The prevalence and causes of mastitis in lactating traditionally managed one-humped camels (Camelus dromedarius) in West Pokot County, Kenya

K C Toroitich, G K Gitau¹, P M Kitala and G C Gitao²

Department of Public Health, Pharmacology and Toxicology, Faculty of Veterinary Medicine, University of Nairobi
gkgitau@uonbi.ac.ke
¹ Department of Clinical Studies, Faculty of Veterinary Medicine, University of Nairobi
² Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi

Abstract

A cross sectional study was conducted to determine the prevalence and causes of mastitis in 95 clinically healthy lactating and traditionally managed one-hump camels (Camelus dromedarius) in Kongelai, Kacheliba, Konyao, Kasei, Kiwawa and Alale divisions of West Pokot County, Kenya. Fifty two households were conveniently selected from a list provided by Kenya Camel Association West Pokot County based on the presence of a lactating camel in the household.

A total of 380 quarter milk samples (56 from Kongelai division, 40 from Kacheliba division, 8 from Konyao division, 148 from Kiwawa division, 92 from Kasei division and 36 from Alale division) were collected observing asepsis. The samples were transferred to the laboratory for bacterial culture. Of the 380 quarter milk samples cultured, 169 samples tested positive for subclinical mastitis which gave a prevalence of quarter infection at 44.5% (169/380). At animal (camel) level the prevalence of subclinical mastitis was 76.8% (73/95 camels).Therefore the results of this study have shown that subclinical mastitis is prevalent in dromedary camels of West Pokot County. The same results showed that, the right hind quarter (RHQ) was the most frequently infected quarter (prevalence of 12.1% (46/380)) followed by the right fore quarter (RFQ) (prevalence of 11.3% (43/380)). The two left quarters, left fore quarter (LFQ) &left hind quarter (LHQ) were least infected. This could point out that the Pokot herders tended to milk the right quarters more often and leave the left quarters to be suckled by the calves and because of poor & unhygienic milking procedures the right quarters become more infected.

The most predominant isolated bacterium was gram-positive Staphylococcus aureus with prevalence of 36.0% (49/136) followed by gram-negative Escherichia coli with prevalence of 27.2% (37/136). Streptococcus agalactiae & Staphylococcus epidermidis were the third predominant isolates with prevalence of 9.6% (13/136) each. Micrococcus spp & pseudomonas were the least isolates with less than 1% prevalences. A diagnosis of ‘no bacterial growth’ was made in 22 cases which is 16.2% (22/136). Several mastitis control strategies should be put in place such as milking procedures, milking order, strict hygiene, post milking teat disinfection, use of antibiotic dry-off therapy and the culling of persistently infected camels.

Keywords: dromedary camels, subclinical mastitis, quarter samples, West Pokot, Kenya

Introduction

In spite of it living in harsh environments of semiarid and arid zones, the dromedary camel is able to produce milk in valuable quantity (Schwartz and Dioli, 1992; Faye, 2005). However, like other dairy animals, dromedary camels could be affected by udder infections such as mastitis, a complex disease occurring worldwide among dairy animals, with heavy economic losses largely due to clinical and subclinical mastitis. The later requires indirect means of diagnosis (Matofari et al., 2003). Camel mastitis is both medically and economically important due to its multiple hazardous effects on human health and animal production (Younan, 2004; Akweya et al., 2010; Njage et al., 2010). In addition to these health concerns, mastitis reduces production (Musinga etal., 2008) and quality (Matofari et al., 2003; Mengistu et al., 2010) of milk of traditionally managed camels. In the arid and the semi-arid areas of Kenya (ASALs), milk is consumed fresh or sour posing a health hazard to consumers (Younan, 2004). It has recently come to light (Younan et al., 2001) that infections of the udder of lactating camels are quite widespread. Generally, bacteria in milk can occur through colonization of the teat canal or an infected udder (clinical or subclinical mastitis), or as contaminants (Younan, 2004).

