Open Veterinary Journal, (2024), Vol. 14(11): 2745-2753

Research Article

10.5455/OVJ.2024.v14.i11.3

A case-control study of risk factors for dog rabies in Northeast Tunisia

Sana Kalthoum^1*, Raja Gharbi¹, Mehdi Ben Ali¹, Imed Ben Sliman¹, Nouha Haboubi², Khaoula Barrak², Khalil Fakhfekh², Rafika Ben Romdhane², Habiba El Hechri², Salma Boughanemi², Chedia Seghaier¹ and Chokri Bahloul³

¹National Center of Zoosanitary Vigilance, Tunis, Tunisia

²Ministry of Agriculture of Tunisia, Tunis, Tunisia

³Pasteur Institute of Tunis, Tunis, Tunisia

*Corresponding Author: Sana Kalthoum. National Center of Zoosanitary Vigilance, Tunis, Tunisia. Email: kalthoum802008 [at] yahoo.fr

Submitted: 12/03/2024 Accepted: 10/10/2024 Published: 30/11/2024

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Abstract

Background: Since 2012, the northeast region of Tunisia has witnessed an increase in dog rabies cases, indicating a concerning emergence of the disease. Previous studies have indicated the widespread nature of rabies in northern Tunisia. However, there remains a lack of comprehensive understanding regarding the associated risk factors.

Aim: This study aimed to identify potential risk factors associated with the occurrence of dog rabies in northeast Tunisia through a case-control approach.

Methods: A case-control study was conducted, involving a case group (n=77) consisting of dogs confirmed positive for rabies at the referral laboratory using the Fluorescent Antibody Test between 2013 and 2019. The control group (n=77) comprised both negative cases received at the laboratory and dogs that underwent a 15-day quarantine period and received a certificate of absence of rabies after observation. Univariate and multivariate logistic regression analyses were performed to explore various potential risk factors, including age, sex, breed, confinement, vaccination status, presence of bites, ownership status, origin of dogs, geographic sector, presence of rabies cases, and proximity to slaughterhouses.

Results: The final logistic regression model revealed several significant findings. The odds of an unconfined dog being affected by rabies were nearly twice as high as for confined dogs odds ratio [OR=1.9; 95% confidence intervals (CI): 1.17–3.27]. Furthermore, the odds of rabies occurrence were 25 times higher in areas where rabies cases had been reported within the previous 3 months to 1 year compared to uninfected areas (OR=25.7; 95% CI: 3.02–219.14). Dogs born at home to the owner’s bitch were also found to be at significantly higher risk of rabies (OR=2.41; 95% CI: 1.14–5.13). Additionally, residing in areas with reported rabies cases in the last 3 months was found to increase the risk of rabies by 2.8 times (OR=2.8; 95% CI: 1.16–6.77). However, vaccination was associated with a 1.6-fold reduction in the risk of contracting rabies (OR=0.6; 95% CI: 0.38–0.97).

Conclusion: This study provides valuable insights into the risk factors associated with dog rabies in northeast Tunisia. The findings underscore the importance of implementing targeted control measures, such as increased vaccination coverage and enhanced confinement measures, to mitigate the spread of rabies in the region. These findings can inform decision-making processes aimed at improving the effectiveness of national rabies control programs.

Keywords: Case-control study, Dogs, Rabies, Risk factors, Tunisia.

