Higher - University of Edinburgh€¦  · Web viewPrevalence was especially high in the Middle Atlas mountains in cattle (48.7%) and in the Loukkos region in cattle and sheep (37.6%

Echinococcus granulosus infection in dogs in Sidi Kacem Province (North-West Morocco)

DAKKAK A.1; EL BERBRI, I.1; PETAVY A.F.2; BOUÉ, F.3; BOUSLIKHANE, M.1,

FASSI FIHRI, O.1, WELBURN, S.4, DUCROTOY, M.J.4*

1 Institute of Agronomy Veterinary Medicine Hassan II, Department of Pathology and

Veterinary Public Health, Rabat Morocco.

2 Université Claude Bernard, Lyon, France.

3 Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du travail, Laboratoire de la rage et de la faune sauvage, Nancy, France.

4 Division of Infection and Pathway Medicine, School of Biomedical Sciences, College

of Medicine and Veterinary Medicine, The University of Edinburgh, Chancellor’s

Building, 49 Little France Crescent, Edinburgh EH16 4SB, United Kingdom.

*Corresponding author: e-mail: [email protected]

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Abstract This study was undertaken in the Province of Sidi Kacem in northwest Morocco

between April 2010 and March 2011. The main objective of the study was to

determine the prevalence of Echinococcus granulosus (Eg) infection in owned dogs.

This province was selected as a case study because of the social conditions,

geographic and climatic diversity making it a model representative of many parts of

Morocco. The survey was carried out in 23 rural communes and in the 5

municipalities (urban districts) of the Province and sampling was undertaken in

randomly selected households. A total of 273 owned dogs comprising 232 from the

23 rural communes (rural dogs) and 41 from the 5 municipalities (urban dogs) were

tested. Arecoline hydrobromide purgation was selected as the diagnostic method of

choice to enable visualisation of expelled worms by dog owners, thereby imparting

messages on the transmission mode of Eg to humans and farm animals. Of the 273

dogs tested, purgation was effective in a total of 224 dogs (82.1%). The overall

estimated prevalence of Eg infection was 35.3% (79/224, 95% CI 22.3-47.0%). Dogs

inhabiting rural communes were at greater risk of infection (38.0%, 95% CI 31.1-

45.3%) than dogs roaming in municipalities or urban areas (18.8%, 95% CI 7.2-

36.4%) and the prevalence of infection was higher in those inhabiting rural

communes with slaughterhouses (62.7%, 95% CI 48.1-75.9%) than in communes

without (29.1%, 95% CI 21.7-37.2%). This first assessment of Eg infection in Sidi

Kacem Province indicates a key role of rural slaughterhouses in parasite

transmission to dogs.

Key words: Echinococcus granulosus, prevalence, dog, northwest Morocco.

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1. Introduction:

Cystic echinococcosis (CE) is a zoonosis caused by cestodes of the Echinococcus

granulosus (Eg) complex and is considered one of the most widespread parasitic

diseases (FAO/WHO, 2014). The disease has a significant economic impact

incorporating the cost of treating human cases and productivity losses for the

livestock industry (Budke et al., 2006). There is evidence that CE is becoming an

increasing public health and socio-economic problem in a number of countries where

control programs have been scaled-down due to lack of resources or where control

measures are lacking altogether (Eckert et al., 2000). CE is currently considered an

emerging or re-emerging disease and its geographic distribution and burden are

recognised to extend well beyond the official reports due to issues of under-reporting

in endemic countries (Moro and Schantz, 2009). Thompson and McManus, 2002).

Cystic echinococcosis affects at least one million people worldwide at any one time

and present estimates put annual costs at 3 billion US dollars for the treatment

human cases and losses to the livestock industry (FAO/WHO, 2014; WHO, 2015).

The lifecycle of the parasite includes domestic and wild carnivores (definitive hosts),

which harbour adult egg producing tapeworms in their small intestine, and

intermediate hosts, in which larval stages develop cyst-like structures in different

organs. Intermediate hosts include domestic and wild ruminants or marsupials (e.g.

sheep, cattle, goats, horses, donkeys, camels, pigs and even marsupial species such

as kangaroos and wallabies). Humans are considered an aberrant intermediate or

dead-end host, as they do not contribute to the perpetuation of the life cycle

(Torgerson et al., 2011).

