THE WORLD OF MASTITIS
K. Larry Smith and J. S. Hogan
The Ohio State University
Wooster, Ohio, USA
Introduction
Despite considerable research on bovine mastitis the disease still remains an economically relevant problem to the dairy industry (6, 11). Economic losses are estimated to be approximately $200 per cow per year in the U.S. and these losses are due to reduced production, increased replacement costs, discarded milk, drug costs, veterinary fees, and labor costs. Losses are incurred with both the subclinical and clinical manifestations of the disease. Additional costs that are seldom mentioned are incurred by the processing industry in terms of reduced cheese yields, and the manufacture of products with reduced shelf life and consumer acceptance.
While we have traditionally sold mastitis control in producer herds based on increased production of milk and thus, increased producer profits, the need to control mastitis is increasingly driven by consumers of milk and milk products (35). Large numbers of consumers from all countries of the world are demanding dairy products that are wholesome, nutritious, safe and produced from healthy cows. Processors are aware that high quality milk results in increased yields of manufactured products with greater shelf life and improved organoleptic properties and finally increased profits. The international trade in dairy products will likely continue to increase and governments will need to know that the quality and safety of imported products meets or exceeds their internal requirements. These quality and safety demands of international trade also continue to apply pressure on producers to control mastitis and these pressures will be greatest in the exporting countries.
As a result of the factors discussed above, most countries recognize that mastitis in dairy herds is a major contributor to decreased milk quality and many believe that mastitis is a food safety and animal welfare issue (34, 35, 36). The food safety issues are of greater concern in countries that produce large quantities of raw milk cheese compared to countries that adopt the opinion that pasteurization eliminates all the possible problems that might be associated with mastitis/mammary pathogens in raw milk. Certainly these opinions differ between many of the E.U. countries, who produce large quantities of raw milk cheese, and the U.S. that produces relatively very little raw milk cheese. Animal welfare issues tend to affect producers in the Northern European countries to a greater extent than in North America and mastitis is an animal welfare issue in the Nordic countries. The concept that mastitic animals are diseased and a welfare issue will grow internationally and increase the need to control mastitis.
Bulk tank milk somatic cell counts (BTSCC) are a measure of the prevalence of mastitis in a dairy herd (10) and are used by regulatory agencies as an indicator of the wholesomeness, safety and suitability of raw milk for human consumption (35). Nearly all developed countries have adopted upper regulatory limits for SCC in milk intended for human consumption. The upper limit for BTSCC establishes the amount of abnormal milk tolerated in the supply. The E.U., New Zealand, Australia, Switzerland, and Norway all accept 400,000 cells/ml as the upper limit (14). The EU is already discussing lowering the regulatory SCC limit to 300,000 or perhaps even 250,000 cells/ml. Canada has now agreed on 500,000 cells/ml throughout all of the provinces and is discussing the possibility of going to 400,000 cells/ml. The limit for SCC in the U.S. is 750,000 cells/ml. The U.S. position is that SCC is an issue of quality but not safety and that the upper regulatory limit is of no consequence since the mean SCC of milk in the U.S. is estimated to be below 400,000 cells/ml. Most of the mastitis research workers in the U.S. do not share the view of the U.S. industry. There is obviously a tendency in the international market place to judge the safety and quality of a milk supply based on the upper acceptable limit for somatic cell count.
Many countries are able to determine a national average SCC, based on all producers in the country, and these averages have been in general declining over the past 10 years and indicate considerable progress in control of subclinical mastitis or increased ability to control/manage the SCC of the herd bulk milk. The national average SCC is currently less than 300,000 cells/ml in most of the E.U. countries as well as New Zealand (37). The national average in the US is estimated to be in the range of 350,000 cells/ml. National statistics from the developing countries or some of the countries of South America with rapidly developing dairy industries are not readily available. The national average SCC of less than 200,000 cells/ml in countries such as Switzerland, Norway, Finland, United Kingdom, West Germany, and New Zealand clearly indicate that producers can control subclinical mastitis.
