Prevalence, risk factors and zoonotic potential of intestinal parasites in dogs from four locations in Morocco.

Dogs can harbor various intestinal parasites that have serious clinical, economic, and zoonotic impact. In Morocco, the epidemiological status of those parasites is largely unknown. This study aimed to obtain data on the prevalence of intestinal parasites in various Moroccan dog populations, to identify associated risk factors, to evaluate people's knowledge regarding zoonotic parasites and to estimate the risk of human infection. A total of 291 fecal samples were analyzed using a 33% Zinc Sulphate (ZnSO4) centrifugal flotation and a sheather's sugar simple flotation techniques. In addition, 100 dog owners were asked to fill out a questionnaire about their knowledge regarding canine zoonotic intestinal parasites. Overall, 58% of sampled dogs were positive for at least one parasite species. Ancylostoma/Uncinaria spp. (31.9%), Toxascaris leonina (27.4%), Toxocara canis (27.1%), Cystoisospora spp. (13.4%) and Giardia spp. (7.2%) were the most frequently isolated parasites. The overall prevalence was associated with the dogs' activity, and feces consistency. More specifically, the prevalence of Ancylostoma/Uncinaria spp., Toxascaris leonina and Cystoisospora spp. was associated with dogs' activity and feces consistency and, additionally with age for Cystoisosporaspp.Toxocara canis prevalence was associated with age and feces consistency, while Giardia spp. prevalence was associated with dogs' activity. A weak awareness among dog owners regarding the zoonotic potential of canine intestinal parasites was noticed (33%) especially when their knowledge was compared to another endemic zoonotic disease, i.e. rabies (85%). Furthermore, the rate of respecting the vaccination protocol (82%) was significantly higher than the rate of respecting the deworming protocol (47%). We conclude that intestinal parasites, including the zoonotic ones, were highly prevalent in the dogs sampled in this study whereas people's knowledge about those parasites was very limited. These findings suggest that the risk of human infection is very likely, which highlights the need for effective control programs and health education.

Feasibility and acceptability of a new integrated approach to control cystic echinococcosis in Morocco: Vaccination of sheep and anthelmintic treatment of dogs.

Cystic echinococcosis (CE) or hydatidosis is a common parasitic disease worldwide, especially in poor and developing countries. In Morocco, CE is a major zoonosis, despite the implementation of a national control program since 2007. Therefore, in 2016, a field trial that associates the EG95 vaccine (lambs) and anthelmintic treatment (dogs) was started in the Mid Atlas, the most endemic region in Morocco, with preliminary positive results. Here, a qualitative approach was used to analyze the feasibility and social acceptability of this strategy. Fifteen focus group discussions were separately conducted with breeders and with their wives, and forty-two individual interviews were performed with private-sector veterinarians and officers from structures responsible for the CE control program. Recordings were transcribed and analyzed with the R software, using the RQDA package. This qualitative research was validated using the credibility, transferability, dependability and confirmability criteria. This study showed that the professionals' views on sheep vaccination and anthelmintic treatment were divided between acceptability and concerns. Conversely, breeders and their wives highlighted the issue of the costs of procedures the utility of which was not immediately clear to them. All participants proposed solutions to improve this strategy, and also stressed the lack of education on CE. By bringing together the views of the communities and the professionals, this study traced the main lines (targeting the different aspects of CE and taking into account the local socio-cultural beliefs) that must be taken into account to ensure the short- and long-term CE control in Morocco.

Using qualitative approaches to explore the challenges of integrated programmes for zoonosis control in developing countries: Example of hydatidosis control in Morocco.