Evidence indicates that subclinical mastitis causes suffering of dairy animals, reduce milk yield, alters milk properties, impairs preservation and processing and is of a public health concern for consumers of camel milk (Fthenakis and Jones, 1990; Tibary and Anouassi, 2000). Very little is known about mastitis concerning their aetiology and occurrence in Camelidae (Abdel Gadir et al., 2006; Kalla et al ., 2008). However, cases of mastitis in camel have recently been reported in Saudi Arabia (Barbour et al., 1985); Egypt (Mostafa et al., 1987); Somalia (Abdurahman et al., 1991); Ethiopia (Bekele and Molla, 2001); Israel (Guliye et al., 2002) and Kenya (Matofari et al., 2003).

Materials and Methods

Description of the Study area

The study was carried out in West Pokot County in the former Rift Valley Province of Kenya as shown in Figure 1.

Figure 1. Map of Kenya showing West Pokot County the study area

The County borders Uganda to the West, Trans Nzoia and Elgeyo-Marakwet Counties to the South, Turkana County to the North and East and Baringo County to the South East. Geographically, it lies between Latitudes 1 ⁰10’ and 3⁰ 40’ N and Longitudes 34⁰ 50’and 35⁰ 50’E (Macmillan Education Ltd., 1999). It has a total area estimated at 9,100 square kilometers and stretches a distance of 132 km from North to South. The County is made up of four sub-counties and14 divisions. The study which took place between the months of August and November 2012 was only carried out in six divisions as shown below in Figure 2.

Figure 2. Map of West Pokot County showing the six study divisions

These divisions are the only divisions with the highest population of camels in West Pokot County and they are located along the border between Kenya and Uganda.

Study Design

The study was a cross-sectional study undertaken on 95 lactating and traditionally managed one-hump camels (Camelus dromedarius) in 52 randomly selected households (manyattas) in West Pokot County. These households (manyattas) were the sampling units.

Data collection

Data on household demographics (human and animal) and known and/or reported diseases of camels, and animal level factors (each camel) such as age, parity number, stage of lactation, breed, current milk yield, milk abnormalities, whether the camel has had mastitis before and presence of udder/teat lesions were collected and recorded in a semi-structured questionnaire (SSQ) during sampling. Data were also gathered through interviews administered to the household head or any other household member conversant with the camel management.

Sample size determination for the number of milk samples

The following formula was used to calculate the sample size (Dohoo et al., 2003):

n = Z_α²pq/L^2, where, n=sample size, Zα = the value of z that gives 95% confidence interval (1.96), p = a priori prevalence (estimated prevalence), q = 1-p and L = allowable error.

The prevalence of mastitis in camels in Kenya was estimated at 25% as was reported by Younan et al., (2001). Thus adopting a p of 25% and L of 5%, then;

n = (1.96²*0.25*0.75)/ (0.05)² = 290 (quarter milk samples).

Collection of milk samples

Prior to the commencement of sample taking, the camel owner’s consent was obtained after explaining the purpose and objective of the study. Milk samples were then aseptically collected from each individual quarter from 95 lactating camels (14 from Kongelai, 10 from Kacheliba, 2 from Konyao, 37 from Kiwawa, 23 from Kasei and 9 from Alale division) during either morning, midday or evening milking time depending on what was logistically convenient. This was done after the calf was allowed to suckle to allow milk let down. Visual examination (by observation and palpation) of all the quarters was also carried out.

About 20 ml of milk was collected from each quarter directly into clean and sterile sample bottles that were clearly labeled and immediately stored in cool boxes with ice packs before refrigeration in the evening at around 5 ⁰C and later transported in cool boxes with ice packs to the Bacteriology Labora­tory at the Department of Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi for bacterial culture.

Bacteriological Examination and Isolations

After culturing, bacteriological examination was carried out following standard methodslaboratory and field handbook on bovine mastitis – (1987), Sears et al – (1993) and Quinn et al – (1994) to identify major bacterial agents associated with mastitis.

Statistical Data Analysis

All data collected were entered in Microsoft Excel 2007 worksheet as database and exported to Instat Plus for statistical analysis. Descriptive statistics were generated using the same statistical package. Differences in proportions were assessed using the chi square at 5% level of significance in univariate analysis.