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Introduction

Rabies is a disease that is widely distributed among animals and humans. Dogs act as the main vector and reservoir for the disease (Kgaladi et al., 2013; Jackson, 2014). In Africa and Asia, dogs are responsible for more than 99% of human cases (Moges, 2015; Taylor and Nel, 2015). The World Health Organization (WHO) has reported that approximately 59,000 people die annually due to rabies, with patients under the age of 15 years being the most affected (World Health Organization, 2020). In Africa, rabies is endemic, with human deaths estimated at 21,000–25,000. A total of 49 of the 54 African countries were classified as moderate- to high-risk categories for human rabies (Broban et al., 2018). It is a preventable disease and a multi-year mass vaccination of the dog population with a high-quality vaccine can reduce the risk of human rabies (Jayasundara, 2016). In Tunisia, rabies is enzootic and the dog is the most important dynamic vector and reservoir (Kalthoum et al., 2021). The history of rabies in Tunisia indicates that at the end of the 19th century, the disease commenced its ascendant phase with a lag of approximately half a century in comparison with Europe. The first recorded cases, which occurred in 1870 in the capital city (Tunis), were associated with the influx of European migrants and other factors such as socio-cultural or ecological changes (Ben Néfissa et al., 2007). National Rabies Control Program (N.L.R.P.), initiates in 1982 under the guidance of the WHO, was primarily focused on awareness campaigns, parenteral vaccination of all accessible dogs, and the management of “stray” dogs (Haddad et al., 1988). Nevertheless, the disease remains enzootic with a high incidence observed particularly since 2011 when rabies cases in animals doubled (Kalthoum et al., 2015). The disease is distributed throughout the entire country, with the northern governorates appearing to be the most affected. It has been demonstrated that a number of factors have potentially contributed to the increase in rabies cases, including the mishandling of waste and landfills, which has led to an increase in the stray dog population (Ripani et al., 2017). In Tunisia, the current data and knowledge of the epidemiology of rabies are limited to descriptive studies. Previous studies have highlighted the structure and the dynamic of the dog population in Tunisia. The annual population turnover was found to range between 30% and 40% while the dog population density exhibited notable variation between rural and urban/suburban zones. In rural areas, dog population density was observed to range between 7 and 30 dogs per km². In urban and suburban zones, the density oscillated between 700 and 1,000 dogs per km². These findings were reported by Wandeler et al. (1993). A phylogenetic study conducted between 1992 and 2003, revealed the existence of two variants of rabies virus circulating within the country. The first lineage showed nucleic affiliation with isolates from Algeria and Morocco. The second lineage shared a strong relationship with Ethiopian and Sudanese strains (Amouri et al., 2011). Despite the existence of significant studies, rabies continues to persist as an endemic disease, underscoring the need for improved implementation of control measures and public health strategies. The most recent occurrence of rabies was observed in regions that were previously considered to be free of the disease in Tunisia (Bouslama et al., 2019). In 2012, the disease had a considerable impact on the northwest governorates (Beja and Jendouba) and subsequently spread to the northeast governorates. A significant number of outbreaks were reported in the Tunis region and the Bizerte governorate over the subsequent 2 years (Kalthoum et al., 2017). The emergence of rabies in unusual zones in Tunisia in the last 10 years has highlighted a fundamental need to understand the disease by exploring the associated risk factors. The availability of reliable data on the risk factors associated with dog rabies represents a fundamental key to the success of the control of the disease and can relatively explain the failure of rabies control measures in Tunisia. In order to eliminate rabies in humans and animals, the implemented measures of control should be updated and adjusted to the epidemiological context of the disease.

This study represents the first case-control study in Tunisia on dog rabies. The principal objective of this study is to elucidate and identify the potential risk factors associated with dog rabies in northern Tunisia with an objective to adapting the strategy and the control measures for rabies.

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Materials and Methods

Study area and study population

The study area comprised the northeast of Tunisia, encompassing five governorates with an area of 3.750 km² (2.25% of the total of the country’s area) and a population estimated at 568 219 inhabitants (INS, 2020). The dog population in these governorates was estimated at 48.500 dogs (http://www.rage.tn//upload/1453203233.pdf) (Fig. 1). These governorates were selected based on the high number of outbreaks of rabies during the period of the study. Indeed, this region has experienced a surge of rabies cases after 2012. The incidence of reported cases of dogs was the highest in the country as documented by Kalthoum et al. (2021).

Study design

A case-control study was conducted in the northeast of Tunisia (Governorates of Bizerte, Tunis, Mannouba, Ben Arous, and Ariana) between 2013 and 2019 to investigate potential risk factors for dog rabies in Tunisia. The sample size was calculated using OpenEpi (http://www.openepi.com/SampleSize/SSCC.htm) and estimated as 154 dogs (77 controls and 77 cases) with a confidence level of 95%, power of 80%, assumed odds ratio (OR) of 2.5, and expected proportion in controls of 40%. The case group was recruited among the positive cases confirmed by the Fluorescent Antibody Test in the laboratory of the Institut Pasteur de Tunis, which serves as the referral laboratory for rabies diagnosis in Tunisia, over a 7-year period (2013–2019) in the study area.

