Molecular Prevalence and Risk Factors of <i>Campylobacter</i> Infection in Puppies in the Nairobi Metropolitan Region, Kenya

Mbindyo, Sharon N.; Kitaa, Jafred M. A.; Abuom, Tequiero O.; Aboge, Gabriel O.; Muasya, Daniel W.; Muchira, Beatrice W.; Gitahi, Nduhiu; Mulei, Charles M.

doi:https://doi.org/10.1155/2023/8813405

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Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 8813405 | https://doi.org/10.1155/2023/8813405

Molecular Prevalence and Risk Factors of Campylobacter Infection in Puppies in the Nairobi Metropolitan Region, Kenya

Sharon N. Mbindyo,¹Jafred M. A. Kitaa,¹Tequiero O. Abuom,¹Gabriel O. Aboge,²Daniel W. Muasya,¹Beatrice W. Muchira,²Nduhiu Gitahi,²and Charles M. Mulei¹

Academic Editor: Tanmoy Rana

Received31 Jan 2023

Revised23 Mar 2023

Accepted25 Mar 2023

Published08 Apr 2023

Abstract

Campylobacter species are widely distributed pathogens; however, data on its epidemiology in puppies remain scanty, especially in Kenya. A cross-sectional study was conducted in the Nairobi Metropolitan Region to determine molecular prevalence and associated risk factors of Campylobacter species infection in puppies. A total of 260 rectal swabs were collected from puppies from breeding kennels, shelters, and the University of Nairobi Veterinary Teaching and Referral Hospital. The samples were subjected to polymerase chain reaction (PCR) assays for identification of Campylobacter species. Data on potential risk factors associated with puppy exposure were collected using a semistructured questionnaire. Multivariable mixed effects logistic regression analyses were performed with kennels as random effects. Campylobacter species were detected in 64 of the 260 sampled puppies yielding an overall prevalence of 24.6%. Multivariable results showed that puppies from shelters, puppies from kennels that are washed daily, puppies with a recent history of vomiting, and those treated with antibiotics in the past month were significantly associated with the presence of Campylobacter species. Being a kenneled puppy and having had concurrent bacterial infections were identified as protective factors. This study provides molecular evidence of puppy exposure to Campylobacter species which could have impact on puppy health and highlights the need to develop awareness and management strategies to potentially reduce the risk of transmitting this pathogen among puppies, to humans, and other animals.

1. Introduction

Campylobacteriosis, caused by thermophilic bacteria of the genus Campylobacter, is a significant zoonotic gastrointestinal disease affecting humans and animals, including dogs, globally [1–4]. The vast majority of Campylobacter infections in humans are attributable to the consumption of contaminated or undercooked poultry [2, 5, 6], contaminated water [7], or raw milk [1]. Close contact with pets has also been identified as a significant source of human Campylobacter species infections [8, 9] with dogs, particularly puppies (less than one year), serving as potential reservoirs of Campylobacter infection for their owners, with infants and young children having a higher risk of infection [10].

Campylobacter species prevalence in dogs varies widely [11–15], depending on age, geographic region, housing, diagnostic method, clinical history (diarrheic versus non-diarrheic dogs), and the presence of infection or concomitant disease [8, 16, 17]. Feeding homemade and commercial diets, compost exposure, and outdoor water access have all been linked to Campylobacter colonization in dogs [18–20]. The infection has also been linked to purebred dogs, concurrent enteric disease, and antibiotic treatment [21, 22]. Furthermore, when compared to adult dogs, younger dogs are more likely to become infected with Campylobacter species [12].

Though the detection of Campylobacter species is generally performed using the conventional culture method, it is time-consuming and labor-intensive, due to the fastidious nature of the species [23]. Hence, molecular-based assays, like polymerase chain reaction (PCR) and sequencing enable rapid and precise detection [1, 24, 25].

Despite reports of puppies serving as essential reservoirs for Campylobacter pathogens, current data on Campylobacter species epidemiology in Kenyan puppies are limited. Therefore, this study aimed at determining the molecular prevalence and associated risk factors of Campylobacter species in puppies in the Nairobi Metropolitan Region, Kenya.

