# Epidemiology of sheep infection by Oestrus ovis in Algeria

A. Benakhla, S. Sedraoui, D.E. Benouareth, Jacques Cabaret, C. Boulard

► To cite this version:

A. Benakhla, S. Sedraoui, D.E. Benouareth, Jacques Cabaret, C. Boulard. Epidemiology of sheep in-fection by Oestrus ovis in Algeria. Parasite, 2004, 11 (2), pp.235-238. 10.1051/parasite/2004112235 . hal-02679357

HAL Id: hal-02679357

https://hal.inrae.fr/hal-02679357

Submitted on 31 May 2020

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# EPIDEMIOLOGY OF SHEEP INFECTION BY OESTRUS OVIS IN ALGERIA

BENAKHLA A.*, SEDRAOUI S.*, BENOUARETH D.E.**, CABARET J.*** & BOULARD C.***

**Summary:**

313 sheep were examined in 1996 to assess the importance and seasonal evolution of Oestrus ovis infection in the Algerian region of El-Tarf. Prevalence was found to be 67.4 %. The larval burden was 18 larvae by infected sheep. The prevalence was higher in older sheep than in lambs; intensity was similar. The different larval stages were found all along the year in sheep with prevalence ranging from 33.1 to 80.5 % for L1, 9.7 to 43.9 % for L2 and 8.4 to 23.0 % for L3. The sheep were the least infected in winter (prevalence from 35.7 to 44 % and intensity seven to ten larvae per sheep). The highest infection was found during the warm season (spring to autumn, prevalence from 62 to 90 % and intensity ranging from 15 to 25). This larval evolution profile suggested the existence of one long cycle (November-April) and possibly two shorts cycles (May-October). This epidemiological pattern is similar to that in Morocco but was slightly different from the situation in Tunisia where the winter cycle was apparently of lesser importance.

**KEY WORDS :** Oestrus ovis, sheep, epidemiology, Algeria.

**MOTS CLÉS :** Oestrus ovis, mouton, épidémiologie, Algérie.

**Résumé :** ÉPIDÉMIOLOGIE DE L'INFESTATION DES OVINS PAR OESTRUS OVIS EN ALGÉRIE

313 têtes d'ovins de la région d'El-Tarf en Algérie ont été examinées en 1996 en vue d'étudier l'infestation des ovins par Oestrus ovis. La prévalence est de 67,4 %. L'intensité d'infestation atteint une moyenne de 18 larves par ovin. La prévalence était plus forte chez les animaux de plus d'un an que chez les agneaux, mais l'intensité était similaire. Les différents stades larvaires ont été retrouvés tout au long de l'année avec des prévalences de 33,1 à 80,5 % pour les L1, 9,7 à 43,9 % pour les L2 et 8,4 à 23,0 % pour les L3. Une période d'infestation minimale des ovins est mise en évidence en hiver avec des prévalences de 35,7 à 44 % et des intensités de sept à dix larves par ovin infesté. Une période d'infestation maximale est enregistrée pendant la saison chaude (printemps, été, automne) avec une prévalence de 62 à 90 % et des intensités de 15 à 25 larves par ovin infesté. Le profil d'évolution de l'infestation des ovins par Oestrus ovis suggère l'existence d'un cycle long (novembre-avril) en période froide et vraisemblablement de deux cycles courts en période chaude (mai-octobre). La situation épidémiologique est similaire à celle du Maroc, mais diffère un peu de celle décrite en Tunisie, qui présente un cycle d'hiver long de moindre importance.

Oestrus ovis is a Diptera belonging to the Oes-
tridae family that infects sheep. Larvae are
found in frontal sinuses and nasal cavities. The
disease may decrease production in infected animals
(Lucker & Foster, 1958; Marsh, 1965), or cause patho-
logy (Dorchies & Alzieu, 1997). It is widely distributed
in small ruminant breeding areas (Babcock, 1953;
Breiev et al, 1980). There is a clear seasonal evolution
of infection in South of France or in the Sahelian coun-
tries of Africa (Tabouret et al., 2001). The seasonal evo-
lution is much less clear in Mediterranean countries
(Morocco: Pandey & Ouhelli, 1984; Tunisia: Kilani et
al., 1986; or Sicily: Caracappa et al., 2000). The situa-
tion in Algeria has not been studied and we intended
to assess the seasonal prevalence and intensity of

infection by *O. ovis* in the region of El Tarf in Algeria
in a Mediterranean comparative approach.