The control group was comprised of two categories. The first category consisted of negative dogs that had been confirmed at the laboratory, which were randomly selected from recorded data maintained by veterinary services. The second category was comprised of suspected dogs that had been observed by official veterinarians for 15 days, with a certificate of absence of rabies being issued after three visits. The control groups were randomly selected within a 10 km radius of the cases, and both control and case groups were selected with consideration of the time of suspicion (suspected or confirmed in the same period, with a lag of 2 months).

Data collection and risk factors

This study was carried out from 2013 to 2019. Rabies surveillance data on positive cases were retrieved from the regional veterinary services database. For each positive case confirmed at the laboratory, regional veterinary services conducted an investigation into the outbreak and collected data on the rabid dog using a standard questionnaire approved by the national veterinary services. For the control group, an epidemiological investigation of all negative dogs was conducted. The same questionnaire was used for both the control and case groups, which included demographic and risk factors related to two groups (cases and controls). The following information was gathered for both case and control: age, sex, breed, geographical localization (imada), date of suspicion, date of diagnosis, owned or free-roaming, vaccination status, presence of old bite, and confinement (confined, free-roaming, or stray dogs). Classification of the imadas (geographical location of control and cases) into three types: urban, suburban, and rural, was provided by the regional veterinary services. In order to ascertain the impact of the municipal infrastructures, the geographical positions of all red meat (ruminants) slaughterhouses, white meat (poultry) slaughterhouses, and weekly markets were collected.

Fig. 1. Map of the study area showing the geographical distribution of cases (red) and controls (green).

Data analysis

The data was curated validated and entered into a Microsoft Excel spreadsheet. Frequencies and proportions were calculated for the quantitative and the qualitative variables, respectively. Descriptive statistics were performed to characterize the case and control groups. The variable age was studied as a categorical variable with three categories (> 3 years old, 1–3 years old, and < 1 year old). The potential risk factors (age, vaccination status, confinement, origin, and sex) were tested in a univariable logistic regression model using the disease status (case/control) as the outcome variable. Those factors with a p-value <0.2 in the univariable model were retained for inclusion in a multivariable model. Collinearity between the explanatory variables retained after univariable analysis was then assessed using the variance inflation factor (VIF) to identify and remove variables that are correlated with each other. The results in the model were expressed as ORs and 95% confidence intervals (CIs). p values <0.05 were considered significant at the 95% confidence level. The model’s predictive ability was evaluated using Hosmer–Lemeshow χ² test (Kazadi Kawaya et al., 2020) and the area under the curve was calculated to evaluate the predictive ability of the model. The statistical analyses were conducted using R software version 3.5.2 (https://www.r-project.org). The shapefile utilized for mapping and analysis, containing the second-level administrative divisions of Tunisia, was downloaded from https://gadm.org/download_country.html. The map was generated using ArcGIS version 10.4.

Ethical approval

This was a national surveillance activity that had been approved by the national and regional veterinary services. Approval by an Ethics Committee was not required. Data on animal owners were not used in the analysis.

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Results

A summary of the sociodemographic characteristics of cases and controls is presented in Table 1. The age group classification revealed that the age group (1–3 years old) was the most prevalent among cases and controls, accounting for 45% of the total number of dogs studied. Of the 154 dogs, 71% were males and 29% were females. The majority of cases and controls (83%) were owned dogs that were unconfined (roamed freely during the day and night) (68%). As shown in Table 1, 36% of the dogs were home-bred or purchased while 64% were bought or adopted. The distribution by habitat shows that about half of the cases and controls were from urban areas and 29.2% and 29.9% were from rural and semi-urban areas, respectively. Regarding rabies vaccination status, only 21% of the dogs were vaccinated against rabies, whereas 60% were unvaccinated and 20% had an unknown status (Table 1).

