Trop Anim Health Prod DOI 10.1007/s11250-013-0403-6

REGULAR ARTICLES

Prevalence, risk factors, and major bacterial causes of camel mastitis in Borana Zone, Oromia Regional State, Ethiopia Alemayehu Regassa & Gelma Golicha & Dawit Tesfaye & Fufa Abunna & Bekele Megersa

Accepted: 12 March 2013 # Springer Science+Business Media Dordrecht 2013

Abstract A cross-sectional study was carried out from November 2010 up to April 2011 to estimate mastitis prevalence and associated risk factors and to assess its bacterial causes in traditionally managed camels in Borana Zone, Southern Ethiopia. Thus, 348 lactating camels were examined clinically, and subclinical cases were checked with California mastitis test (CMT). The overall prevalence of mastitis was 44.8 % (156/348), comprising clinical (19, 5.4 %) and subclinical (137, 39.4 %) cases. The quarter level prevalence of mastitis was 24.0 % (334/1,392). Of the total 1,392 examined teats, 30 were blind, and hence, from the 1,362 non-blind CMT-examined teats, 22.3 % (304/1,362) were CMT positive. Of the 304 CMT-positive samples, 264 were culture positive (197 Gram-positive, 41 Gram-negative, and 26 mixed isolates), and 40 were culture negative. The prevalence of Staphylococcus aureus was found to be the highest at both the animal (12.8 %, 39/304) and quarter level (2.9 %, 39/1,362). Regression analysis revealed higher likelihood of mastitis occurrence among camels from Dharito (OR= 3.4, 95 % confidence interval (CI)=1.8, 6.4), Gagna (OR= 3.4, 95 % CI=1.8, 6.5), and Haro Bake (OR=2.6, 95 % CI= 1.3, 5.1) than camels from Surupha. Likewise, there was higher chance of mastitis occurrence among camels at the early lactation stage (OR=2.3, 95 % CI=1.1, 4.6) and camels with udder/teat lesions (OR=13.7, 95 % CI=1.7, 109.4) than A. Regassa (*) : G. Golicha : D. Tesfaye : F. Abunna : B. Megersa School of Veterinary Medicine, Hawassa University, P.O. Box 05, Hawassa, Ethiopia e-mail: [email protected] B. Megersa Institute of Animal Production in the Tropics and Subtropics Garbensrae 17, Universitäte Hohenheim, 70599 Stuttgart, Germany

among camels at late lactation stage and camels with healthy udder/teats, respectively. In conclusion, this study reveals the current status of camel mastitis in Southern Ethiopia. Keywords Mastitis . Camel . Prevalence . Risk factors . Bacterial isolation . Ethiopia

Introduction Camels (Camelus dromedarius) are the most capable animal species in utilizing marginal areas and in survival and production under harsh environmental conditions (Schwartz and Dioli 1992). Hence, it makes an important contribution to human survival and utilization of the dry and arid lands (Abdurahman and Younan 2004). Camels play a significant role as source of milk, meat, and draft power. It also serves as a financial reserve (asset) and security (drought-prone risk management) for pastoralists, as well as an indication of social prestige and wealth. In Ethiopia, camels are kept in arid and semiarid lowlands of Borana, Somali, and Afar regions, which cover 50 % of the pastoralist areas in the country (Teka 1991). The Borana pastoralists, who traditionally based on cattle husbandry for milk production and wealth storage, have recently developed considerable interest in camel production. Economical changes, social conditions (religion, marriage linkage, and conflict), and extensive seasonal movements have been the main driving forces behind the increased camel production in the Borana plateau (Biffa and Chaka 2003). Although the exact number of current camel population of Borana Zone is not known, data from Zonal Department of Planning and Economic Development indicated that about 106,366 camels are found in the 13 districts of the zone (BZDPED 2006).

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Occurrence of mastitis in camel has been reported from some of camel-keeping countries including Somalia (Abdurahman et al. 1995), Sudan (Obied et al. 1996), Kenya (Younan et al. 2001), Israel (Guliye et al. 2002), and from different parts of Ethiopia (Almaw and Molla 2000; Woubit et al. 2001; Abdul-Gadir et al. 2006; Abera et al. 2010; Bekele and Molla 2001). However, still there is lack of recent reports regarding the status of camel mastitis and mastitis-causing pathogens in the pastoral parts of the country. Therefore, this study was designed to identify the causative pathogens of camel mastitis, to estimate the prevalence of camel mastitis, and to assess the impact of various associated risk factors on the occurrence of mastitis in camels.

