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Table of Contents
RESEARCH ARTICLE
Year : 2017  |  Volume : 54  |  Issue : 3  |  Page : 263-269

Bovine trypanosomiasis in tsetse-free pastoral zone of the Far-North region, Cameroon


1 Department of Animal Biology and Physiology, Faculty of Science, University of Yaoundé I, Cameroon
2 Department of Parasitology and Parasitological Diseases, School of Veterinary Medicine and Science, University of Ngaoundéré, Cameroon
3 Mission Spéciale d’éradication des glossines, Cameroon
4 The Higher Institute of the Sahel University of Maroua, Cameroon
5 College of Veterinary Medicine, Department of Veterinary Preventive Medicine, Ohio State University, USA

Date of Submission12-Dec-2016
Date of Acceptance26-Jun-2017
Date of Web Publication7-Nov-2017

Correspondence Address:
P F Suh
Department of Animal Biology and Physiology, Faculty of Science, University of Yaoundé I, P.O. Box– 812
Cameroon
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.217618

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  Abstract 

Background & objectives: The Far-North region of Cameroon has been considered free of tsetse and trypanosomiasis for the past three decades. But recent reports by pastoralists indicate its reappearance in the region. This study was aimed to confirm the existence of cattle trypanosomiasis and determine its prevalence, and to establish pastoralists knowledge and practice (KP) of the disease in Ndiyam Shinwa pastoral zone of Cameroon.
Methods: A total of 118 herds were surveyed for a descriptive, cross-sectional study in Ndiyam Shinwa pastoral zone from May to November 2014. Out of these, 110 herds were visited in the beginning of the rainy season, 22 of the 110 herds (suspect cattle) were revisited along with the remaining eight herds in the end of the season. The blood samples of 635 suspect cattle and 135 nonsuspect cattle were collected. Samples were subjected to two diagnostic tests: Buffy coat test (BCT) and packed cell volume (PCV) determination. A survey on pastoralist’s (n = 118) KP about trypanosomiasis was also undertaken.
Results: Parasitological analyses revealed six infections by Trypanosoma vivax: Four in suspect cattle against two in nonsuspect cattle, corresponding respectively to apparent prevalence of 0.63 and 1.46% and true prevalence of (0.79–3.15%) and (1.82–7.30%). The proportion of cattle found infected in the PCV as well as BCT tests was 33.26% for suspect cattle. More than 75% of followed-up suspects showed persisting symptoms nearly three months after initial examination. The most common diagnostic signs for pastoralists were ruffled hair, lacrimation, anorexia and emaciation.
Interpretation & conclusion: Cattle trypanosomiasis has reappeared in the Far-North region and seems to be in the inter-epizootic phase. Pastoralists have a good knowledge of the disease, but their perception of its importance seems to be influenced by the persistence of symptoms attributed to this disease in suspect cattle.

Keywords: Cameroon; cattle; Far-North region; pastoralists, trypanosomiasis


How to cite this article:
Suh P F, Njiokou F, Mamoudou A, Ahmadou T M, Mouhaman A, Garabed R. Bovine trypanosomiasis in tsetse-free pastoral zone of the Far-North region, Cameroon. J Vector Borne Dis 2017;54:263-9

How to cite this URL:
Suh P F, Njiokou F, Mamoudou A, Ahmadou T M, Mouhaman A, Garabed R. Bovine trypanosomiasis in tsetse-free pastoral zone of the Far-North region, Cameroon. J Vector Borne Dis [serial online] 2017 [cited 2020 Feb 18];54:263-9. Available from: http://www.jvbd.org/text.asp?2017/54/3/263/217618




  Introduction Top


With a cattle population of >2.1 million, the Far-North region of Cameroon is considered to be one of the major regions of the country for pastoral activities[1]. It is also an important destination for pastoralists of neighbouring countries who come from as far as Niger on transhumance to exploit its seasonal pasture[2]. However, the pastoral potential of this region is impeded, due to several factors including endemic animal diseases.

