| Livestock Research for Rural Development 30 (3) 2018 | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
This study for the first time reports the composition and microbial quality of raw camel milk produced in Tsabong, south western Botswana. Milk samples were obtained from dromedary camels kept at Tsabong Ecotourism Camel Park and examined for physicochemical properties and microbial quality. The milk samples analyzed had average total solids, solids-not-fat, fat, protein, lactose, pH, titratable acidity, specific gravity and ash contents of 12.2 ± 0.75%, 10.2 ± 0.61%, 2.0 ± 0.14%, 1.8 ± 0.19%, 2.9 ± 0.16%, 6.35 ± 0.09, 0.163 ± 0.019% lactic acid, 1.027 ± 0.01 and 0.77 ± 0.13%, respectively. The average (log10 cfu/ml) total plate and coliform counts of the milk samples were 3.1 ± 0.97 and 3.9 ± 1.46, respectively. Staphylococcus aureus and Salmonella were detected in 20% of the samples tested. The results suggest that the microbial quality of camel milk produced in Tsabong is generally poor. Thus, this calls for strict hygienic measures during production and handling and the need for heat treatment of the milk in order to improve the quality and safety of camel milk produced in Tsabong.
Keywords: Africa, dromedary, hygiene, Kgalagadi
Dromedary camels (Camelus dromedarius) play an important role as a primary source of subsistence in the Middle East, North and East Africa. They live in arid and semi-arid areas, which are not suitable for crop production and where other livestock species hardly thrive. The primary reason for keeping camels in these areas is milk production although transportation and meat production are also important services provided by camels. In arid and hot environments, camels are the preferred dairy animals and they produce more milk for a longer period of time, even, during the dry season than local cattle (Bekele et al 2002). Farah (1993) reported that camels are very reliable milk producers during dry seasons and drought years when milk from cattle, sheep and goats is scarce. At such times camels can contribute up to 50% of the nutrient intake of the people.
The advantage of camels in arid or marginal areas is that the camel needs little or no supplementation for milk production as compared to full supplementary feeding for cattle. Apart from producing milk, camels can also be used as tourist attraction. In some areas, owners provide camel rides and in turn get income. The camel is also used as a means for transportation and for domestic use such as drawing water from wells, rivers and dams (Farah 1993).
Camel milk is considered as one of the most valuable food sources for nomadic people in arid and semi-arid areas and has been consumed for centuries due to its nutritional values and medicinal properties (Kenzhebulat et al 2000; El Zubeir and Nour 2006; Farah et al 2007; Lorenzen et al 2011). It is considered to have anti-cancer (Magjeed 2005) and anti-diabetic (Agrawal et al 2005; Agrawal et al 2011) properties. Camel milk contains high levels of iron and vitamin C (Mullaicharam 2014; Sharma and Singh 2014). The high vitamin C content of camel milk is of significant importance for human health especially in arid and desert environments where green vegetables and fruits are not readily available.
In Botswana, camels are kept in Tsabong which is a semi-arid region in Kgalagadi District. They are kept in an enclosed park known as Tsabong Ecotourism Camel Park. The camels are under the care of the local community with the help of Botswana Tourism Organization. Despite the potential of camels in Botswana, no research has been carried out on camels or their products to date. Camels kept in Tsabong are mainly used for tourism (riding) purpose. The camels are hand milked in an open kraal under unhygienic conditions. The milk produced is consumed raw and is not processed into value-added products. To date, no study has been conducted to assess the quality of camel milk produced in Tsabong. This study was, therefore, conducted to determine the chemical composition, microbial quality and safety of camel milk produced in Tsabong.
Tsabong is the administrative center of the Kgalagadi District located in south western Botswana. The human population of the area was 8939 according to the 2011 census. The geographical coordinates of Tsabong are 26° 3' 0" South, 22° 27' 0" East. The study area, Tsabong Ecotourism Camel Park, is found in this region and is located at a distance of 520 km from the capital city Gaborone and 10 km north of Tsabong town. The area is characterized by poor and unreliable rainfall with an annual precipitation of less than 250 mm and with an average ambient temperature of above 35°C during summer and less than 2°C in winter (Kgaudi 2014). The area has sparsely distributed vegetation dominated by Acacia and Grewia species and some species of grass.
