Mastitis occurrence and constraints to mastitis control in smallholder dairy farming systems in Uganda

D K Byarugaba, J L Nakavuma, M Vaarst* and C Laker**

Department of Veterinary Microbiology and Parasitology, Faculty of Veterinary Medicine, Makerere University,
P.O. Box 7062, Kampala, Uganda
dkb@vetmed.mak.ac.ug
*Danish Institute of Agricultural Sciences, P.O. Box 50, DK - 8830 Tjele , Denmark
**Farming in Tsetse control areas (FITCA) Project Ministry of Agriculture, Animal Industry and Fisheries, Entebbe

Abstract

A study was conducted in the district of Jinja in Uganda to explore the pattern of mastitis including the occurrence of antibiotic resistant mastitis pathogens and to understand the constraints that limit effective control of mastitis in smallholder dairy farming systems.  A questionnaire was administered to 60 farmers to collect data regarding their farm circumstances and management of their farms and the risk factors to mastitis. Quarter milk samples were collected from the milking cows and screened for mastitis using the California Mastitis Test (CMT). The milk samples were cultured for isolation of pathogens and assessment of their susceptibility to commonly used antibiotics. A total of 172 milking cows were sampled corresponding to 688-quarter milk samples.

The prevalence of CMT-positive cows was 61.3%, of which sub-clinical mastitis was 60.7%. The levels of hygiene on most of the farms were very low. Farmers had no knowledge on sub-clinical mastitis. Staphylococcus species were the most common isolates and more than 50% of the isolates were resistant to the commonly used antibiotics penicillin and tetracycline.  

Key words: Antimicrobial resistance, hygiene, milking cows, zero-grazing

Introduction

Smallholder dairy production in Uganda contributes significantly to the incomes of the poor and middle class urban dwellers, who typically keep 1-5 cows that are either pure exotic (most often a Holstein-Friesian type of cow) or crosses between exotic and local breeds. However there are still many constraints that limit maximal production among these intensive smallholder dairy farming systems including limited feed resources, uncontrolled market factors and diseases (Nakiganda et al 2006).

Bovine mastitis is described as one of the major constraints and most costly diseases in dairy production that limit enhanced milk production efficiency in many dairy herds despite the amount of knowledge available on the subject (Hogeveen  2005). It is a complicated problem associated with almost every conceivable factor of management and the environment (Blood and Radostitis 1989).

Earlier studies in Uganda have reported high prevalence levels and variations among risk factors (Okello-Uma and Gibson 1976, Nakavuma et al 1994, Byarugaba et al 1998, Kintu et al 2000). Some of these risk factors responsible for the high prevalence have been described including among others poor hygiene, management practices as well as cow factors (Kivaria et al 2004, Mdegela et al 2004, van Schaik et al 2005).  The level of infection can, however, be reduced to an economically feasible minimum (Omore 1997, Hall et al 2004). Several control options including improvement in management are available aiming at reducing the rates of new infections and or the duration of existing infections (Brown et al 1998). The adoption of these control options however depend on the ability of the farmer to comprehend the problem and its associated risk factors as well as other factors that limit milk production efficiency. Effective control therefore requires understanding of the farming system, the constraints that limit milk production efficiency and the risk factors under each particular farming system and different farm circumstances and adoption of possible and affordable options for control. A study was carried out from 2002-2004 with the objective to investigate major constraints to effective mastitis control among smallholder farming systems in Jinja, Uganda.

The aim of this article is to present and discuss the occurrence of mastitis and constraints to mastitis control including antibiotic resistance in mastitis pathogens in smallholder dairy farms in Jinja, in order to identify potential mastitis control measures relevant to smallholder dairy farmers.

Materials and methods 

Selection  of herds

In order to include a broad spectrum of herds working under widely different circumstances, we included Jinja Municipality (urban), Mafubira, Kakira, Mpumudde (peri-urban), Budondo and Butagaya (rural) sub-counties. The study involved 60 randomly selected smallholder (1-15 cows) dairy farms according to described procedures (Martin et al 1987), which were intensively or extensively managed and included zero-grazed and free-grazing cows (either tethered or paddocked). A total of 172 cows on these farms were included in the study.

Data collection

Questionnaire survey

A questionnaire was administered to 60 participating farmers, who answered questions about occupation, education, farm management and animal husbandry practices including disease control methods, distribution of work and responsibilities related to this, hygiene, knowledge about mastitis, and associated disease problems were obtained. The questions were asked by an extension agent during milking, where observation and verification of some of the information could be done.