Animal African trypanosomiasis (AAT) is a vector-borne parasitic disease caused by Trypanosoma congolense, T. vivax and T. brucei brucei. The first two species are more virulent and responsible for majority of the bovine trypanosomiasis cases[3]. Trypanosomes are mostly transmitted cyclically by the tsetse fly (Diptera: Glossinidae); however, mechanical transmission of these parasites by tsetse fly or other haematophagous insects such as Tabanids has also been demonstrated[4]. This explains the occurrence of T. vivax outside the tsetse belt in Africa and even out of the continent[5].

During the 1960’s this disease was reported as one of the most important constraints to animal husbandry in the Far-North region of Cameroon, precisely between the Logone River and two tributaries (Serbwell and Taftaf) of the Chari River[6]. This zone was also known as an important human African trypanosomiasis (HAT) focus, reporting cases since 1900[7]. Both human and animal trypanosomiases were successfully controlled in the middle of the 1970’s after the eradication of tsetse fly[7],[8]. The last cases of these diseases were documented in the end of the seventies. Trypanosoma vivax was the only trypanosome species reported in the infected cattle of the canton of Serbwell, and mechanical transmission by Tabanids was also suspected to occur[9]. Since, then no investigation attempted to describe the epidemiological situation of this animal disease in the region. Recent surveys of pastoralists highlighted bovine trypanosomiasis, as one of the most important animal health issues encountered in the region[2],[10],[11]. Considering the importance of the disease, pastoralists have increased the use of trypanocides with the possible risk for the development of trypanosomal drug resistance (TDR), defined as the loss of sensitivity of a species of trypanosome to a compound (drug) which it had previously been susceptible. The pastoralists-reported disease prevalence, based solely on clinical signs, is widely used in veterinary epidemiologic studies[12]; but the validation of this simple and cheap method is absolutely necessary for its usefulness in control decisions. For veterinarians of poor countries, the diagnostic methods of choice for the validation of the reported cases on the field, depend heavily on the accessibility of the equipment and on their capacity of quick disease identification.

The buffy coat test (BCT) is a parasitological technique that concentrates trypanosomes in blood. It is particularly important when the parasite is undetectable in thin or thick smear microscopic examination[3]; but the detection threshold for this method remains low: 200–1000 trypanosomes/ml of blood[13]. BCT is nevertheless preferred over the serological anti-trypanosomal antibody detection tests which require laboratory facilities and do not differentiate infected animals from cured animals because of the persistence of antibodies[14]. Packed cell volume (PCV) determination is another accessible mean for the diagnosis of infected animals; it measures anaemia, a well-recognized and inevitable consequence of an infection with pathogenic trypanosomes, including T. congolense and T. vivax in livestock; and in the absence of other anaemia causing factors it stands as a reliable indicator for trypanosome infection in animals[15]. Moreover, PCV determination increases the sensitivity of BCT when used in combination[16]. Both methods can be used in field veterinary laboratory to assess animal trypanosomiasis prevalence.

This study was undertaken to ascertain the existence of trypanosomes in cattle in the Far-North region of Cameroon, decades after tsetse elimination, to determine the importance of bovine trypanosomiasis and to establish pastoralists' knowledge and practice (KP) of the disease.


  Material & Methods Top


Study area

The Far-North region of Cameroon (9°40'N–13°05'N and 12°15'E–16°45'E) is a Sudano-Sahelian zone covered by savannah and steppes; it is characterized by three main seasons: Rainy season (June–October), cold dry season (November–February), and hot dry season (end of March–May). Pastoralists of the region can be grouped into two categories: The sedentary and the mobile pastoralists. For feeding cattle the first group relies on cotton seed cakes so as to overcome the lack of pasture during the dry season, whereas mobile pastoralists practice transhumance by taking their animals to rangelands. Mobile pastoralists belong to two general ethnic groups: Arab and FulBe. The FulBe are divided into transhumant and agro-pastoral groups; the transhumant pastoralists are permanently dependent on transhumance meanwhile the agro-pastoralists may go on transhumance and come back to the village once or twice a year for a few weeks where they cultivate crops[10].

