# Poor efficacy of the most commonly used anthelmintics in sport horse nematodes in Morocco in relation to resistance

H. Zouiten, B. Berrag, M. Oukessou, A. Sadak, Jacques J. Cabaret

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H. Zouiten, B. Berrag, M. Oukessou, A. Sadak, Jacques J. Cabaret. Poor efficacy of the most commonly used anthelmintics in sport horse nematodes in Morocco in relation to resistance. Parasite, 2005, 12 (4), pp.347-351. 10.1051/parasite/2005124347. hal-02680333

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# POOR EFFICACY OF THE MOST COMMONLY USED ANTHELMINTICS IN SPORT HORSE NEMATODES IN MOROCCO IN RELATION TO RESISTANCE

ZOUITEN H.*, BERRAG B.**, OUKESSOU M.***, SADAK A.* & CABARET J.****

**Summary:**

Sport and leisure horses in Morocco are treated with several anthelmintics, organophosphates (dichlorvos), benzimidazoles (mostly thiabendazole) or tetrahydropyrimidines (mostly pyrantel pamoate) against nematodes. We studied three horse stables in Rabat, one in Meknes and one in Bouznika. Two of the Rabat and Bouznika stables had introduced a large number of horses from countries (Argentina or Europe) where resistance to benzimidazoles is frequent, whereas the Meknes stud farm remained without foreign introduction. The number of treatments was not very frequent (twice a year in adult horses) but the same anthelmintics were used repeatedly. No resistance to dichlorvos was detected whereas benzimidazole and pyrantel pamoate resistances were detected for the first time in African horses, outside South Africa.

**KEY WORDS:** anthelmintic, horse, nematode, Morocco, resistance.

**Résumé:** EFFICACITÉ RÉDUTTE DES ANTHELMINTHIQUES LES PLUS UTILISÉS CHEZ LE CHEVAL AU MAROC EN RELATION AVEC LA RÉSISTANCE

Les chevaux de sport et de loisirs au Maroc sont traités pour les infections par les nématodes avec plusieurs anthelminthiques, des organophosphorés (dichlorvos), des benzimidazoles (principalement le thiabendazole) ou des tétrahydropyrimidines (principalement le pamoate de pyrantel). Nous avons étudié trois écuries à Rabat, une à Meknes et une autre à Bouznika. Deux des écuries de Rabat et celle de Bouznika ont introduit des chevaux en grand nombre d'Argentine ou d'Europe, qui sont des régions avec des résistances très fréquentes, alors que le site de Meknes restait sans introduction. Le nombre de traitements n'était pas très élevé (deux par an chez les adultes), mais les mêmes molécules ont été utilisées de manière répétitive au sein de chaque écurie. Aucune résistance au dichlorvos n'a été enregistrée, mais par contre des résistances aux benzimidazoles ou au pamoate de pyrantel ont été mises en évidence pour la première fois chez des chevaux africains (hors Afrique du Sud).

**MOTS CLÉS:** anthelminthique, cheval, nématode, Maroc, résistance.

## INTRODUCTION

Horses are important in Morocco, as a working or a leisure animal (360.000 heads in 2001). The internal parasitic diseases are frequent in working donkeys and horses of Morocco (Pandey & Dakkak, 1979; Cabaret & Pandey 1980; Pandey & Cabaret, 1993). Horses harbour small and large strongyles, and other nematodes such as *Habronema* sp. or *Trichostrongylus axei*, and insect larvae, *Gasterophilus* spp. (Ouhelli *et al.*, 1979). In Morocco, small strongyles are considered as playing an important role in severe diarrhoea and colitis (Berrag & El Kohen, 1999). Large strongyles were a major cause of diseases in horses and frequent treatments programs were implemented in

order to control infection; it resulted in an increase of small strongyles which were considered as much less pathogenic than large strongyles (Kaplan, 2002). The first reports of thiabendazole resistance in the cyathostomes (= small strongyles) were recorded by Drudge & Lyons, 1965; later, it has been extensively reported in many countries (Lyons *et al.*, 1999). Resistance to pyrantel was reported only in recent years although it has been used since the 1970's, and mostly in places were daily feeding with pyrantel is practised (Kaplan, 2002). Resistance to organophosphate is not documented in horse nematodes. The majority of resistance studies are based on the faecal egg reduction test (FECRT) and Bauer *et al.* (1986) stated that a reduction of less than 80 % after treatment was indicative of resistance. Resistance is then a common feature in horse small strongyles in South Africa (Matthee *et al.*, 2000), USA (Drudge & Elam, 1961; Wood *et al.*, 1998), Brazil (Pereira *et al.*, 1991), Denmark (Bjorn *et al.*, 1991), Australia (Waller, 1993), Belgium (Geerts, 1995) and Ukraine (Borgsteede *et al.*, 1996) among others.