Fundamental Principles of Mastitis Control
Mastitis is an inflammation of the mammary gland and the presence of an intramammary infection (IMI) is not required for mastitis to exist. However, the vast majority of mastitis cases are due to an intramammary infection caused by a microorganism (4). Over 100 different microorganisms have been shown to cause IMI but most of the economic losses are associated with species of staphylococci, streptococci, and the coliform bacteria. Mastitis pathogens are often categorized as contagious, environmental and skin flora opportunists based on their primary reservoir within dairy herds that leads to teat end exposure and subsequent infection. The skin flora opportunists are basically the coagulase negative species of staphylococci (32).
These designations should not be interpreted as black or white, but they do reflect the basic epidemiology in dairy herds and the control practices likely to be effective in control of a particular pathogen within a herd. The contagious pathogens are spread from infected cows and quarters to uninfected cows and quarters primarily during the milking operation (4). Effective post-milking teat dipping reduces the spread of the pathogen by reducing the numbers of pathogens remaining on the teat post-milking. Teat end contamination by contagious pathogens during the interval between milkings is minimal compared to teat end contamination during the time the cow is being milked. Just because Staphylococcus aureus is labeled as a contagious pathogen does not mean that S. aureus cannot be found in the environment and does not mean that 100% of new S. aureus IMI are a result of teat contamination during the milking operation. Likewise, Escherichia coli is an environmental pathogen but it could be spread from an infected quarter to an uninfected quarter during the milking operation. In our opinion, the latter is a low frequency event compared to teat contamination from the environment in which the cow is living. In recent times there has been a tendency to look at the exception rather than the rule. To argue that E. coli can at times be a contagious pathogen is to overlook the bigger picture that is of most importance for it’s control. In our opinion, cow to cow transfer of E. coli accounts for only a small percentage of E. coli infections in a dairy herd.
Regardless of the pathogen the fundamental principle of mastitis control is that the disease is controlled by either decreasing the exposure of teat ends to potential pathogens or by increasing the resistance of dairy cows to infection. The means by which exposure is influenced will vary depending upon the epidemiology of the various pathogens in dairy herds (33). Resistance, on the other hand, can be influenced specifically, as with vaccination (18), or generally as is the case with teat end health, diets (8), genetic improvement (30), and stress alleviation. Herd bulk milk SCC is a function of the prevalence of cows and quarters infected at any one point in time. To reduce the prevalence of IMI in dairy herds a control program must reduce the rate of new IMI and/or the duration of infection (4). Rate of IMI is reduced by decreasing teat end exposure to pathogens, increasing the resistance mechanisms of the cow, and by the prophylactic use of antibiotics such as is done with dry cow therapy. Duration of IMI is influenced by resistance mechanisms (spontaneous cure) and also by the use of antibiotics during the dry period and during lactation. A critical element of reducing teat end exposure is to attack and decrease the reservoir of the pathogen in the herd.
A common characteristic of the contagious pathogens S. aureus, Str. agalactiae, and C. bovis, is their ability to colonize and grow on teat skin and within the teat duct. This ability likely contributes to their contagious nature and the fact that prevalence of infected quarters and cows can be very high in herds lacking effective control methods. Prior to the development of teat dipping and dry cow therapy, infection prevalence of 50% of cows infected in 50% of quarters was not uncommon (4).
Contagious pathogens are major contributors to subclinical infections that elevate BTSCC) (4, 9, 11, 33). The reduction in BTSCC that has occurred is largely do to increased control of the contagious pathogens Str. agalactiae and S. aureus. The “five point plan” developed forty years ago in the U.K. has been responsible for the reduction of contagious pathogens in many but not all countries. The elements of the five point plan are 1) post-milking teat disinfection; 2) total dry cow therapy; 3) therapy of clinical cases during lactation; 4) proper maintenance of the milking machine; and 5) culling problem cows. The basic principles are to reduce the spread of pathogens from infected to uninfected cows during the milking process and to reduce the reservoir of the pathogens in the dairy herd. Teat dipping has been shown to effectively reduce the spread of contagious pathogens and total dry cow therapy will significantly reduce the number of infected quarters, the primary reservoir of contagious pathogens.