Mastitis occurrence

Quarter milk samples were indirectly screened for somatic cell count level by means of California Mastitis Test (CMT) as described by Hogan et al (1999). The CMT result was scored basing on the gel formation and categorized as negative if there was no gel formation, or positive  if the there was gel formation ranging of 1+ or more. Mastitis was therefore defined at cow level if one or more quarters were CMT positive or at quarter level if the quarter was CMT positive with or without isolation of microorganisms in both cases. Individual quarter milk samples were also cultured for isolation and identification of the pathogens using standard procedures (Carter et al 1991). Based on an estimated mastitis prevalence of 70% (other studies in Uganda) and at 95% confidence interval, samples were collected from 172 cows. Quarter samples were cultured on routine bacteriological media (Blood agar, Nutrient agar and MacConkey agar) and incubated aerobically at 37°C for up to 48h. The isolates were tested for their susceptibility to antibiotics by the Bauer-Kirby disc diffusion method against a panel of antibiotics including erythromycin, penicillin, oxacillin, ampicillin, gentamycin, sulfa-trimethoprim and tetracycline and results interpreted according to the disc manufacturers (Remel, USA)

Data analysis 

All the collected data was entered into Epi Info database (Coulomber et al 2001) and descriptive statistics and data analysis was carried out in SPSS version 11.5 (SPSS Inc. 2002) after data editing. Desriptive statistics in terms of frequency distributions and contingency tables with CMT+/- as outcome variable of the various variables are presented.

Results

Description of the farms and characteristics of the farmers

The demographic characteristics of the farmers are summarized in Table 1. Most of the farmers were peasant farmers without formal employment and with almost an equal distribution of male and female farmers most of whom had secondary school education but there was no significant difference in the occurrence of mastitis accounted for by the difference in the demographic characteristics of the farmers.

The farming system in smallholder dairy was mainly characterized by predominantly zero grazing (71.7%) fed on cut and carry elephant grass and supplementation with grain or concentrate during milking  with herds of 1-5 cows with an average milk production in the herds was 242 kg per month (SE  =  13.76). Cows were mainly kept in open shelters with concrete floors. In most cases, no beddings (81.4%) were provided. Most of the cows (75%) were exotic breeds and had higher CMT positivity as compared to the crosses and only a few local indigenous breeds none of which had mastitis at the time of the survey (Table 2). There were also variations in other cow-related risk factors to mastitis. The cows were mainly kept inside by walls made of wood or barbed wire (68.3%) and water was provided ad libitum (89.5%), throughout the day mainly from piped water (63.3%) and the houses were mainly cleaned using spade only.

Farmer’s knowledge, practices and perceptions related to mastitis

Many of the farmers (83.3%) had knowledge about clinical mastitis but none of them knew about subclinical mastitis and most of them considered mastitis a major constraint to their milk production (Table 3). A small fraction believed the disease arose from contaminated beddings or environment (36.8%), through milker’s hands (37.9%) and other means (23%).  The majority checked for mastitis at milking time and could tell that a cow had clinical mastitis from the symptoms, or change in milk production levels. Many of the farmers (72.9%) accessed information about mastitis from extension agents. 

All farmers hand milked their cows mainly twice (96.6%) a day and most (66.7%) did not follow any particular order of milking of the cows. Most of the farmers cleaned the milking place after milking (72.2%), using a spade only and a few with water only. Almost all milkers (98.3%) cleaned their hands before milking each cow using water and soap (78.9%) or water (21.1%) only while the udder was washed or cleaned before milking by 95% of the respondents using water only (66.7%) and others with water and soap (19.3%). The milking was done by employees (52.5%), family members (30.5%) or both (16.9%), depending on whoever was available.   

Methods used for mastitis control on the farms

The majority of the farmers controlled mastitis by treating the clinical cases and only one respondent practiced dry cow therapy and one was practicing teat dipping as illustrated in Figure 1.

Animals with chronic mastitis were sold off (16.7%), slaughtered (40%) or were treated further with advice from a veterinarian (43.3%). The majority of farmers (98.3%) were aware of the losses caused by mastitis and the losses included reduced milk production (52.6%), treatment costs (16.5%), reduced income (13.4%), low milk quality (8.2%) and deformed udder (2.1%).

Major Constraints to Mastitis control

Farmers expressed various factors that constrain them in controlling mastitis. As illustrated in Figure 2, the major constraints to mastitis control included high treatment costs, insufficient or lack of veterinary services, difficulty in diagnosing the disease, low income, poor hygiene especially during the rainy season and lack of equipment for controlling the disease.  

Causative agents

Milk samples were collected from 172 animals and the results of the isolates obtained are shown in Table 4 with staphylococi being the predominant of the isolates.

Of the 688 quarter samples, 357 (51.9%) contained microorganisms, 59 of which had mixed infections. Staphylococci isolates which were the majority of the isolates were tested for their susceptibility to a panel of drugs. The resistance patterns are shown in table 5.

Over 50 of the isolates were resistant to penicillin and tetracycline which are among the most commonly used drugs in intramammary formulations used by the farmers. The isolates were least resistant to gentamycin which also happens to be the most expensive drugs available to the farmers.