Univariate analysis of rabies risk factors showed that vaccination status ( p=0.0002), confinement (p=0.004), and the origin of the dog (p=0.007) were potentially associated with rabies occurrence (Table 2). Similarly, the presence of rabies cases in the area in the last 3 months (p=0.01) or between 3 months and 1 year (p=0.001) showed a significant association with the disease. However, the other factors (age, sex, presence of bites, presence of a slaughterhouse or a poultry shop, and sector type) were not significant. The final logistic regression model showed that the risk of rabies was about 2 times higher for dogs that were allowed to roam all day (OR=1.9; 95% CI: 1.17–3.27) compared to confined dogs. Dogs born at home to their own bitch were almost 2.5 times more likely to have rabies than dogs that are bought or adopted (OR=2.41; 95% CI: 1.14–5.13). Living in areas with rabies cases in the previous 3 months increased the risk of rabies by 2.8 times (2.8; 95% CI: 1.16–6.77). Similarly, dogs living in areas where rabies cases have been reported between 3 months and 1 year were 25 times more likely to develop rabies (25.7; 95% CI: 3.02–219.14). However, vaccination was found to be a protective factor, reducing the risk of contracting rabies by a factor of 1.6 times (0.6; 95% CI: 0.38–0.97) (Table 3). The Hosmer-Lemeshow goodness of fit test showed that the model fit the data well indicating that the number of predicted cases was not significantly different from the number of observed cases (χ²=1.960, df. 8, p=0. 659). The VIF of the variables included in the model was approximately one. The model had a good predictive ability (ROC=0.76).

Table 1. Sociodemographic characteristics of the case and control groups in northeast Tunisia.

Table 2. Univariate logistic regression analysis of potential risk factors of rabies northeast Tunisia.

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Discussion

Rabies is endemic in Tunisia and efforts deployed to control the disease have not been sufficient to eliminate it. On the contrary, the resurgence of rabies has been observed in recent years and the disease has remained confined to the north of the country (Kalthoum et al., 2021). Historically, rabies has circulated for a long time in northeastern Tunisia which was considered an endemic area. Despite the control program and the establishment of sterilization and vaccination centers that act to reduce the risk of rabies outbreaks. The northeast was chosen for the study because of the observed high incidence of canine rabies in this region and one of the objectives was to identify the factors that caused the increase of the disease in order to understand the particularities of canine rabies in this region. The results of this study provide an important information base for adapting and adjusting the rabies control program. In Tunisia, knowledge of risk factors for canine rabies is poor, and to our knowledge; this study represents the first detailed research focusing on potential risk factors associated with the occurrence of canine rabies in Tunisia.

In this study, we investigated several potential risk factors for rabies occurrence, including age groups, sex, origin, presence of bites, vaccination status, confinement, presence of rabies cases (with 3 and 9 months lag), presence of slaughterhouses, and type of sector (urban, suburban, and rural). Through univariate analysis, we assessed the relationship between each of these factors and the occurrence of rabies in dogs. Of the ten variables examined, only five were found to have a statistically significant association with rabies occurrence. No association was found between rabies and age groups or sex. Our results suggest that dog rabies is prevalent in all age groups which is consistent with previous studies in neighboring countries (Yahiaoui et al., 2018; Khayli et al., 2019) and elsewhere in the world (Douangngeun et al., 2017). Similarly, canine rabies was not gender-specific (Medley et al., 2017; Ma et al., 2020). In addition, our research showed that the type of area (rural, urban, and semi-urban) was not associated with the disease. This was an unexpected finding and contradicts with studies from other countries (Knobel et al., 2005; Noman et al., 2021), suggesting that rural areas are more exposed to dog rabies occurrence than urban areas. In the final logistic regression model, we found that the historical record of rabies cases serves as a good predictor of future rabies occurrence. One possible explanation is that initial cases may be under-detected or not reported promptly, leading to a silent spread of the disease. This delayed detection can result in secondary cases appearing later, which could explain the higher risk observed in areas with a historical record of rabies between 3 and 12 months ago. This finding was not surprising as the incubation period can exceed 6 months (Consales and Bolzan, 2007). Therefore, regions with a history of rabies cases are likely to continue facing risks due to ongoing epidemiological and environmental conditions. This underscores the importance of rigorous outbreak management and continuous monitoring of historical data in reducing the risk of rabies occurrence (Laager et al., 2018) and highlights the role of ring vaccination in its prevention.

