RESEARCH ARTICLE
Epidemiology, ecology and human
perceptions of snakebites in a savanna
community of northern Ghana
Yahaya Musah1, Evans P. K. Ameade1,2, Daniel K. Attuquayefio1, Lars H. Holbech 1ID *
1 Department of Animal Biology and Conservation Science, University of Ghana, Accra, Ghana,
2 Department of Pharmacology, University for Development Studies, Tamale, Ghana
* l.holbech@gmail.com
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Background
Worldwide, snakebite envenomations total ~2.7 million reported cases annually with
~100,000 fatalities. Since 2009, snakebite envenomation has intermittently been classified
as a very important ‘neglected tropical disease’ by the World Health Organisation. Despite
OPEN ACCESS
this emerging awareness, limited efforts have been geared towards addressing the serious
Citation: Musah Y, Ameade EPK, Attuquayefio DK,
public health implications of snakebites, particularly in sub-Saharan Africa, where baseline
Holbech LH (2019) Epidemiology, ecology and
human perceptions of snakebites in a savanna epidemiological and ecological data remain incomplete. Due to poverty as well as limited
community of northern Ghana. PLoS Negl Trop Dis infrastructure and public health facilities, people in rural Africa, including Ghana, often have
13(8): e0007221. https://doi.org/10.1371/journal. no other choice than to seek treatment from traditional medical practitioners (TMPs). The
pntd.0007221
African ‘snakebite crisis’ is highlighted here using regionally representative complementary
Editor: Jean-Philippe Chippaux, Institut de data from a community-based epidemiological and ecological study in the savanna zone of
Recherche pour le Développement, BENIN
northern Ghana.
Received: February 1, 2019
Accepted: June 25, 2019
Methodology and findings
Published: August 1, 2019
Our baseline study involved two data collection methods in the Savelugu-Nanton District (in
Copyright: © 2019 Musah et al. This is an open
2019 the district was separated into Savelugu and Nanton districts) in northern Ghana, com-
access article distributed under the terms of the
Creative Commons Attribution License, which prising a cross-sectional study of 1,000 residents and 24 TMPs between December 2008
permits unrestricted use, distribution, and and May 2009. Semi-structured interviews, as well as collection of retrospective snakebite
reproduction in any medium, provided the original
and concurrent rainfall records from the Savelugu-Nanton District Hospital and Ghana Mete-
author and source are credited.
orological Authority respectively over 10-years (1999–2008) were used in the study. Vari-
Data Availability Statement: All relevant data are
ables tested included demography, human activity patterns, seasonality, snake ecology and
within the manuscript and its Supporting
Information files. clinical reports. Complementary data showed higher snakebite prevalence during the rainy
season, and a hump-shaped correlation between rainfall intensity and snakebite incidences.
Funding: This paper formed part of a study that did
not receive funding of any kind from any Almost 6% of respondents had experienced a personal snakebite, whereas ~60% of
commercial or non-commercial organisation. respondents had witnessed a total of 799 snakebite cases. Out of a total of 857 reported
Competing interests: The authors have declared snakebite cases, 24 (~2.8%) died. The highest snakebite prevalence was recorded for
that no competing interests exist. males in the age group 15–44 years during farming activities, with most bites occurring in
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Snakebite epidemiology in northern Ghana
the leg/foot region. The highest snakebite rate was within farmlands, most severe bites fre-
quently caused by the Carpet viper (Echis ocellatus).
Conclusion
The relatively high community-based prevalence of ~6%, and case fatality ratio of ~3%, indi-
cate that snakebites represent an important public health risk in northern Ghana. Based on
the high number of respondents and long recording period, we believe these data truly
reflect the general situation in the rural northern savanna zone of Ghana and West Africa at
large. We recommend increased efforts from both local and international health authorities
to address the current snakebite health crisis generally compromising livelihoods and pro-
ductivity of rural farming communities in West Africa.
Author summary
Snakebite envenomations cause tens of thousands of deaths and hundred thousands of
injuries in many developing tropical countries annually, and sub-Saharan Africa repre-
sents an epitome example of this ‘neglected tropical disease’. We here present data col-
lected over a 10-year period applying different methodologies across a typical rural
savanna community of northern Ghana. Our data corroborates previous findings from
the region that snakebites represent a serious public health threat, and that young and
active farmers are particularly at risk, hence compromising both livelihoods and economic
wealth of the people. We highlight that many interrelated factors involving both snake
ecology and human behaviour in particular, are responsible for the past and current high
snakebite prevalence recorded. We conclude that our findings support increased and con-
certed efforts from both local authorities and state institutions to address the African
snakebite crisis that continues unabated. Such interventions require generation of more
general baseline data on snake ecology and human behaviour, combined with public
awareness campaigns, education and information. To achieve this, we recommend com-
munity-based stakeholder meetings involving local people, traditional authorities, as well
as public institutions aiming at addressing the ongoing snakebite menace in this part of
the world.
Introduction
Snakebite envenomations constitute one of the most important human-wildlife conflicts, caus-
ing considerable yet largely insufficiently known magnitudes of socio-economical losses, mor-
bidity and death [1]. Globally, out of>3,500 snake species, ~600 are venomous, and ~280 are
considered medically important, causing a conservatively estimated >1.2 million snakebite
envenomations with ~100.000 deaths and>400,000 cases of morbidity annually [1, 2, 3, 4].