2. Materials and Methods

2.1. Ethical Approval

This study was approved by the Biosecurity, Animal Use, and Ethics Committee (BAUEC) of the Faculty of Veterinary Medicine, University of Nairobi, Kenya (FVM BAUEC/2019/237). Verbal consent was sought from breeders, kennel managers, and puppy owners prior to sampling.

2.2. Study Area and Design

Study areas and design have been previously described [26] (Figure 1). In brief, this study was a cross-sectional study undertaken between January 2021 and August 2021 in breeding kennels, shelters, and the University of Nairobi Veterinary Teaching and Referral Hospital in the Nairobi Metropolitan Region, Kenya. These facilities were selected purposefully based on the high populations of puppies (less than one year) and the diversity of puppy breeds and management practices. Puppies in these facilities were randomly selected and sampled.

2.3. Sample Collection

The sampling methods have been previously described [26] (Figure 1). In brief, in order to determine potential risk factors associated with Campylobacter species infection, a detailed questionnaire was administered to collect puppy-level factors (age, breed, sex, vaccination status, and deworming status) and management factors (type of food, type of housing, kennel hygiene, and environmental hygiene). Prior to sampling, each puppy was assigned a body condition score (BCS) in accordance with the Waltham Size, Health, and Physical Examination (SHAPE) Score™ which contains seven scores from A (underweight) to G (obese) based on the presence and amount of subcutaneous and abdominal fat [27] (https://www.slideshare.net/WalthamCPN/waltham-pocket-book-of-healthy-weight-maintenance-for-cats-and-dogs-71137293). The Canine Inflammatory Bowel Disease Activity Index (CIBDAI) clinical scoring system by Jergens et al. [28] was used for the assessment of the puppies’ general health status concerning gastrointestinal infection. The numerical index assesses the severity of illness based on the presence and frequency of six cardinal signs of gastrointestinal infection. Based on the total cumulative scores, the infection was classified as follows: clinically insignificant (0 to 3), mild (4 to 5), moderate (6 to 8), or severe (9 or greater). A total of 260 rectal swabs were then collected from the puppies: breeding kennels (n = 210), shelters (n = 6), and veterinary hospital (n = 44).

2.4. Polymerase Chain Reaction (PCR) Analysis for Identification of Genus Campylobacter

The isolates utilized in this study were obtained from a previous study on culture prevalence in puppies in Kenya [26] (Figure 1). Campylobacter isolates were isolated on mCCDA (Oxoid, CM0935) and identified by biochemical tests (oxidase and catalase tests). Genomic DNA was obtained from these presumptive Campylobacter species isolates using the boiling method as described by Wang et al. [29]. Polymerase chain reaction (PCR) amplifications were performed using a thermal cycler (Bio-Rad T100™ Thermal cycler). To confirm members of the genus Campylobacter, primers (C412GF 5′-GGATGACACTTTTCGGAGC-3′ and C1228R 5′- CATTGTAGCACGTGTGTC-3′) [30] targeting the 16S rRNA gene were used. The polymerase chain reaction was performed in a total volume of 12.5 μl containing mastermix of 6.25 μl and 0.25 μl each of forward and reverse primers, 5 μl of DNA template, and 0.75 μl of sterile distilled water.

The thermocycling conditions used were initial denaturation at 95°C for 15 minutes, followed by 25 cycles each of denaturation of 95°C for 30 seconds, annealing at 58°C for 1.5 minutes, extension at 72°C for 1 minute, and final heating at 72°C for 7 minutes. Samples were held at 4°C prior to analysis.

Controls were used for all PCR assays, and 10 μl of amplified products was identified by electrophoresis in a 1.5% (weight/volume) agarose gel in 1X Tris-Borate-EDTA (TBE) buffer, subsequently stained with ethidium bromide and ran for 30–45 minutes at 200 V, and visualized by UV-illuminator (UVP GelMax 125 Imager, USA). The sizes of the amplicons were determined using 100 bp molecular ladder. Specific amplified fragments expected were of size 816 bp which corresponded to the Campylobacter genus.

