Livestock Research for Rural Development 18 (8) 2006 Guidelines to authors LRRD News

Citation of this paper

Udder health and milk quality among camels in the Errer valley of eastern Ethiopia

O A Sh Abdurahman

Division of Comparative Reproduction, Obstetrics and Udder Health, Department of Clinical Sciences,
Swedish University of Agricultural Sciences (SLU), P. O. Box 7054, SE-750 07 Uppsala, Sweden
omar_abdurahman@yahoo.com
(Present address: Swedish Board of Agriculture, 551 82 Jönköping, Sweden)

Abstract

Quarter milk samples (n=205) from 53 camels were examined to study the occurrence and causes of mastitis in traditionally managed camels in the Errer valley of eastern Ethiopia and to observe factors affecting udder health.

The study revealed tick infestation and lesions on the teats and udder skin 26 (49,1%). Seven (3.3%) camels had blind teats and 5(9.4%) had clinical mastitis. Seventy-seven (37.6%) quarters yielded bacteria. Staphylococcus aureus, Streptococcus agalactiae and coagulase negative staphylococci were the main organisms isolated. A high proportion (80%) of bacteria positive milk samples had CMT score 2 or more, while a similar proportion (80%) of bacteriologically negative samples showed CMT score 1. Quarters infected with bacteria had significantly higher mean values for somatic cell counts than non-Infected ones log12.5 and 13.6 respectively. The demographic parameters of age, parity, and lactation stage did not influence the ability to predict whether a quarter was normal, when judged on percentage correctly classified. The significance of the findings in relation to production system, hygiene and public health aspects were discussed.

It is concluded that early problem recognition and improved hygienic measures will result in reduced losses due to mastitis and increase the availability of milk for consumption and sale.

Key words: camels, Horn of Africa, mastitis, milk hygiene, udder health


Introduction

Countries in the Horn of Africa i.e. Ethiopia, Somalia, Sudan, Kenya, Djibouti and Eritrea have proportionately higher number of camels (one humped) than any other part in the world (FAOSTAT database 2005). In recent years, the region has witnessed frequent famine and competition for scarce resources leading to ethnic conflicts and instability. Camels are important milk producers in arid lands and camel milk is an essential food for livelihood of people and it may be the only milk available in places where other milking animals cannot be maintained. In pastoral conditions, milk is always consumed either fresh or in varying degrees of sourness, in the raw state without heat treatment, and it can pose a health hazard to the consumer.

Despite the importance of camel milk in this region, camels have not been selected for milk production. As a result detailed milk production data are scanty. The length of lactation varies from 8 to 18 months and total lactation yields are from 800 to 3600 litres with mean daily yields ranging from 2.8 to 11.0 litres (Wilson 1984). Camel milk is popular among pastoralists and has been steadily gaining popularity among urban dwellers in many countries (Mehaia 1993) with milk processing plants equipped with modern small-scale pasteurisation facilities to collect and distribute pasteurised milk to consumers. The industrial production of camel milk cheese was suggested to overcome the seasonal fluctuations in milk supply and demand (Abeiderrahmane 1997). In addition, procedures for the manufacture of camel milk products such as ice cream (Abu-lehia et al 1989), butter (Farah et al 1989) and soft and hard cheese (Mohamed and Larsson-Raznikiewicz 1990; Mehaia 1993) have been studied. In the UAE for example a survey on health and lifestyle showed that one in every six UAE nationals in urban areas regularly consumes camel's milk and this ratio goes up significantly in the peripheral regions and rural areas (Kazmi 2002).