(Dharito, Gagna, Haro Bake, and Surupha) were randomly selected and considered for the study. The calculated sample size was then proportionally allocated to the respective PAs based on their total target population in such a way that these herds are representative for camel herds in the zone. Accordingly, 75 camels from Dharito, 65 from Gagna, 96 from Haro Bake, and 112 from Surupha were sampled. From each PA, the lists of camel owners (households) were obtained, and then, the household was randomly selected with lottery system. Then, all lactating camels of the selected household (30 households) were included in the study. In case when the selected household had no lactating camels, the next household in the list was included till the 348 camels were obtained.

Materials and methods

Physical examination of the udder

Study area

Clinical mastitis was defined as a swollen, reddened, and hardened udder which was painful upon palpation, and there could be alteration in the color and consistency of milk (Radostits et al. 2007). On the other hand, subclinical mastitis was characterized by apparently normal milk and increased leukocyte counts. In both cases, pathogens were often detected by bacteriological culture. Additionally, blind teats were also considered as clinical cases as the blockage of the teat is the chronic stage of mastitis which can be clinically diagnosed. In line with this definition, the general udder abnormalities and anatomical malformations were recorded as clinical cases. The size of the rear and forequarters, indurations, and fibrosis were also examined by deep palpation. Tick infestations and use of anti-suckling devices (materials put on teats to protect the continuous calf suckling) were also noted.

The study was conducted from November 2010 to April 2011, in Yabello District, Borana Zone, Oromia Regional State, Ethiopia. Yabello town is geographically found at 5° 23′ 49″ N, 39° 31′ 52″ E, and located at a distance of 565 km south of Addis Ababa. Borana Zone has 13 districts under which there are 23 pastoral associations (the lowest administrative unit), and each pastoral association is composed of villages. Of these, only eight pastoral associations (PAs) were relatively accessible. A settlement of pastoralists in Borana Zone is characterized by clustering of households with close proximity to each other in a village. According to BZDPED, the altitude of the zone ranges from 1,650 in the north to 1,000 m above sea level in the south. The climate is generally semiarid with annual average rainfalls ranging from 300 mm in the South to >700 mm in the North. The rain pattern is of a bimodal type with the main rainy season (Ganna) extending from March to May and the small rain season (Hagayya) from September to November. The other two seasons are the cool dry season (Adolessa) extending from June to August and the major dry season (Bona) from December to February. Sample size and sampling procedure The study animals were lactating camels that were kept under traditional management system of pastoralist area of Borana Zone. Sample size was calculated using the formula for simple random sampling (Thrusfield 2005) with 66.8 % expected prevalence (Bekele and Molla 2001), 95 % confidence level, and 5 % desired absolute precision. Accordingly, the estimated sample size was determined to be 348 camels. Regarding the sampling procedure, Yabello district was selected purposively due to its accessibility. Of the eight relatively accessible PAs of Yabello district, half (four) PAs

Milk sample collection, bacterial isolation, and identification Each camel was sampled once, and the sampling time was either early in the morning or late in the afternoon at the time of milking based on the owner's milking schedule. Before sampling, teats were disinfected with cotton moistened with 70 % alcohol. Then, milk samples were taken aseptically and examined for visible abnormalities and were screened by the California mastitis test (CMT) according to Quinn et al. (1999). From each quarter of the udder, a squirt of milk sample was placed in each of the cups on the CMT paddle, and an equal amount of 3 % CMT reagent was added to each cup and mixed well. The interpretation was in such a way that CMT score 0 was considered as negative, while CMT scores with trace, 1+, 2+, and 3+ were considered as positive, thus forming five categorical classes. The milk samples that were positive for CMT were kept in an icebox and were transported immediately to Yabello

