INTRODUCTION
Since the domestication of wild dogs about 12,000 years before, animal-bite injuries posed a major risk to human health. In the recent past, it gained attention of public health professionals. 1 Despite the fact that animal-bite injuries contribute significantly to global morbidity and mortality data, it remained a neglected emerging public health problem. 2,3 Annually, tens of millions of animal-bite injuries are reported. 2 The highest number of animal-bite injuries in humans is caused by dogs (approximately 85–90%) followed by cats (5–10%), humans, and rodents (2–3%). 4 About 76–94% of cases of rabies are attributed to dog bites, leading to higher fatality rates due to poor access to anti-rabies postexposure treatment (PET) in low-income countries. 5–7 In developing countries of Asia like Pakistan, India, and Bangladesh, the burden of morbidity and mortality due to rabies is highest. 6,8 Because of the lack of sophisticated patient care and management system, the real number of the rabies cases is underestimated. 9
Rabies is one of the highly fatal zoonotic diseases with a case fatality rate approaching 100% 8,10 and causes an estimated 59,000 human deaths per year globally, more than 3.7 million disability-adjusted life years, and about 8.6 billion United States Dollar economic loss annually, mainly due to premature deaths (productivity losses) and PET costs. 8 Countries like Pakistan, with resource-constraint settings, usually have flawed surveillance systems, lack of reporting of epidemiological data and routine laboratory diagnostic services. 11,12 Consequently, the actual burden of disease is unknown because of underreporting. 11 Despite the underreporting and misdiagnosis, one person dies every 20 minutes from rabies, and most of them are children. 13 Asia and Africa had 95% of cases of rabies among all reported globally. The estimated annual death toll in Asia is more than 31,000, and around 2.5 billion people are at risk of rabies in Asia. 6,10
Pakistan has estimated 2,000–5,000 human cases per year, which is one of the world’s highest rates of rabies. 14 Currently, the Health Management Information System reporting program is used to conduct routine surveillance of dog bites and rabies in Pakistan. But the data collected through this system are of poor quality and prevent development of evidence-based disease control efforts. 11 Lack of an integrated surveillance system and variation in reporting procedures put barriers to estimate accurate incidence rates of dog bites. The issues of increasing stray dog populations, rabies outbreaks, and the incidents of dogs biting in humans have been frequently reported by the media in Pakistan. 15–17
The Swat Valley, with snow-capped mountains, lush green landscapes, and clear lakes, is a popular destination for tourists looking for skiing, hiking, fishing, and ancient statues of Buddha. 18 Swat district remained a Taliban stronghold during 2006–2009, who not only destroyed the tourist industry but also unleashed a reign of terror on the local population. 19 About 29% of health facilities in the province of Khyber Pakhtunkhwa were damaged during the conflict between the Taliban and the government forces. 20 Inadequate medical services including lack of diagnostics, poor surveillance, shortage of vaccines, shortage of medical and paramedical staff, and insufficient veterinary support due to damage to the health facilities by the Taliban enhanced the spread of infectious and zoonotic diseases including rabies. Accurate data are very scarce relating to the burden of animal bites and post-exposure prophylaxis (PEP) practices in Swat district. The findings of the current study will provide updated estimates of animal-bite injuries, characteristics of patients and biting animals, and spatial distribution of cases. The information will be helpful for health policy makers and veterinary, medical, and other allied professionals to devise appropriate control measures for rabies.
METHODS
Aims of the study.
The current prospective study was planned to estimate the cumulative incidence of animal bites among residents of Swat district treated at Tehsil Headquarter (THQ) Hospital, summarize characteristics of humans bitten by animals and biting animal, and collect information about PEP.
Study area.