Mastitis means inflammation of the mammary gland. Bacterial infections are considered the primary causes of mastitis in domestic animals. There are few data concerning the aetiology, occurrence and pathogenesis of mastitis in the genus Camelidae (Abdurahman et al 1995; Abdel Gadir et al 2006). As in other dairy animals, clinical mastitis in the camel can be detected by examination of the udder, the milk, or both. Detection of sub-clinical mastitis is, however, difficult and depends on various test procedures aimed at detecting the cause or products of inflammation in milk (IDF 1987). Methods for evaluating somatic cells in milk and their threshold values are developed for dairy cows. In an earlier study we have attempted to evaluate the somatic cell contents (SCC), California mastitis test (CMT), Adenosine triphosphate (ATP), N-acetyl-D-glucosamimidase (NAGase) and Serum albumin as indirect diagnostic tools for infected and non-infected quarters of the camel mammary gland (Abdurahman 1995a,b; Abdurahman et al 1995; Abdurahman 1998). There has been a problem in interpreting the results because the basal levels of cells and their physiological variations in the camel were and are still not yet established (Abdurahman et al 1992). As camels are important dairy animals in arid lands, information on the udder health situation is essential for future development. This work was carried out to monitor udder health and milk hygiene, determine udder pathogens and to detect udder inflammation using milk SCC and CMT.


Materials and methods

The area

Errer is situated approximately 25 km east of the ancient city of Harar with an altitude ranging from 1300 m in the south to 1600 m in the north. There are two main rainy seasons, one during March-April and the other during July September. Shrubs and thorny bushes of acacia and cacti origin dominate the vegetation.

Study herds and sampling procedure

Camel milking is a labour intensive activity, especially morning milking when camels are desired to be on browsing before the peak of the tropical heat and humidity. During preparatory visits we followed and observed their working routines and our sampling procedure was adjusted to minimize disruption of their work routines. Trial sampling performance was exercised so that sampling was finished in time and camels released for grazing without delay.

Camels were kept by nomadic pastoralists under traditional management. All camels that were lactating and accessible during the visit were sampled. Information on age, lactation stage, parity, milk yield was gathered. Few camels were still milking at 18 months postpartum. Visual observation and palpation of the mammary gland quarters was done and macroscopic examination of the milk streaks was undertaken in strip cups for the presence of abnormal colour, consistency, flakes and other abnormalities.

Camels in Africa's horn are milked by hand. The calf is allowed to suckle for a short time, prior to milking, to stimulate milk letdown. Teat ends were cleaned with cotton moistened in 70% alcohol. The first streams of milk from each quarter were discarded, and about 5 to 10 ml of foremilk were collected into 10-ml polyethylene tubes. Some of the milk sample was used for preparation of smears for SCC. The remaining milk was frozen and transported to Uppsala, Sweden for further analysis.

Bacteriological examination

Milk was thawed at room temperature and samples (0.01 ml) from each quarter were streaked on blood agar plates and incubated for 48 hours at 37°C. Individual colonies were picked for identification according to the routine procedure of Swedish National laboratory, SVA, based on the Scandinavian recommendations (Klastrup 1975).

California Mastitis Test (CMT)

CMT was carried out principally according to Schalm and Noorlander's (1957) method. An equal volume of CMT reagent and milk was mixed and the reaction was graded 1, 2, 3, 4, or 5 according to the Scandinavian recommendations (Klastrup and Schmidt Madsen 1974).

Microscopic somatic cell counts (SCC)

The milk samples were allowed to reach room temperature and shaken carefully before smearing. Milk samples (0.01 ml) were spread over 1 cm2 of an ordinary alcohol pre-cleaned glass slide by means of a micro-syringe (Applied Research Institute, New York, USA). Four such squares were prepared from each sample. The film was dried, stained with methylene blue (Prescott and Breed 1910) and examined under oil immersion using Zeiss microscope. An attempt was made to count only nucleated cells.

Statistical analysis

Because of the skewed distribution, SCC values were transformed to "log base 10" prior to statistical calculations. Data were tabulated and analysed by least square analysis of variance using the general linear models (glm) procedure of the statistical analysis system SAS (2003). The effects of age, parity, lactation stage, presence of ticks were analysed using LSM and SE of the mean. Age of camels varied between 5 and 24 years and was grouped into 3 categories (5-9, 10-14 and ≥15. Lactation stage was grouped into 3 categories (0-1, 2-3 and ≥3 months). Parity was grouped into five categories (1, 2, 3, 4, and ≥5).