Discussion

The present study investigated the occurrence of mastitis and associated constraints faced by farmers in controlling the disease in smallholder dairy farming system in Uganda. The prevalence of mastitis was indeed high with sub-clinical mastitis responsible for more than 95% of the disease which is comparable to other studies (Byarugaba et al 1998; Kassa et al 1999, Kivaria et al 2004, Mdegela et al 2004). This could be partly explained by the management conditions in the farms under this study which were dominated by zero-grazing where animals were stall-fed and hygiene standards were usually low and difficult to manage especially during rainy seasons (Byarugaba et al 2003). It could also be due to several factors related to farmers’ practices and the fact the majority of the cows were exotic pure breed that are more susceptible to mastitis than exotic*indigenous breeds or pure indigenous breeds. Most of the farmers in this study did not follow any order of milking and therefore there was a risk of spreading infection from sick animals to healthy ones. One farmer indicated that he starts with stubborn ones (including diseased) and milks the normal one afterwards without washing hands in between milking of each cow. Many others used the same towel for all cows and such practices have been reported to spread and sustain mastitis in herds (Kassa et al 1999, Mdegela et al 2004, Kivaria et al 2006) which becomes very difficult to eliminate from the herds.

It has been suggested that mastitis can never be eradicated from dairy operations and its occurrence can only be minimized to acceptable levels (Blood and Radostitis 1989). There are variations in the type of constraints that farmers face related to their ability to comprehend the problem, accessibility to control supplies and sophistication of farming enterprises as well as management routines. In the present study, the major constraint to mastitis control by farmers was high treatment costs of clinical cases. In general, farmers had only knowledge about clinical mastitis, despite the fact that clinical mastitis accounted for less than 5 percent of the total mastitis cases. This explained that fact that farmers could only think of constraints associated with clinical mastitis, and that their major mastitis control method was treatment. This lack of knowledge on subclinical mastitis has also been reported among smallholder farmers in other areas (Karimuribo et al 2006) and it was also evident that farmers had no means to detect subclinical mastitis. Lacking knowledge on subclinical mastitis and its importance may explain the lack of adequate preventive measures, e.g. as indicated by the fact that only one farmer practiced teat dipping. 

The high costs of treatment can partly be related to the high resistance of the common and cheap antibiotics like penicillin and tetracycline that was observed in the bacteria isolated from the samples. Similar high resistance patterns among mastitis pathogens have been reported elsewhere (Nakavuma et al 1994, Kambarage et al 1996). Farmers are able to obtain antibiotics over the counter in Uganda without prescription which often results in misuse and contribution to development of resistance as has been reported (Byarugaba 2004). Some of them do not complete the recommended regimes, and some have reported using one intra-mammary tube in all the four teats to minimize costs which results in exposure of the pathogens to sub-lethal doses that impart selective pressure and thus promote resistance. The high resistance of pathogens observed in this study is cause for worry.

Hogeveen (2005) concludes that mastitis still continues to cause significant losses to farmers, despite the availability of extensive knowledge on mastitis and its control strategies. In this study, the major constraints to mastitis control was primarily farmers’ lack of good daily practice routines such as hygiene, and much of this was caused by lack of knowledge. Only few studies have examined effective ways of knowledge dissemination in promoting animal health. Bell et al (2005) examined the effects of different knowledge dissemination methods for mastitis control in smallholder dairy farmers in Tanzania and found that a combination of methods were more effective. They also noted association of knowledge uptake with the level of education. In the present study, whereas the majority were of secondary level education, there was no difference on the levels of mastitis on the various farms with different education background.

Motivation for improved investment, management and adoption of health improvement programmes is usually associated with increased production and increased income (Hall et al 2004). While mastitis reduces milk yield (de Graaf and Dwinger 1996), several other factors such as inadequate nutrition and long calving intervals have been suggested to be the most serious constraints to improved milk production efficiency.  Farmers therefore are not motivated to invest in better mastitis control programmes when they do not realize immediate improvement in milk production. We have previously demonstrated that participatory livestock farmer training where farmers visit each other’s farms and discuss all issues related to improving milking efficiency comprehensively with the help of a facilitator has resulted in improved their milk production and consequently reduced mastitis considerably (Vaarst et al 2007).

In the present study milk production was very low at the start of the study before intervention was done and therefore farmers had no motivation for investment in mastitis control. It has also been suggested that in low yielding cows, mastitis is hardly associated with decreased milk yield (Omore et al 1996) which further confirms the observation that farmers were not putting much input in mastitis control except when the cows came down with clinical disease. The purpose why smallholder farmers keep dairy animals is to produce milk that can generate income to meet their monetary requirements as well supplement their family nutritional requirements (Nakiganda et al 2006). Although mastitis is one of those constraints that limit milk production efficiency and one of the most costly diseases in dairy production (Omore 1997), mastitis control alone does not result in increased milk production if other issues such as sufficient nutritional demands are not met.

Acknowledgement 

This work was supported by the DANIDA supported Livestock Systems Research project (LSRP) component of the Agricultural Sector Programme Support (ASPS I) to the Uganda Government

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Received 10 September 2007; Accepted 14 October 2007; Published 1 January 2008

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