Cystic echinococcosis is principally maintained in a domestic dog-sheep-dog cycle,

with the parasite being transmitted between stray or owned dogs and number of

domestic ruminant species (WHO, 2015). Even though the common sheep/dog cycle

is considered as the major source of human contamination, recent evidence from

Algeria has demonstrated that cattle act as reservoirs of sheep strains (Bardonnet et

al., 2003). The combination of people and dogs living in close proximity, scare water

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resources, and conditions with poor hygiene provide the ideal conditions environment

for Eg transmission (WHO/OIE, 2001).

Although common, it may be an oversimplification to say that dogs and domestic

herbivores maintain the CE cycle. Interaction between sylvatic cycles and domestic

cycles can occur, and in some contexts, intermediate hosts belonging to diverse taxa

(e.g. marsupial species such as kangaroos and wallabies in Australia) can be far

better hosts than domestic species and probably contribute significantly to the cycle

even where there are numerous cases of domestic CE (Barnes et al., 2012).

Cystic echinococcosis has been recorded in a large number of wild animals (Otero-

Abad and Torgerson, 2013). As a general rule, however, sylvatic epidemiology of CE

is poorly understood in most geographical areas (Barnes et al., 2012). To the best of

the author’s knowledge, no studies have investigated sylvatic cycles of CE in

Morocco. Among the neighbouring countries, it has been studied in Algeria only

where the golden jackal (Canis aureus) has been found to be definitive hosts for Eg

(Anderson et al., 1997).

In Morocco, current evidence demonstrates that the transmission cycle of Eg relies

primarily on a domestic cycle involving dogs and livestock species (sheep, cattle,

camels, goats and equines) (Azlaf and Dakkak, 2006). Stray dogs in urban areas and

free or roaming dogs in rural areas are the main definitive host and are pivotal in

transmission in this context (Azlaf and Dakkak, 2006; Azlaf et al., 2007; El Berbri et

al., 2015a).

The importance of the domestic dog-livestock cycle is also recognised in

neighbouring countries of the Mediterranean region (Anderson et al., 1997; Dakkak,

2010). E. granulosus is endemic in dogs and livestock in all North African countries

including Algeria, Egypt, Libya and Tunisia (Sadjjadi, 2006). The estimated

prevalence of Eg infection in stray and owned dogs was found to be 21.6% and

25.8% respectively in Libya (Buishi et al., 2005) and 21.0% (stray dogs) in Tunisia

(Lahmar et al., 2001). Cystic echninococcosis infection rates of 2.5%, 0.3%, 0.7%

and 6.4% have been reported for camels, sheep, goats and buffaloes respectively in

Egypt (Haridy et al., 2006). In Libya, prevalence estimates of 0-37.9%, 0-8.2%, 13.6-

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55.2% and 11% have been reported in sheep, goats, camels and cattle respectively

(Ibrahem and Craig, 1998; (Tashani et al., 2002). In Tunisia, the importance of small

ruminants as intermediate hosts has been demonstrated (Lahmar et al., 1999).

Camels are considered to be important for local maintenance of the life cycle, as

evidenced by prevalence estimates of 0.8% (2/250) and 10.1% (19/188) in Algeria

(WHO/OIE, 2001) and Tunisia (Lahmar et al., 2004) respectively.

In Morocco, CE represents a serious public health problem impacting both on the

economy and social welfare. In 2012, 1,627 human surgical cases (5.2 cases per

100,000 inhabitants) were recorded for the whole country (DELM, 2012). Surgeries

need to be repeated in 3% of cases, and a mortality of 3% was found. The cost of

treatment was estimated to be approximately US$ 1,700 and US$ 3,200 for simple

and repeat cases respectively; a financial burden to the health sector (Anderson et

al., 1997). Indirect costs due to recurrence and re-examination, reduced quality of life

following surgery, morbidity due to undiagnosed CE and expenses loss of income in

fatal cases were not considered in these burden calculations and if added would

increase the burden estimate (Anderson et al., 1997).