The Logone floodplain is one of the key resource areas in the region for livestock. In the dry season, it attracts thousands of pastoralists. Most of them then move north of the floodplain or south to the grazing lands that surround Lake Maga, also called Ndiyam Shinwa[2] [Figure 1], by the end of the dry season. At the start of the rains they return to the higher elevated dunes of the Diamaré area or to their villages[2].
Figure 1: The Far-North region of Cameroon (the arrows) broadly indicate the general direction of the transhumance orbits of mobile pastoralists in the study area of Ndiyam Shinwa.

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Study design

Sampling procedure and collection of data: A descriptive, cross-sectional study was carried out in Ndiyam Shinwa pastoral zone from May to November 2014. Mobile pastoralists were sampled in pasture and in five agro-pastoral villages: Manga, Gavra, Boukroy, Yanga and Barkaya of Kaikai sub-division. Sedentary pastoralists from the above villages were equally sampled.

The heads of Guirvidig, Kaikai and Manga Centres Zootechnique et de Contrôle de Santé Vétérinaire (CZV) were involved in the survey as facilitators to reach the maximum number of pastoralists and to construct a sample that reflected the composition of pastoralists in the zones under their sanitary authority.

Ethics: The study was carried out in compliance with the Regional Delegation of the Ministry of Fishery, Livestock and Animal Husbandry (MINEPIA) protocol for animal disease surveillance. Research authorization was obtained from the same delegation. Pastoralists were initially informed of the purpose of the study and those who voluntarily consented to participate were subjected to a questionnaire.

In total 118 herds were surveyed in the study: 110 were visited in the beginning of the rainy season (May–July); and eight in the end of the rainy season (October–November). An experienced veterinary technician clinically examined cattle suspected with trypanosomiasis. A total 22 of the 110 herds sampled during May–July were re-visited in October to identify suspect cattle with persisting symptoms (old cases). Characteristics of individual animals such as breed, sex, age, and treatment history were recorded; and the size of each herd was estimated visually.

Additionally, 135 non-suspect cattle were examined and included in a trypanocide sensitivity survey. These cattle were sampled in the beginning of the rainy season from four of the herds in which suspect cattle were selected. Based on the methods of randomization for clinical trials as described by Pocock[17], each uninfected animal was attributed a random number generated from the table of random digits, then a random starting point was chosen, from which animals were either included into group one (treated) or group two (control). Group one included 75 animals, which received a preventive dose of Trypamidium (Trypamidium®, Merial, France) at 0.5 mg/kg. Group two contained 60 animals which received a placebo. The weight of each animal was measured with a Rondo® ribbon which associates weight with girth circumference. Animals were re-examined after 3.5 months. Pastoralists knew each of their animals by name on the basis of the color of animal’s coat, horn shape or on the basis of the name of the dam[18]. A combination of four parameters was used as identifiers for each animal: The name given by pastoralists, the sex, the age and the colour of the coat. All confirmed cases of trypanosome infection were treated with Diaminazen (Veriben®, Ceva, France) at 7 mg/kg through intramuscular injection as recommended by the manufacturer and were re-examined two weeks later.

Diagnosis of trypanosome infections

Blood of cattle was collected from the jugular vein into an EDTA tube and used for parasitological (detection of trypanosomes by BCT)[13] and paraclinical (PCV determination) analyses. Blood in each EDTA tube was transferred into capillary tubes which were centrifuged immediately in a micro-haematocrit centrifuge for 5 min at 9000 rpm. After centrifugation, the PCV was measured. Animals with PCV values <24% were considered anaemic[19] and presumed infected. The buffy coat and the upper most layers of red blood cells from each capillary tube were extruded onto a microscope slide, stained with Giemsa and examined under 100× oil immersion objective lens for the detection of trypanosomes.