The unit of observation corresponded to an individual sample, and each sample represented an individual puppy. If Campylobacter was detected by PCR in a sample, the puppy was considered infected.

2.5. Data Entry and Analysis

Questionnaire data and PCR results were entered into Microsoft Excel version 2016 (Redmond, WA, USA) before being exported to STATA 17.0 (StataCorp LLC, USA) for analysis. Campylobacter species prevalence and other demographic parameters were computed using descriptive statistics. The chi-square test was used to compare Campylobacter species carriage ratios between different categorical groups. Potential factors associated with Campylobacter species carriage in puppies were investigated using univariable logistic regression analysis. Covariates were retained in the model if statistically significant at p ≤ 0.2 using a backward stepwise elimination procedure. All variables that showed an association with the outcome variable in the univariable logistic regression analysis (p < 0.05) were considered in the final mixed effects logistic regression analysis. Potential clustering of puppies within kennels was controlled by including kennels as a random effect in the modeling. Model fit was assessed by checking for multicollinearity, overall goodness of fit of the model, influential data points, and outliers.

3. Results

3.1. Molecular Prevalence of Campylobacter Species Infection in Puppies in the Nairobi Metropolitan Region, Kenya

Polymerase chain reaction was used to identify Campylobacter species isolates obtained from a previous study [26]. This was done by targeting the 16S rRNA gene specific to Campylobacter species which produced a specific band corresponding to the expected size of 816 bp (Figure 2). The results from PCR analysis revealed a molecular prevalence of 24.6% (64/260).

3.2. Descriptive Statistics of Variables and Univariable Logistic Regression Analysis of Potential Risk Factors for Puppy Campylobacter Species Positivity ( ≤ 0.2)

The distribution of various puppy-level and management factors associated with Campylobacter species infections based on PCR is described in Table 1. A higher prevalence of Campylobacter species was observed in puppies from shelters (50% (3/6)) and those kept as pets (29.7% (11/37)). Similar observations were noted in puppies sharing a kennel (25.1% 55/219)), whose kennels were washed on a daily basis (27.1% (62/229)), from kennels with wooden floors (27.8% (49/176)), and puppies fed homemade diets (30.7% (27/88)).

Univariable logistic regression identified 11 factors to be associated ( ≤ 0.2) with positive Campylobacter species PCR status (Table 1). Four of the factors were associated with higher Campylobacter species carriage. They include kennels with concrete floors (OR: 2.3; = 0.12), kennels that are washed daily (OR: 6.7; = 0.0001), puppies with a history of recent vomiting (OR: 1.5; = 0.2), and puppies treated with antibiotics in the past month (OR: 1.7; = 0.093). Seven factors were associated with lower Campylobacter species carriage: puppies from breeding kennels (OR: 0.6; = 0.003), puppies from shelters (OR: 3; = 0.0001), puppies kept for security (OR: 0.3, = 0.029), kenneled puppies (OR: 0.8, = 0.005), puppies more than 5 months of age (OR: 0.3; = 0.016), puppies with an ideal body condition or are moderately obese (OR: 0.6; = 0.14), and puppies with concurrent bacterial infections (OR: 0.5, = 0.2).

3.3. Multivariable Mixed Effects Logistic Regression Analysis of Significantly Associated Explanatory Variables for Puppy Campylobacter Species Positivity ( < 0.05)

Multivariable logistic regression analysis revealed that the factors significantly associated with higher Campylobacter species positivity at < 0.05 were puppies from shelters (OR: 2.6, 95% CI: 1.9–3.6, = 0.0001), kennels that are washed on a daily basis (OR: 11.4, 95% CI: 2.8–46, = 0.001), puppies with a recent history of vomiting (OR: 3.4, 95% CI: 1.01–11.4, = 0.046), and puppies treated with antibiotics in the past month (OR: 2, 95% CI: 1.11–3.6, = 0.02). Protective factors identified were puppies from breeding kennels (OR: 0.65, 95% CI: 0.44–0.94, = 0.024) and puppies with concurrent bacterial infections (OR: 0.18, 95% CI: 0.04 = 0.87, = 0.033).