In a study conducted by Azlaf and Dakkak (2006) across five regions1 of Morocco

during the period 2001-2004, the CE prevalence estimates were: 10.1-48.7% in

cattle, 1.2-31.7% in sheep, 0.0-2.2% in goats, 10.9-63.0% in camels and 17.8% in

horses (central Morocco only), demonstrating considerable variation among host

species and region. Prevalence was especially high in the Middle Atlas mountains in

cattle (48.7%) and in the Loukkos region in cattle and sheep (37.6% and 31.7%

respectively). E. granulosus infection in dogs was investigated in the same regions1

and showed that infection rate at regional level was high, ranging from 22.0% to

62.8%. Consequently, these high prevalence lead to a very high contamination of the

environment with eggs (Gemmell et al., 2001), and hence the risk of transmission to

farm animals and humans is predicted to be very high. For these reasons, and in line

with WHO/OIE (2001), detection of infection in dogs is an essential component of

epidemiological studies and implementation of CE control programmes.

1 the Rif (Mediterranean coast and high mountains of the Rif), the Loukkos (Atlantic northwest plain), the center (Rabat and Casablanca regions), the Middle Atlas mountains and the south (arid and semi desert areas).

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The high incidence of surgical cases in humans (annual average of 6.5 surgical

cases per 100,000 inhabitants in Sidi Kacem Province compared to the national

average of 5.1 surgical cases per 100,000 inhabitants recorded for 2003-2010 by the

Ministry of Health of Morocco), and the high incidence of CE in cattle (42.9%) and in

sheep (11.0%) reported by El Berbri et al. (2015b), were suggestive of the

importance of dog infection in this province. Despite the rate of infection in dogs

probably being the best indicator of the degree of transmission of Eg in a region

(Barnes et al., 2012; Craig et al., 2003), data for Eg infection in dogs are lacking for

this region.

For these reasons, surveys in dogs were undertaken as part of a large collaborative

project funded by the EU under FP7, entitled the “Integrated Control of Neglected

Zoonoses” (ICONZ, www.iconzafrica.org) conducted in this region. Investigations on

CE included 1) prevalence of infection in livestock (cattle and small ruminants) as

part of abattoir surveys, 2) Eg prevalence in dogs, 3) evaluation of knowledge,

attitudes and practices with regards to the presence, transmission factors, impact,

and control of CE and, 4) piloting a control intervention.

The investigations on the prevalence of infection in livestock as part of abattoir

surveys showed high prevalence in cattle (42.9%) and in sheep (11.0%), and a low

prevalence in goats (1.5%) (El Berbri et al., 2015b). Using molecular analysis, these

authors identified genotype G1, G2 and G3 of Eg sensu stricto (s. s.) in 87% of

selected samples from cattle, sheep and goats. Overall, a higher number of

infections due to the genotype G1 (96%) was observed than the G3 (3%) and G2

(1%) genotypes, with similar rates of infection in cattle and sheep. The genotype G1

of Eg s.s. is the most widespread genotype.

The survey on knowledge, attitudes and practices with regards to the presence,

transmission factors, impact, and control of CE (El Berbri et al., 2015a) showed that

of 543 people interviewed, only 50% have heard of the disease, and of those, only

21% are aware of the dog’s role in disease transmission. These results showed that

health education is of the utmost importance to successfully roll out a CE control

program in the Sidi Kacem region. Health education was an important component of

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our CE control program, and results of an integrated health messaging intervention

for multiple neglected zoonoses have already been published (Ducrotoy et al., 2015).

Usually, diagnosis of Echinococcus spp. infection in dogs requires evidence of

Echinococcus spp eggs in faeces, or detection of adult worms in the intestinal tract of

dogs during necropsies. Microscopic detection of eggs in faecal samples has low

sensitivity as eggs of Echinococcus spp. cannot be differentiated from those of

Taenia spp. (Barnes et al., 2012; Deplazes et al., 2003). Coproantigen testing is a

useful procedure for population studies providing the limitations of these tests - low

sensitivity in low worm burdens, potential cross-reactivity with other helminths

depending on strain of Eg - are taken into consideration. The gold standard is the

sedimentation and counting technique performed at necropsy on intestinal material

and has an estimated sensitivity of 96-100% (Barnes et al., 2012), but it requires

euthanasia of dogs. Arecoline hydrobromide (AH) purgation is an alternative non-

invasive method for direct parasite detection. Despite its low sensitivity (39%) for Eg

diagnosis and propensity to cause adverse reactions in dogs (Schantz, 1997)

Ziadinov et al., 2008), it has a specificity of 100% and enables the parasite to remain

intact.