Swat, an administrative district in Khyber Pakhtunkhwa, is situated at 35° north latitude and 72° and 30° east longitude. On the north of the valley lies Chitral and Ghizer districts (Gilgit-Baltistan), and Kohistan and Shangla districts are in the east, and Buner district and Malakand protected area cover it from south and districts of Upper and Lower Dir in the west 21,22 (Figure 1). The estimated population of Swat district in 1998 census was 1,257,602 individuals. 23 At an annual population growth rate of 3.3%, the reported population of Swat district in 2009 from all union council was 1,810,859. 24 A total of 86.6% of the population live in rural areas, whereas only 13.4% live in urban areas. In 2008, Taliban militant insurgency captured most of the Swat district and destroyed schools, hospitals, and other infrastructure. 24
Study site (Swat district).
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Study design.
A prospective epidemiological study was conducted for four months (May–August 2014) at emergency departments of three public hospitals (Saidu Teaching Hospital, THQ Hospital Khwazakhela, and THQ Hospital Matta) of Swat district to estimate the cumulative incidence (May–August 2014) of animal-bite injuries.
Selection of subjects.
All patients with animal bites, who visited emergency wards of these hospitals, were contacted to record their history of bites and wound evaluation. Patients who were willing to participate in the study were enrolled in the study.
Data collection and analysis.
A predesigned questionnaire (Supplemental Annexure 1) containing closed questions about the sociodemography, circumstances of bite (provoked or unprovoked), injury pattern, severity of wounds, animal type, PEP, and vaccination, was presented to the patients in a face-to-face interview. A surrogate interview of the close family member was conducted in cases where the victim was deceased or a child. Information about the location of the incident was also collected from the patient. The geographical locations (street addresses) of patients from Google Maps were recorded. A spot map of incidence of animal-bite injuries was produced using QGIS software version 3.2 (Open Source Geospatial Foundation Project, Boston, MA, available at http://qgis.osgeo.org).
We analyzed descriptive data using R software version 3.2.3 (2015) (R core Team, Vienna, Austria) for statistical analysis and Microsoft Excel 2010 (Microsoft Corporation, Redmond, WA) to generate graphs. Proportions of animal-bite injuries by different characteristics, for example, age, gender, and location, were computed for the study period. Cumulative incidence (per 100,000 population for May–August 2014) was calculated by using WinPepi software (version 11.43) (Abramson, 2011, Jerusalem, Israel). For calculation purposes, the number of animal-bite injuries was used as the numerator and the total district population as the denominator. 25 The cumulative incidence at a union council level was calculated by dividing the number of bites reported from a specific union council by the total population of the union council. Bar graphs were used to demonstrate temporal trends of incidence from May to August 2014. Chi-square tests were used to compare the differences in proportions of animal bites between reporting hospitals, gender, and other characteristics, with a P value < 0.05 considered statistically significant. Associations among different variables were assessed using chi-square tests. Time elapsed to visit hospital for PEP was categorized into a dichotomous variable “delayed” (i.e., delayed for more than 2 days = 1, not delayed = 0), and odds ratios (OR) were calculated for “delayed” and the area of residence and seeking other treatment options.
Ethical approval and consent to participate.
The study protocol and consent procedure were approved by the Institutional Review Committee for Biomedical Research, University of Veterinary and Animal Sciences, Lahore, Pakistan (Reference No. 081/IRC/BMR). The consent form was translated into local language, that is, Pashto. All participants and their attendees were briefed about the purpose of research, interview, questions, voluntary participation, and other aspects of the study. Written consent was obtained from the individual patients and the parents (in case of children) who verbally consented to participate in the study. Confidentiality of data was maintained in the study by coding questionnaires.
RESULTS
Cumulative incidence of animal bites.