Prevailing conservative estimates of the global burden of snakebite envenomations and fatali-
ties are probably highly underrated as majority are based on conventional health facility
reports, largely neglecting cases treated by local traditional medical practitioners (TMPs) [1, 5,
6]. Perhaps more realistic annual estimates indicate between 4.5–5.4 million snakebites, 1.8–
2.7 million envenomations and up to 138,000 deaths [6, 7]. Snakebite envenomation is largely
a disease of poverty, with developing countries in the tropics recording the highest rates of
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Snakebite epidemiology in northern Ghana
incidence, morbidity and mortality [4, 8, 9]. People engaged in farming, hunting, fishing and
other rural activities are at highest risk, mostly bitten on their limbs during work [9, 10]. In
many parts of sub-Saharan Africa, the high mortality and morbidity rates are attributed to
increased vulnerability caused by both high work risk and exposure to diverse snake habitats,
as well as poor infrastructure and limited access to appropriate medical treatment and health
facilities [1, 4, 6]. Currently, an estimated ~100 million people, particularly in southeast Asia
and Africa, live in vulnerable areas with very high exposure to snake envenomation and lack of
effective antivenom therapy [4]. The current ‘global snakebite crisis’ as a disease of poverty,
has been misunderstood, underrated, ignored or neglected as a public health issue [5, 8, 11,
12], and has lately regained prominence as one of the most important ‘neglected tropical dis-
eases’ [7].
In order to mitigate the inadequate health care and treatment of victims of snakebite enven-
omations, concerted international effort is essential to gather steady and inclusive data on the
epidemiological nature of snakebites with socio-demographic and geographic dimensions as
well as aspects of snake biology and ecology [4, 5, 12, 13]. Mapping of comprehensive datasets
is imperative for understanding the dynamics of human-wildlife conflict such as snakebite vul-
nerability, and constitute the baseline information needed to provide adequate health facilities
and supply of antivenom and other therapeutical innovations [1, 2, 6, 14]. However, inclusive
community-based information is currently limited from many high-risk areas particularly in
sub-Saharan Africa [15, 16]. There is therefore the need for detailed information from studies
combining both field and hospital data [4, 6, 9]. Here, we present a comprehensive and com-
plementary epidemiological dataset of snakebite envenomations from northern Ghana, com-
prising both household and TMP surveys as well as retrospective hospital reports covering the
period 1999–2009. Apart from contributing baseline epidemiological snakebite data, our sur-
vey, conducted by snake ecologists, also targeted human-wildlife conflict dynamics, with the
purpose of providing insight into measures for improving snakebite prevention and facilita-
tion of effective therapeutic methods. We note that the vast majority of snakebite studies are
undertaken solely by medical officers, and as such mainly focused on clinical-pharmaceutical,
socio-demographic and epidemiological aspects, with much less attention to biology and ecol-
ogy of humans as well as snakes. An additional objective of this paper was to apply an integra-
tive approach involving snake ecology and common snakebite epidemiology, in order to
increase our understanding of the complex human-wildlife conflict that snakebites truly repre-
sent. We consider that such holistic research foci are vital and urgently required by interna-
tional funding agencies and national public health institutions in their joint efforts to address
the ongoing global snakebite crisis [2, 4, 7, 10, 12, 13].
Methods
Study area
The Savelugu-Nanton District, covering ~2023 km2, is located in the Northern Region of
Ghana. It is bordered by five other districts (Fig 1), notably West Mamprusi (north), Karaga
(east), Tolon-Kumbungu, and Tamale Metropolitan Area (west) and Yendi (south). Based on
a 2010-population census count of 139,283 (female/male %-ratio = 51.5/48.5) and an annual
growth rate of about 2.5% for northern Ghana [17], we estimated the total population of the
district as ~130,000 in 2008, translating to a mean density of ~64 persons km-2. The district
falls within the Guinea Savanna vegetation zone of northern Ghana, with a single-peak, erratic
rainfall pattern, increasing rapidly from April, peaking in August-September, then sharply
decreasing during October, and ranging between ~600 to ~1,000 mm annually on average
[18]. Mean daily temperatures are usually high, averaging 34˚C, with maximum of>42˚C and
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Snakebite epidemiology in northern Ghana
Fig 1. Map of the Savelugu-Nanton District in northern Ghana, showing major roads, rivers, and the seven selected townships for the study. Line
drawings produced with CorelDraw version 13.
https://doi.org/10.1371/journal.pntd.0007221.g001
minimum of<15˚C [18]. Retrospective monthly rainfall data during 1999–2008 were obtained
from the Ghana Meteorological Authority in Accra. The sparsely-populated northern parts of
the district have denser vegetation, mostly with regenerating woodlands, compared with the
more urbanized south around the Tamale Metropolis characterised by more intensive farming,
bush burning and tree felling for charcoal production. Many woodland tree species are
drought-resistant and foliage is largely retained during the prolonged dry season (November-
March).
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Snakebite epidemiology in northern Ghana
Data collection
Ethics Statement. Prior to conduction of interviews, traditional authorities were con-
sulted and appropriate customary rites duly performed with consent of all participants. No
ethical clearance was required from any public institution in Ghana for this kind of study, but
all patient data was treated with anonymity and permission was granted from hospital authori-
ties at the Savelugu District Hospital in line with codex of conduct.
We conducted a six-month cross-sectional respondent study between December 2008 and
May 2009 in the seven most populated communities (= study sites) in the district (Fig 1),
comprising 1,000 community residents and 24 TMPs operating in these communities. Both
residents and TMPs were subjected to similar, detailed, independently-administered, semi-
structured questionnaires. Prior informed consent (PIC) was obtained from traditional
authorities in each community after explanation of the scope, purpose and procedure of the
study [19]. Such independent administration of interview protocols and PIC enhance the reli-
ability and inclusiveness of respondent information and hence both the quantity and quality of
informant data [20, 21]. The selection of residents was stratified across three age-groups, each
with gender equality;>30 years (400); 15–30 years (300); <15 years (300). This was attributed
to higher encounter frequency of, and more precise and perceptive information gathered
from, the elderly. The number of residents sampled from each of the seven study sites generally
reflected community size and were; Savelugu (200), Diare and Pong-Tamale (150 each),
Nanton, Zoggu, Moglaa and Tampion (125 each). Within each of the seven communities,
household units were selected on ad hoc basis, inclusively conforming to the gender-age strati-
fication criteria. The selection applied an approach of consecutively enumerating units in a
sequence, and adopting an arbitrary criterion of a minimum distance of about 25–50 m and
maximum distance of about 50-100m, with longer distances between units in the sparsely pop-
ulated community fringes, and narrower selection in densely populated community centres.