The objectives of this study were to estimate the prevalence of Eg in owned dogs in

Sidi Kacem Province using AH purgation and to analyse risk factors for infection.

2. Materials and methods 2.1. Study area Sidi Kacem is located in the northwest of Morocco (Figure 1). It has a total area of

about 3094.33 km2 and is divided into 5 municipalities or urban districts and 24 rural

communes (ONSSA, 2010). In 2012, the human population was nearly 489,400

inhabitants representing 1.6% of the national population. More than 70% of the

population live in rural areas, and the rate of poverty is estimated at 21.4% compared

with 14.2% at the level of the Kingdom of Morocco (MAPM, 2010).

The climate is of a sub-humid Mediterranean type with oceanic influence and an

annual rainfall of 560 mm. The cold, rainy and humid season extends from October

to May and the coldest month is January with an average temperature of 4.5°C. This

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period is followed by the hot and dry season which extends from June to September

and the hottest month of the year is usually August with an average temperature of

36.5°C. The topography of the Province is characterized by the plain to the West

(altitude 112 m), hills in the centre (altitude 200-300 m) and mountains to the East

and Northeast (altitude 443 m).

Agriculture plays an important role, because of the strategic location of Sidi Kacem

close to the major towns “Fez, Meknes, Kenitra, Rabat”. Livestock populations are

estimated at 120,000 cattle, 380,000 sheep and 21,000 goats. Citrus crops and

commercial dairy farming are dominant in the irrigated plains and lower hills. Grain

farming and pastoralism are dominant in the hills and higher altitude areas. The

province has 5 municipal or urban slaughterhouses and 5 rural slaughterhouses, with

slaughter generally taking place once a week during the souk or market day.

Two dog populations can be identified: i) owned dogs (including sheep and cattle

dogs), which despite being owned are free ranging, and ii) stray or un-owned dogs,

with a population estimated at 18,520 and 2,260 respectively. It is interesting to note

that there are wild boars and foxes in the mountainous and hilly zones of the

province.

Figure 1. Geographical location of the province of Sidi Kacem (Morocco).

2.2. Research design

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Dog sampling was conducted in 23 rural communes and in all of the 5 municipalities.

For each of the rural communes and municipalities, one to two douars (villages) were

randomly selected from the list of villages in each commune obtained from the Caïd

(an appointed commune government official). At village level, 5 to 20 households

were randomly selected from lists of households in each village obtained from the

Cheikhs (locally appointed village heads).

The inclusion criteria established by Gemmell (1973) were used in this study. All

dogs two months older and younger than 10 years, except pregnant females, were

selected to undergo AH purgation. For households owning more than one dog, only

one dog was randomly selected for purgation. For each dog sampled, data on age,

sex, and village/commune of origin was recorded. Age was estimated according to

dentition using the Luquet (1971) criteria if the owner did not know the age of the

dog. Dogs sampled were further categorised into three groups: 1) dogs owned by

households from the 5 municipalities with urban slaughterhouses (urban dogs with

potential access to urban abattoir); 2) dogs owned by households from the 5 rural

communes with rural slaughterhouses (rural dogs with potential access to rural

abattoir); 3) dogs owned by households from the 18 rural communes without

abattoirs (rural dogs with limited or no access to rural abattoir, due to distance of

nearest abattoir).

Visits were undertaken on a regular basis (for 3 to 4 consecutive days at 3 monthly

intervals) from April 2010 to March 2012 and dogs were examined using AH

purgation to observe the presence or absence of Eg in faeces. Arecoline

hydrobromide (TCI Europ N.V., Belgium) purgation was carried out according to the

protocol described by OIE (2012). As AH has no ovicidal properties resulting in

contamination of the environment and increasing health risks to persons handling

infected dogs or faeces contaminated with Eg eggs, health and safety guidelines of

the OIE (2012) were strictly adhered to. Personnel wore protective clothing, footwear

and disposable gloves. Clothing was boil washed after use and boots were

disinfected in 10% hypochlorite solution.