Almost all countries still list S. aureus as a major problem and control by the “five point plan” is reduced compared to control of Str. agalactiae. This is likely due to differences in the nature of infections caused by these two pathogens and the fact that S. aureus are often resistant to antibiotics and infection foci are often not accessible to the drugs (9). In addition, the only known source of Str. agalactiae in a dairy herd is an infected mammary gland while other sources are likely to occur for S. aureus.
Countries such as the U.K., the U.S., and Canada have adopted the “five point plan” and when applied properly Str. agalactiae is generally eradicated and S. aureus is reduced to less than 1% of quarters infected (16). Other countries have adopted only parts of the “five point plan”. Producers in New Zealand, for example, rarely use total dry cow therapy and tend to use dry cow therapy on cows likely to be infected at drying off, generally based on SCC, or who have had a case of clinical mastitis during the previous lactation (selective dry cow therapy). However, recent evidence from New Zealand (42, 43) has shown that Streptococcus uberis infections at calving are a problem in many herds and the use of total dry cow therapy helps reduce the number of quarters infected at calving with this environmental pathogen. These results are similar to findings in the US (38) and UK (11).
Not all countries have adopted the principles of the “five point plan” and yet many have successfully reduced the prevalence of contagious pathogens and BTSCC. The Nordic countries are particularly noteworthy in this regard. Post-milking teat dipping is not practiced as there is concern regarding potential residues in the milk. Dry cow therapy is used selectively on known infected cows or cows that have experienced clinical mastitis in the lactation just completed. The Nordic countries are more sensitive to issues of developing antibiotic resistance than might be encountered in the U.S. and the use of prophylactic antibiotics is seen as a likely contributor to the development of antibiotic resistance (2). Most of the herds in the Nordic countries are small, many with less than 10 cows. All antibiotic treatments are done by veterinarians and all treatments are recorded into national health monitoring systems. Contagious pathogens are controlled by surveillance of individual cow SCC and microbiological culture of high SCC cows. Problem SCC cows are often treated during lactation in an effort to eliminate the infection and reduce SCC. Culling rates tend to be 30% to 50% of the herd per year as most all of the milk producing cows are the dual purpose breeds and are a major source of beef in these countries. Culling is definitely a tool that contributes to maintenance of low herd SCC in these countries.
Environmental Mastitis Pathogens
The environmental pathogens are major contributors to clinical cases of mastitis (11, 16, 34) and have reduced impact on BTSCC as many of these infections are clinical and the milk is discarded as it is visually abnormal and often accompanied by antibiotic therapy. Their impact on BTSCC is also limited as they tend to cause infections of short duration by comparison to the contagious pathogens and, as a result, the prevalence of quarters infected at any one point in time seldom exceeds 10% of quarters. Environmental pathogens are the major cause of clinical mastitis cases in most countries, and a common occurrence is that contagious pathogens are brought under control, BTSCC are low, but the incidence of clinical cases is not reduced or may actually increase.
One of the major weaknesses of the “five point plan” is that it fails to control the environmental pathogens (4). The epidemiology of environmental pathogens differs markedly from that of the contagious pathogens and contributes to the lack of control exerted by the “five point plan”. The major reservoir of these pathogens is the environment in which the cows are living and not another infected quarter in the herd. Contamination of the teat end occurs during milking, between milkings, during the dry period, prior to first calving in heifers and is not limited to the milking operation. Factors that contribute to exposure are type of housing, ventilation, bedding materials and in some cases udder preparation for milking (31). Some mastitis research workers would argue that environmental mastitis is actually increased following the reduction in contagious pathogens and the coagulase negative species of staphylococci (CNS) that occurs following the implementation of the “five point plan” (32). Others argue that SCC in mammary quarters are becoming too low and low SCC quarters are more susceptible to infection by the environmental pathogens (29). One could also argue that once the contagious pathogens are brought under control, the pool of quarters available for new infection has increased. If exposure to the environmental pathogens is not reduced as the contagious pathogen IMI are brought under control, then it may be very likely that environmental pathogen infections will increase in the herd.