3.4. Prevalence of Campylobacter Species Infection Based on the Canine Inflammatory Bowel Disease Activity Index (CIBDAI) Clinical Scoring System

Fifty-four out of 260 puppies exhibited one or more of the six cardinal signs of gastrointestinal infection used to assess the degree of illness. Polymerase chain reaction identified Campylobacter species in 36.4% and 13.7% of the puppies whose infection status was classified as severe and clinically insignificant, respectively (Table 2).

4. Discussion

The study of zoonotic diseases such as campylobacteriosis is necessary due to the increasing number of people keeping dogs in their homes. Given that dogs, especially puppies, can be reservoirs of pathogenic Campylobacter, it is necessary to increase information about the epidemiology of this disease in these animals.

Polymerase chain reaction (PCR) detected 64 Campylobacter species (24.6%, 64/260) by targeting the 16S rRNA gene specific for these microorganisms. This proportion was within the range of 8.58% to 75.7% reported in studies done in the past five years [15, 31–33]. The relatively high prevalence of thermophilic Campylobacter species observed in this study among puppies is a cause for concern, as their feces contaminate the environment and may serve as a source of infection for humans, particularly children.

Though clinical manifestations of gastroenteritis include diarrhea and vomiting [34], this study found no significant association between diarrhea occurrence and Campylobacter-positive status, a finding that is in agreement with previous research [35, 36]. However, this study found a statistically significant association between vomiting in puppies and the isolation of Campylobacter species. This finding contradicts those of Verma et al. [11], who found no correlation between Campylobacter species infection and the incidence of vomiting in dogs. Findings of this study, however, concur with those of Guest et al. [37], who found a link between gastrointestinal signs and Campylobacter species infection in puppies.

Shelter-housed puppies were at a higher risk for Campylobacter species carriage. These findings are in agreement with those of previous studies [36, 38]. Campylobacter species carriage is more prevalent among puppies who share a habitat with other puppies such as in shelters [12, 39, 40]. This may be due to the fact that puppies are from multiple sources and the stress of comingling predisposes them to stress and vices such as coprophagia which may lead to the ingestion of these bacteria, resulting in further infection, shedding in feces, and contamination of the environment [41]. The puppies may also roll in the feces, contaminating their fur [42] and further spreading the bacteria to surfaces with which they come into contact.

It is recognized that kennel hygiene is a potential risk factor for Campylobacter species carriage in dogs [43]. In this study, the daily washing of kennels was a highly significant risk factor for Campylobacter species carriage in the studied puppies. Despite the fact that daily washing of kennels improves hygiene, Campylobacter species are sensitive to desiccation and do not survive in dry environments [44], and thus daily washing increases their survivability in kennels as well as increases the chance of contamination of water sources [45], allowing water to be a vehicle for dissemination [46]. Puppies may also lick the residue water, resulting in pathogen ingestion.

Treatment with antibiotics in the past month was greatly significant with the risk of Campylobacter species carriage which was in agreement with a study by Leonard et al. [18]. This could be due to the inappropriate use of antibiotics in the treatment of other systemic infections with campylobacteriosis co-infection, thus promoting the emergence of antimicrobial resistant strains of Campylobacter species.

5. Conclusion

This study has shown that puppies in Kenya carry Campylobacter species which can be transmitted to humans and other animals through contaminated environmental sources. Polymerase chain reaction (PCR) should be regarded as indispensable in clinical and epidemiological research. It is important to develop awareness and management strategies to potentially reduce the risk of transmitting this pathogen from puppies to humans and other animals.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

The authors thank the Faculty of Veterinary Medicine, University of Nairobi, where the experiments were performed. Special appreciation goes to the breeders, kennel managers, and puppy owners who gave their consent to sample their puppies.

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Copyright © 2023 Sharon N. Mbindyo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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