Results

The camels examined belonged to 22 herds composing of 362 camels. Of these 266 were mature female camels. Table 1 shows age structure (1a), parity (1b), lactation stage (1c) and milk yield (1d) on the 53 clinically examined and studied camels.

Table 1a.   Age distribution

Age

Number of animals n=53

percent

1

25

47.2

2

14

26.4

3

14

26.4

Table 1b.  Number and percentage distribution of parity

Parity

Number of animals n=53

percent

1

20

37.7

2

11

20.8

3

3

5.7

4

7

13.2

5

12

22.6

Table 1c.  Distribution of lactation stage

Lactation stage

Number of animals n=53

percent

1

8

15.1

2

9

17.0

3

36

67.9

Table 1d.  Daily milk yield among studied camels

Milk yield/liter

Number of animals n=53

percent

2

10

18.9

4

19

35.8

5

14

26.4

6

7

13.2

7

2

3.8

8

1

1,9

The age of the camels examined varied from 5 to 25. Clinical examination of udders revealed tick infestation (49.1%) and lesions on the teats and udder skin were widespread. Seven (3.3%) camels had blind teats where passage of milk was obstructed and 5  had clinical mastitis manifested by swollen udder, sometimes accompanied by enlarged mammary lymph glands, severe thelites, and visible alteration on the strip cup of the colour and consistency of milk. Of 205 quarter milk samples cultured 77 (37.6%) yielded bacteria. Results of bacteriological examination are shown in Table 2a and b. Micro-organisms recovered were; Staphylococcus aureus, Streptococcus agalactiae, Streptococcus equisimilis, Streptococcus spp, coagulase negative staphylococci, Micrococcus spp. Twenty-two (10.7%) quarter milk samples yielded unspecified mixed cultures, and 128 (62.4%) yielded no bacterial growth.


Table 2a.  Bacteriological finding of quarter milk samples

Bacteria isolated

n=205

percent

Staphylococcus aureus

26

12.7

Streptococcus agalactiae

18

8.8

Streptococcus equisimilis

1

0.5

Streptococcus spp

1

0.5

Coag neg staphylococci

8

3.9

Micrococcus spp

1

0.5

mixed flora

22

10.7

No growth

128

62,4

Table 2b.  Bacteriological finding of quarter milk samples

Bacteria isolated

n=77

percent

Staphylococcus aureus

26

33.8

Streptococcus agalactiae

18

23.4

Streptococcus equisimilis

1

1.3

Streptococcus spp

1

1.3

Coag neg staphylococcus

8

10.4

Micrococcus spp

1

1.3

mixed bacteria

22

28.5

Table 3 shows distribution of CMT scores in relation to the bacteriological finding (presence or absence of bacterial finding). 80% of bacteria positive milk samples had CMT score 2 or more, while 80% of bacteriologically negative samples had CMT score 1.

Table 3.   CMT distribution in relation to bacteriological findings

CMT score

Bacteria negative

percent

Bacteria positive

percent

Total

1

105

82.7

22

17.3

127

2

17

43.6

22

56.4

39

3

6

19.6

25

80.7

31

4

0

0

5

100

5

5

0

0

3

100

3

Total

128

62.4

77

37.6

 

Quarters infected with bacteria had higher LS mean values for somatic cell counts than non-infected quarters (P < 0.0001). Inclusion of the mastitis indicators SCC and CMT in addition to the demographic variables of age, parity, and lactation did not influence the ability to predict whether a quarter was normal, when judged on percentage correctly classified. Somatic cells from inflamed and non-inflamed udder quarters are shown in figures 1a and 1b respectively.

Figure 1a.  Somatic cells from inflamed camel udder

Figure 1b.  Somatic cells and cell fragments from non-inflamed camel udder

In inflamed quarters polymorph nuclear granulocytes dominate the section. The dominant cells in non-inflamed quarters were epithelial cells and cell fragments.