Data collection: Knowledge and practice questionnaire A standardized survey was employed to generate information on the participants’ KP on trypanosomiasis; it focused mainly on knowledge of clinical trypanosomiasis and treatment. Focus group discussions were conducted guided by a questionnaire containing open and close-ended questions on the etiology of trypanosomiasis and use of trypanocides. Participants included in the discussion were agro-pastoralists who were regrouped according to their quarter of origin in nine focus groups consulting 7–12 peoples.

Statistical analysis

Data were recorded in Microsoft Excel. The Z-test and chi-square (χ2) were used to compare proportions, and the t-test was used to compare means. All statistical tests were performed at a precision level of 5% in SPSS Statistics 17.0 software (SPSS Inc. Chicago, USA). Real BCT prevalence was estimated with the formula below[20].




  Results Top


Parasitological tests results

A total of 635 suspect cattle were identified in the study—496 in the beginning of the rainy season and 139 in the end of the rainy season. Out of the 139 suspect cattle, 73 were old cases (animals with persisting symptoms found among the revisited herds). They represented 75.26% of the total number of cattle followed-up; the others either recovered or were simply removed from the herds. The mean age of the study population was 8.01 yr (SD = 3.33); 48.50% (308/635) of selected cattle had attained the age of 10 yr.

Parasitological analyses revealed four trypanosome infections in suspect cattle. The apparent prevalence was 0.63% (4/635). The BCT sensitivity was assumed to be between 0.2 (lowest parasitaemia) and 0.8 (highest parasitaemia). Estimates of true prevalence ranged from 0.79 to 3.15%. Trypanosoma vivax was the only species identified. One of the animals infected with T. vivax and treated with diaminazen remained positive for two weeks after treatment.

Of the 135 non-suspect cattle included in isometamdium study, two cases were detected with T. vivax infection, corresponding to an apparent prevalence of 1.46% and an estimated true prevalence varying between 1.82 and 7.30%. A total of 101 animals were followed-up successfully. One positive case was detected within the control group (1.92%) and none in the treated group.

Paraclinical results

The mean PCV was 27.38 (SD = 6.91) in suspect cattle and 29 (SD = 7.38) in non-suspect cattle; the difference was statistically significant between these two categories (t = 2.368; p = 0.018). Suspect cattle whose clinical status remained unchanged over the survey period had PCV values of 27.86 (SD = 5.44) in the beginning of the study and 28.67 (SD = 5.38) in the end; the PCV values were not statistically different (t = 0.891; p = 0.376).

PCV values did not vary significantly between the control group (28.90; SD = 6.94) and the treated group (28.20; SD = 5.15) at the beginning of the study (t = 0.498; p = 0.620). But at the end of follow-up, a reduction in PCV was recorded in the control group (2.10; SD = 8.03), whereas a slight increase in PCV was observed in the treated group (0.57; SD = 6.59). The proportion of cases detected on combining BCT with PCV results was 33.26% (165/496) for suspect cattle against 25.92% (35/135) in non-suspect cattle.

Pastoralist ‘s knowledge and practice for trypanosomiasis

A total of 118 pastoralists were interviewed in the study—60 agro-pastoralists, 39 transhumant pastoralists and 19 sedentary pastoralists. All of them knew about animal trypanosomiasis and reported it as an important health issue in herds. Ruffled hair, emaciation, lacrimation and anorexia were the most frequently reported signs [Table 1]. Most pastoralists (66.10%; 78/118) used two clinical signs for trypanosomiasis diagnosis; 82.05% (64/78) of them used ruffled hair in combination with lacrimation, anorexia or emaciation [Figure 2]. About 22.03% of the pastoralists (26/118) used three signs. Similarly, 9.32 and 2.54% of the pastoralists used one and four clinical signs, respectively for diagnosing trypanosomiasis.
Table 1: Frequently observed clinical signs of cattle trypanosomiasis by pastoralists for diagnosis

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Figure 2: (a) The proportion of pastoralists who used two clinical signs as diagnosis pattern for trypanosomiasis against others (those who used one, three or four clinical signs); and (b) The most frequently used pairs of clinical signs for trypanosomiasis diagnosis by pastoralists; Rh—Ruffled hair; An—Anorexia; L—Lacrimation; Pa—Progressive emaciation.