As recommended by Gemmell (1973), purgation was considered to be successful if

liquid or semi-liquid faeces containing mucus-like material were passed 20 to 30

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minutes after AH administration. In the event of failure of the first purgation, a second

administration at a dosage of 2 mg/kg was performed. Faeces and mucus were

collected and checked for presence of parasite over a dark plate, diluting the material

with water.

Parasites were shown to dog owners, who were simultaneously briefed on the mode

of transmission and pathological effects of CE both in humans and farm animals.

Faeces and mucus were then placed in sealed vials and preserved in 70% ethanol

for laboratory analysis. Because dogs may continue to pass eggs, proglottids and

worms after purgation, owners were informed of the need (1) for dogs to remain

tethered for 3 hours after purgation, (2) to incinerate faeces, mucus and the general

area where dogs had defecated by subjecting to high heat for a minimum of 5

minutes with a blow torch. A member of the research team always stayed back to

ensure this was undertaken.

Further laboratory investigations were undertaken using the flotation technique as

described by Le Riche and Jorgensen (1971). This method detects worms or

segments of helminths of the Taeniidae family. The worms were then identified

according to Soulsby (1982) and Kassai (1999).

2.3 Statistical analysis WinPepi® v11.42 (Abramson, 2013a, b) software was used for the statistical analysis

of risk factors. Data were categorised according to age and sex of dog, whether the

dog was from a rural (commune) versus urban (municipality) area and

presence/absence of rural or urban abattoir in commune or municipality respectively.

Comparison of proportions of infected dogs across variables was firstly undertaken

by calculating 95% confidence intervals (CI) using Fisher’s exact method. Overlap of

confidence intervals means that no conclusion can be drawn on a difference in

infection rate between different categories. Odds ratios (with Fisher’s exact 95% CI)

and Pearson’s chi-square were also calculated.

2.4 Study approvalApproval for the study went through the official channels of the Institut Agronomique

et Veterinaire Hassan II and authorisation was granted by the Office National de

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Securite Saniture des produits Alimentaires (ONSSA, subsidiary of Ministry of

Agriculture). Consent for the study was then sought from the Governor of Sidi

Kacem, and the Caid (appointed local authority representative of the ‘cercle’, which

consists of multiple communes) of each individual commune and the Chaïkh (locally

appointed head of multiple villages) and/or Mokaddem (locally appointed head of a

single village) from each village selected. Once approval had been obtained, the

Chaïkh or Mokaddem would accompany the research team into the community and

read out the text on the consent form for participation in the study, and only dog

owners that had sufficient understanding of the study specifics and had given oral

consent were permitted to participate in the study.

3. ResultsPurging efficacy, prevalence of infection and risk factor analysis:A total of 273 dogs (184 males and 89 females) were AH tested (Table 1). Arecoline

hydrobromide purgation was effective in a total of 224 (82.1%) dogs; 196 after the

first and 28 after the second purgation. Of the 224 dogs successfully purged, 141

were from the 18 rural communes without abattoirs, 51 were from the 5 rural

communes with abattoirs and 32 from the 5 municipalities with urban abattoirs (Table

1).

Table 1. Number of rural and urban dogs tested and successfully purged

TestedTotal

PurgedTotal

Purged (%)M F M F

Rural dogs

From 18 rural districts with no

abattoir115 56 171 95 46 141 82.5

From 5 rural districts with rural

abattoir41 20 61 34 17 51 83.6

(Subtotal 1) 156 76 232 129 63 192 82.8

Urban dogs

From 5 municipalities with urban

abattoir

(Subtotal 2)

28 13 41 22 10 32 78.0

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Total (subtotal 1 + subtotal 2) 184 89 273 151 73 224 82.1

M- male; F-female.

3.2. Prevalence of infection and risk factor analysisOnly dogs successfully purged were considered for calculating prevalence of Eg

infection. The overall prevalence was 35.3% (95% CI 29.0-41.9%), with 79 out of 224

dogs found to be positive. No difference was observed between prevalence of Eg

across different age or sex groups (p = 0.980 and p = 0.824 respectively).

Prevalence was significantly higher (p<0.05) in rural dogs (38.0%, 95% CI 31.1-

45.3%) than in urban dogs owned by households located in the municipalities

(18.8%, 95% CI 7.2-36.4%) (Table 2).