Milk samples were collected from dromedary camels kept in Tsabong Ecotourism Camel Park in March 2016. A total of ten camels that were in the same stage of lactation were randomly selected among the lactating camels and used as a source of milk. All the camels gave birth in July 2015 and thus the camels were at their 8th months of lactation at the time of milk collection. Raw milk samples (250 ml) collected from 10 individual camels were placed into sterile bottles and transported to the laboratory by placing them in a cooler box. Up on arrival at the laboratory, the samples were kept in the refrigerator at 4°C (<24 h) pending analysis. The samples were analyzed for chemical composition, total viable count, coliform count and were also tested for presence of the pathogens Salmonella and Staphylococcus aureus.
The pH of milk samples was measured using digital pH meter (Richardson 1985). Titratable acidity was determined according to AOAC (2000). Specific gravity of the milk samples was determined by a Lactometer according to O’Connor (1995). Total solids (TS) content was determined according to AOAC (2000). Fat content was determined by the Gerber method (Richardson 1985). Solids-not-fat (SNF) content was determined by difference as reported by Harding (1995). Total nitrogen (N) content was determined by the Kjeldahl method as described by the International Dairy Federation (IDF 1993). The crude protein content of milk was calculated by multiplying N by 6.38. The ash content was determined according to Bradley et al (1993). Lactose content was estimated by quantitative Benedict method (Harvey and Hill 1967).
Milk samples were diluted in 0.1% peptone water and mixed thoroughly. After preparation of serial dilutions up to 10-8, volumes (1 ml) of appropriate dilutions were plated by the pour plate technique in duplicate using standard plate count agar (Oxoid, Hampshire, England). Colonies were counted after incubation at 32°C for 48 hours (Roberts and Greenwood 2003).
Enumeration of total coliforms was done using Violet Red Bile Agar (VRBA) (Oxoid, Hampshire, England) as follows. Nine ml of sample was aseptically transferred into 90 ml of sterile peptone water and decimal dilutions of up to 10-6 were prepared. Duplicate dilutions from each dilution level were plated by pipetting 1 ml of the dilution onto sterile petri dishes and adding molten agar (VRBA) and mixing the content. The agar was allowed to set and an overlay of a thin layer (about 5 ml) of sterile VRBA was added. Then the agar was allowed to solidify and the plates were incubated inverted at 30°C for 48 hours (McLandsborough 2004). Pink colonies surrounded by bile precipitation were counted as coliforms.
Staphylococcus aureus was detected according to McLandsborough (2004) as follows. Nine ml of sample was aseptically transferred into 90 ml of sterile peptone water and mixed thoroughly, then decimal dilutions up to 10-6 were prepared. Dilutions were mixed thoroughly and plating was done in duplicate by transferring 0.1 ml from each dilution level onto the surface of Baird Parker Agar medium (Oxoid, Hampshire, England). Glass rod spreader was sterilized by flaming in alcohol and used to quickly spread the inoculum over the surface of the media, by starting with the highest dilution. The agar was allowed to solidify and the plates were incubated inverted at 37°C for 48 hours.
For confirmation test, sterile loop was used to pick one representative colony of presumptive Staphylococcus aureus colony and inoculate into 2 ml of brain heart infusion (BHI) broth. The BHI broth was incubated at 37°C for 24 hours. After incubation, 0.2 ml of the culture was mixed with 0.5 ml of EDTA coagulase plasma. This was incubated in water bath at 37°C for 24 hours and examined for agglutination. In addition, Gram stain was done in order to observe the cell morphology.
Salmonella spp. was detected according to the procedure outlined by the Food and Drug Administration (FDA 2001). Twenty five ml of milk was pre-enriched in 225 ml of buffered peptone water at 37°C for 24 hours. Then, 10 ml of pre-enrichment sample was incubated in Selenite Cystine Broth at 42°C for 24 hours. About 0.1 ml of the selective enrichment was then streaked onto Xylose Lysine Desoxycholate agar plates (Oxoid, Hampshire, England). The plates were then incubated at 37°C for 24 hours. Cells of typical colonies with large, glossy black centers or that appear almost completely black were picked and observed under the microscope to determine their cell arrangement and shape.
Descriptive statistics was used to analyze the data generated using the SPSS software. Quantitative data are presented as mean with standard error. Prevalence of pathogens is presented as percentage of total samples analyzed.
Average values for the physicochemical parameters of camel milk produced in Tsabong are indicated in Table 1. Fat content of camel milk obtained in this study agrees with the fat content of 1.8 to 5.0% reported by Khaskheli (2005) for camel milk produced in Pakistan. Meiloud et al (2011) reported average fat content of 2.92±0.59% for Mauritanian camel milk. On the other hand, Kouniba et al (2005) reported a fat content of 2.65% for camel milk produced in Morocco. The low fat content observed in the present study could be attributed to the feed of the camels in the study area. The composition of fatty acids in camel milk is influenced by environmental factors such as nutrition and physiological factors such as stage of lactation as well as difference in the breed of the animal (Farah et al 1989).