From May to August 2014, a total of 700 cases of animal bites were presented to emergency departments of the three hospitals of Swat (Saidu Teaching Hospital: 473; THQ Hospital Khawazakhela: 94; and THQ Hospital Matta: 133), and all these patients consented to participate and were included in the study. The incidence of bites differed significantly (χ2 = 559.29; degree of freedom [DG] = 2; P < 0.001) between the reporting hospitals. The maximum number of cases reported in a day was 21 and minimum 1 (Figure 2). The overall incidence of animal-bite injuries was 39 per 100,000 persons (95% CI: 36.0–42.0) from May to August 2014 in Swat district. The highest incidence (191 per 100,000 people) was seen in union council Qalagay, whereas the lowest incidence (4.7 per 100,000 people) was reported from union council Darmai. The spatial distribution of cases is shown in Figure 3. The highest number of incidents was reported in the month of June (n = 246), followed by May (n = 182) and July (n = 164). The lowest number of bites was reported in August (n = 108) (Figure 4). Significantly more cases (n = 544) were reported from rural regions (77.7%) than urban areas (22.3%) (χ2 = 430.13; DF = 1; P < 0.001).
Temporal distribution of animal-bite cases (per day) during the study period.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Spatial distribution of animal-bite cases in different union councils of Swat district.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Monthly distribution of animal-bite cases.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Sociodemographic characteristics of patients.
The proportion of animal bites were significantly high among male individuals (76.6%) compared with female individuals (23.4%) (χ2 = 395.38; DF = 1; P < 0.001). Children younger than 10 years were the major victims of animal bites (37.3%), and there were significant differences in the proportion of bite victims between various age categories (χ2 = 654.41; DF = 6; P < 0.001). Figure 5 depicts distribution of animal-bite cases by age and gender and shows that children aged 0–10 years and male individuals are the major victims of animal bites, compared with female individuals and with other age-groups. About 68% (475/700) of victims were literate. The highest number of animal bites was found in school students (47.3%), and there was significant differences in proportions of animal bites and occupation of participants (χ2 = 840.65; DF = 6; P < 0.001).
Distribution of animal-bite cases by age of patients and gender.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Post-exposure prophylaxis for rabies.
All victims of animal bites received PEP for rabies. About 35% of the victims sought PEP from hospital within 12 hours of the exposure, 26% visited hospital for PEP within 24 hours, and only 19% (n = 132/700) of victims delayed visit to hospital for PEP more than 2 days (> 48 hours) (Figure 6). A predominately higher number of respondents (77.7%) reported that they washed the wound with water before arrival at hospital. Among patients who delayed PEP for more than 48 hours, 40% (n = 54/132) sought other treatment options (chili powder application, hakim/traditional healer, and spiritual healer/peer). Victims who sought other treatment options were 2.79 times more likely to delay visit to hospital for PEP for > 2 days (95% CI = 1.82–4.17; P < 0.001). The odds of delaying visit to hospital for PEP for > 2 days were 9.2 times more (95% CI = 3.69–22.91, P < 0.001) in patients living in rural areas (n = 127) than those living in urban areas (n = 5). All patients completed their treatment regime. Table 1 shows details of sociodemographic characteristics of the patients.
No. of cases by time elapsed since bite and got post-exposure prophylaxis in hospital.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0208
Sociodemographic characteristics of patients
| Characteristic | Frequency (no.) | Percent |
|---|---|---|
| Area of residence of victims | ||
| Rural | 544 | 77.7 |
| Urban | 156 | 22.3 |
| Gender | ||
| Male | 536 | 76.6 |
| Female | 164 | 23.4 |
| Age category (years) | ||
| 0–10 | 261 | 37.3 |
| 11–20 | 203 | 29.0 |
| 21–30 | 108 | 15.4 |
| 31–40 | 56 | 8.0 |
| 41–50 | 36 | 5.1 |
| 51–59 | 15 | 2.1 |
| 60 and above | 21 | 3.0 |
| Qualification | ||
| Illiterate | 225 | 32.1 |
| Literate | 475 | 67.9 |
| Occupation | ||
| Employee | 23 | 3.3 |
| Farmer | 76 | 10.8 |
| Businessman | 58 | 8.3 |
| Student | 331 | 47.3 |
| Dependents (children not enrolled in school) | 139 | 19.8 |
| Housewife | 57 | 8.1 |
| Others | 16 | 2.3 |
| Washed with soap before arrival at hospital | ||
| Yes | 544 | 77.7 |
| No | 156 | 22.3 |
| Time lapsed to seek post-exposure prophylaxis (hours) | ||
| 0–12 | 246 | 35.1 |
| 13–24 | 182 | 26.0 |
| 25–48 | 140 | 20.0 |
| > 48 | 132 | 18.9 |
| Other treatment options (chili, hakim/traditional healer, spiritual healer/peer) | ||
| No | 533 | 76.1 |
| Yes | 167 | 23.9 |
Characteristics of animal exposure.