Discussion

Mastitis continues to be the most important economic disease problem among dairy cows worldwide (Radostits et al 2000). Camels are still multipurpose animal increasingly kept for milk, but specialization is maybe on the way (Abdurahman 2005). Reports of mastitis in traditionally managed camels are on the rise and are likely to increase further as the milk production per individual camel is increased. Two decades ago there was no mention of mastitis problem at herd level; today it is reported from almost all camel rearing countries (Mohammed et al 2005, Abdurahman and Younan 2004, Khedid and Soulaimani 2003, Guliye et al 2002, Bekele and Molla 2001, Al-Ani and Al-Shareefi 1997, Al-Mohizea 1986, Mostafa et al 1987). Whether the occurrence of the disease has earlier been underestimated, or an upsurge of the disease took place due to dairying interest remains unclear. However, it is an undeniable fact that camels are kept in infrastructure and resource poor marginal areas. In addition, the multi-purpose nature of the animal, the subsistence production system, and the prevalence of other major diseases occupies the concerns of herders and specialists. Early problem recognition and improved hygienic action reduce the losses due to mastitis.

It has been reported that camels lack a milk cistern and therefore do not store milk in the udder, so the duration of milk letdown is short (Yagil et al 1999). First the calf is allowed to suckle to stimulate milk letdown and then the calf is removed and usually two men (each two teats) carry out milking as fast as they can.  Herders try to avoid any distraction at milking time as that can stop the milk flow entirely. It is important to avoid stress during milking and observe familiar routines during sampling.

The udder is a predilection site for tick infestation which causes skin and teat lesions, facilitates bacterial entry and leaves behind permanent tissue damage. Lesions due to ticks and poor udder hygiene (Abdurahman et al 1995, Obeid et al 1996, Woubit et al 2001) are a big problem to overcome if udder health and milk hygiene is to be improved. It is a good practice to remove ticks even when the animal is not lactating. This can be done by gripping the tick as close to the host's skin as possible and removing it by a gentle rotation and firm downwards pulling motion. This will strip the tick's mouthparts encased in the cement material from the host's skin, sometimes leaving a small wound that might bleed for a few minutes. The potential danger of ticks transmitting infection will also be avoided. In traditional husbandry practice, fibres from plants are tied to the teat to prevent the calf from sucking the dam. This device is damaging to the udder and is predisposing to mastitis. A major improvement among Errer herders is that teats are no longer tied with fibres and we found none, although lesions of teat and udder skin are still prevalent.

In the present study milk bacteriology was done on frozen milk samples. Sanchez et al (2003) reported that frozen milk samples can be useful in goat sub-clinical mastitis control programs. In another study, freezing of milk had no effect on bacteria isolated from cow's milk (Schukken et al 1989). The bacteria isolated from camel milk are known mastitis-causing organisms in the cow, sheep and goat. Staphylococcus aureus, Streptococcus agalactiae and coagulase negative staphylococci seem to be important udder pathogens in the camel (Abdurahman 1996) as in other dairy animals. However, the camel has not been the subject of experimental mastitis studies and the epidemiology and pathogenicity of mastitis causing organisms remain unclear. Camels affected by mastitis are reported to have considerably shorter lactation periods (Barbour et al 1985). The disease is not usually treated in traditionally managed camels and will often take a natural course to chronicity resulting in permanent loss of milk production (Abdurahman et al 1991, Obeid et al 1996).

An increase in the number of somatic cells, particularly granulocytes, in camel milk is a good indication of inflammation. As in the cow, the intensity of the cellular reaction correlates with the degree of irritation of the mammary gland. However, a cellular fragment in the size range of somatic cells found in camel milk makes both enumeration and differentiation of somatic cells difficult (Abdurahman et al 1992). CMT reagent reacts only with deoxyribonucleic acid present in nucleated cells and gives a good estimate of the number of somatic cells in camel milk as well.

Poor management and unhygienic milking practices prevalent in the traditional husbandry systems include tying the teats with soft parks to prevent the calf from suckling, tick infestations and cauterisation of the udder skin (Abdurahman et al 1995, Obeid et al 1996, Almaw and Molla 2000, Woubit et al 2001). It is therefore cheaper and easier to prevent mastitis by improving hygienic measures than to treat by medication. The cost of the latter includes veterinary fee, cost of medicine and loss of milk production.


