Epidemiology of canine gastrointestinal helminths in sub-Saharan Africa

Background Dogs have a close association with humans providing companionship, security and a source of dietary protein. However, dogs are also potential carriers of zoonotic pathogens. Dogs, therefore, pose a public health risk and a good understanding of canine diseases is important for planning and implementing control measures. The aim of this study was to characterise canine helminthiasis in sub-Saharan Africa using a systematic approach. Methods Pubmed and Google Scholar were searched for relevant primary studies published from 2000. Forty-one eligible studies were included in the meta-analysis. Pooled prevalences were estimated using the quality effects model. Results and conclusions Twenty-six genera of enteric helminths were reported and the pooled estimate of canine helminthiasis was 71% (95% CI: 63–79%). Species of Ancylostoma and Toxocara, causative agents of larva migrans in humans, were the most frequently reported helminths with pooled estimated prevalences of 41% (95% CI: 32–50%) and 22% (95% CI: 16–29%), respectively. Dipylidium caninum and Taenia spp. were the most frequently reported cestodes with pooled estimated prevalences of 20% (95% CI: 12–29%) and 9% (95% CI: 5–15%), respectively. Trematodes were rarely reported. There was a high level of heterogeneity in most pooled estimates (I2 ˃ 80%). The results of this study show that canine helminthiasis is highly prevalent in sub-Saharan Africa and there is need for regular deworming programmes to improve the health status of the dogs and minimise the potential health risk to humans. Electronic supplementary material The online version of this article (10.1186/s13071-018-2688-9) contains supplementary material, which is available to authorized users.


Eligibility criteria
The titles and abstracts were reviewed and articles were selected based on the following criteria: English language; full-text journal articles published from 2000; conducted in a country in sub-Saharan Africa; crosssectional or prospective studies. Articles were excluded if they did not report prevalence data, were case-control studies, clinical trials or pharmacological studies.

Quality of the studies
Eligible studies were assessed for quality of reporting and selection for bias using a quality assessment checklist [11,12] (Additional file 1).

Data extraction
The following data were extracted where possible: location of the study, sample size, overall prevalence, genus and prevalence of detected helminths, sampling method, type of sample collected, sample processing and diagnostic method, age and sex of the dogs. For simplicity, dogs were characterised as puppies (≤ 6 months), juveniles (˃ 6-12 months), immature (≤ 12 months) and mature (> 12 months). Relevant data was stored in Microsoft Excel.

Data analysis
MetaXL version 3.1 (http://www.epigear.com/), a tool for meta-analysis in Microsoft Excel, was used to pool prevalences from each study [13,14]. Pooled estimated prevalences and their 95% confidence intervals (CI) were calculated using the quality effects model. The quality effects model uses quality scores to weigh studies according to sample size and study quality [13]. Pooled prevalence estimates were calculated for genera where prevalence data was extracted from a minimum of five studies. Heterogeneity among studies was evaluated by I 2 . I 2 values of 25%, 50% and 75% were considered as having a low, moderate and high degree of heterogeneity, respectively [15]. Publication bias was assessed using funnel plots and doi plots. The symmetry of the doi plots was evaluated using the LFK index. LFK index values within ± 1, exceeding ± 1 but within ± 2, and exceeding ± 2 were considered as having no asymmetry, minor asymmetry and major asymmetry, respectively [14].
Potential sources of heterogeneity were further assessed by arranging the studies in subgroups according to sex, age (puppy and juvenile or immature and mature) and geographical regions (East Africa, West Africa and southern Africa). Regional subgroup analysis was conducted for helminth genera reported in at least 50% of the articles.