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Regional Veterinary Laboratory for culture. The bacteriological examinations were carried out following standard procedures of National Mastitis Council (NMC 1990). A loopful of each milk sample was streaked on defibrinated sheep blood agar, and the plates were incubated aerobically at 37 °C for 24–48 h. Presumptive identification of the isolates was made based on colony morphologic feature, Gram stain reaction, hemolytic characteristics, and catalase test. Based on the Gram stain, there was pure Gram-positive cocci, pure Gram-negative, and mixed isolates. Mixed isolates are both Gram-positive and Gram-negative isolates recovered from a single specimen after culture. Staphylococci and micrococci were identified based on their growth characteristics on mannitol salt agar. Gram-positive cocci were tested for catalase, and catalase-positive isolates were further tested with DNase and other biochemical tests. Isolates that were tentatively identified as streptococci were evaluated according to CAMP reaction, growth characteristic on Edwards's medium (oxoid), hydrolysis of esculin, reffinose, salicin, and insulin tests. Gram-negative isolates were subcultured on MacConkey agar and were further tested using triple sugar iron agar, testing motility, and the IMViC test (indole, methyl red, Voges–Proskauer, and citrate utilization tests) and by using oxidase test.

Data analysis Data that were collected from 30 households (348 camels) were recorded in Microsoft Excel spreadsheet for statistical analysis. Mastitis positivity of the lactating camels across different categories of categorical variables such as age, parity, lactation stage, physical condition of the camels, the presence of udder/teat lesion, and the pastoral associations were all summarized using percentages. Further, the CMT result was considered as a dependent variable, and the effect of the selected risk factors on the CMT result was analyzed using univariate, multivariable, and stepwise logistic regression analysis using Stata version 9 (Stata-9 2007). In stepwise logistic regression analysis, the fit of the model was evaluated using the likelihood ratio test. The influence of removing each variable included in the final model was also evaluated using change in log-likelihood. As a measure of effect, odds ratio (OR) and 95 % confidence interval (CI) around the OR were used. p values of <0.05 were used to decide on statistical significance of a given estimate.

Results Animal and quarter level prevalence

Questionnaire data collection Questionnaire survey was administered to all the 30 household leaders/heads. The questionnaire was designed to gather information about the study animals such as age, parity and lactation stage, presence of tick infestation, and udder/teat lesions. Data about parity and lactation stage were gathered by interviewing the owners. The parity number record during the study was parity 1 to 6, and it was then categorized into four as categories 1 (first parity), 2 (second parity), 3 (third and fourth parities), and 4 (fifth and sixth parities). Lactation stage was categorized in to three categories as early (1–2 months), middle (3–9 months), and late (10–18 months) to see if there is any significant difference in the occurrence of mastitis during these stages. Age estimation was carried out by dentition. Furthermore, the objectives of the interview were to assess the understanding of the camel breeders about mastitis as disease, its means of transmission, and preventive measures. Activities like premilking udder preparation for hygiene keeping were assessed. The administered questionnaire was approved by the School of Veterinary Medicine, Hawassa University, Ethiopia. The questions were reviewed by all the investigators and other collaborator at Hawassa University and a field Veterinarian in Borana Zone. After a common understanding on the questionnaire, the interview was conducted personally by one of the authors using the structured questionnaire.

A total of 348 lactating camels were examined during the study period clinically as well as subclinically by using CMT. The CMT-based mastitis prevalence was 39.4 % (137/348). Additionally, 19 (5.5 %) camels were found with blind teats, and no samples were taken for CMT and culture. Hence, the animal level prevalence (39.4 %) is based on the CMT result excluding the 19 camels with blind teats. Similarly, of the total 1,392 examined teats, 30 (2.2 %) were blind. Thus, milk samples were taken only from 1,362 teats, out of which 304 teats were found to be positive for CMT. Accordingly, the CMT-based quarter level prevalence was 22.3 % (304/1,362) (Table 1). The CMT positivity significantly (x2 =8.9, p=0.0310) varied among the four quarters with the highest percentage (96, 7.0 %) observed on left quarter. Analysis of risk factors The prevalence of camel mastitis significantly (p<0.05) varied with peasant association, lactation stage, and presence of different types of lesion. Hence, there was a higher likelihood of mastitis occurrence among camels from Dharito (p=0.000, OR = 3.4), Gagna (p = 0.000, OR = 3.4), and Haro Bake (p=0.010, OR=2.6) than camels from Surupha. Likewise, higher likelihood of mastitis occurrence was observed in camels at the early lactation stage (p=0.014, OR=2.3) and among the camels with udder/teat lesions (p=0.020,