## MATERIAL AND METHODS

REGION OF STUDY AND SHEEP FARMING

El-Tarf is located at the north-east of Algeria. The yearly rainfall is 700 mm, and maximum and minimum temperatures are respectively 41° C (July-August) and 4° C (January-February). The rainfall season extends from October to April. Sheep are grazed on pastures all the year. They graze on fallow fields in winter and stubble fields in summer. A part of sheep are bred in peri-urban conditions and kept near house. The lambing periods are November-December and April-May.

SAMPLE COLLECTIONS

The sheep heads were collected at the Ai-Assel slaugh-
terhouse from January to December 1996. The animals

<footnote>* Institut Agro-Vétérinaire, BP 05, 36000 El-Tarf, Algérie.</footnote>

<footnote>** Département de Biochimie, Faculté des Sciences, Université d'Annaba, Algérie.</footnote>

<footnote>*** INRA, Bio-Agresseurs Santé Environnement, 37380 Nouzilly, France.
Correspondence: Jacques Cabaret.
E-mail: cabaret@tours.inra.fr</footnote>
<figure><img src="image_2.png" /><figcaption>Fig. 1. – Monthly *Oestrus ovis* prevalence in sheep.</figcaption></figure>

less than one year were male and female lambs; the sheep older than one year were mostly old ewes. Most of the sheep originated from the El Tarf area but some could have been bred in distant regions. *O. ovis* were collected weekly on 6-9 sheep heads using a technique described in Testé (1979) and Yilma (1992). The sheep characteristics (region of origin, age based on tooth growth, and sex) and localisation of *O. ovis* were recorded. The identification of larvae was done using the keys of Zumpt (1965).

## STATISTICAL ANALYSES

One-way analysis of variance (ANOVA) and Newman-Keuls comparison tests, GLM (General linear model), and chi-square analyses were performed using a Simstat software (Peladeau & Lacouture, 1993). A test was considered as significant when the probability of the result was equal or less than 0.05.

## RESULTS

### OVERALL PREVALENCE AND INTENSITY OF *O. OVIS* INFECTION

211 heads out of 313 were positive for *O. ovis* (prevalence 67.4). 129 sheep (61.1%) harboured the three larval stages of *O. ovis*, 61 (28.9%) had two larval stages and only 21 (9%) were infected with only one larval stage. Mean intensity of infection was 18.6 larvae (range: 1-113). The proportion of L1, L2 and L3 stages were respectively 59.5%, 24.6% and 15.9%.

### SEASONAL EVOLUTION OF PREVALENCE AND INFECTION

Prevalence (Fig. 1) is lower in January to March (36% to 44%) and remained over 60% for the most of the rest of the year, and a maximum was recorded in July (90%). No month effect was demonstrated using one-way ANOVA (p = 0.12), but comparing winter with spring, summer and autumn yielded significant difference (Chi-square, p = 0.0001).

<figure><img src="image_3.png" /><figcaption>Fig. 2. – Seasonal evolution of intensity of *Oestrus ovis* infection.</figcaption></figure>

<figure><img src="image_4.png" /><figcaption>Fig. 3. – Monthly proportions of the three *Oestrus ovis* instars.</figcaption></figure>

Intensity seasonal pattern (Fig. 2) followed that of prevalence. The lowest intensities were found in January (9.5 larvae by sheep) and February-March (six to seven larvae by sheep) and the highest intensities (> 20 larvae by sheep) were recorded from April to October. There is a significant difference between winter and the other seasons (GLM; p = 0.0002) but no difference could be found during the period from April to October (p = 0.18).