Acknowledgements

The author expresses his gratitude to EARO and the Errer pastoralists for their cooperation and help. This study was supported by Sida/Sarec (Swedish International Development Cooperation Agency).


References

Abdel Gadir Atif E, Hildebrandt G, Kleer J N, Molla B, Kyule M N and Baumann M P 2006 Comparison of California Mastitis Test (CMT), Somatic Cell Counts (SCC) and bacteriological examinations for detection of camel (Camelus dromedarius) mastitis in Ethiopia Berl Munch Tierarztl Wochenschr 119 1-2:45-9

Abdurahman O A Sh 1995a Milk N-acetyl-B-D-glucosaminidase and Serum Albumin as Indicators of Subclinical Mastitis in the Camel, Journal of veterinary medicine A 42, 643-647.

Abdurahman, O A Sh 1995b The detection of subclinical mastitis in the camel(Camelus bactrianus) using somatic cell count and California mastitis tests Veterinary Research Communication 20, 9-14.

Abdurahman O A Sh 1996 Studies on Mastitis in the Camel: Cytological, Bacteriological and Diagnostic Aspects. Doctoral thesis, Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala.

Abdurahman O A Sh 1998 Detection of subclinical mastitis in camels: relationship between udder infection and inflammatory indicators in milk. In Bonnet P (editor) Dromadaires et chameaux, animaux laitiers/Dromedaries and camels, milking animals. Actes du colloque 24 - 26 octobre 1994, Nouakchott, Mauritanie. Montpellier, France, Cirad p. 31 - 34.

Abdurahman O A Sh 2005 Udder health, milk quality and constraints to camel pastoralism in the Horn of Africa. Structures of vulnerability: mobilisation and resistance. Interdisciplinary research conference, Stockholm University 12th-14th of January.

Abdurahman O A Sh, Agab H, Abbas Band Astrom G 1995 Relations Between Udder Infection and Somatic cells in Camel(Camelus dromedarius) Milk, Acta Veterinaria Scandandinavica 36 4, 423-432.

Abdurahman O S, Bornstein S, Osman K S, Abdi A M and Zakrisson G 1991 Prevalence of mastitis among camels in Southern Somalia: a pilot study Camel forum, Working paper No 37, Somali Academy of Arts and Sciences.

Abdurahman O S, Cooray R and Bornstein S 1992 The Ultrastructure of Cells and Cell Fragments in Mammary Secretions of Camelus bactrianus, Journal of veterinary medicine A 39, 648-655.

Abdurahman O and Younan M 2004 Udder health, In Farah and Fischer (editors) Milk and Meat from the camel, handbook on product and processing. Vdf Hochschulverlag AG an der ETH Zurich, Zurich/Singen Page 73-76.

Abeiderrahmane N 1997 Camel milk and modern industry. Journal of Camel Practice and Research,. 4: 223-228

Abu-Lehia I H, Al-Mohizea I.S and El-Behry M 1989. Studies on the production of ice cream from camel milk products Australian Journal of Dairy Technology 44 1 31-34

Al-Ani F K and Al-Shareefi, M R 1997 Studies on mastitis in lactating one humped camels (Camelus dromedarius) in Iraq. Journal of Camel Practice and Research 4 1, 47-49.

Almaw G and Molla B 2000 Prevalence and etiology of mastitis in camels (Camelus dromedarius) in eastern Ethiopia, Journal of Camel Practice and Research 7 1 97-100.

Al-Mohizea I S 1986 Microbial quality of camels' raw milk in Riyadh markets, Egyptian Journal Dairy Science, 14 173-180.

Barbour E K, Nabbut N H, Frerichs W M, Al-Nakhil H M and Al-Mukayel A A 1985 Mastitis in Camelus dromedarius in Saudi-Arabia, Tropical Animal Health and Production 17 173-179.

Bekele T and Molla B 2001 Mastitis in lactating camels(Camelus dromedarius) in Afar Region, North-eastern Ethiopia, Berl Munch Tierarztl Wochenschr 114 5-6 169-72.