Table 3. Final multivariable logistic regression model of risk factors associated with dog rabies in the northeast of Tunisia.

Our study demonstrates that unrestrained dogs allowed to roam freely all day are at a significantly higher risk of contracting rabies compared to restrained dogs. The role of free-roaming dogs in rabies transmission is well-documented, with studies linking roaming behavior to increased disease spread (Dürr and Ward, 2014; Bombara et al., 2017; Jane Ling et al., 2023). For instance, Kazadi Kawaya et al. (2020) reported that a single free-roaming dog could interact with up to 27 other free-roaming dogs. Our findings corroborate previous research indicating that a substantial proportion of owned dogs in our study were free-roaming, further highlighting the association between roaming behavior and increased rabies risk (Hergert et al., 2018; Van Sittert et al., 2009; Savadogo et al., 2021; Naveenkumar et al., 2022).

Dogs born at home to their own bitch were more exposed to rabies than dogs that are bought or adopted. This finding may be indirectly related to the vaccination status of the dogs. Previous studies have found that dogs born to the owner’s bitch are twice as likely to be unvaccinated as dogs that would have been purchased (Flores-Ibarra and Estrella-Valenzuela, 2004; Hergert et al., 2016). Another explanation may be that the behavior of dogs’ owners plays an important role in the status of their dogs. In a study conducted in KwaZulu-Natal, South Africa, more than 30% of owners believed that their dog was too young to be vaccinated (Hergert et al., 2016). It has also been reported that rabid bitches can transmit rabies to their puppies during pregnancy (Kolster, 2022).

In this case-control study, we showed that vaccination of dogs decreased the odds of rabies occurrence compared to unvaccinated dogs. Similar results have been reported, with the risk of rabies being 1.7 times higher in unvaccinated dogs than in vaccinated dogs (Thiptara et al., 2011). Non-vaccination of dogs has been found to be a risk factor for the occurrence of rabies (Corrêa da Costa and Fernandes, 2016; Costa et al., 2018; Chikanya et al., 2021). In fact, the WHO recommends a vaccination coverage of 70% to control rabies in dogs and a previous modeling paper on rabies showed that with this vaccination coverage, rabies can be controlled and 90% of human rabies cases can be prevented (Hergert et al., 2016).

Finally, the risk factors investigated in our study were almost individual. The main limitations of this study were the unavailability of updated data on the dog population size and human density and the non-inclusion of environmental risk factors [accessibility, presence of garbage, presence of natural barriers (rivers and mountains)] which play a very important role in spreading or stopping the spread of the disease (Tian et al., 2018). To properly identify potential risk factors for canine rabies, further research is needed and should include environmental factors. Similarly, increasing the number of cases and controls could lead to a better measure of the association between the disease and the risk factors.

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Conclusion

The dog remains the main source of rabies transmission to humans and other species in Tunisia and adapting and adjusting its control strategy is a priority. Our study examines the potential risk factors for the occurrence of canine rabies and shows that dog management (confinement, origin of dogs) and history of rabies (delays of 3 and 9 months) are strongly associated with the disease. Vaccination reduces the risk of rabies. Our study provides baseline information on risk factors for rabies and further studies including environmental risk factors of rabies are recommended to improve rabies surveillance and control in Tunisia.

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Acknowledgments

The authors are grateful to the “Institut Pasteur de Tunis” for their reactivity in the diagnosis of rabies and to the regional veterinary services for their collaboration in collecting data.

Conflict of interest

The authors declare that the study was carried out in the absence of any financial relationships that could be interpreted as a potential conflict of interest.

Funding

The research described in this paper was conducted without external funding.

Authors’ contributions

Kalthoum Sana: Conceptualization; Methodology; Formal analysis, Writing-original draft, Writing-review & editing. Gharbi Raja: investigation. Ben Sliman Imed: investigation. Nouha Haboubi: investigation. Barrak Khaoula: investigation. Khalili Fakhfekh: investigation. Rafika Ben Romdhane: investigation. Habiba El Hichri: investigation. Salma Boughanemi: investigation. Chedia Seghaier: Writing-review & editing. Bahloul Chokri: Writing-review & editing.

Data availability

Data are available from the corresponding author on reasonable request.

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