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All interviewees used trypanocide and only 18 of them had their sick animals treated by a veterinarian. Most of them (100/118) treated their sick cattle themselves or by other pastoralists of the camp. The majority of pastoralists (98/102) who responded to the question on syringe utilization, declared using a single needle to treat all animals, and none of them knew about sterilizing needles before re-use. Of the 106 pastoralists who responded to treatment questions, almost all reported treating only suspect cattle within their herd (100/106), whereas only 6 of 106 treated both suspect and the rest of the herd preventively at the start of the rainy and dry seasons.

Tsetse flies (Pechi) were cited as the first cause of the disease (100%; 9/9 focus groups), but none of the pastoralists in all nine quarters/groups were able to identify tsetse flies. Other causes of trypanosomiasis cited, included ticks (44.44%; 4/9) and dirty water (33.33%; 3/9). Tabanids also called Boubi in Fulfuldé area were known and easily recognized by all quarters (9/9); they were pointed as an important nuisance by pastoralists of all quarters (100%; 9/9), but never as potential vector for trypanosomiasis. Pastoralists of all quarters use smoke to repel biting insects and/or grazed their cattle at night and/or kept the animals inside huts during the peak hours of insect biting activity; a few of them (11.11%; 1/9) use insecticides to repel biting insects.

The annual prevalence of trypanosomiasis estimated by pastoralists was 9.51% (646/6792). This prevalence was 5.95% (183/3076), 12.42% (373/3003) and 12.62% (90/713) respectively in agro, transhumant and sedentary pastoralists; it differed significantly only between the first pastoral group and the last two ones (χ2=68.9498; p < 0.00001).


  Discussion Top


This study confirms the circulation of trypanosomes in cattle of the northern most region of Cameroon. Trypanosoma vivax is the only species identified. Earlier entomological surveys, in areas formerly infested by Glossina tachinoides reported the absence of this Dipteran insect after tsetse eradication campaigns[7]. This vector has receded southward to the north region[21]. Contacts between local cattle and tsetse are therefore deemed unlikely in the study zone.

Infections by T. vivax alone have already been reported in tsetse free areas in northern Cameroon[22]. The presence of this parasite has also been described in tsetse free areas of countries bordering the study zone. In Lake Chad, an infection rate of 1.6% from 933 examined cattle was reported in the year 2000[23]. In Maidugouri, Nigeria, high T. vivax parasitaemia was reported after post mortem examination of 10 sick calves[24]. Animal trypanosomiasis with T. vivax as the only or the most prevalent causative agent has always been associated with mechanical transmission; this animal trypanosome is known to have a 25-fold chance to be transmitted mechanically than T. congolense[25].

The parasitological prevalence in suspect cattle was nearly nil in this study. A similar observation was made in French Guyana, Venezuela and Columbia, in Latin America[26] and in Assalé, a tsetse free locality around Lake Chad[9], in Africa. The low infection rate observed in the survey seems to reflect the reality and may refer to the inter-epizootic period of the epidemiological cycle of mechanically transmitted animal trypanosomiasis[27]. The huge difference between reported clinical and parasitological cases in this study suggest implicitly that the perception of cattle trypanosomiasis’ importance by pastoralists is exaggerated. But with >75% of followed-up cattle displaying the same symptoms three months after first examination, one could postulate that the perception of cattle trypanosomiasis’ importance by pastoralists result from fact that, unlike other cattle health issues, the symptoms attributed to the disease persist for a long period in spite of the repeated administration of trypanocide or other medicines prescribed by veterinarians. The majority of suspect cattle seem to be chronically infected. parasitaemia is usually low in these animals[16] and buffy-coat tests are more likely to be negative[28].