The sport and leisure horses in Morocco benefit from anthelmintic treatments, some of them are imported from countries where prevalence of resistance is high,

<footnote>* Faculté des Sciences, Département de Biologie, Avenue Ibn Battouta, BP 1014, Rabat, Maroc.</footnote>

<footnote>** Institut Agronomique et Vétérinaire Hassan II, Département de Parasitologie, BP 6202, Rabat-Instituts, Rabat, Maroc.</footnote>

<footnote>*** Institut Agronomique et Vétérinaire Hassan II, Département de Physiologie et Thérapeutique, BP 6202, Rabat-Instituts, Rabat, Maroc.</footnote>

<footnote>**** INRA, Bio-Agresseurs Santé Environnement, 37380 Nouzilly France.</footnote>

<footnote>Correspondence: jacques.cabaret@tours.inra.fr</footnote>
<table><caption>Table I. – Characteristics of horse stables studied in Morocco.</caption><thead><tr><th>Site</th><th>Breeds and origins</th><th>Activity</th><th>Previous use of the anthelmintics in the last ten years</th><th>Tested anthelmintics for efficacy in present study</th></tr></thead><tbody><tr><td>Raf-Unit 1</td><td>English, Argentina, Arab, and Barb thoroughbreds and their crosses (introduction from Europe and Argentina in 1996 and before)</td><td>Polo, Escort, Fantasia, Racing competition</td><td>Dichlorvos 53 %<br>Thiabendazole 29 %<br>Oxibendazole 18 %</td><td>Dichlorvos</td></tr><tr><td>Raf-Unit 2</td><td>Argentina, Holland, Barb thoroughbreds and their crosses (introduction from Europe and Argentina in 1996 and before)</td><td>Polo, Escort, Fantasia, Racing competition</td><td>Thiabendazole 68 %<br>Piperazine 11 %<br>Dichlorvos 11 %<br>Oxibendazole 8 %<br>Mebendazole 2 %</td><td>Thiabendazole<br>Dichlorvos</td></tr><tr><td>El Harka</td><td>Arab-Barb, Arab, English thoroughbreds</td><td>Riding school</td><td>Pyrantel pamoate 60 %<br>Oxibendazole 40 %</td><td>Pyrantel pamoate</td></tr><tr><td>Bouznika<br>Stud-farm</td><td>English and Arab thoroughbreds (massive importation from Europe in 1994)</td><td>Exchange of studs between stables</td><td>Pyrantel pamoate 50 %<br>Dichlorvos 40 %<br>Oxibendazole 10 %</td><td>Pyrantel pamoate</td></tr><tr><td>Meknes<br>Stud-farm</td><td>Barb and Arab thoroughbred and their crosses (no importation from other countries)</td><td>Exchange of studs between stables</td><td>Pyrantel pamoate 100 %</td><td>Pyrantel pamoate</td></tr></tbody></table>

and they may distribute resistance genes along their movements from one racing place, polo competition, or through mouvements of studs. According to pro and cons for acquiring resistance (Silvestre et al., 2002) these horses are good candidates for harbouring resistant cyasthostomes. The same family of anthelmintics are apparently repeatedly used, which would be a major pro for selection of resistance. We recorded the main anthelmintics used in different leisure or stud horse farms from Morocco and we checked their efficacy using faecal egg counts or in vitro tests and tentatively deduced the resistance status of nematode communities.

## MATERIALS AND METHODS

Several sites in Morocco were investigated in Rabat (Raf-1, Raf-2, El Harka), one in Meknes and one in Bouznika (Table I) from 1999 to 2002. Only adult horses were studied.

The efficacy was first evaluated on faecal egg counts (FEC) using McMaster technique (one egg seen = 50 eggs per gram or EPG, Manual of veterinary parasitology laboratory techniques, 1986) and the most used anthelmintic(s) during the last 10 years was (were) tested (Table I). The decrease of the FEC (FECRT faecal egg count reduction test in faeces) was evaluated on day of treatment (arithmetic average T1) and 10-12 days after (arithmetic average T2). The reduction was calculated as ((T1-T2)/T1) × 100. According to Sangster, 1996 or Bauer et al., 1986, resistance is suspected when FECRT < 80 % whereas Coles et al., 1992 propose FECRT < 90 %. The faecal individual reduction

(Cabaret & Berrag, 2004) and bootstrap confidence interval were also calculated using the Resivers program (Cabaret et al., 2001). The evaluation of resistance was also done on egg development for benzimidazole (using thiabendazole at various concentrations: Coles et al., 1992) and motility of third stage larvae for pyrantel pamoate based on a similar test provided by Coles et al., 1992, replacing development by motility and thiabendazole by pyrantel pamoate. The evaluation of confidence interval at 95 % of the LD50 (lethal dose on eggs) or ID50 (immobilizing dose of 50 % of larvae) was performed with the probit program (Raymond, 1985).