The most common environmental pathogens causing problems in dairy herds are the environmental streptococci, primarily Str. uberis, and the coliform bacteria (31). Escherichia coli is the coliform genera most often isolated from clinical cases of mastitis but Klebsiella spp. are common in some countries, such as the U.S. and Canada. Klebsiella spp. infections are often associated with the use of sawdust bedding in dairy herds in the U.S. and Canada, and while sawdust is also used in Europe, Klebsiella spp. appear to be less frequently associated with intramammary infection compared to the frequency reported in the U.S. and Canada. Many studies in Europe and New Zealand would indicate that Str. uberis is more of a problem than the coliform bacteria while similar studies in the U.S. would indicate that the coliform bacteria are a more frequent cause of clinical mastitis in most herds. These differences may reflect differences in housing and possibly, the higher production of U.S. dairy cows. Factors that have been shown to reduce the impact of the environmental pathogens include: improvements in housing (ventilation, stall design) (31), the use of inorganic bedding materials (15), vaccines (11, 18, 40), adequate dietary levels of vitamins and trace minerals (8, 19), and pre-dipping in some herds (26).
Progress on the control of the environmental pathogens is more difficult to assess given their limited impact on subclinical infections and BTSCC, and the lack of records involving clinical mastitis cases. There is the implication that environmental mastitis is less prevalent in countries with small herds and where pastures are used for a significant portion of the year. Clearly confinement housing or zero grazing is associated with increased incidence of environmental mastitis. While clear programs are in place to control the contagious pathogens, there is no single program comparable to the “five point plan”, recommended for control of the environmental pathogens.
The Coagulase Negative Staphylococci (CNS)
Historically, coagulase-negative species of staphylococci (CNS) have been referred to as minor or secondary pathogens of the mammary gland (32). This designation was based on the observations that these pathogens caused only a mild inflammation of the mammary gland with modest increases in somatic cell count (SCC), and were infrequently associated with clinical mastitis. As mastitis control schemes for the major pathogens have evolved and been implemented, there is increasing awareness that these control schemes are less effective in control of CNS intramammary infections. The result is that CNS are the leading cause of intramammary infection on most modern dairy farms implementing control practices effective against the major contagious pathogens, S. aureus and Str. agalactiae. The CNS are also the primary cause of intramammary infection in heifers at calving. Most developed countries would now report that the CNS are the leading cause of intramammary infection.
Thirty years ago the mild inflammation caused by CNS was relatively unimportant to the production of milk with SCC below legal limits. However, the elevation in SCC caused by the CNS can no longer be ignored or viewed as unimportant (27). The upper legal limit for SCC continues to decline and is currently at 400,000 cells/ml in many important dairy countries. In addition, numerous milk procurement agencies now pay premium prices for low SCC milk with maximum payment achieved at SCC values of less than 100,000 cells/ml. The "modest" elevation of SCC caused by the CNS is increasingly of concern as most CNS intramammary infections are associated with SCC of greater than 100,000 cell/ml and many produce intramammary infections with SCC greater than 400,000 cells/ml. An additional concern is that CNS intramammary infections do contribute to the clinical cases of mastitis within most dairy herds although they are seldom, if ever, the major cause of clinical mastitis cases within a herd.
The control measures of post-milking teat dipping and total dry cow therapy generally reduce the prevalence of CNS intramammary infection in dairy herds using these control practices compared to herds not implementing these control measures. However, prevalence of CNS IMI is generally greater than 10% of quarters even when these control measures are implemented and better approaches to control of CNS intramammary infection in dairy herds is warranted given the increasing trend of lower legal limits for SCC in milk. While quarters infected with the CNS show increased resistance to infection by the major mastitis pathogens in some studies (32), maintenance of these IMI or attempts to increase their prevalence in order to achieve reduced rates of major pathogen infection, cannot be justified given the current trend to pay for low SCC milk and to reduce the upper legal limit of SCC to values below 500,000 cells/ml. In addition, some studies of natural infections indicate that quarters infected with the CNS and particularly C. bovis are actually more susceptible to infection by Str. uberis and the coliform bacteria (17)
Future Needs
Gaps in our knowledge regarding mastitis control in dairy herds do exist and many of the physiological aspects of the infection process are either not, or are poorly understood. The mechanism(s) by which bacteria penetrate the streak canal is one such example. Studies are just beginning to elucidate the mechanisms involved in the immune suppression associated with periparturiet period (7, 21). Likewise the interrelationship between the high incidence of metabolic diseases in early lactation and increased susceptibility to mastitis (23) could provide important answers for additional control of mastitis in herds. Newer evidence suggests that mastitis may interfere with reproduction and studies of the mechanisms involved could increase fertility in herds (25). Clearly, events occurring in the mammary gland are not isolated and can impact other physiological processes within the cow.