The infection rate was twice as high in non-suspect cattle as in suspect cattle. This difference suggests that infected non-suspect cattle were suffering from early infections; which are more likely to be detected through parasitological diagnostic tools[16].

When PCV was used as a discriminating diagnostic tool along with BCT, one-third of suspect cattle were diagnosed infected; the accuracy of pastoralists-reported disease is higher with this approach. One quarter of non-suspect cattle were diagnosed with anaemia; which might be due to infections other than trypanosomes. This situation highlights the need for more sensitive diagnostic methods like molecular detection tool to confirm the infection status of cattle, otherwise the importance and accurate prevalence of the disease would be misleading.

In the present study, one case of repeated BCT positive results was observed in the same animal after treatment, indicating the possible presence of a resistant strain of T. vivax to diaminazen in the region. No evidence of resistance was observed with isometamedium in this small trial. Cattle treated with isometamedium had a slight increase in PCV contrary to control cattle where a decrease in PCV was observed. The apparent benefit of trypanocide in treated group implies that anaemia causing factors in cattle may include pathogens susceptible to this drug.

Pastoralists noticed eight different signs which they associated with trypanosomiasis. This number is fewer than that reported in Ethiopia[29]. Nevertheless, the frequencies of the most frequently noticed signs are similar in both studies. The majority of the interviewed pastoralists administer drug to sick animals themselves; other studies in West Africa reported similar observations[30]. In tsetse free area of northern Ethiopia, a different observation was reported; pastoralists of this area send their cattle to veterinary clinics or animal health post for trypanosomiasis cases[31]. This difference may be due to a higher accessibility of pastoralists to veterinary services and/or a higher trust for veterinarians in this area. The fact that the majority of interviewees used a single needle for treating all suspect cattle suggests that there is an additional risk for mechanical transmission of trypanosomes and other pathogens among cattle through this mechanism. Moreover, maintaining animals for >10 yr within herds, as observed in this study, constituted another disease risk factor i.e. the animals might act as reservoirs and silently affect the occurrence of disease.

The presence of T. vivax in cattle of the Far North region, raises the alarm on the need for epidemiological surveillance particularly in its rangelands; where the high density of livestock, regular migration of animals from countries bordering the Lake Chad[2], and the abundance of Tabanids of the genus Tabanus and Atylotus[32] (recognized as better mechanical vectors), increase the risk for epidemics[23],[26].


  Conclusion Top


Cattle trypanosomiasis is present in the Far-North region of Cameroon and seems to be in the inter-epizootic phase of its epidemiological cycle. The reappearance of this disease in the region calls for routine epidemiological surveillance in pastoral zones. Pastoralists have a good knowledge of animal trypanosomiasis but their perception of its importance is influenced by the persistence of symptoms in suspect cattle. More work is necessary to determine the etiology of the morbidity attributed to this disease in suspect cattle as well as to anaemia in non-suspect cattle.

Conflict of interest

The authors declare no conflict of interest.


  Acknowledgements Top


This study was supported by the National Science Foundation through a grant (DEB-1) to the Disease Ecology and Computer Modeling Laboratory (DECML) at the Ohio State University (USA). The authors thank the Centre d’Appui à la Recherche et au Pastoralisme (CARPA) team for technical assistance, the Regional delegation of MINEPIA for their administrative support, and pastoralists who participated in the study.



 
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    Figures

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This article has been cited by
1 A meta-analysis of the prevalence of bovine trypanosomiasis in some African countries from 2000 to 2018
F. Ebhodaghe,C. Isaac,J.A. Ohiolei
Preventive Veterinary Medicine. 2018; 160: 35
[Pubmed] | [DOI]



 

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