Trop Anim Health Prod Table 1 The number and proportion of CMT-positive teats and blind teats in each quarters with respect to the different categories of reactivity (n=1,392) Quarters

Number of blind teat (n=30)

CMT-positive teats (n=1,362)

Proportions Comparison

No. (%) of positive teats in each category

Total no. (%) CMT

Trace

+

++

+++

Positive

Left Hind Left front

8 (0.6) 6 (0.4)

54 (4.0) 49 (3.6)

27 (2.0) 17 (1.2)

11 (0.8) 4 (0.3)

4 (0.3) 0 (0.0)

96 (7.0) 70 (5.1)

x2 =8.9

Right hind Right front Total

10 (0.7) 6 (0.4) 30 (2.2)

44 (3.2) 33 (2.4) 180 (13.2)

17 (1.2) 19 (1.4) 80 (5.9)

8 (0.6) 6 (0.4) 29 (2.1)

8 (0.6) 3 (0.2) 15 (1.1)

77 (5.7) 61 (4.5) 304 (22.3)

p=0.0310

OR=13.7) than camels at late lactation stage and camels with healthy udder/teats, respectively. No association was observed between mastitis prevalence and the remaining risk factors (age, parity, and tick infestation) (Table 2). Culture result From the 304 CMT-positive-cultured milk samples, 264 (86.8 %) were culture positive. Of the 264 growths, 197 Table 2 Association between selected risk factors and CMT positivity (mastitis) of lactating camel in Borana Zone, Southern Ethiopia

Risk factors

No. of tested

No. (%) of positive

Crude OR (95 % CI)

Adjusted OR (95 % CI)

Adjusted OR and 95 % CI from SWLR

PA Surupha

112

42 (37.5)

1

1

1

96 65 75

36 (37.5) 29 (44.6) 49 (65.3)

2.3 (1.2, 4.6) 3.1 (1.7, 5.9) 3.1 (1.7, 5.8)

2.5 (1.2, 5.1) 3.4 (1.8, 6.7) 3.5 (1.8, 6.6)

2.6 (1.3, 5.1) 3.4 (1.8, 6.5) 3.4 (1.8, 6.4)

18 174 134 22

6 (33.3) 77 (44.3) 59 (44.0) 14 (63.6)

1 1.6 (0.6, 4.4) 1.8 (0.6, 4.4) 3.5 (0.9, 13.0)

1 1.9 (0.6, 6.2) 1.4 (0.4, 18.2) 2.8 (0.4, 5.3)

67 69 186 26

27 30 84 15

(40.3) (43.5) (45.2) (57.7)

1 1.1 (0.6, 2.2) 1.2 (0.7, 2.2) 2.0 (0.8, 5.1)

1 1.0 (0.5, 2.2) 1.2 (0.3, 6.1) 1.4 (0.5, 2.7)

107 190 51

41 (38.3) 86 (45.3) 29 (56.9)

1 1.6 (1.1, 3.0) 2.2 (1.1, 4.2)

1 1.6 (1.1, 3.0) 2.4 (1.1, 4.8)

204

84 (41.2)

1

1

Positive 144 Udder/teat lesion Present 12 Absent 336

72 (50.0)

2.1 (0.9, 3.7)

1.6 (1.0, 2.6)

11 (91.7) 145 (43.2)

1 14.5 (1.8, 113.5)

1 11.3 (1.4, 94.3)

Haro Bake Gagna Dharito Age <5 6–9 10–14 15–18 Parity 1st 2nd 3rd to 4th 5th to 6th Lac.S 10–18 m 3–9 m 1–2 m Tick Negative No. number, OR odds ratio, CI confidence interval, SWLR stepwise logistic regression, PA peasant associations, BCS body condition score, mmonth, Lac.S lactation stage