Prevalence was significantly higher (p < 0.01) in rural dogs from communes with a

slaughterhouse (62.7%, 95% CI 48.1-75.9%) than in rural dogs from rural communes

without a slaughterhouse (29.1%, 95% CI 21.7-37.2%) (Table 2). Moreover,

prevalence was significantly higher (p< 0.01) in dogs from rural communes with a

slaughterhouse than in dogs from municipalities with rural slaughterhouses (18.8 %,

95% CI 7.2-36.4%) (Table 2).

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Table 2. Prevalence of E. granulosus infection in dogs and risk factor analysis

VariableNo. purged

No. positive

% positive 95% CI1 Comparison OR (95% CI)1 Chi-square (DF, p)2

AGE OF DOG

3-12 months (A) 62 21 33.9 22.3-47.0 A & B 0.93 (0.45-1.93) 0.043 (1, 0.836)

2-4 years (B) 93 33 35.5 25.8-46.1 A & C 0.90 (0.41-1.97) 0.080 (1, 0.777)

5-9 years (C) 69 25 36.2 24.5-48.7 B & C 0.97 (0.48-1.96) 0.010 (1, 0.922)

A, B & C 0.040 (2, 0.980)

SEX OF DOG

Male 151 54 35.8 28.1-44.0 1.07 (0.57-2.02) 0.49 (1, 0.824)

Female 73 25 34.2 23.5-46.3

LOCATION OF HOUSEHOLD

Rural (commune) 192 73 38.0 31.1-45.3 2.66 (1.00-8.25) 4.462 (1, 0.035)*

Urban (municipality) 32 6 18.8 7.2-36.4

LOCATION OF HOUSEHOLD/PRESENCE OF ABATTOIR

Commune with rural abattoir (D) 51 32 62.7 48.1-75.9 D & E 4.11 (1.99-8.56) 18.015 (1, <0.001)**

Commune without rural abattoir (E) 141 41 29.1 21.7-37.2 D & F 7.30 (2.33-25.12) 15.332 (1, <0.001)**

Municipality with urban abattoir (F) 32 6 18.8 7.2-36.4 E & F 1.78 (0.65-5.66) 1.406 (1, 0.236)

D, E & F NA 23.057 (2, <0.001)**1 Fisher’s exact 95% CI; 2 Pearson’s chi-square; *statistical significance at 5% level; **statistical significance at 1% level.

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4. Discussion This is the first report on Eg in dogs in Sidi Kacem Province, Morocco. High incidence

of surgical cases in humans, and data reported by El Berbri et al. (2015b) on CE

infection in livestock, have previously confirmed the presence of the infection in this

Province. These data indicated that the life cycle of Eg is being completed in the final

host, however Eg prevalence in the dog population of this Province was unknown

until this study. Determining the prevalence of infection in dogs is thought to be the

best indicator of the degree of transmission of Eg in a region as reported by Craig et

al. (2003).

Previous surveys to assess the knowledge, attitudes and practices of public health

significance to human and animal CE in the same Province (El Berbri et al., 2015a),

have shown that health education is an essential element of control campaigns

targeting CE in this region. Masala and Parodi (2004) reported that ‘sight’ accounts

for 87% of the learning process, followed by ‘hearing’ (7%), demonstrating the

potential for high impact of showing dog owners the parasite in their dogs’ faeces as

part of an education strategy. The technique of arecoline purgation used in this study,

which expels worms, was found to be visually powerful and helped dog owners

understand the mode of transmission to humans and animals. This technique

provides a significant contribution to health education with regards to improving the

knowledge of dog owners (Ducrotoy et al., 2015).

Purgation efficacy using AH was found to be 82.1% after the second purgation, which

is similar to the 76.9%, 80% and 85% reported by Lahmar et al. (2007), Gemmel and

Lawson (1986) and Schantz (1997) respectively. Schantz (1997) highlighted the

disadvantages of AH purgation of dogs and reported that only 68% of the dogs

purged after the first arecoline dose and 12% of dogs failed to purge after a second

dose. Moreover, Economides and Christofi (2000) reported that this test should not

be used on pregnant bitches and young puppies, and occasionally fatalities have

been reported. According to Gemmel (1973), Trejos et al. (1975) and Eckert et al.