Results

Characterization of camel milking practices

The results of the study showed that, many Pokot camel owners generally milked their camels thrice a day (90.4% (47/52)); at dawn or early in the morning; at 10 am (limo in Pokot) and at night about 8.00pm (2-3 hours after returning from grazing). Only 9.6% (5/52) milked their camels twice a day. Majority of the milkers (82.7% (43/52)) washed their hands once before milking all livestock beginning with goats, cows and lastly the camels compared with 17.3% (9/52) who do not wash their hands at all. On washing the udder before milking, 76.9% (40/52) do not wash the udder. They believed that the calf would clean the udder by suckling. About 7.7% (4/52) washed the udder before milking. These were mostly camel keepers around trading centres. None respondents were 15.4% (8/52).

Most (75% (39/52)) of the treatment of camel mastitis was done by the owners. Few (26.9% (14/52)) went for some assistance from the Community based animal health workers (CBAHWs). Veterinarians (VOs) and animal health assistance (AHAs) were not consulted on treatment of mastitis. During mastitis infection, 75% (39/52) do not follow the milking order where you start milking the clean camels first and the infected camels last.

Amongst the Pokot people, camels are mostly milked by young boys (herders) (42.3% (22/52)) and adult women (30.8% (16/52)). In the absence of women, the men (26.9% (14/52)) could also milk the camels as shown in Table 1.

Household demographics

Age and sex distribution

Of the 52 households interviewed 86.5% (45/52 households) were headed by males and 13.5% (7/52 households) were headed by females. 100% (52/52) of the households were settled in communal land; therefore most of the camels were reared in communal range land. The age brackets of the camel owners were <20 yrs 3.8% (2/52); 21-30 yrs 15.4% (8/52); 31-40 yrs 36.5% (19/52); 41-50 yrs 26.9% (14/52); 51-60 yrs 9.6% (5/52) and >60 yrs 7.7% (4/52) as in Figure 3 below. Majority of the camel owners were between 31 and 40 years of age while the least were below 20 yrs and above 60 years of age.

Figure 3. Age and sex distribution of the households' heads interviewed

Laboratory results on bacterial culture and identification

A total of 380 quarter milk samples (56 from Kongelai division, 40 from Kacheliba division, 8 from Konyao division, 148 from Kiwawa division, 92 from Kasei and 36 from Alale) from 95 apparently clinically healthy dromedary camels were collected and cultured in the laboratory to identify subclinical mastitis and its causative agents.

Prevalence of subclinical mastitis at animal (camel) level in the study area

The overall animal (camel)-level prevalence of subclinical mastitis in the study area was 76.8% (73/95) out of which 23.2% (22/95 camels) had only one mammary quarter affected, 21.1% (20/95 camels) had two quarters affected, 17.9% (17/95 camels) had three quarters affected while 14.7% (14/95camels) had all the four quarters affected.

According to divisions, subclinical mastitis at animal level was highest in Kongelai division (100% (14/14)) followed by Kasei division (82.6 % (19/23) then Kacheliba division (80% (8/10)). The lowest prevalence was in Konyao division at 0% (0/2) prevalence as shown in Figure 4 below.

Figure 4. Prevalence of subclinical mastitis at animal (camel) level per division

Prevalence of subclinical mastitis at quarter level

Out of the 380 quarter samples cultured for bacteria, 44.5% (169/380) tested positive for subclinical mastitis giving a prevalence of quarter-level mastitis at 44.5% while the rest 55.5% (211/169) of the samples tested negative (Table 2).

The results showed that the right quarters were more affected compared to the left quarters with a prevalence of 23.4% (89/380) and 21.1% (80/380) for right and left quarters respectively.

The results further showed that the RHQ was the most frequently infected quarter at a prevalence of 27.2% (46/169) followed by the RFQ at a prevalence of 25.4% (43/169) (Figure 5).