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Table 1. Physiochemical properties of camel milk produced in Tsabong |
|
|
Variables |
Mean ± SEM |
|
Fat % |
2.0 ± 0.14 |
|
Lactose % |
2.9 ± 0.161 |
|
Protein % |
1.8 ± 0.19 |
|
Total solids % |
12.2 ± 0.75 |
|
Solids-not-fat % |
10.2 ± 0.61 |
|
Ash % |
0.77 ± 0.13 |
|
pH |
6.35 ± 0.09 |
|
Titratable acidity (% lactic acid) |
0.163 ± 0.019 |
|
Specific gravity |
1.027 ± 0.01 |
|
SEM = standard error of the mean. |
|
The lactose content of camel milk observed in the present study (Table 1) is slightly lower than the value of 3.1±0.5% reported by Dowelmadina et al (2014) for camel milk produced in Sudan. Khaskheli et al (2005) reported that the lactose content of camel milk produced in Pakistan varied from 2.91 to 4.12 %. Large differences in lactose content may be associated to nutrition of the animal, that is, dependent on the kinds of plants which the animals feed on (Khaskheli et al 2005).
The protein content of camel milk observed in the current study (Table 1) is within the range of 1.8-3.20 % reported by Khaskheli (2005) for protein content of camel milk produced in Pakistan. However, it is lower than the value 2.1-2.5% reported by Raghvendar et al (2003) for protein content of camel milk from India. Other studies reported higher values: 3.90% (Dukwal et al 2007), 4.02% (Mukasa-Mugerwa 1981) and 4.50% (Knoess 1976) for camel milk protein. It is reported that protein content of the feed as well as water intake can have a direct effect on the protein content of camel milk (Yagil 1982). Stage of lactation also has a profound effect on protein content of milk. Looper (2013) reported that the concentration of milk fat and protein is highest in early and late lactations and lowest during peak milk production through mid-lactation.
The total solids content of camel milk observed in the present study (Table 1) is in line with other reports. Khaskheli (2005) reported total solids content for camel milk ranging from 7.76 to 12.13%, whereas Dowelmadina et al (2014) reported the value 11.9 ±1.5% for total solids content of camel milk produced in Sudan. The ash content of camel milk observed in the present study (Table 1) is also in line with values reported by earlier workers. Omer and Eltinay (2008a) reported an ash content of 0.88% for camel milk from United Arab Emirates. Sesh et al (2012) on the other hand reported ash content ranging from 0.60-1.0% for camel milk from India.
The pH of fresh camel milk observed in the present study (Table 1) is lower than pH value (6.5-6.7) reported by Yagil (1982) for camel milk. However, it is higher than the pH value 5.67 reported for raw camel milk from Algeria (Benyagoub and Ayat 2015). It appears that camel milk is slightly acidic as compared to cow’s milk which has an average pH value of 6.7. The titratable acidity of camel milk observed in the present study (Table 1) is in agreement with the values 0.19% and 0.133% lactic acid reported by Babiker and El-Zubeir (2014) and Omer and Eltinay (2008a), respectively for camel milk from Khartoum State of Sudan.
The specific gravity of camel milk observed in the present study (Table 1) is in line with earlier reports. Benyagoub and Ayat (2015) reported a density of 1.0268 g/ml for camel milk from Algeria. On the other hand, Omer and Eltinay (2008a) reported a density of 1.028 g/ml for camel milk from Sudan. It seems that camel milk has lower density as compared to cow’s milk, which has an average specific gravity of 1.032. The solids-not fat (SNF) content of camel milk observed in this study (Table 1) is higher than the values 8.49%, 8.03% reported by Babiker and El-Zubeir (2014) and Jemmali et al (2016) for solids-not-fat content of camel milk produced in Sudan and Tunisia, respectively. Khaskheli (2005) also reported a lower SNF content of 7.12% for camel milk from Pakistan. The higher SNF content observed in the present study could be attributed to the lower percentage of fat in the camel milk.
In general, the fat, protein and lactose contents of milk of camels kept in Tsabong is lower than values reported in the literature. This variation could be attributed to the feed of the animals, stage of lactation, parity and breed of the camels. Further study is needed to investigate the effect of each of these factors on the composition and quality of camel milk produced in Tsabong.