(2001) AH purgation can be used to obtain baseline data on the Eg prevalence in

dogs and, in association with studies on prevalence in intermediate hosts in the same

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region, as is the case in this study, AH purgation can provide valuable

epidemiological information on CE to inform control programmes (Heath et al., 2006).

The high overall prevalence of 35.3% (95% CI 29.0-41.9%) for Eg obtained in this

study indicates a high risk for humans and ruminant intermediate hosts in Sidi Kacem

Province. Indeed, a retrospective study (2003-2010) of human CE in the Province of

Sidi Kacem, showed a high incidence of this disease in the region, with an annual

average incidence of 6.5 surgical cases per 100,000 inhabitants compared to the

national average of 5.1 recorded for 2003-2010 (DELM, 2012). Data are also

available for the same period (2009-2013) on infection rate for ruminants in the

Province as part of study undertaken in the 10 Sidi Kacem abattoirs: 42.9% of cattle

and 11.0% of sheep in the province harbour hydatid cysts, and these cysts had a

fertility rate of 54.9% and 50.3% in sheep and cattle, respectively (El Berbri et al.,

2015b). Motassian et al. (1977) reported that an average prevalence of 20% or more

of CE in one or more species of definitive or intermediate host is regarded as severe

infection and corresponds to endemicity of disease.

Although the Eg prevalence found in this study is higher than that of 22.8% (n=57)

reported by Pandey et al. (1987) in the region of Rabat, it is lower than that of 58.8%

(95% CI 46.2% - 70.6%) in two regions in the North and of 55.4% (95% CI 44.1-

66.3%) in two regions in the South of Morocco (Azlaf et al., 2007) (Azlaf et al., 2007).

This may be linked to the urban setting of Rabat, which has better abattoir

infrastructure as compared to the other two regions, which are more rural in

character and have rural slaughterhouses (see below), although differences in period

of study, sample size and diagnostic methods could also account for these

differences.

A number of factors including sex, age and access of dogs to uncooked and infected

offal, community knowledge, attitudes and practices related to CE have previously

been found to influence the frequency of Eg infection in dogs in Morocco (Dakkak,

2010). The results of this study showed that there was no significant difference in the

Eg prevalence between male and female dogs. This is in agreement with the findings

of Otero-Abad and Torgerson (2013) who reported in a recent systematic review of

the epidemiology of echinococcosis in domestic and wild animals that only one study

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in Urugay conducted by Parada et al. (1995) found sex to be a risk factor. The

equivalent prevalence in both male and female dogs is probably due to similarities in

management of both sexes. In Morocco both male and female dogs are encouraged

to roam freely and are fed offal (El Berbri et al., 2015a).

Higher Eg prevalence is commonly reported in dogs less than two years old (Acosta-

Jamett et al., 2010; Sharifi and Zia-Ali, 1996). Dogs older than 5 years showed lower

coproantigen positivity, and even lower parasite abundance, compared to younger

groups (Buishi et al., 2005; Inangolet et al., 2010). In the present study age

dependent differences in prevalence were not found to be statistically significant.

This is similar to the results reported by Azlaf et al. (2007) in four other regions in

Morocco and by El Shazly et al. (2007) in Egypt, Eslami and Hosseini (1998) Maleky

and Moradkhan (2000) in Iran, and Adediran et al. (2014) in Nigeria. The differences

in age profile of infection was thought by Azlaf et al. (2007) to be dependent on the

equilibrium between infection pressure in terms of prevalence rate of the infection

and abundance of the parasite in dogs and acquisition of immunity, which occurs at

different ages depending on the infection pressure in an area.

The only factors positively associated with infection were dog population type (urban

versus rural) and presence or absence of rural or urban slaughterhouse. This study

showed that dogs in rural communities were at greater risk of infection than dogs in

municipalities or urban areas. This corroborates the results reported in neighbouring

countries by Benchikh-Elfegoun et al. (2008) and Bentounsi et al. (2009) in Algeria,

Lahmar et al. (2001) in Tunisia, Buishi et al. (2005) in Lybia and El Shazly et al.

(2007) in Egypt.

Moreover, for rural communes, Eg prevalence was found to be higher in those with

slaughterhouses (62.7%, 95% CI 48.1-75.9%) than in those without (29.1%, 95% CI

21.7-37.2%). Dogs inhabiting the five rural communities with slaughterhouses were

found to have a higher prevalence than those inhabiting municipalities with urban

slaughterhouses (18.8%, 7.2-36.4%), which suggests that access to rural

slaughterhouses is a major source of transmission.