Characteristics of eligible studies
A total of 41 articles  from eight countries were identified ( Fig. 1) and included in this study. The sample size of individual studies ranged from 33 to 1000 dogs. The quality of the selected studies ranged from 1 to 9. Additional file 2: Table S1 and Additional file 3: Figure  S1 give an overview of characteristics of eligible studies. A total of 12,029 samples, consisting of 11,717 faecal samples and 312 intestinal samples were included in the study. All samples were analysed using microscopy and processed using flotation (39%), sedimentation and flotation (39%), Kato-Katz (10%), sedimentation (5%) and washing and decantation (2%).
Sex and age prevalences are summarised in Table 2. The overall estimated pooled prevalence of gastrointestinal helminths in male dogs was 62% (95%: 45-78%) while the prevalence in female dogs was 56% (95% CI: 40-71%). Prevalence of helminths in immature and mature dogs were 74% (95% CI: 56-89%) and 62% (95% CI: 42-81%), respectively. Juveniles had lower overall estimated pooled prevalence compared to puppies. In addition, estimated pooled prevalences of Ancylostoma spp. and Toxocara spp. were lower in mature dogs compared to immature dogs. Additional file 6: Figure S4 and Additional file 7: Figure S5 show the forest plots of the estimated prevalences in the sex and age subgroups.
There was a high level of heterogeneity in most pooled estimates (I 2 > 80%) which could not be reduced with subgroup analysis by sub-region, age and sex. Assessment of the funnel plot and doi plot ruled out significant publication bias (Additional file 8: Figure S6).

Discussion
This study summarised the prevalence of canine gastrointestinal helminths in sub-Saharan Africa. The prevalence of canine helminths in sub-Saharan Africa is high with an estimated pooled prevalence of 71% (95% CI: 63-79%) across 36 studies. The high prevalence of gastrointestinal helminths may be due to inadequate deworming of dogs [17,19,23,26,35,38,40,41,43,53]. The highest prevalence was recorded for Ancylostoma spp. These findings are comparable with studies in Portugal [57],   Mexico [58,59], Brazil [60] and Argentina [61]. However, other studies in the Czech Republic [62], Poland [63], Canada [64], Denmark [65] and southern Wisconsin [66] reported Toxocara spp. as the most prevalent helminth. These findings suggest that Ancylostoma spp. and Toxocara spp. are more prevalent in the tropical/sub-tropical and temperate regions, respectively. Dipylidium caninum was the most prevalent cestode. This is in agreement with other studies conducted in China [26], Mexico [58,59], Brazil [60] and Poland [63]. The estimated pooled prevalence of helminths in males was higher than in females. This result is not in agreement with other studies [58,[66][67][68]. A possible reason for the male-biased helminth prevalence may be the high Ancylostoma spp. prevalence. Male-biased Ancylostoma prevalences have been reported in some studies [61,66,69]. It is possible that male-biased helminth prevalence may occur when the prevalence of Ancylostoma spp. is higher than other helminths, as seen in this study. Another possible reason for the malebiased prevalence is the low deworming and neutering prevalences in the dog populations included in this study. Dogs in sub-Saharan Africa receive limited veterinary care and are irregularly dewormed and rarely neutered [26,70]. Regular deworming and high neutering may significantly reduce the influence of sex on helminth susceptibility in studies that did not demonstrate male-biased prevalence. Unfortunately, the effect on sex on the prevalence of specific helminth genera could not be investigated as the data was not provided in the primary studies.
The overall estimated pooled prevalence of canine intestinal helminths was higher in young dogs than in adults. These results are in agreement with other studies that demonstrated a higher overall prevalence in young animals [67,68,71]. Higher prevalence in immature animals has been attributed to lower immune competence in this age group [69]. It would have been interesting to investigate the effect of both age and sex on helminth prevalence; however, this data was not reported in the primary studies.
This study has many limitations. First, the data displayed a large degree of heterogeneity across the studies across and sub-regions. Secondly, the studies were conducted in only eight countries: Nigeria, Ethiopia, Tanzania, Gabon, Ghana, Cameroon, Zambia and South Africa. Moreover, Nigeria and Ethiopia were overrepresented. Therefore, the results may not reflect the real situation in the region. The lack of studies from the majority of countries in sub-Saharan Africa may be due to limited research on canine diseases conducted in the region. Alternatively, it may be due to studies not being published in journals accessible online. Another limitation of this study is the incomplete information provided by some studies. For example, some studies provided limited information on study area while other studies did not report the helminths to species level; consequently, the results could not be further analysed to identify the source of the heterogeneity.

Conclusions
Despite the limitations of the study, the results indicate that the canine gastrointestinal helminths are highly prevalent in sub-Saharan Africa and there is a need for regular deworming programmes to improve the health status of the dogs and minimise the potential health risk to humans.