Cystic echinococcosis, rabies and bovine tuberculosis are major neglected zoonoses in many developing countries, including Morocco. A common step in their control strategies is the management of slaughterhouses and/or the control of dog populations. This study used a qualitative approach to identify the barriers to the implementation of the cystic echinococcosis control programme in Morocco that focused on slaughterhouses and dog control. This approach could be used to understand the causes leading to the defective management of other zoonoses, and to go beyond the often-invoked 'lack of means' reason to explain failure in disease control in the Global South. Specifically, slaughterhouse observation and in-depth individual interviews with stakeholders involved in the cystic echinococcosis control programme were carried out in five Moroccan regions (Rabat-Sale-Kenitra, Mellal-Khenifra, Sous-Masaa, Laayoune-Sakia El Hamra and Guelmim-Oued Noun) for 3 years (from 2014 to 2016). Interviews (n = 81) were with agents responsible of the services managing slaughterhouses and dog population control, and also with slaughterers. Recordings were fully transcribed and narratives were analysed with the RQDA package and the R software. Triangulations and the criteria proposed by Guba and Lincon were used to assess the approach validity. This analysis revealed that in addition to 'lack of means', zoonosis control programmes can be hindered by overlapping authority/functions among the involved authorities, conflicts of interest, lack of proper training and professional practices. Zoonosis control requires the commitment of all structures, the establishment of a national and inter-regional strategy, and the updating of the legislative arsenal.

Stakeholder analysis to improve the national control program of cystic echinococcosis in Morocco.

Cystic echinococcosis (CE) is a major zoonosis in Morocco. Despite a national hydatidosis control programme (NHCP) established in 2005, CE burden is still high nationwide. The aim of this study was to carry out an NHCP stakeholders' analysis to identify weak points and propose improvement strategies. In total, 164 semi-structured interviews were carried out with national and local stakeholder representatives, and one stakeholders' workshop was organized. Classical categories of stakeholder analysis (i.e. involvement, interest, importance, influence, priority, and power) were semi-quantified. Based on these categories, an analytical framework was proposed, by selecting elements from the stakeholder analysis, to structure the assessment around three criteria: measure appropriation, political agency, and socio-technical agency. Besides specific weak points of the NHCP, the analysis highlighted the complexity of implementing a zoonotic disease control programme due to the involvement of many different stakeholders. Finally, this study provides a simplified stakeholder analysis method that could be used to assess other health programmes targeting zoonotic diseases, in Morocco and in similar countries.

The socio-economic burden of cystic echinococcosis in Morocco: A combination of estimation method.

Cystic echinococcosis (CE) is a major zoonosis in Morocco despite the launch of a national control programme in 2005. As its economic consequences have not been studied yet in Morocco, this study estimated CE impact in terms of monetary losses, disability-adjusted life years (DALY), and DALY for zoonotic diseases (zDALY) in the entire country and in specific regions for the 2011 to 2014 period. The direct monetary losses were related to organ seizure from infected animal in slaughterhouses, and to healthcare expenses as well as lost wages for infected humans. Animal production losses concerned milk yield, fertility, carcass weight, and wool production. Losses due to human infection were also composed of disability and productivity losses at work. Monte Carlo simulations were used to estimate monetary losses and zDALY values. Nationwide, the estimated DALY was 0.5 years per 100,000 persons per year, and the zDALY was 55 years per 100,000 persons per year. Total yearly losses were estimated at 73 million USD (54-92 million USD). However, losses differed significantly among regions. Most of the economic losses consisted of unperceived consequences, i.e. decreased animal production and reduced productivity of asymptomatic individuals. Future studies should determine the socioeconomic and epidemiological factors underlying the differences in economic losses among regions to develop better adapted control programmes.

Cystic Echinococcosis in Three Locations in the Middle Atlas, Morocco: Estimation of the Infection Rate in the Dog Reservoir.

A longitudinal study was carried out in Middle atlas, Morocco (locality of Had Oued Ifrane) in a population of 255 dogs from three localities, including two categories of dogs (owned and stray dogs). The dogs were investigated three times over a period ranging from 4 to 8 months between December and August. At each investigation, dogs were treated with arecoline, inducing defecation and allowing feces collection. Dogs were further treated with praziquantel to clear them from Echinococcus granulosus. Microscopic examination of feces was performed to assess the infection status of dogs at each investigation, and positive samples underwent copro-PCR to determine the circulating strain of E. granulosus. A high prevalence of infestation ranging from 23.5% to 38.8% and from 51.3% to 68.5% was, respectively, found in owned and in stray dogs. The PCR results revealed the presence of G1 strain in all positive samples. A logistic regression model was used to determine the incidence of infestation and showed that stray dogs underwent a significantly higher risk of infection (odds ratio = 14; 95% confidence interval: 6-30; p < 0.001) compared with owned dogs. Only anthelmintic treatment intervals of 2 months efficiently prevented egg shedding in owned and stray dogs. The seasonal effect was also significant, with the highest risk of reinfestation in winter and the lowest risk in summer. This study confirms that stray dogs undergo an increased risk of infestation by E. granulosus and indicate that infective pressure is influenced by season.