To minimize inconsistencies from recall biases during interviews, the reliability of information
and credibility of informants were continually considered. The principal investigator assisted
by his local counterpart exercised particular patience and pedagogical skills to explain the
topics and agendas involved. The 24 TMPs were selected opportunistically using ‘Snowball
sampling’ [19], utilising the confidence gained from one participant to the next, aiming at
including nearby as well distant TMPs, in order to minimize selection biases in that regard.
Interviews of household respondents (HR) and TMPs aimed at producing three types of data:
1) personal snakebite cases experienced by HR and TMPs; 2) knowledge of snakebite cases of
other community members by HR; 3) perception on various variables rather than personal
experiences of cases by HR and TMPs. By asking the same questions to both HR/TMPs we
were able to test the similarity in responses by using %-ratios for both dichotomous (e.g. male/
female, dry/wet season) or polychotonous (e.g. habitat categories for snake encounters, day-
time and symptoms) questions. Estimates on derived snakebite rates could then be compared
from the two complementary datasets (HR vs. TMPs) across the sections of the communities.
As some HR were unable to recall all information pertaining to sub-group variables of each
question (e.g. habitat type or symptoms), the %-ratios were based on different totals (n), for
which analyses were accounted. Complementing the community-based surveys was a retro-
spective study of reported cases of snakebites over a 10-year period (1999–2008) that were
obtained from the Savelugu-Nanton District Hospital, the largest district hospital that manages
snakebite victims. Patient data were analysed anonymously by the lead author and a local assis-
tant, after obtaining formal approval and ethical clearance from the Savelugu-Nanton District
Hospital authorities. These data were largely inconsistent and incomplete with other data than
date, gender, age and fatalities, so data analysis unfortunately did not include details on
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Snakebite epidemiology in northern Ghana
treatment, snake culprits and prior TMP consultation. Note that the survey data presented
here were parallel to other ecological studies of abundances and distribution of snakes, just as
many snake culprits were brought to us for identification. The principal investigator (lead
author) identified snakes from secondary data by using local names and using a photo guide of
the commonest snakes in the area.
Data analysis
Frequencies of occurrence (%) in each respondent category were compared among different
sub-groups, and associations tested for statistical differences with Fisher’s exact test for 2×2
contingency tables (two sub-groups compared) or χ2 G-test for three or more sub-groups com-
pared (2×3 contingency tables). Associations between rainfall and snakebite incidences were
determined using both GLM and polynomial regression with Pearson’s (r) or Spearman rank
(rs) correlation coefficients. To test the similarity in responses (%-ratios only) among various
types of data sets (e.g. encounters vs. cases from HR data only, or HR vs. TMP perception
data) we used non-parametric Spearman rank (rs) correlation coefficients and Wilcoxon’s
signed rank tests (two-tailed). Whereas retrospective hospital records readily provided esti-
mates of actual annual snakebite incidence and mortality rates per 100,000 inhabitants, the
simple interview-based prevalence and case fatality ratios (CFR) expressed as % of totals, only
merited such estimates based on particular non-validated assumptions, and therefore reserved
for the Discussion only. Hospital and informant data were analysed using Microsoft Excel and
GraphPad version 5.01. Significance level was determined at p< 0.05.
Results
Household survey
Educational level of respondents. Majority (518) of 1,000 respondents (~52%) had no
formal education whereas ~44% had only basic primary education (7–9 years of schooling).
Only ~4% had additional secondary education (10–12 years of schooling), with<0.5% having
tertiary education (>12 years of schooling) only (Table 1). Hence, respondents were primarily
made up of either illiterates or people with modest schooling.
Table 1. Basic socio-demographic characteristics and snake encounter statistics of the respondent community
population (n = 1,000 residents) comprising seven communities surveyed in the Savelugu-Nanton District of
northern Ghana (Dec 2008-May 2009).
Respondent variable No. of respondents (%)
Males 500 (50.0)
Females 500 (50.0)
<15 years old 300 (30.0)
15–30 years old 300 (30.0)
>30 years old 400 (40.0)
No formal education (illiteracy) 518 (51.8)
Basic primary school level (7–9 yrs) 439 (43.9)
Secondary school level (10–12 yrs) 39 (3.9)
Tertiary educational level (> 12 yrs) 4 (0.4)
Experienced a snake encounter 934 (93.4)
Experienced a snakebite personally (E) 58 (5.8)
Witnessed a snakebite (including personal snakebites)� 604 (60.4)
Snakebite incidences witnessed in their community (W)� 799 (79.9)
Total snakebite incidences reported (E+W) 857 (85.7)
�The breakdown of 799 cases witnessed by 604 respondents is found in Table 4.
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Snakebite epidemiology in northern Ghana
Table 2. Associations of reported personal snakebite incidences (n = 58) with gender and age-group of 1,000 community members (male/female = 500 each) inter-
viewed in the Savelugu-Nanton District of northern Ghana (Dec 2008-May 2009).
Variable Sub-group variable Frequency (%) Test-statistics p-value
Gender Male 36 (62.1) Fisher’s exact test (2×2) 0.0778
Female 22 (37.9)
Age <15 years 11 (19.0) χ2 G-test (2×3) = 14.616 0.00067
15–30 years 10 (17.2)
>30 years 37 (63.8)
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Snakebite prevalence based on personal experience: Comparing gender and age of vic-
tims. Considerably more males (~62%) than females (~38%) were reportedly bitten by
snakes (n = 58 cases), although the difference was not statistically significant (Fisher’s exact
test; p = 0.0778, df = 1), at the 5% level (Table 2). With regards to age, significantly (χ2 =
14.616; p = 0.00067, df = 2) more victims were in the age group >30 years (~64%), whereas the
group of 15–30 years (~17%) and <15 years (~19%) were similar in snakebite prevalence
(Table 2).
