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.

Control of cystic echinococcosis in the Middle Atlas, Morocco: Field evaluation of the EG95 vaccine in sheep and cesticide treatment in dogs.

BACKGROUND: Cystic echinococcosis (CE) is an important cause of human morbidity and mortality worldwide, particularly in Morocco and other North African countries. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the potential of three strategies to reduce Echinococcus granulosus transmission: (1) 4-monthly treatment of dogs with praziquantel, (2) vaccination of sheep with the EG95 vaccine and (3) a combination of both measures. These measures were implemented during four consecutive years in different areas of the Middle Atlas Mountains in Morocco. The outcome of the interventions was assessed through hydatid cyst (viable and non-viable) counts in liver and lungs using necropsy or in vivo ultrasound examination of the liver. A total of 402 lambs were recruited for annual vaccination with the EG95 anti-E. granulosus vaccine and 395 similar lambs were selected as non-vaccinated controls. At approximately four years of age the relative risk (estimated as odds ratio) for vaccinated sheep to have viable hydatid cysts compared with non-vaccinated controls was 3% (9.37% of the vaccinated sheep were found infected while 72.82% of the controls were infected; p = 0.002). The number of viable cysts in vaccinated animals was reduced by approximately 97% (mean counts were 0.28 and 9.18 respectively; p<0.001). An average of 595 owned dogs received 4-monthly treatment during the 44 months trial, corresponding to 91% of the owned dog population. Approximately, 5% of them were examined for E. granulosus adult worms by arecoline purge or eggs in feces (confirmed by PCR). The proportion of infected dogs significantly decreased after treatment (12% versus 35%; p<0.001). Post-treatment incidence of re-infestation corresponded to a monthly risk of 4% (95% CI: 3-6%). Treatment of owned dogs on a 4-monthly basis did not reduce the level of transmission of E. granulosus to sheep, nor did it enhance the level of control generated by vaccination of sheep with EG95, possibly because of unowned dogs and wild canids were not treated. CONCLUSIONS/SIGNIFICANCE: These data suggest that vaccination of sheep with EG95 has the potential to reduce the level of CE in Morocco and in other parts of the world with similar transmission dynamics. Under the epidemiological circumstances existing in the trial area, 4-monthly treatment of owned dogs with praziquantel was insufficient to have a major impact of E. granulosus transmission to sheep.

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.