Figure 5. Prevalence of subclinical mastitis per quarter

Bacterial Isolation Analysis

The bacteria isolated from the 380 quarter samples were as shown in Table 3 and Figure 6 below. A total of 114 bacteria were isolated with the most predominant bacterium being Staphylococcus aureus with prevalence of 36.0% (49/136) followed by Escherichia coli with prevalence of 27.2% (37/136). Streptococcus agalactiae and Staphylococcus epidermidis were the third predominant isolates with prevalence of 9.6% (13/136) each. Micrococcus spp & pseudomonas were the least isolates with less than 1% prevalence. A diagnosis of ‘no bacterial growth’ was made in 22 cases which is 16.2% (22/136). There were no contaminated samples recorded. Overall all milk samples produced mixed types of bacterial growth in the primary cultures. This indicated that there was a multiple infection of the quarter

Figure 6. Bacterial isolation rates and their prevalences

Discussion

The observed milking frequencies practiced by the Pokot herders in this study were in agreement with earlier studies in Kenya by Schwartz and Dioli (1992) which indicated that milking frequencies depends on season, yield and stage of lactation, the availability of alternative food and the sex and the health of the calf. McGovern (1995) reported that in times of wet seasons the Pokot people milk their camels up to 4 times a day (morning, noon, evening and night), but in dry seasons the frequency is reduced to a single milking at night only.

The high overall prevalence (44.5 %) of bacterial isolates from apparently normal camel milk samples indicated a high percentage of subclinical mastitis in camels in West Pokot County. However, the present finding from this study was con­sistent with the findings from Woubit Salah et al. (2001) who reported high preva­lence (51 %) of mastitis in dromedary camels in Borena areas of South-Western Ethiopia.

The most predominant bacterium isolated from this study wasStaphylococcus aureus with prevalence of 36.0% followed byE. coli with prevalence of 27.2% andStreptococcus agalactiae & Staphylococcus epidermidis at 9.6% prevalence each. This finding is in agreement with other findings from Eastern Sudan by Obied et al., (1996), Ethiopia (Workneh et al., 2002; Kerro and Tareke, 2003; Biffa et al,. 2005 and Almaw et al., 2008) and from Kenya by Younan et al., (2001) who reported that Staphylococcus aureus and Streptococcus agalactiae were the most common causes of camel mastitis. It has also been reported in Kenya (Maina, 1984, Omore, 1997) that Staphylococcus aureus was the major cause of subclinical mastitis in bovine (63%). As was also described by Younan et al. (2001), the prevalence of Staphylococci varies according to different studies, but there is nearly no publication on bacteriological hygiene of milk where Staphylococci are not mentioned (Eberlein, 2007).

The prevalence of E. coli has been reported by other authors to be between 1.0 and 17.3 % in samples taken from healthy camels (El-Jakee, 1998; Abdel Gadir et al., 2005). Therefore the prevalence of E. coli from this study is higher than what has been reported earlier in other studies.

The results further showed that there was cross infection from different quarters of individual camels and from camels within the same herd because identical pathogens were isolated from them. The above suggested that there was strong probability of direct transmission by the milkers from one camel to another through poor milking procedures.

Given that consumption of raw camel milk is a common occurrence among camel keepers in Kenya, the results from this study have indicated the importance of pasteurization of camel milk before consumption since potentially infective bacterial agents were isolated.

Most of the bacteria isolated in this study were gram-positive cocci. This finding is in agreement with what was reported previously by Obied et al., (1996) and Woubit et al., (2001).

The results also indicated that the most affected quarters were the right quarters with high prevalence of 48.4% in the right hind quarter (RHQ) and 45.3% in the right fore quarter (RFQ). This suggested the likelihood that in most cases during milking, the calf was left to suckle the left quarters and the right quarters were milked by the owners and due to poor hygienic milking procedures these quarters were at a higher risk of getting infected.

The results further showed that the Pokot commonly keep camels together with other livestocks such as cattle, sheep and goats. During milking of the livestock, it was observed that the camels were the last to be milked therefore there was a high possibility of direct transmission of mastitis pathogens from other species of livestock to the camel. It was also noticed during this study that camel herders (mostly young boys) kept on milking camels throughout the day during grazing. This practice might have also contributed to the higher transmission rates of camel mastitis among camels in the same herd. Frequent milking and suckling by the calf keeps flushing the mastitis pathogens out but some studies have shown that it is the major cause of mastitis in camels (Obeid et al., 1996; Abdurahman, 1996).