Personal encounters with snakes and witnessing of snakebites. As many as 934 (~93%)
respondents had encountered snakes during their lifetime and hence been exposed to snake-
bite risk, and 58 respondents (~6%) claimed to have been bitten by snakes, irrespective of
actual envenomation or hospitalisation (Tables 1 and 2). Of the 934 snake encounters
(Table 3) majority encountered snakes on their farms (604; ~65%), but also in the bush
(~16%) or in their homes (~11%). Considerably lower encounter frequencies were attributed
to roads and footpaths (~6%), school facilities (~2%) and open urban drains (<1%). Snake
encounters were predominant during afternoon (~50%) and morning (~40%) hours, particu-
larly during the rainy season, accounting for ~72% of yearly records by respondents (Table 3).
A total of 604 (~60%) respondents provided knowledge about 799 snakebite cases in total
from their respective communities (Tables 3 and 4). Thus, the total number of recorded cases
of snakebites, including personal experiences (n = 58) was 799 + 58 = 857, with a total of 24
(CFR ~2.8%) reported deaths (Tables 1 and 5). A total of 13 (~54%) died at hospitals and 11
(~46%) at local TMPs according to the 604 HRs who reported 24 fatalities out of the 857 cases
they had witnessed from other community members (W) and experienced (E) personally (E
+ W = 857; Table 1).
Table 3. Characteristics of personal snake encounters and witnessing of bites reported (n = 934 encounters and n = 670, 828 or 857 incidences) among 1,000 com-
munity members interviewed in the Savelugu-Nanton District of northern Ghana (Dec 2008-May 2009).
Respondent variable Sub-group variable Encounters (%) Bites (%)
Encountering habitat location Farmlands 604 (64.7) 543 (81.0)
Bushes 145 (15.5) 56 (8.4)
House and yards 100 (10.7) 54 (8.1)
Paths and roads 60 (6.4) 5 (0.7)
School facilities 19 (2.0) 9 (1.3)
Open city drains 6 (0.6) 3 (0.5)
Encountering time of the day Afternoon 471 (50.5) 334 (40.3)
Morning 372 (39.8) 315 (38.0)
Evening and night 91 (9.7) 179 (21.6)
Encountering season of the year Rainy season 669 (71.6) 610 (71.2)
Dry season 265 (28.4) 247 (28.8)
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Snakebite epidemiology in northern Ghana
Table 4. Snakebite cases reported by each of 604 respondents out of 1,000 community members interviewed in
the Savelugu-Nanton District of northern Ghana (Dec 2008-May 2009).
Cases Respondents Total
One 449 449
Two 121 242
Three 30 90
Four 3 12
Six 1 6
Total 604 799
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Of the 857 snakebite victims, majority (~70%) were males, predominantly in the 15–30
year- (~54%) and>30 year- (~35%) age groups (Table 5). Farmlands were the most frequently
reported locations (~81.0%) for snakebite, primarily during the rainy season (~71%), in the
mornings (~40%) and afternoons (~38%) (Table 5). Snakebites occurred mainly on the
extremities, with lower limbs (legs and feet; ~65%) and upper limbs (arms and hands; ~34%)
being the most vulnerable, for which swelling (~53%) and bleeding (~39%) were the common-
est symptoms reported (Table 5).
The associations between %-respondents for the concurrent data sets of snake encounters
versus snakebite experiences showed highly significant positive correlations across the six hab-
itat types (rs = 0.9908, p = 0.000127, two-tailed, n = 6,), as well as across the six habitat types,
three daytime periods and two seasons combined (rs = 0.9545, p< 0.00001, two-tailed,
n = 11).
Traditional medical practitioner (TMP) survey
Knowledge and perceptions of snakebite victims and snake culprits. From their percep-
tions (not actual cases), the 24 TMPs reported that majority of patients were males (~92%), in
the>30 year- (~54%) and 15–30 year- (~42%) age groups, most often bitten on farmlands
(~67%) and bushes (~29%), during the rainy season (~83%), in the morning (~46%) and after-
noon (~42%) hours (Table 5). According to the TMPs, most susceptible human body parts are
legs and feet (~79%), followed by the arms and hands (~21%), with bleeding (~48%) and swell-
ing (~33%) as most frequently reported symptoms (Table 5). The general snake descriptions
provided by the TMPs indicated that three snake species were most likely involved in ~81% of
all cases reported (Fig 2); Carpet Viper Echis ocellatus (~35%), Night Adder Causus maculatus
(~26%), and Black-necked Spitting Cobra Naja nigricollis (~20%). The %-responses to 27 simi-
lar questions (i.e. the first 27 sub-group variables = rows tested pair wise in Table 5) among
857 HRs matched well with those %-responses of the 24 TMPs (Table 5), as shown by the two
datasets not being significantly different (rs = 0.8469, r = 0.9245, p< 0.00001, two-tailed,
n = 27; z = 0.0721, p = 0.9442).
Retrospective hospital study
Snakebite prevalence: comparing gender and age of victims. Based on the 10-year
(1999–2008) retrospective records of snakebite cases (n = 450) at the main district hospital, sig-
nificantly more males, particularly in the 15–44 years age group (χ2 G-test = 29.56,
p< 0.00001, df = 2), were bitten than females, as well as males in the <15 year- and>44 year-
age groups (Table 6).
Across all three age groups, males dominated in number of reported cases, whereas the
females constituted relatively fewer cases in the youngest age group (2.7%) but 4–8 times more
in the two older groups (Table 6). For both males and females, the 15–44 years group
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Snakebite epidemiology in northern Ghana
Table 5. Comparison of actual reported cases and perceptual characteristics of snakebite victims and incidences based on household surveys (HR; �nmax = 857
cases) and traditional medical practitioners (TMP; ��n = 24 respondents’ perceptions, not cases; ���n = 42 and 65 cases), respectively among 1,000 community mem-
bers and 24 TMPs, interviewed in the Savelugu-Nanton District of northern Ghana (Dec 2008-May 2009). For perception of best treatment, n� = 1000 cases.