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These results can be explained by the lower awareness of transmission risks, higher

engagement in risky behaviour in rural areas and the poorer infrastructure and

practices of rural versus urban slaughterhouses in this region (Bardosh et al., 2016 -

in press; El Berbri et al., 2015a). Indeed the five rural slaughterhouses were

observed to have very low levels of hygiene and poor infrastructure. Hydatid cysts

were frequently discarded on the floor, then removed together with other livestock

waste using a pitchfork and wheelbarrow and dumped on the ground outside the

slaughterhouse. This is in contrast to that for the five municipal slaughterhouses,

where hydatid cysts were removed together with other livestock waste and then

placed in waste open bins to which dogs have easy access. (although these were

later brought to the municipal garbage dump to which dogs have easy access, hence

transmission although lower can still occur in this setting).

The main risk factors for Eg infection in dogs, as identified through a questionnaire

survey undertaken in Sidi Kacem by El Berbri et al. (2015a), were accessibility of

dogs to infected offal (through traditional home slaughter and inadequate disposal of

condemned organs at slaughterhouses), uncontrolled roaming of owned and stray

dogs (and access to livestock rearing areas and carcasses) and low socioeconomic

and education status of dog owners, leading to poor knowledge of echinococcosis

and engagement in risky practices such as feeding of infected organs to pets. These

findings are in agreement with the results of this study.

The association between inappropriate disposal of viscera and a high risk

of Eg infection in dog was also reported in other studies performed in Morocco

(Pandey et al., 1987) and in neighbouring countries including Algeria (Benchikh-

Elfegoun et al., 2008; Bentounsi et al., 2009), Tunisia (Aoun et al., 2009), Lybia

(Buishi et al., 2005), and Egypt (El Shazly et al., 2007; Mazyad et al., 2007).

Even though this study has confirmed the importance of the dog-livestock cycle in

this setting, further studies are required to investigate sylvatic cycles and their

potential interaction with domestic cycles in Morocco (Barnes et al., 2012). The

presence of wild boars and foxes in Sidi Kacem Province raises questions about their

potential role as intermediate and definitive hosts respectively in the life cycle of the

parasite.

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5. ConclusionOne of the most important factors found to influence the prevalence of Eg infection in

dogs in this Province of Northern Morocco was presence of rural slaughterhouses,

promoting access of dogs to infected offal through poor infrastructure and hygiene

practices.

The human population is highly exposed to CE because, as reported by the same

team (Ducrotoy et al., 2015) in the same area, in addition to high Eg prevalence in

dogs, only 50.3% respondents are aware of the disease, and only 21.3% recognise

the dog's role in transmission to humans and domestic animals.

Arecoline hydrobromide purgation of dogs enables determination of the prevalence of

Eg infection in dogs which is considered to be the single most reliable indicator of the

potential risk of transmission of CE to humans and animals in a region.

Because whole worms passed by treated dogs can be shown to dog owners, it is

interesting to use AH purgation as part of a health education, which is an important

component of CE control program.

Finally, dog and ruminant CE prevalence data combined from the same region

generates a more complete epidemiological picture to inform the implementation of a

control program (prioritisation of control measures in hot spots, for example). The

baseline data generated can also be subsequently used to evaluate the impact of

control strategies.

AcknowledgementsThis research was supported by European Union Seventh Framework Program

(FP7/2007-2013) under grant agreement nº 221948, ICONZ (Integrated control of

Neglected Zoonoses). The contents of this publication are the sole responsibility of

the authors and do not necessarily reflect the views of the European Commission.

We would like to thank the ONSSA, the local authorities of Sidi Kacem Province, the

local veterinarians and veterinary technicians and the farmers for their help in

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carrying out the fieldwork. We are grateful to Professor Ian Maudlin for a critical

reading of the manuscript.

Conflict of interestThe authors declare that they have no financial and personal relationships with other

people or organizations that can inappropriately influence their work and there are no

professional or other personal interests of any nature or kind in any product, service,

and/or company that could be construed as influencing the position presented in, or

the review of, this paper.

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