or survivors by number treated with antivenom. n.a. - Not available or not relevant.

  4. ** Variable range (minimum, maximum) observed in study groups. When available for only one study group, range within the observed studies in that group.

    †† Pooled estimates for ‘Hours to treatment’, ‘Number treated with antivenom’ and ‘Survived by antivenom’ were from hospital studies only.

Appendix 2—table 2
Systematic review summary of state coverage by years of 78 studies.
No. of studiesTotal no. of snakebitesTotal no. of snakebite deathsSources of studiesPublication year/number of studies
StateAutopsyCommunity surveyEMSHospital199920022004200520062007200820092010201120122013201420152016201720182019
1Andhra Pradesh4628314571111.....1......111...
2Bihar31171291212
3Chandigarh42976...4...1...11.1.......
4Chhattisgarh1208452..1...............1...
5Dadra and Nagar Haveli13841..1...............1...
6Daman and Diu112..1...............1...
7Goa1244..1...............1...
8Gujarat1362891..1...............1...
9Haryana117...1............1.....
10Himachal Pradesh4144228..13............211...
11Jammu and Kashmir110...1.........1........
12Jharkhand135619...1.............1....
13Karnataka20528113911181214413111
14Kerala53169131...5.............3.11.
15Maharashtra1848844322161111112321121
16Meghalaya113..1...............1...
17New Delhi162....1...1..............
18Odisha210133...2.............1...1
19Pondicherry1509...1....1.............
20Tamil Nadu751,19837121431111
21Telangana1395692..1...............1...
22Uttar Pradesh4249901..3..........11.11...
23Uttarakhand13294..1...............1...
24West Bengal6237034524111111
Total9087,590332974126711142143148991315446
  1. Note:

    The 78 studies we reviewed were published over 20 year’s period and data are corresponding to 1999–2019 from 24 different states. Except in a few studies, data of individual studies were confined to a single state. Therefore, possibility of overlapping of study data within states would be minimal and we verified the areas when several studies were conducted in the same year within the same state. One study from 1999 was included because no other studies were found around the year of 2000.

Appendix 3—table 1
Parameter estimates for covariates in the geostatistical Bayesian Poisson model.
Relative risk of snakebite mortality
0.5 quantile0.025 quantile0.975 quantile
(Intercept)1.0110.4561.705
Urban vs rural0.2800.2290.338
Female illiteracy in rural areas1.4271.2761.596
Altitude (below 400 m)1.9050.8124.392
Altitude (above 400 m)0.5080.3050.824
Temperature (below 20°C)4.7741.65815.764
Temperature (above 20°C)1.1700.5022.641
range/1000 (ϕ/1000)442.001244.373847.835
sd of spatial random effect (σ)0.5870.4420.796
sd of random walk two for year0.0030.0010.007
sd of sampling unit effect (τ)0.5560.4660.655

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  1. Wilson Suraweera
  2. David Warrell
  3. Romulus Whitaker
  4. Geetha Menon
  5. Rashmi Rodrigues
  6. Sze Hang Fu
  7. Rehana Begum
  8. Prabha Sati
  9. Kapila Piyasena
  10. Mehak Bhatia
  11. Patrick Brown
  12. Prabhat Jha
(2020)
Trends in snakebite deaths in India from 2000 to 2019 in a nationally representative mortality study
eLife 9:e54076.
https://doi.org/10.7554/eLife.54076