In the majority of cases (n = 608, 86.9%), biting animals reported were dogs, followed by rats (4.7%), cats (4.0%), donkeys/horses (2.1%), cattle/buffalos (1.3%), rabbits (0.7%), and wild animals (0.3%). In the majority of incidents, bites were unprovoked (87.6%) rather than provoked (12.4%) (χ2 = 790.5; DF = 1; P < 0.001). Significantly higher numbers of victims (75.6%) reported that they were static when the animal attacked them, and the remaining 24.4% described that they were running during the incident (χ2 = 366.18; DF = 1; P < 0.001). More than 50% (398/700) of bites occurred on lower extremities. A larger number (68%) of participants reported that they were bitten by stray animals, rather than by domestic animals (χ2 = 178.57; DF = 1; P < 0.001), and among domestic animals, only one animal was reported to be vaccinated against rabies. After an eclipse phase (animal observation period) of 10 days, 394 of biting animals did not develop signs of rabies, although 44 (10.0%) animals developed signs of rabies (Table 2).
Characteristics of exposure animal
| Variable | Frequency (no.) | Percent |
|---|---|---|
| Animal type | ||
| Dog | 608 | 86.9 |
| Cat | 28 | 4.0 |
| Donkey/horse | 15 | 2.1 |
| Rabbit | 5 | 0.7 |
| Cattle/buffalo | 9 | 1.3 |
| Rat | 33 | 4.7 |
| Others (wild animals) | 2 | 0.3 |
| Ownership status of animal | ||
| Domestic pet | 225 | 32.1 |
| Stray/wild | 475 | 67.9 |
| Bite circumstances | ||
| Provoked | 87 | 12.4 |
| Unprovoked | 613 | 87.6 |
| Patient status at time of bite | ||
| Running | 171 | 24.4 |
| Static | 529 | 75.6 |
| Site of injury | ||
| Head/neck | 33 | 4.7 |
| Upper extremities | 194 | 27.7 |
| Lower extremities | 398 | 56.9 |
| Multiple cuts | 75 | 10.7 |
| Observation of animals after bite for 10 days | ||
| Yes | 438 | 62.6 |
| No | 262 | 37.4 |
| Vaccination status of animal | ||
| Vaccinated | 1 | 0.1 |
| Non-vaccinated | 213 | 30.4 |
| Unknown (stray or wild) | 486 | 69.4 |
| Development of rabies signs in animal (n = 438) | ||
| Yes | 44 | 10.1 |
| No | 394 | 89.9 |
DISCUSSION
Animal-bite injuries are considered as an important cause of morbidity and mortality around the globe and have a significant public health burden. 4,8 In Pakistan, rabies remains a neglected disease, although the incidence of dog bites in the country has been reported to be very high. 26 The country has been placed in the list of countries having higher risk of rabies. 27
In the current prospective epidemiological study, we reported that animal-bite injuries are a significant cause of morbidity in Swat district, with an overall incidence of 39 per 100,000 persons per 4 months (May–August 2014), which is considerably higher than the estimate (38–53 per 100,000 persons per year) reported for Karachi, the most populous city of Pakistan. 11 However, this difference in estimates might be due to the study design and variation in the time frames of both studies. We used actual data of cases reported from May to August 2014, whereas Zaidi et al. 11 used an estimation method for incidence in the study from Karachi during a time frame of February 2009–February 2011. Approximately 700 people visited the three public hospitals in Swat district from May to August 2014, which reflects a significant health and economic burden due to animal bites. In Asia, a significant economic burden has been attributed to animal bites because of the cost of PEP. 28,29 The proportion of animal-bite victims was highest at Saidu Teaching Hospital (n = 473) compared with the other two hospitals (THQ Hospital Khwazakhela and THQ Hospital Matta). This hospital is the main tertiary-care hospital affiliated to Saidu Medical College with better treatment facilities than other hospitals in the capital city of Swat district. This could be the main reason of a larger proportion of patients visiting this hospital for PEP.