The average total plate count (TBC) of camel milk observed in the present study (Table 2) is lower than the values 5 log10 cfu/ml, 5.4 log10 cfu/ml and 5.6 log10 cfu/ml TBC reported by Al-Mohizea (1994), Semereab and Molla (2001), El-Ziney and Al-Turki (2007), respectively for camel milk. It is also lower than the values 5.2 log10 cfu/ml 5.25 log10 cfu/ml for aerobic plate count reported by Adugna et al (2013) and Omer and Eltinay (2008b) for camel milk produced in eastern Ethiopia and in the United Arab Emirates, respectively. High total bacterial counts in raw milk mainly reflect poor hygienic condition under which the milk was handled and poor health of milking animals (Hayes and Boor 2001). The microbiological quality of raw milk should be of major concern to the producers, the processors and the general public because bacteria in milk can degrade milk components, decrease shelf life and acceptability of processed products, and cause illnesses in human beings (Hayes and Boor 2001).
The mean coliform count (CC) observed in the present study (Table 2) is greater than the CC values 2.9 log10 cfu/ml, 1.4 log 10 cfu/ml and 2.83 log10 cfu/ml reported by Adugna et al. (2013), El-Ziney and Al-Turki (2007) and Omer and Eltinay (2008b) for camel milk produced in eastern Ethiopia, Saudi Arabia and the United Arab Emirates, respectively. However, it is lower than the CC of 6.8 log 10 cfu/ml reported by Benkerroum et al. (2003) for Moroccan camel milk. The high coliform count observed in the present study could be attributed to fecal contamination of the milk and poor sanitary practices during milking and handling of the milk.
Generally, the quality of camel milk produced in Tsabong is poor. Camels in Tsabong are hand milked in an open kraal exposed to manure and dirt. Milk is collected in unsanitised plastic containers which may pose a health risk to the public consuming unpasteurized milk. Milking in an area which is full of dust and dung and without shade could have a negative impact on the quality of the milk produced in terms of presence of pathogenic microorganisms. Thus, education of the farm workers about the importance of sanitary milking practices would help solve the problem in the future. Washing of the udder and teats of the camels before milking is not practiced in the farm. Besides, it was observed that the milkers do not wash their hands and the milking vessels prior to milking camels. Thus, hygienic milking procedures and hygienic production systems should be followed in order to increase milk production and improve the quality and safety of camel milk produced in Tsabong.
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Table 2. Mean total plate and coliform counts (log10 cfc/ml) of camel milk produced in Tsabong |
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Variable |
Mean ± SEM |
|
|
Total plate count |
3.1 ± 0.97 |
|
|
Coliform count |
3.9 ± 1.46 |
|
|
SEM = standard error of the mean. |
||
Staphylococcus aureus was detected in two of the ten camel milk samples (20%) analyzed (Table 3). This is much higher than the values reported earlier. Abera et al (2011) reported that S. aureus was detected in 7.14% of camel milk samples examined in north eastern Ethiopia. Similarly, Asfour and Anwer (2015) reported that S. aureus was detected in 3.33% of camel milk samples tested in Egypt. On the other hand, Semereab and Molla (2001) reported higher rates (31.5%) of isolation of S. aureus from camel milk in Afar region of Ethiopia.
Salmonella species was detected in two of the ten camel milk samples (20%) analyzed (Table 3). Isolation of Salmonella spp. from camel milk in the present study is in line with the report of Adugna et al (2013) who found Salmonella in camel milk produced in eastern Ethiopia. Detection of Salmonella in the camel milk samples is of major public health concern since all Salmonella species are pathogenic. This calls the need for proper hygienic measures during production and handling of camel milk and mandatory pasteurization of the milk before consumption.
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Table 3. Isolation and detection of Salmonella and Staphylococcus aureus from camel milk produced in Tsabong |
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|
Samples |
Salmonella |
Staphylococcus aureus |
|
1 |
Not detected |
Not detected |
|
2 |
Detected |
Detected |
|
3 |
Not detected |
Not detected |
|
4 |
Not detected |
Not detected |
|
5 |
Not detected |
Not detected |
|
6 |
Detected |
Detected |
|
7 |
Not detected |
Not detected |
|
8 |
Not detected |
Not detected |
|
9 |
Not detected |
Not detected |
|
10 |
Not detected |
Not detected |
The authors would like to thank Tsabong Ecotourism Camel Park workers for their assistance during the camel milk sample collection. We would also like to extend our appreciation to Botswana Tourism Organization for giving us permission to collect camel milk samples from the park. This study was funded by the Department of Tertiary Education of Botswana.
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Received 14 December 2017; Accepted 30 January 2018; Published 1 March 2018