L1 instars were the most frequent along the year (Fig. 3) except in April, when L2 were more frequent (43.9 L2 vs 33.1 L1). The seasonal evolution of proportions was as follows (Fig. 3): L1 decreased during winter (80.5%
<table><caption>Table I. - *Oestrus ovis* in Algerian sheep: intensity of the three instars and prevalence.</caption><thead><tr><th>Sheep</th><th>Intensity of the three instars (no of instar/infected sheep)</th><th>Prevalence % (no positive/no sheep sampled)</th></tr></thead><tbody><tr><td>Age (number)</td><td>L1 L2 L3</td><td></td></tr><tr><td>&lt; 1 year (123)</td><td>11.6 5.4 3.2</td><td>58.9 (209)</td></tr><tr><td>&gt; 1 year (88)</td><td>10.4 3.4 2.7</td><td>84.6 (104)</td></tr></tbody></table>

in January to 33.1 % in April, when it then increases steadily from May to December (47.4 to 77.1 %). Seasonal differences were recorded for the three instars (L1: p = 0.006; L2: p = 0.009; L3: p = 0.046)

## INFLUENCE OF AGE ON PREVALENCE

AND PROPORTIONS OF THE THREE-INSTAR INTENSITY OF INFECTION (Table I)

Prevalence was significantly higher in sheep older than one year (Anova: p = 0.048).

Intensity of infection was 20.1 in younger sheep and 16.5 in older sheep.

A general analysis (GLM using the following model: proportions of each instar = age + month + interaction age × month) did not show any influence of age, on L1 (p = 0.24), L2 (p = 0.14) or L3 (p = 0.66).

## DISCUSSION

Ovis prevalence in El Tarf is comparable to that found in Morocco (prevalence: 69.2 %, Pandey & Ouhelli, 1984) and lower to that in Tunisia (93 %, Kilani et al., 1986). The intensity of infection (18.6 by sheep) is higher than in Morocco (6.7 by sheep) and lower than in Tunisia (34 by sheep). These discrepancies between the North African countries might be related to conditions of survey (age of sheep, microclimate, etc.). The influence of age of sheep is comparable to the findings of Yilma (1992). Prevalence was higher in older sheep whereas intensity was not very different according to age.

Infection of sheep in Algeria might be classified into two periods: i) winter, with low intensity and prevalence, possibly due to low temperature (< 16° C) that does not permit the activity of flies and development of pupae (Rogers & Knapp, 1973; Yilma, 1992) and ii) spring to autumn, with high prevalence and intensity. The rise occurring in the beginning of spring has also been noticed in France (Yilma, 1992) and Morocco (Pandey & Ouhelli, 1984). The prevalence in winter (January to March: approximately 40 %) was compa-

rable to that recorded in Morocco (40 %) but was different from that recorded in Tunisia (nearly 95 %). This could be due to sampling as Tunisian sheep were all older than one year, and thus winter prevalence was higher due to age and probably not to location. The Morocco and Algeria winter prevalences were higher than those recorded by Yilma (1992) in the Limousin region of France in lambs (22 %), but were similar to those recorded in ewes (40 %). First instars are found over all the year but they represent more than 75 % of all instars from November to February (see Fig. 3). The seasonality of L1 is weak in Mediterranean countries (monthly percentages: 35 to 65 %) compared to that recorded in South West of France (30 to 100 %) (Tabouret et al., 2001). The period of predominance of the L1 in South of France is clear: September to February in French Pyreneans (Yilma & Dorchies, 1991) and October to March in French Limousin (Yilma, 1992). The seasonality of L3 is also lower: monthly percentages 10 to 30 % in Mediterranean countries against 0 to nearly 40 % in South West of France. These colder periods may correspond to inhibition of development. In the El-Tarf region we may consider an end of autumn-winter long cycle in relation to inhibition of development and several shorter cycles during spring to beginning of autumn, considering the duration of one life cycle). The data obtained in Morocco (Pandey & Ouhelli, 1984) on tracer lambs indicate that infection occurs from April to November and that probably two generations in warm period do occur, one with a peak in June and another in September; this does not clearly appear on slaughterhouse results, resulting from overlap in these warm season generations. These two peaks are not seen during the warm season neither in Tunisia (Kilani et al., 1986) nor in Algeria slaughterhouse data. The knowledge on epidemiology of *Oestrus ovis* is important to control the disease. The risk of infection in Mediterranean countries is high during most of the year and control relies on frequent treatments. In Algerian and Moroccan conditions, a short winter period is not at risk and treatment given at the end of the fly season will interrupt the life-cycle, and although it could not be as efficient as it has been in South West of France (Jacquiet & Dorchies, 2002), it may reduce risk during the warm season.