The results also showed that most Pokot pastoralists were using various traditional herbs to manage camel mastitis. This is consistent with what has been observed elsewhere as reported by Bornstein, (1993) and Hussein, (1993) who reported that pastoralists use various traditional (ethno-veterinary) practices to treat sick camels in Ethiopia.

Conclusions

• Since the main pathogens isolated from camel milk samples in this study were bacteria that cause both environmental and contagious mastitis, this study concludes that proper management of lactating camels and adequate hygienic conditions of the environment were not observed optimally and are therefore required in order to minimize occurrence of mastitis in the study areas.
  
  
• More efforts are required to improve the general udder health in order to prevent and control subclinical mastitis in camels.
  
  
• It can also be concluded from the results of this study that mastitis was prevalent in camels in West Pokot and was a serious problem that affected camels that were essential for livelihoods of many nomadic tribes that live in the ASAL.

Acknowledgements

This study was supported by ASAL-Based Livestock and Livelihood Support Project (ALLPRO). We thank the camel keepers for allowing us to access their camels.

References

Abdel Gadir A E, Hildebrandt G, Kleer J N, Molla B, Kyule M and Baumann M 2005 Prevalence and risk factors of camel (Camelus dromedarius) mastitis based on bacteriological examinations in selected regions of Ethiopia. J. Camel Pract. Res. 12, 33 - 36

Abdel Gadir A E, Hildebrandt G, Kleer J N, Molla B, Kyule M and Baumann M P 2006 Comparison of California Mastitis Test (CMT), Somatic Cell Count

Abdurahmann, O A S, Bornstein S, Osman K S, Abdi A M and Zakrisson G 1991 Prevalence of mastitis among camels Emir. J. Food Agric. 2011. 23 (1): 48-58 http://ejfa.info 56 in South Somalia: a pilot study. Mogadishu, Somalia, Somali Acad. Arts and Sci., p. 1-9 (Camel forum working paper 37)

Abdurahman O A S 1996 The detection of subclinical mastitis in the Bactrian camel ( Camelus bactrianus) by somatic cell count and California mastitis test. Vet. Res. Commun., 20, 9-14

Akweya B A, Gitao C G and Okoth M W, 2010 The prevalence of common milk pathogens and antibiotic resistance of the organisms in milk from North Eastern province. Proceedings of the International Camel Symposium held in Garissa on 7^th -11 ^th June 2010.

Almaw G, Zerihun A and Asfaw Y 2008 Bovine mastitis and its association with selected risk factors in smallholder dairy farms in and around Bahir Dar, Ethiopia. Trop. Anim. Hlth Prod., 40(6), 427-432

Barbour E K, Nabbut N H, Frerichs W M, Al-Nakhli H M and Al-Mukayel A A 1985 Mastitis in Camelus dromedarius in Saudi Arabia. Trop. Anim. Hlth Prod., 17: 173-179

Bekele T and Molla B 2001 Mastitis in lactating Camels (Camelus dromedarius) in Afar Region, North-Eastern Ethiopia. Berl. Munch. Tierz. Woch., 114(5-6),169-172

Biffa D, Debela E and Beyene F 2005 The Intern. J. Appl. Res. Vet. Med., 3 (3), 189.

Bornstein S 1993 Camel health and disease veterinary projects. In: Hjort af Ornäs, A. (Ed.), The multipurpose camel. interdisciplinary studies on pastoral production in Somalia. Environmental Policy and Society (EPOS), Uppsala, Sweden, pp. 189- 205

Eberlein V 2007 Hygienic status of camel milk in Dubai (United Arab Emirates) under two different milking management systems. Doctorate thesis, Veterinary Faculty, Ludwig-Maxmillians Universitat Munchen, 120 pp

El-Jakee J 1998 Microbiological studies on mammary glands of one humped she-camels in Egypt. J. Camel Pract. Res. 5, 243-246

Fthenakis G C and Jones J E T, 1990 Subclinical mastitis and milk loss. Brit. Vet. J., 146, 43

Guliye AY, Van Creveld C and Yagil Y 2002 Detection of subclinical mastitis in dromedary camels (Camelus dromedarius) using somatic cell count and the N-acetyl-beta-D-glucosaminidase test. Trop. Anim. Hlth. Prod., 34, 95-104.