FAOSTAT database 2005 http://faostat.fao.org/faostat/collections?subset=agriculture

Farah Z, Streiff T and Bachmann M R 1989 Manufacture and characterization of camel milk butter. Milchwissenschaft 44: 412-414.

Guliye A Y, Van Creveld C and Yagil R 2002 Detection of subclinical mastitis in dromedary camels (Camelus dromedarius) using somatic cell counts and the N-acetyl-beta-D-glucosaminidase test, Tropical Animal Health and Production, 34 2 95-104.

IDF (International Dairy Federation) 1987 Bovine mastitis: Definition and Guidelines for Mastitis Diagnosis Bulletin- International Dairy Federation no 211, Brussels, Belgium.

Kazmi A 2002 Camel's milk more nutritious than cow's Gulf news, online edition http://archive.gulfnews.com/articles/02/07/20/58230.html

Khedid K, Faid M and Soulaimani M 2003 Microbiological characterisation of one humped camel milk in Morocco, Journal of Camel Practice and Research 10 2 169-172

Klastrup O 1975 Nordic recommendations of quarter milk samples. Annual Bulletin. International. Dairy Federation. 85 41-52.

Klastrup O and P Schmidt Madsen 1974 Nordic recommendations concerning mastitis control of quarter samples. Nordisk Veterinar Medicine 26 197-204.

Mehaia M A 1993 Fresh soft white cheese (Domiati-type) from camel milk: composition, yield and sensory evaluation. Journal of Dairy Science 76 2845-2855 http://jds.fass.org/cgi/reprint/76/10/2845

Mohamed M A and Larsson-Raznikiewicz M 1990 Hard cheese making from camelmilk Milchwissenschaft 45 11 716-718

Mohammed A, Ruiz-Bascaran M and Abera B 2005 Cross-sectional study of mastitis in camels (Camelus Dromedarius) In Somali Region, Southeastern Ethiopia Bulletin of Animal Health and Production in Africa 53 3 195-201

Mostafa A S, Ragab A M, Safwat E E, El-Sayed Z, Abd-el-Rahman M, El-Danaf N A and Shouman M T 1987 Examination of raw she-camel milk for detection of subclinical mastitis, Journal Egyptian Veterinary Medical Association, 47 117-128.

Obeid A I, Bagadi H O and Mukhtar M M 1996 Mastitis in Camelus dromedarius and the somatic cell content of camels' milk, Research Veterinary Science 61 1 55-58.

Prescott, S C and Breed R S 1910 The determination of the number of body cells in milk by a direct method. Journal of Infectious Diseases 7 632- 640.

Radostits C, Gay C, Blood D C, Hinchcliff K W and Arundel J H 2000 A Textbook of the Diseases of Cattle, Sheep, Pigs, Goats and Horses, 8th edition, London, Balliere Tindall.

Sanchez A, Contreras A, Jimenez J, Luengo C, Corrales J C and Fernandez C 2003 Effect of freezing goat milk samples on recovery of intramammary bacterial pathogens, Veterinary Microbiology 94 1 71-77.

SAS Users Guide 2003 Statistics Version 6 Edition, SAS Inst, Inc, Cary, NC, USA.

Schalm O W and Noorlander D O 1957 Experiments and observations leading to development of California Mastitis Test Journal Of American Veterinary Medical Association, 130 199-204.

Schukken Y H, Grommers F J, Smit J A, Vandegeer D and Brand A 1989 Effect of freezing on bacteriologic culturing of mastitis milk samples. Journal of Dairy Science 72 7 1900-1906.

Wilson R T 1984 The Camel, Longman, London and NewYork

Woubit S, Bayleyegn M, Bonnet P et J ean-Baptiste S 2001 Camel (Camelus dromedarius) mastitis in Borena lowland pastoral area, Southwestern Ethiopia, Revue d'Elevage et de Medecine Veterinaire des Pays Tropicaux 54 (3/4) : 207-212

Yagil R, van Creveld C, Abu-R'Kaik G and Merin U 1999 Milk "let-down" in camels. Journal of Camel Practice and Research 6 1 27-29.


Received 4 April 2006; Accepted 30 June 2006; Published 6 September 2006

Go to top