## RESULTS

The number of treatments was twice a year for adults and three times a year for yearlings in all the sites. Nematodes were mostly cyasthostomes (more than 80 % of larvae) as evaluated in Raf-2.

<table><thead><tr><th>Sites</th><th>No of horses</th><th>Eggs per gram D0</th><th>Eggs per gram D10</th><th>FECR (%)</th></tr></thead><tbody><tr><td>Raf-Unit 1</td><td>30</td><td>945*<br>(0-6,150)**</td><td>5<br>(0-150)</td><td>99.5</td></tr><tr><td>Raf-Unit 2</td><td>8</td><td>970<br>(1,350-6,050)</td><td>0</td><td>100</td></tr></tbody></table>

<caption>Table II. – Dichlorvos faecal egg count reduction test (FECR 10 days after treatment) in horses from two sites (33 mg/kg body weight) (1999).</caption>

<footnote>* arithmetic average and ** range.</footnote>
### Efficacy of dichlorvos (Table II)

The efficacy of dichlorvos (Equigard®) remained high, and no resistance was evidenced in the two horse stables we investigated.

### Efficacy of pyrantel pamoate (Table III)

The efficacy of pyrantel pamoate (Strongid®) was low (69 or 72 reduction of FEC) and the in vitro test on

motility of larvae (the values were three times higher than in a susceptible community) corroborated that the Meknes stud farm harboured a resistant worm community.

### Efficacy of thiabendazole (Tables IV and V)

The efficacy thiabendazole (Thibenzole®) was low (32-53 % on average value) in the five stables of Raf-2 as

<table><thead><tr><th>Sites</th><th>No of horses</th><th>Eggs per gram D0</th><th>Eggs per gram D10</th><th>FECR (%, average, and individual based estimations and 95 % confidence interval**)<br>(paralysis dosis µg/mL***)</th></tr></thead><tbody><tr><td>Bouznika</td><td>6</td><td>175*<br>(50-500)**</td><td>8<br>(0-50)</td><td>95* (97: 94-99)**<br>(Not done)</td></tr><tr><td>Meknes</td><td>10</td><td>970<br>(300-3,200)</td><td>300<br>(0-950)</td><td>69 (72: 62-82)<br>(0.95: 0.48-2.02)</td></tr><tr><td>Rabat (El Harka)</td><td>10</td><td>725<br>(300-2,650)</td><td>60<br>(0-150)</td><td>92 (88: 78-98)<br>(0.34: 0.25-0.42)</td></tr></tbody></table>

<table><caption>Table III. – Faecal egg count reduction test (FECR 10 days after treatment) with pyrantel pamoate in horses from three sites (6.6 mg/kg body weight).</caption><thead><tr><th>Stable</th><th>Eggs per gram D0</th><th>Eggs per gram D12</th><th>FECR (%, average or individually based-with 95 % confidence interval)</th></tr></thead><tbody><tr><td>N° 1 (n = 20)</td><td>1,952*</td><td>1,140</td><td>42</td></tr><tr><td>Argentina thoroughbreds</td><td>(50-5,500)**</td><td>(0-3,850)</td><td>37 (19-55)</td></tr><tr><td>N° 2 (n = 8)</td><td>594</td><td>281</td><td>53</td></tr><tr><td>Mostly English thoroughbreds and Anglo-arab crosses</td><td>(0-1,750)</td><td>(0-900)</td><td>64 (45-83)</td></tr><tr><td>N° 3 (n = 25)</td><td>2393</td><td>1,412</td><td>41 %</td></tr><tr><td>European thoroughbreds</td><td>(500-8,850)</td><td>(0-6,950)</td><td>22 (9-41)</td></tr><tr><td>N° 4 (n = 20)</td><td>2,640</td><td>1,808</td><td>32 %</td></tr><tr><td>Arab-Barb crosses</td><td>(500-8,150)</td><td>(450-4,900)</td><td>26 (13-37)</td></tr><tr><td>N° 5 (n = 26)</td><td>2,376</td><td>1,162</td><td>51 %</td></tr><tr><td>Argentina thoroughbreds</td><td>(550-4,900)</td><td>(150-3,850)</td><td>42 (22-59)</td></tr></tbody></table>