Community perception and knowledge of cystic echinococcosis in the High Atlas Mountains, Morocco.

BACKGROUND: Cystic echinococcosis (CE), a neglected zoonosis caused by the larval stage of the tapeworm Echinococcus granulosus, remains a public health issue in many developing countries that practice extensive sheep breeding. Control of CE is difficult and requires a community-based integrated approach. We assessed the communities' knowledge and perception of CE, its animal hosts, and its control in a CE endemic area of the High Atlas Mountains, Morocco. METHODS: We conducted twenty focus group discussions (FGDs) stratified by gender with villagers, butchers and students in ten Berber villages that were purposefully selected for their CE prevalence. RESULTS: This community considers CE to be a severe and relatively common disease in humans and animals but has a poor understanding of the parasite's life cycle. Risk behaviour and disabling factors for disease control are mainly related to cultural practices in sheep breeding and home slaughtering, dog keeping, and offal disposal at home, as well as in slaughterhouses. Participants in our focus group discussions were supportive of control measures as management of canine populations, waste disposal, and monitoring of slaughterhouses. CONCLUSIONS: The uncontrolled stray dog population and dogs having access to offal (both at village dumps and slaughterhouses) suggest that authorities should be more closely involved in CE control. This study also highlights the need for improved knowledge about the transmission cycle of the parasite among communities and health professionals. Inter-sectoral collaboration between health staff, veterinarians, and social scientists appears to be crucial for sustainable control of this parasitic zoonosis.

A review of cutaneous leishmaniasis in Morocco: A vertical analysisto determine appropriate interventions for control and prevention.

Leishmaniasis is considered one of the most neglected diseases worldwide. In Morocco, cutaneous leishmaniasis is an important public health problem. Leishmania major and Leishmania tropica are the two major species in this country. Despite all efforts, monitoring and control of the cutaneous leishmaniasis is still challenging. We used for the first time a vertical analysis of the control of cutaneous leishmaniasis in Morocco from the document review and publications. This analysis allowed us to develop an epidemiological model that emphasized key possible interventions. No evaluation studies of these interventions in Morocco were done. Global Evidence underline the effectiveness of preventive interventions produced in integrate inter-sectorial strategy framework (e.g use of insecticide-treated bednets, indoor residual spraying and rodents' control) rather than treatments such as based thermotherapy, cryotherapy, photodynamic therapy, CO2 laser and paromomycin. Therefore, integrated vector management control (IVMC) with communityc participation is recommended as effective strategy. Strengthening of the IVMC with community involvement are necessary conditions to improve the program of cutaneous leishmaniasis and prevent epidemic foci appearance.

Intersectoral collaboration between the medical and veterinary professions in low-resource societies: The role of research and training institutions.

BACKGROUND: Neglected zoonoses continue to significantly affect human health in low-resource countries. A symposium was organised in Antwerp, Belgium, on 5 November 2010 to evaluate how intersectoral collaboration among educational and research institutions could improve the situation. RESULTS: Brucellosis and echinococcosis were presented as models for intersectoral collaboration. Low-resource societies face evident knowledge gaps on disease distribution, transmission within and across species and impact on human and animal health, precluding the development of integrated control strategies. RECOMMENDATIONS: While veterinarians have been the main driver of the One Health initiative, the medical profession does not seem to be fully aware of how veterinary science can contribute to human public health. It was postulated that transdisciplinarity could help fill knowledge gaps and that encouraging such transdisciplinarity should start with undergraduate students. Furthermore, intersectoral collaboration on zoonoses should not ignore the social sciences (e.g. assessment of indigenous knowledge and perception; participatory surveillance), which can contribute to a better understanding of the transmission of diseases and improve communities' participation in disease control activities.