Respondent variable Sub-group variable Survey frequency (%)
(n = responses) Household TMP
Gender Male 584 (70.1) 22 (91.7)
(�n = 833; ��n = 24) Female 249 (29.9) 2 (8.3)
Age-group of victim 15–30 years 222 (53.9) 13 (54.2)
(�n = 412; ��n = 24) >30 years 146 (35.4) 10 (41.6)
<15 years 44 (10.7) 1 (4.2)
Day time hours of snakebite Morning 334 (40.3) 11 (45.8)
(�n = 828; ��n = 24) Afternoon 315 (38.0) 10 (41.7)
Evening and night 179 (21.6) 3 (12.5)
Season of snakebite Rainy season 610 (71.2) 20 (83.3)
(�n = 857; ��n = 24) Dry season 247 (28.8) 4 (16.7)
Habitat location of snakebite Farmlands 543 (81.0) 16 (66.6)
(�n = 670; ��n = 24) Bushes 56 (8.4) 7 (29.2)
House and yards 54 (8.1) -
Paths and roads 5 (0.7) 1 (4.2)
School facilities 9 (1.3) -
Open city drains 3 (0.5) -
Position of snakebite infliction Legs and feet 540 (65.2) 19 (79.2)
(�n = 828; ��n = 24) Arms and hands 280 (33.8) 5 (20.8)
Head 7 (0.8) -
Trunk 1 (0.1) -
Symptoms most often reported Swelling 431 (52.5) 14 (33.3)
(�n = 821; ���n = 42) Bleeding 320 (38.9) 20 (47.6)
Local pain 67 (8.2) -
Dizziness 3 (0.4) -
Blood spitting - 4 (9.5)
Sweating - 2 (4.8)
Shivering - 2 (4.8)
Likely causal snake species Carpet Viper 23 (35.4)
(���n = 65) Night Adder n/a 17 (26.2)
Black-necked Spitting Cobra 13 (20.0)
Puff Adder/other Bitis sp. 8 (12.2)
Grass snakes/Psammophis sp. 4 (6.2)
Treatment methods Hospital 392 (59.8) -
(�n = 655; ��n = 24) TMP 262 (40.0) 24 (100.0)
Self-help 1 (0.2) -
Preferred treatment Hospital 798 (79.8) n/a
(�n = 1,000 respondents) TMP 196 (19.6)
Self-help 6 (0.6)
�Household survey (HR): For cases where total responses ntot < 857, are explained by failure of respondents to recall details (see Methods).
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dominated in almost 50% of all cases reported. These results are largely consistent with age-
gender trends of personally experienced snakebite cases (n = 58) reported among 1,000
respondents in the 2008–2009 household survey, with dominance of males across all age
groups, and in particular for the>30 year age group (Table 2). In summary, the most and least
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Snakebite epidemiology in northern Ghana
Fig 2. Top-Left (A): Carpet Viper Echis ocellatus (Y. Musah, 28 April 2009, Moglaa). Top-Right (B): Black-necked
Spitting Cobra Naja nigricollis (Y. Musah, 26 January, 2019 Tamale). Down-Left (C): Night Adder Causus maculatus
(Y. Musah, 4 May 2009, Moglaa). Down-Right (D): Elegant Sand Racer Psammophis elegans (Y. Musah, 5 February
2019, Nanton).
https://doi.org/10.1371/journal.pntd.0007221.g002
vulnerable to snakebites were young to middle aged men and younger girls respectively. Out
of the 450 recorded snakebite cases only one death was recorded, producing a CFR per 10 year
of 1/450 = 0.22%, and thus an annual CFR = 0.022%.
Correlations between rainfall and snakebites for the period 1999–2008
By comparing concurrent data sets of mean monthly rainfall with monthly records of snake-
bites reported to the district hospital in 1999–2008 (Fig 3), we were able to evaluate the
Table 6. Statistically-tested associations of snakebite cases (n = 450) with gender and age-group reported at the
Savelugu-Nanton District Hospital in northern Ghana (1999–2008).
Sub-group variable Gender Total (%)
Age group (years) Males (%) Females (%)
<15 90 (20.0) 12 (2.7) 102 (22.7)
15–44 133 (29.6) 91 (20.2) 224 (49.8)
>44 73 (16.2) 51 (11.3) 124 (27.5)
Total 296 (65.8) 154 (34.2) 450 (100.0)
Statistical Test: χ2 G-test (2×3) = 29.56, p < 0.00001, df = 2
https://doi.org/10.1371/journal.pntd.0007221.t006
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Snakebite epidemiology in northern Ghana
Fig 3. Mean monthly precipitation (black circles and solid line) and mean monthly number of snakebite
incidences (grey triangles and broken line) recorded at the Savelugu District Hospital (1999–2008).
https://doi.org/10.1371/journal.pntd.0007221.g003
perception reported among community members (HRs and TMPs) that snakebites were more
prevalent during the rainy season (Tables 3 and 5). The 10-year plot of rainfall-snakebite
monthly means depicted a clear unimodal rainfall curve with a single peak from July to Sep-
tember, whereas snakebite incidences displayed a trimodal pattern with peaks in March, June-
July and October (Fig 3). Hence, the largely overlapping rainfall-snakebite trend demonstrated
a positive association between rainfall and snakebite frequency, in line with respondent (both
HR victims/witnessing and TMPs) perceptions (Tables 3 and 5). We tested this apparent posi-
tive association by plotting 10-year pair-wise data of mean monthly rainfall with mean
monthly snakebite cases, and found a weak statistically significant (rs = 0.587, p = 0.0446, two-
tailed, n = 12) positive linear correlation between the two variables (Fig 4). However, the
Fig 4. Correlation between mean monthly precipitation and mean monthly number of snakebite incidences
recorded at the Savelugu District Hospital (1999–2008).
https://doi.org/10.1371/journal.pntd.0007221.g004
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Snakebite epidemiology in northern Ghana
correlation for GLM-regression using Pearson’s correlation coefficient was not significant
(r = 0.521, p = 0.0822, two-tailed, n = 12). We also performed a 2nd degree polynomial regres-
sion which showed a higher level of significance (r = 0.652, p = 0.022, two-tailed, n = 12) com-
pared with the GLM-regression, thereby indicating a hump-shaped association pattern (Fig 4).