Hussein M A 1993 Traditional practices of camel husbandry and management in So­malia. In: Hjort af Ornäs, A. (Ed.), The multipurpose camel: interdisciplinary stud­ies on pastoral production in Somalia. Environmental Policy and Society (EPOS), Uppsala, Sweden, pp. 123-140

Kalla D J, U, Butswat I S R, Mbap S T, Abdussamad A M, Ahmed M S and Okonkwo I 2008 Microbiological Examination of camel (Camelus dromedarius ) milk and sensitivity of milk microflora to commonly available antibiotics in Kano, Nigeria Sav. J. Agric. 3, 1-8.

Maina P W 1984 Study of bovine mastitis control in Nyeri, Kenya. M.Sc. thesis University of Nairobi, Kenya.

Matofari J W, Mario Y, Mwatha E W and Okemo P O, 2003 Microorganisms associated with sub-clinical mastitis in the Kenyan camel ( camelus dromedaries). J. Trop. Microbiol. Biotechnol., 2(1), 11-16

Mengistu F, Molla B and Ali A 2010. Camel mastitis, associated with bacterial pathogens and its impact on milk quality in Gewane district, Afar regional state, North Eastern Ethiopia. Bull. Anim. Hlth. Prod. Afri., 58,249 -259.

Mostafa A S, Ragab A M, Safwat E E, El-Sayed Z, Abd-el-Rahman M, El- Danaf N A, and M T Shouman M T 1987 Examination of raw she-camel milk for detection of subclinical mastitis . J. Egyp. Vet. Med. Assoc., 47,117-128

Musinga M, Kimenye D and Kivolonzi P 2008 The camel milk industry in Kenya: Results of a study commissioned by SNV to explore the potential of camel milk from Isiolo District to access sustainable formal markets

Njage P K M, Jans C, Wanjohi J, Farah Z, Lacroic C and Meile L 2010 Biodiversity and genotyping of Staphylococci isolated in raw milk in East Africa. Proceedings of the International Camel Symposium held in Garissa on 7^th -11^th June 2010.

Obied A I, Bagadi H O and Muctar M M 1996 Mastitis in Camelus dromedaries and somatic cell count of camel’s milk: Res. Vet. Sci. 61, 55-58

Omore A 1997 Epidemiology and economics of mastitis in small holder dairy sector of Kiambu District, Kenya. A PhD thesis University of Nairobi

Schwartz H J and Dioli M 1992 The One-humped Camel in Eastern Africa: A pictorial guide to Diseases, Health Care and Management. Verlag Joseph Margraf Publ. Germany, 282 pp

Tibary A and Anouassi A 2000 Lactation and udder diseases. International Veterinary Information Service (www.ivis.org). Reproductive Disorders in the Female Camelid

Woubit S, Bayleyegn M, Bonnet P and Jean-Baptiste S 2001 Camel (Camelus dromedarius) mastitis in Borena lowland pastoral areas, southwestern Ethiopia. Revue Élev. Méd. Vet. Pays Trop., 54 (3-4), 207-212

Workneh S, Bayleyegn M, Mekonnen H and Potgieter L N D 2002 Bovine Mastitis: Prevalence, Risk Factors and Major Pathogens in Dairy Farms of Holeta Town, Central Ethiopia Vet. World, 3(9), 397- 403

Younan M, Ali Z, Bornstein S and Müller W 2001 Application of the California mastitis test in the intramammary Streptococcus agalactiae and Staphylococcus aureus infections of camels (Camelus dromedarius) in Kenya. Prev. Vet. Med., 51, 307-316

Younan M 2004 Milk hygiene and udder health. Milk and meat from the camel, handbook on product and processing. Farah and Fischer, Eds. Vdf Hochschulverlaf AG an der ETH Zurich, Zurich/Singen 2004; pp67-76

Received 7 July 2016; Accepted 15 February 2017; Published 1 April 2017

Go to top