(64.8 %, n=264) were Gram positive, 41 (15.5 %) were Gram negative, and 26 (9.8 %) were mixed isolates (mixed growth of Gram positive and Gram negative). From the remaining 40 (13.1 %, n=304) samples, no bacterial growth was observed. Based on the culture growth, the highest prevalence was recorded for Staphylococcus aureus (12.8 %, 39/304), followed by Streptococcus dysgalactiae (10.5 %), Staphylococcus hyicus (8.9 %), Bacillus species (7.6 %), Streptococcus agalactiae (7.2 %),

1 1.5 (1.2, 2.9) 2.3 (1.1, 4.6)

1 13.7 (1.7, 109.4)

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DNase-negative Staphylococcus (5.6 %), Streptococcus uberis (4.3 %), Staphylococcus intermedius, and Micrococcus species (3.9 % each). Likewise, the quarter level prevalence of each pathogen was also recorded with the highest isolation rate of S. aureus (2.9 %, 39/1,362), followed by the above respective bacteria (Table 3). Questionnaire result Of the 30 household heads interviewed, 70.1 % were aware of mastitis as disease and locally call “Buda (dhiiga bahu)” for acute mastitis and “dhukkubaa gurruu” for chronic mastitis. However, they are not aware of subclinical mastitis. They thought that they can control the spread of the disease by milking affected camels at the end of milking. Most respondents (57 %) do not aware of the way of transmission of disease and its control. They milk the entire herd in the same container (that made from locally available tree wood), and milking is usually carried out by one person. While preparing utensils for milking, they wash and smoke milking utensils with “Qoraasuma” before milking, considering it will improve the shelf life of milk. Qoraasuma is a local name of olive tree, and they use it as a disinfectant. Of the 30 interviewed individuals, the majority of respondents (90 %) reported that they are not practicing washing their hands prior to milking, and 96.7 % of camel owners explained the use of anti-suckling device to protect continuous calf suckling. This was done by tying two pairs of teat together with tree fiber, and this can result in trauma which in turn predisposes to mastitis. Table 3 Number and relative proportion of bacterial isolates from pure culture growth of camel milk taken from CMT-positive quarters

a

Growth rate=(Number of isolates for each bacteria)/(Total number of growth=304)×100

Gram stain result

Discussion The overall prevalence (44.8 %) of camel mastitis in the current study was higher than the reports of Abera et al. (2010) who reported an overall mastitis prevalence of 29 % in Jijiga Zone, Somali Regional State, Ethiopia. However, the prevalence report in the current study is lower than the report from Afar Region, North Eastern Ethiopia (59.8 %) by Bekele and Molla (2001), and 66.8 % prevalence from Sudanese camel herds by Obied et al. (1996). On the other hand, the proportion of clinical (5.4 %) and subclinical (39.4 %) mastitis reported in the current study is consistent with the finding of Megersa (2010) who reported a prevalence of subclinical mastitis ranged from 28.6 to 37.6 % and clinical mastitis ranged from 10 to 17 % in dromedary camels in Borana area of Southern Ethiopia. Regarding the clinical mastitis, the finding of this study is also in agreement with the 5.9 % prevalence report of Abdurahman et al. (1995) in Sudan. Abera et al. (2010) also recorded 8.3 % prevalence of clinical mastitis in Jijiga. A relatively lower prevalence of 2.1 % clinical mastitis was also reported by Woubit et al. (2001). On the other hand, higher clinical mastitis prevalence of 15, 17, and 19.5 % was also recorded by Barbour et al. (1985) in Saudi Arabia, Megersa (2010) in Borana, Southern Ethiopia, and Obied et al. (1996) in Sudan, respectively. In this study, the presence of udder/teat lesions was observed to be one of the important risk factors for the occurrence of mastitis. It is one of many factors that predispose camels to mastitis as the lesions facilitate bacterial entry and

Bacterial species

Number of isolates

Growth ratea (95 % CI) (n=304)

Quarter level prevalence (95 % CI) (n=1,362)

Gram positive

Staphylococcus aureus Staphylococcus hyicus Staphylococcus intermedius DNase-negative Staphylococcus Streptococcus dysgalactiae Streptococcus agalactiae Streptococcus uberis Micrococcus species Bacillus species Subtotal