Thus, although snakebite rates are generally linked to rainfall levels, extreme amounts of rain
appear to reduce this positive correlation.
Discussion
Our study applied a regionally representative set of complementary epidemiological data from
different community sectors for northern Ghana, by targeting various demographic sub-
groups as well as both traditional and conventional management of snake envenomations at
the district level. With a relatively large sample size of 1,024 respondents (~0.8% of district
level population) covering both dry and wet seasons, and a retrospective 10-year bivariate data
sample of snakebite incidences and rainfall patterns, our study represents an important contri-
bution to epidemiological snakebite studies for this typical West African savanna region. Pre-
vious epidemiological studies have largely been limited to short-term data series with smaller
sample sizes of predominantly retrospective hospital records for Ghana [22, 23, 24] and sub-
Saharan Africa [25, 26, 27, 28, 29], where complementary or nationwide long-term published
studies remain scarce [1, 16, 30, 31]. Estimates of regional or national snakebite burdens based
exclusively on hospital records inevitably neglect many snakebite cases treated at home or by
TMPs [1, 4, 16, 30]. In contrast, our study provided a rare opportunity to test consistencies in
epidemiological baseline information gathered from different sections of a typical rural
savanna community in West Africa [16], regarding general demography and human-snake
conflict, as well as snake toxicology and ecology. In order to enhance advances in public health
capacity to address snakebite envenomation, it is important to provide inclusive and holistic
evaluations of implicating factors across the whole community and over long periods of time,
including ecological aspects [2, 4, 7, 30]. Specifically, it is important to ask where, when and
why snakebites occur, and to identify and evaluate pertinent factors that preclude or facilitate
their occurrence, treatment and prevention [1, 4, 10, 12].
We recognise that despite a relative to the small sample area (~2,023 km2) large sample size
of complementary data, biases are inevitable from the study design as well as sample procedures
and protocols. We are also aware that randomized standard sociological census procedures
were not adhered to, but we truly believe that by spreading sampling across seven distinct town-
ships including both outskirts and centres enabled us to get a good representative sample,
emphasising strict adherence to age-gender stratification criteria. Some margin of recall bias in
ability was acceptable based on a general assumption that 10 years remembrance can only be
completely accurate in few cases. In that context, we found high consistencies of responses both
within and between our complementary data set, indicating that conclusions drawn from both
datasets (e.g. HR vs. TMP) are similar, and the information most likely reliable for fair general-
isations. The comparison of snake encounters and cases based on HR data likewise suggests that
an increase in snake encounters results in increased snakebites, and the implication is that
snake encounters represent a crude index of snake-human conflict. We also recognise that our
CFR is probably underestimated due to the fact that the 799 witnessed cases could be shared
among independently-selected respondents, hence the 24/857 = 2.8% would be higher accord-
ingly. We however have no means of assessing that potential bias but if say 10% of the 799 cases
are overlapping, then it will result in a CFR = 3.1%, and if 50% shared, CFR = 5.2%.
Our study confirms the general assertion that snake envenomations leading to significant
levels of morbidity and mortality are symptomatic of rural deprivation and poverty in sub-
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Snakebite epidemiology in northern Ghana
Saharan Africa, where educational levels are pronouncedly low within farming communities
subject to limited infrastructure and mobility [4, 8, 9, 12]. Our respondents were primarily
either illiterates or people with modest schooling, a demographic feature characteristic of the
mostly deprived rural areas of northern Ghana, and a tendency particularly pronounced
among women and the elderly. We located 24 TMPs in seven larger communities, demonstrat-
ing that the TMP-inhabitant ratio of at least 1:5,000 (~24/130,000) is ~10 times lower than the
regional doctor-patient ratio for northern Ghana in 2009 [32]. As the road network in the
Savelugu-Nanton District was fairly well developed during our study, we attribute the high
patronage of TMPs mainly to low educational level and income, limited access to orthodox
medical facilities as well as high costs or lack of sufficient and effective antivenom administra-
tion. This TMP-seeking behaviour is widespread in Asia [33] and Africa [16, 34, 35, 36] where
herbal extracts of diverse medicinal plant assemblages [37] are often either culturally preferred
or are the only affordable or alternative therapeutic treatment available among low-income
rural communities with high levels of illiteracy and strong superstitious beliefs [16, 19, 38, 39,
40, 41]. Recent newspaper articles in Ghana indicate that this situation has not improved and
probably even aggravated lately [42, 43].
Based on the 1,000-respondent household survey, we conservatively estimated a snakebite
prevalence of ~6% (58 personal cases out of 1,000), and a CFR of ~3% (24 out of 857 personal/
witnessed cases; 2.8%). This translates to 58×130 equivalent to 7,540 snakebite incidences and
7,540×0.028 equivalent to ~210 deaths at the district level, for a total district population esti-
mated at ~130,000 in 2008. In comparison, a CFR of 1% was found in a similar community-
based study in Senegal [16]. We recognise that our incidence and mortality data are based on
unknown individual informant recollection periods, and we can therefore not explicitly trans-
late these district level figures into annual snakebite and mortality rates. However, assuming a
recollection period of about 10 years retrospectively for each HR respondent on average
(n = 1,000), the estimated annual snakebite cases and fatalities at district level (population of
130,000) may probably reach 7540/10 = 754, equivalent to 754/1.3 = 580 per 100,000 per year
or ~0.58%, and 210/10 = 21, equivalent to 21/1.3 ~ 16 per 100,000 per year or ~0.016% respec-
tively. A longer average respondent recollection period is unlikely, as both young and old
respondents exhibited limited memory beyond 10 years. Moreover, if such a period was ~5
years, it would translate to a doubling of cases and fatalities, which likewise appears unlikely.