Most characteristics of animal-bite patients reported in the current study are similar to those described in other studies reported from other regions. 12,28,29 In the present study, most of the victims of animal bites were children aged 0–10 years, primary school students, and males. Previously, a number of studies have demonstrated a similar pattern of animal-bite injuries in male children. 29–32 Children have increased risk of animal bites because of their extremely curious and adventurous behavior, unawareness about dog behavior, and inability to defend themselves in case of attack. 29,30,33 Second, bite injuries in children are more likely to be reported because of parental care and severity of bites. 33 Contrary to these findings, it is also believed that minor scratches and bites are not reported by children to their parents because of mildness of wound, which could increase the likelihood of rabies infection. 34 Similar to our results, many studies have reported that male individuals are more prone to bite injuries because they have a more adventurous and aggressive nature than female individuals, who spend more time at home because of childcare and regional customs. 12,35 Contact of animals with men is also more likely because of their outdoor occupational activities as compared with women who stay indoors and have less access to health care in countries like Pakistan. 11,12 Primary school children usually travel to school unaccompanied and on foot in Pakistan. 17 This factor might expose them to increased risk of animal bites.
This study found that the majority of animal bites (87.6%) are inflicted by dogs, both domestic and stray. This is in agreement with many studies from Asia and Africa which have reported that most bites are inflicted by dogs. 3,12,31,36
Animal bites have been reported in response to provocation by the victims, usually children, or due to unprovoked circumstances where victims are attached by aggressive dogs. 29,37,38 Our finding showed that the majority of bites were unprovoked (87.6%) and attacks were mostly by stray animals (67.9%). Developing countries including Pakistan have a high population density of stray dogs in streets. 15–17,39 Dogs have high rates of behavioral abnormalities (aggression and anxiety), and any threat to their territory may incite them to attack. Common human activities may be perceived by frightening dogs as invasion to their territory and can provoke them to bite. 37,40 In the case of a rabid animal, it will attack victims without any provocation. 29 In the current study, most cases of animal bites (77.7%) occurred with residents of rural areas. The rural population of Swat is 88%. 22 In many developing countries, people in rural areas keep dogs for territory or livestock guarding, 41–43 and lack of training of dogs for this role may result in higher risk of bite injuries. Our study reported that animal-bite incidence was higher in the month of June than May and July. These results may have limitation of bias as the current study was not conducted for the whole year because of financial and logistic issues. However, other studies from developed countries have reported greater incidence of bites in summer and spring because of having more interactions between unaccompanied children and pet animals during school breaks in these warmer months. 33 Other behavioral changes in dogs corresponding to the breeding season around March–April and September–October could contribute to the aggressive behavior of dogs. 35 In Pakistan, June–August is the summer vacation period, and children play outdoor in streets and have higher chances to interact with stray dogs, cats, and other animals, which put them at risk of bites. 29,30,44 The most common site on the cbody for animal-bite injuries was lower extremities (56.9%) compared with other parts, in all age-groups. In developing countries, most incidences of bite occur in the street by stray dogs, which usually attack victims on lower extremities. 29,42 Contrary to this, bites to the upper extremities are more frequent in children with short height and playful nature from developed countries with a larger proportion of pet animals. 1,30,40 Bites on the upper extremities are more commonly caused by aggressive pet animals (known dogs) to owners/children during playing or petting. 1,33,45 Cleaning dog-bite wounds with soap and water and application of any antiseptic (tincture iodine or alcohol) have been found to be effective in preventing rabies in significant numbers of cases. 