## REFERENCES

* BABCOK O.G. Note on the biology of *Oestrus ovis*. L. USDA, Association Bureau Entomology of Plant Quarterly Bulletin, 1953, E-871, 4 p.

* BREIEV K.A., ZAGRETDINOV R.G. & MINAR J. Influences of constant and variable temperature on pupal development of the sheep bot fly (*Oestrus ovis* L.). *Folia parasitologica*, 1980, 27, 350-365.
CARACAPPA S., RILLI S., ZANGHI P., DI MARCO V. & DORCHIES P.
Epidemiology of ovine oestrosis (*Oestrus ovis* Linné 1761,
Diptera: Oestridae) in Sicily. *Veterinary Parasitology*, 2000,
92, 233-237.

DORCHIES P. & ALZIEU J.P. L'oestrose ovine : revue. *Revue de Médecine Vétérinaire*, 1997, 7, 565-574.

JACQUIET P. & DORCHIES P. Towards a lower prevalence of *Oestrus ovis* infections in sheep in temperate climate (south west France). *Veterinary Research*, 2002, **33**, 437-640.

KILANI M., KACEM H., DORCHIES P. & FRANC M. Observations sur le cycle d'Oestrus ovis en Tunisie. *Revue de Médecine Vétérinaire*, 1986, **137**, 451-457.

LUCKER J.T. & FOSTER A.O. Parasites and parasitic diseases of sheep. *USDA Farmer's Bulletin*, 1958, **13** (30), 10-12.

MARSH H. Newsom's sheep disease. 3rd Ed. Williams and Wilkins Co., Baltimore, Md., 1965.

PANDEY V.S. & OUHELLI H. Epidemiology of *Oestrus ovis* infection of sheep in Morocco. *Tropical Animal Health and Production*, 1984, **16**, 246-252.

PELADEAU N. & LACOUTURE Y. Simstat: bootstrap computer simulation and statistical program for IBM personal computers. *Behavior Research Methods, Instruments and Computers*, 1993, **25**, 410-413.

ROGERS C.E. & KNAPP F.W. Bionomics of sheep bot fly *Oestrus ovis*. *Environmental Entomology*, 1973, **2** (1), 11-23.

TABOURET G., JACQUIET P., SCHOLL P. & DORCHIES P. *Oestrus ovis* in sheep: relative third-instar populations, risk of infection and parasitic control. *Veterinary Research*, 2001, **32**, 525-531.

TESTÉ C. L'oestrose ovine en France: essai d'étude épidémiologique dans le sud du pays. Thèse Vétérinaire, ENVA, 1979, 67 pp.

YILMA J.M. Contribution à l'étude de l'épidémiologie, du diagnostic immunologique et de la physiopathologie de l'oestrose ovine. Thèse de Doctorat es Science. Institut National Polytechnique de Toulouse, France, 1992.

YILMA J.M. & DORCHIES P. Epidemiological study of *Oestrus ovis* in southwest France. *Veterinary Parasitology*, 1991, **40**, 315-323.

ZUMPT P. Myiasis in man and animals in the old world. A text book for physicians veterinarians and zoologists, 1 vol. London, Butterworths, 1965, 267 p.

Reçu le 18 juillet 2003
Accepté le 22 novembre 2003

PARUTION

ÉPIDÉMIOLOGIE DES MALADIES PARASITAIRES
Tome 3 "Opportunistes"

C. RIPERT

Éditions Médicales Internationales, 2003, 440 pages, 140 €

http://www.eminter.fr

ISBN : 2 7430 0632 3

Ce troisième tome fait suite aux deux premiers consacrés
à l'épidémiologie des maladies parasitaires : protozooses et
helminthoses. 17 auteurs ont participé à la rédaction de cet
ouvrage avec la coordination du Pr Ripert de Bordeaux.
Après une description des causes et des mécanismes de
l'immunodépression, avec une note particulière concer-
nant le sida tropical, les parasitoses opportunistes sont
passées en revue selon un plan standard déjà utilisé dans
les précédents tomes. L'accent est mis sur le diagnostic bio-
logique, la recherche et l'identification des parasites dans
l'environnement, les traitements, la prévention et le contrôle.
Un ouvrage de référence et un outil de travail pour les pro-
fessionnels de la santé humaine et vétérinaire !