The mean monthly number of cases reported to the largest district hospital was 3.9 over the
10-year period (1999–2008), which equals an average of 46.6 cases yearly (Fig 3). Based on hos-
pital records, the whole district therefore probably has a burden of at least 50 reported cases
yearly, and will probably double if the reporting percentage is up to 50% as estimated in similar
studies [12, 16, 41]. In this context, we found that out of 655 cases witnessed by HRs, as much
as 40% were claimed to have been treated by TMPs, and 60% at the hospital, which is close to
the 50–50% reporting ratio found in similar studies [12, 16, 41]. Our upper-lower limits of
annual snakebite envenomations during the 10-year period therefore range from ~100–750
per 130,000 (2008-population), equivalent to ~77–580 per 100,000 inhabitants (~0.08–0.6%),
with a mortality rate of ~2–16 per 100,000 (~0.002–0.016%). The population of Savelugu-Nan-
ton District in 2008 was ~130,000, constituting ~6% of the population in the Northern Region
of Ghana [17], so we conservatively estimate about 1,700–12,500 envenomations with about
50–350 fatalities annually (CFR ~3%) in the northern part of the country with a 2008 popula-
tion of ~2.2 million. This estimated range of fatalities constitutes 20–95% of a Ghana national
estimate of about 250–375 [40], and is within the range of current available estimates for the
sub-region [1, 9] and other estimates from northern [23] and central [22, 44] Ghana, but 5–10
times higher than southwest Ghana [24]. Our conservative estimates also indicate that in the
Northern Region (NR) of Ghana, the approximate requirement of AV snakebite treatment
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Snakebite epidemiology in northern Ghana
ranges from 500–600 units annually (not vials) per 100,000 inhabitants. With an approximate
2019-population in the NR of ~3 million, this estimate translates to 15,000–18,000 treatment
units annually.
The human deprivation, psychosocial despair, and loss of income resulting from snakebite
morbidity and mortality [7, 35, 40], are clearly highlighted by our complementary data from
the northern part of the savanna zone in Ghana, where annual snakebite burdens are the most
severe across the entire country [45]. Our data also suggest that a large proportion (40–85%,
based on estimates from hospital records versus HR data = 650/750 ~ 85%; actual percentage
from 655 cases reported ~40%) of snakebites are never reported to conventional medical treat-
ment facilities but managed by TMPs, treated at home treatment or left untreated, often with
fatal consequences [16, 24, 46]. Long delays in antivenom treatment often lead to severe cases
of morbidity (e.g. amputations) or death, even if such treatment is administered correctly [22,
44, 47, 48]. Our data support this assertion as the 10-year hospital records revealed a CFR of 1/
450 = 0.22% equivalent to 0.022% per year, in relation to the 2.8% CFR reported from HR
data, of which 60% died at the hospital, probably due to delays and prior TMP consultation.
Reportedly, some severe cases brought to the hospital were never recorded if patients died
upon arrival, and hence never admitted and treated. It is therefore important to ascertain the
extent of both untreated and delayed treatments in order to address these clinical and epidemi-
ological shortcomings in the management of snakebites in remote rural parts of Ghana and
sub-Saharan Africa [2, 13, 15, 40, 44]. We hope our snakebite data analyses from the Savelugu-
Nanton District, a typical northern savanna community in Ghana, will aid in this direction.
We consistently found that young to middle-aged males (age group = 15–44 years) were
most at risk of snakebites, corroborating similar findings from Ghana [22, 23, 24], other parts
of West Africa [15, 25, 26, 27, 47, 49, 50] and Africa in general [30, 34, 51, 52, 53]. Adolescent
and young men in their twenties are among the most active and adventurous, albeit least cau-
tious, section of rural African people [24, 27, 47, 54]. They expose themselves to snake encoun-
ters by risky behaviour during land clearing, harvesting, bush and charcoal burning, hunting
and commuting on foot during dark or early morning hours with impaired visibility in dim
light and dense vegetation [24, 50, 53]. Minors and the elderly who are traditionally home-
bound, are less involved in farming activity, and are generally more cautious in their behav-
iour, which possibly explains their much lower snakebite vulnerability [31]. Some girls and the
elderly were however bitten at home or in school facilities, indicating that everyone is at risk of
snakebites [7, 24, 31, 46, 54, 55]. Contrary to our findings, some studies in Africa actually
report relatively higher snakebite prevalence in children, including girls, probably as a result of
higher child-labour engagement or poorer parental care and supervision in such areas [23, 31,
53, 54, 56, 57, 58, 59].
Our data from HRs and TMPs indicated that farmlands and bushes, and to a lesser extent,
residential areas and roads are typical habitats for snakebite, as corroborated by several other
studies in rural Africa [16, 31, 38, 53, 54]. Likewise, majority of bites occur during the peak
farming periods (e.g. shea nut, millet and yam) when land is prepared for planting (March-
April), maintained by weeding (May-June), and harvested (June-October) [23, 50, 54]. Our
long-term bivariate rainfall-snakebite data indirectly reflect the strong link between peak sea-
sons of farming and rainfall, partly because artificial water sources are largely unavailable to
the small-scale peasant farmer in northern Ghana and other parts of arid savanna zones in
Africa. However, even though rainfall and snakebites are generally positively-correlated, our
data also suggest that very intense rainfall reverses the trend, possibly caused by decreased
activity of both snakes and humans as well as lower snakebite reporting rates due to the
reduced mobility from flooding and erosion of basic road infrastructure. Although the dry sea-
son recorded lower snakebite incidences, farmers are also at risk during this period, often
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Snakebite epidemiology in northern Ghana
being bitten during bush or charcoal burning, hunting, harvesting firewood, and at home dur-
ing reduced farming activity in November-April [22, 50, 53].
As agricultural mechanisation is particularly low in northern Ghana, predominantly man-
ual activities using the limbs expose farmers to snakes concealed in vegetation, soil and crops.
This may explain why those extremities are the most prone to snakebites [23, 47, 50, 54]. Farm-
ing activities primarily take place during morning or late afternoon in order to avoid excessive
sun exposure and heat during midday. Such factors also result in the poikilothermic snakes
seeking warm areas during morning hours and shade in the hot midday and early afternoons.
Nocturnal snakebites were mostly confined to homes and roads, a pattern found in many
other rural areas of Africa, and attributed to walking barefoot, or inappropriate footwear and
poor domestic lighting conditions [25, 31, 48, 54].