32 Our study showed that about 78% of patients washed their wounds with soap and water before visiting hospital. Wound washing is an inexpensive and effective method to reduce the viral load and mortality by 50%, 46 and awareness of the public and healthcare providers through health promotion can enable communities to fight rabies. Application of any irritants (chili powder, plant juices or extracts, acids, etc.) or using any kind of wound dressing is not recommended by the WHO. 29,47 About 40% of cases (n = 54) who delayed PEP for more than 2 days reported that they sought other treatments including chili powder application (OR = 2.79). The use of alternative treatments (chili powder, plant juices, or consulting hakim/traditional healers or spiritual healers) has been reported from other countries in Asia and Africa. 38,47–49 Human rabies burden can be prevented by washing wound with soap and water and providing proper PEP and rabies immunoglobulins (RIGs) as soon as possible. 10,28,50,51 Our study reported that more than 60% of the victims were administered PEP from the hospital within 24 hours of the exposure and about 19% victims delayed PEP more than 2 days (> 48 hours). Patients living in rural areas were 9.2 times more likely to delay visit to hospital for PEP for more than 2 days. Although rabies PEP is free at designated health centers in Pakistan, annually 2,000–5,000 deaths occur because of rabies in Pakistan, 14 most of them attributed to noncompliance, unavailability of PEP, or delaying rabies PEP, especially in rural areas, where health centers with PEP facilities are scarce. 15,32,52 To reduce the burden of rabies in Pakistan, the government should increase the number of health centers with PEP services. This will sufficiently decrease the travel time from rural areas to the PEP service center, and this will subsequently reduce the delay in PEP or noncompliance. 11 The WHO guidelines recommends washing of wounds with soap and water and administration of rabies PEP and RIG as soon as possible as a first aid response to neutralize the virus before immunity from vaccination develops. 53,54 However, a One Health approach integrating human and animal sector collaborations has been shown to improve the compliance of the PEP schedule and to reduce the unnecessary burden of rabies PEP for non-rabies exposure. 7,55
In the current study, only 10.1% animals (n = 44) that were observed for 10 days developed sign of rabies, and this number might be an underestimate of actual figures of rabid animals as the majority of biting animals were stray and could not be followed by victims. Our study demonstrated that the healthcare burden of dog bites and rabies is substantial in post-conflict Swat district, Pakistan, despite the availability of free PEP. Stray dogs are the major contributors of all animal-bite injuries exposing victims to rabies, especially male children younger than 15 years. Our estimates of the burden of animal-bite injuries in Swat district could provide important baseline data to develop evidence-based policy focusing on potential benefits of implementing cost-effective and coordinated intervention activities, for example, awareness programs to sensitize the general public about the benefits of wound washing and PEP coupled with vaccination of domestic animals and reduction of stray dogs through neutering or spaying. Rabies is a vaccine-preventable and notifiable disease, and its control could be coordinated and achieved at the national level using the “One Health” approach with a special focus on strengthening the rabies surveillance system. 12 Moreover, extensive rebuilding of healthcare facilities damaged by the Taliban would be required in Swat to cope with the increasing threats of zoonotic diseases like rabies.
Our study had some limitations as do most observational studies. As the current data were collected only from patients visiting three public hospitals for PEP, cases attending private clinics, hakim/traditional healers, spiritual healers, or home-based remedies have not been represented, making it a conservative estimate of animal bites and suspected rabies cases because of selection bias and might not be generalized to other areas with varying exposures and health-seeking behaviors. 56 The current study was a prospective design enrolling patients with a fresh memory of biting incidents, therefore has less recall bias; however, as this study was only conducted for 4 months, these estimates do not represent the annual burden of animal bites.
ACKNOWLEDGMENTS
We are very grateful to the dog-bite victims and their families who participated in the study, and the medical staff and administration of all hospitals who supported data collection. Without their cooperation, the current study would not be completed. We are thankful to Peter Thomson, School of Life and Environmental Sciences, the University of Sydney, for English language editing. The American Society of Tropical Medicine and Hygiene (ASTMH) assisted with publication expenses.
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