<table><caption>Table IV. – Faecal egg count reduction test after treatment (FECR based on D12, 12 days) in five stables of Raf-2 after thiabendazole treatment using a unique dose of 18.75 g per horse which corresponded to 26-55 mg/kg body weight depending on horse (1999).</caption><thead><tr><th>Sites</th><th>No of horses</th><th>Eggs per gram D0</th><th>Eggs per gram D10</th><th>FECR (%, average or individually based-with 95 % confidence interval) (%)</th></tr></thead><tbody><tr><td>Raf-Unit 2<br>50 mg/kg, 1999</td><td>10</td><td>2,340*<br>(600-10,250)**</td><td>1,965<br>(450-9,500)</td><td>16<br>17 (10-41)</td></tr><tr><td>Raf-Unit 2<br>100 mg/kg, 1999</td><td>10</td><td>2,815<br>(900-8,150)</td><td>1,430<br>(0-4,150)</td><td>49<br>43 (20-65)</td></tr><tr><td>Raf-Unit 2<br>100 mg/kg, 2002</td><td>10</td><td>3,780<br>(300-8,700)</td><td>1,785<br>(150-440)</td><td>53<br>52 (34-68)</td></tr></tbody></table>

<caption>Table V. – Faecal egg count reduction test (FECR) after treatment with thiabendazole in horses from two sites (50 mg-100 mg/kg body weight) (1999-2002).</caption>

<footnote>* arithmetic average and ** range.</footnote>

<footnote>* arithmetic average and ** range.</footnote>

<footnote>* arithmetic average and ** range.</footnote>
the practice is to give the same amount of drug to horses of diverse weights, which correspond to 26-55 mg dosage/kg body weight. The low efficacy was either due to low dosage or resistance. The average reductions at 50 and 100 mg/kg body weight were indicative of resistance. The lethal dose that inhibited the egg development *in vitro* was high in Raf-2 in 1999: 0.42 µg/mL compared to the 0.06 µg/mL of the susceptible El Harka strongyle community.

## DISCUSSION

The horse stables we choose were often dedicated to a unique or nearly unique scheme of anthelmintic treatments for the last ten years. Lack of efficacy was then expected due to repeated use of the same anthelminthic and to the repeated introductions of new horses from other countries (Europe or Argentina) where resistance to benzimidazoles is a very common feature. The helminth control practices are not that much different from Europe (O'Meara & Mulcahy, 2002 in Ireland); the worming interval is somewhat larger (twice a year which represents 28 % of parasite control in Ireland) and the drug rotation is lower (rapid-59 % or annual-13 % of horse stables) in Morocco conditions. The intensity of treatments is also lower than that recorded in South Africa (Matthee et al., 2002), five times per year in adult horses; an average of 3.4 different drugs were used annually which is not the case in Morocco (one in most cases or two different drugs per year). Morocco is then a candidate for resistance in stud or leisure horses. The extent of resistance in horse nematodes throughout the world is recognized, particularly for benzimidazoles (Conder & Campbell, 1995; Kaplan, 2002) which were used from 1960's. Resistance to benzimidazoles is common in horses (Dorny et al., 2000; Fisher et al., 1992; Varady et al., 2000; Woods et al., 1998, and see review by Kaplan, 2002) as it has been used for decades (Uhlinger, 1992). Resistance to benzimidazole in horses cyathostoms is then recorded for the first time in Morocco and Africa (South Africa excluded), which was expected when considering pro and cons for building up of resistance. It might be a case of introduced resistance if we consider the introductions of horses harbouring resistant worms from Argentina (Tolosa et al., 1999) or Europe (see Kaplan for review, 2002). The selective pressure remained low but permanent (the Raf-1 or Raf-2 cases) and it probably helped the diffusion of introduced resistant genes in nematodes. The introduction of resistant worms as a major factor is the most probable hypothesis.

Although pyrantel pamoate has been used since the 1970's, it is only in recent years that reports of resistance are available in United States, Norway and Denmark (in Kaplan, 2002) or Italy (Genchi et al., 1992).

The first record of resistance to pyrantel pamoate in Morocco is acknowledged, in a situation where intensive use of the drug and limited introduction of infected horses is the rule. This resistance is probably of local origin due to selective pressure for many years. This again is the first record of resistance to pyrantel pamoate in Africa, outside South Africa.

The repeated use of dichlorvos did not result into selection of resistant nematodes; and no others records worldwide are indicative of resistance.

Resistance of sport or stud horse nematodes (mostly small strongyles) to anthelmintics in Morocco is already present. The small strongyle resistant species should be identified in future. The present investigation was dedicated to horses with a good environment and investigations in ordinary small holder horses should be undertaken, in order to see if resistance remained within sport/leisure horses or invaded common horses and donkeys.

## ACKNOWLEDGEMENTS

We thank the staff of veterinary services of the national Stud-farms of Bouznika and Meknes as well as the Army Forces (Raf-1 and Raf-2). The help of Dr A. Bouchiba is gratefully acknowledged. We are also grateful to the veterinary students (R. Boukhris and A. Nouhi) who participated in the surveys. The financial support through PRAD (France-Morocco programmes: 2001-2004) or PRFI (Morocco) helped organizing practically the investigations.

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Reçu le 19 juillet 2005
Accepté le 4 août 2005