Snakebite prevalence, risk and rates are determined by several interrelated factors pertain-
ing to both snakes and humans, notably the density, activity and behaviour of the snake cul-
prits and their victims. Snake density appears the most important factor, as the commonest
species are also often the most prevalent as culprits [23, 49]. Snake density is related to habitat
type and human disturbance, as well as food sources and hiding places. It is also inversely
related to human density in many parts of sub-Saharan Africa [27, 30, 49], and therefore
directly related to both destruction of suitable habitats as well as human persecution, especially
in most African cultures with great dislike of snakes. Snakebite prevalence is lower in urban
centres devoid of natural vegetation, and where snakes are at higher risk of being detected and
killed [30]. Our data were in line with this inverse human-snake density-relationship, as evi-
denced by lower snakebite incidences in the more densely populated communities (e.g. Save-
lugu and Nanton) closer to Tamale, the regional capital with>300,000 inhabitants.
Apart from densities of both humans and snakes, activity patterns and behaviour are two
other important factors highly correlated with habitats, daytime hours and season. During
rains, in which farming activities peak in the savanna zone, snakes often synchronise their
breeding periods with high prey abundances [60, 61]. Likewise, density and activity of prey
such as amphibians, birds, lizards, murid rodents and other snakes increase during rains, due
to prey availability (mainly invertebrates) increasing along with the flourishing vegetation. The
number of active farmers, combined with actively-hunting and breeding snakes tends to
increase human-snake encounters, often resulting in bites and envenomations [49]. Similarly,
the density-activity influence on human-snake encounters and the behaviour of the snake cul-
prits as well as victims are important factors. Risky behaviour during farming, hunting and
firewood collection (e.g. using unprotected limbs to grasp, cut, dig, lift and pick tools, foods
and other important farm-related items), increases the probability of unintendedly provoking
and even attacking snakes [31, 54]. In response, the disturbed snakes may vigorously defend
themselves either by hissing, inflating hoods, whipping tails, venom spitting or biting. Certain
species appear more docile and reluctant to strike even if trodden, such as Gaboon Viper Bitis
gabonica or grass snakes/sand racers (e.g. Psammophis elegans) while others tend to be
extremely aggressive and prone to strike at the least provocation or threat such as Black-
necked Spitting Cobra Naja nigricollis and Carpet Viper Echis ocellatus (Fig 2). Some species
retreat long before humans are even close, whereas others stay put and motionless until it is
too late to detect their presence before they strike. Highly mobile species may enter houses,
garages and even cars in search of prey or warm places (e.g. cobras and small vipers), while
other slow-moving species (e.g. large vipers) avoid such human-trafficked areas which pose
great human-detection risks. As in the majority of West African studies, and as recorded from
all sections of our study population, three snake species were by far the commonest snakebite
culprits; Carpet Viper, Night Adder Causus maculatus and Black-necked Spitting Cobra [16,
23, 26, 35, 40, 46, 48, 49]. These three species were also among the commonest found in our
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Snakebite epidemiology in northern Ghana
study area, as shown by extensive ecological censuses [62]. Polyvalent antivenom of these spe-
cies in particular, is therefore essential in this part of northern Ghana [22, 23, 44].
Conclusion
Our community-based complementary data clearly demonstrate the gravity of snakebite
envenomations in the savanna zone of northern Ghana, and the relatively high burden of inci-
dence, morbidity and mortality. These findings cannot be overemphasised with respect to
their negative implications for public health, agricultural productivity, social welfare and eco-
nomic growth. In order to address the shortcomings of adequately-trained personnel, effective
treatment with antivenom, and other efficient therapy, we recommend concerted efforts from
both conventional and TMPs to monitor, map and analyse snakebite incidences at district lev-
els, including scientific efficacy testing of complementary therapy to expensive and unavailable
polyvalent antivenoms. We also conclude that unnecessary delays at TMPs often result in futil-
ity and complicates subsequent conventional hospital treatment, hence the need to improve
infrastructure, information on risks associated with TMP treatment, and availability of effec-
tive polyvalent AV therapy (e.g FAV-Africa). We recommend that each district hospital in the
NR of Ghana has a capacity of treating 5–600 snakebites annually per 100,000 inhabitants, and
a total treatment capacity in the NR of maximum 20,000 cases annually. Additionally, commu-
nity members, particularly the youth, should be sensitised on risky snakebite behaviour, snake
biology and measures to prevent and minimise the likelihood of snakebites. Such interventions
could be achieved through community meetings, education and awareness sessions, and
steady contact in the field with public health authorities liaising with traditional rulers and
TMPs.
Acknowledgments
We would first like to thank the local communities that participated in the survey, notably the
elders, traditional rulers and TMPs, as well as staff at the Savelugu-Nanton District Hospital
and the Meteorological Survey Department in Accra. Special appreciation goes to Mohammed
Mukhtar, Imoro Abdul Rashid, Issah Shaban, Abubakari Abdul Fatawu and Yakubu Abdul
Latif.
Author Contributions
Conceptualization: Yahaya Musah, Daniel K. Attuquayefio, Lars H. Holbech.
Data curation: Yahaya Musah.
Formal analysis: Yahaya Musah, Lars H. Holbech.
Investigation: Yahaya Musah, Daniel K. Attuquayefio.
Methodology: Yahaya Musah, Daniel K. Attuquayefio, Lars H. Holbech.
Project administration: Yahaya Musah.
Resources: Yahaya Musah.
Software: Lars H. Holbech.
Supervision: Daniel K. Attuquayefio, Lars H. Holbech.
Validation: Lars H. Holbech.
Visualization: Lars H. Holbech.
PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0007221 August 1, 2019 16 / 20
Snakebite epidemiology in northern Ghana
Writing – original draft: Yahaya Musah, Evans P. K. Ameade, Lars H. Holbech.
Writing – review & editing: Yahaya Musah, Evans P. K. Ameade, Daniel K. Attuquayefio,
Lars H. Holbech.
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