39 27 12 17 32 22 13 12 23 197

12.8 (9.4, 17.2) 8.9 (6.1, 12.8) 3.9 (2.1, 6.9) 5.6 (3.4, 9.0) 10.5 (7.4, 14.6) 7.2 (4.7, 10.9) 4.3 (2.4, 7.4) 3.9 (2.1, 6.9) 7.6 (5.0, 11.3) 64.8 (59.1, 70.1)

2.9 (2.1, 4.0) 2.0 (1.4, 2.9) 0.9 (0.5, 1.6) 1.2 (0.7, 2.0) 2.3 (1.6, 3.3) 1.6 (1.0, 2.5) 1.0 (0.6, 1.7) 0.9 (0.5, 1.6) 1.7 (1.1, 2.6) 14.5 (12.7, 16.5)

Gram negative

Enterobacter species Escherichia coli Klebsiella species Subtotal

15 21 5 41 26 264

4.9 (2.9, 8.1) 6.9 (4.4, 10.5) 1.6 (0.6, 4.0) 13.5 (10.0, 18.0) 8.6 (5.8, 12.5) 86.8 (82.4, 90.3)

1.1 (0.6, 1.9) 1.5 (1.0, 2.3) 0.4 (0.2, 1.0) 3.0 (2.2, 4.1) 1.9 (1.3, 2.8) 19.4 (17.4, 21.6)

Mixed isolates Total

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leaves behind permanent tissue damage (Abdurahman and Younan 2004). Of the 12 camels having udder/teat lesions in the current study, 91.7 % (11/12) were mastitis positive. Penetrating and non-penetrating superficial skin lesions of the udder/teat were observed, and this could be due to the thorny plant in the area. Higher prevalence of mastitis (72.2 %) in camels with udder lesion was also reported by Teketelew and Bayeleyegn (2001) in Afar region and by Woubit et al. (2001) in Borana lowland, Southern Ethiopia. Abdurahman et al. (1995) also explained this fact mentioning that trauma can be responsible directly to mastitis which can predispose the udder to bacteria invasion. On the other hand, the presence of tick was also assessed expecting it as a risk factor for the occurrence of camel mastitis in the study area, but it was not found to be important factor. In the previous studies, it was recorded that tick infestation could predispose udder by creating a favorable situation for the entrance of majority of mastitis-causing pathogens. It was recorded that udder is the predilection site for tick infestation which causes skin and teat lesions (Abdurahman and Younan 2004), although this was not the case in the current study. The significantly higher mastitis prevalence among camels from Dharito, Gagna, and Haro Bake (p<0.05) than Surupha might be due to the higher camel population of the area, and they are the higher milk-producing pastoral associations in the district. Additionally, there could be management variation and lack of experience in the utilization of the veterinary service given in the area. A positive relation was observed between mastitis and stage of lactation in this study with a significantly higher (p=0.02) prevalence in an early stage. This was explained by Radostits et al. (2007) that most new infections occur during the early time of dry period and in the first 2 months of lactation, especially with environmental pathogens. Bacteriologically, camel milk samples showed that Grampositive cocci were the main cause of camel mastitis and constitute 74.6 % (197/264) of the total isolates. The higher report of the Gram-positive cocci in this study is in line with the 75 % prevalence of cocci by Abdul-Gadir et al. (2006) in Dire Dewa and Gewane and 74 % prevalence by Woubit et al. (2001) in Negele Borana. The predominantly higher proportion of S. aureus (19.8 %, 39/197) among the Gram-positive isolates in the current study is also comparable with the report of Woubit et al. (2001) who found 21.1 % S. aureus from the isolates. S. dysgalactiae (16.2 %, 32/197) was the second most common cause of mastitis in the camel herds examined in this study. Similarly, S. agalactiae and S. aureus were reported to be the most common cause of camel mastitis in eastern Sudan (Obied et al. 1996) and in Kenya (Younan et al. 2001) with relative percentage of 12 % for S. aureus and 11 % for S. agalactiae, respectively.

Acknowledgments The study was supported by the Hawassa University, the Yabello Agricultural Research Center, and the Yabello Regional Laboratory. The willingness and cooperation of camel owners were also indispensable inputs for the accomplishment of this study. All contributions and supports are gratefully acknowledged.

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