Using biotechnology to alter resistance to mastitis through gene insertion is scientifically of great interest and such studies should continue. However, given the current negative consumer attitudes regarding food produced from animals that have been genetically engineered, the acceptance of such technology and it’s wide spread application to the dairy industry would seem to be several years in the future.
A major weakness in current mastitis control is the control of environmental pathogens. Work on vaccines is on going and vaccines with a degree of efficacy against the coliform bacteria are available in some countries (18, 33). A vaccine for Str. uberis is under study and, if successful, could have wide spread application (22). However, exposure to environmental pathogens can be extreme in some housing conditions and vaccines or nutrition are not likely to completely compensate for the great exposure to which some teat ends are subjected (39). Recent cow behavioral studies in Canada could significantly alter our current thinking with regard to appropriate cow housing that maximizes cow comfort and minimizes stress (1). There is still a need to design housing environments that minimize pathogen exposure to teat ends. This is particularly important in countries that rely on confinement housing such as the US. Perhaps the goal should be to design housing systems that would mimic the teat end exposure to pathogens that occurs on well groomed pastures. We are of the opinion that the majority of cows in the US live in substandard housing.
Antibiotics are an integral part of most mastitis control schemes. There is a rapidly increasing concern among human health officials and regulatory agencies regarding the growing resistance of many bacterial strains to antibiotics (2). The contribution of animal agriculture to developing resistance is being targeted by regulatory agencies and given that mastitis is the major disease of dairy cattle it is not surprising that the use of antibiotics for mastitis control is being questioned. Total dry cow therapy is often criticized but there is little hard evidence to substantiate the contribution of total dry cow therapy to developing resistance in human pathogens. Never the less, new approaches to dry cow therapy are needed. Organic dairy farming is gaining in popularity in many countries and particularly the Nordic countries (5, 41). Where rules for organic dairy farming prohibit the use of chemicals such as post-milking teat dips or drugs such as dry cow therapy, optimal management schemes need to be developed and tested. New non-chemical methods to prevent the transfer of contagious pathogens at milking time would be beneficial.
The milking machine contributes to teat end health and IMI (24, 28). Modern milking machines are a significant improvement over those of 20 to 30 years ago and more improvements are very likely. Efforts to optimize the interaction of the machine with the teat end are likely to pay big dividends. Robotic milking systems have clearly been accepted by a growing segment of the dairy industry (20). A problem with robotic milking systems is detection of clinical mastitis and the elimination of abnormal milk from the supply. It is very likely that new developments with milking systems, robotic or conventional, will include improvements in inline sensing to detect mastitis milk (13). The technological advances made by the milking machine manufactures are often slow to be realized by producers as replacement of the milking equipment is one of the most costly capital expenditures for dairy producers. Improved transfer of this technology would likely serve the industry well and significantly improve mammary health and the quality of milk produced.
Conclusions
Progress on mastitis control has been achieved since the first AABP NMC International Symposium on Bovine Mastitis and many dairy producers clearly profit from reduced mastitis in their herds. However, consumer demands for safe, high quality dairy products that are produced by healthy cows in welfare friendly environments are likely to be the driving force behind the need to further improve mastitis control in the world’s dairy herds. Improved methods for control of the environmental pathogens and the contagious pathogen S. aureus, would be beneficial to the dairy industry. The problem of antibiotic resistance in human pathogens and the contribution of animal agriculture to this problem will be an important issue in the immediate future. Animal welfare issues will continue to grow and impact the types of mastitis research conducted. Advances in milking machine technology that improve teat health and help reduce mastitis will occur. Efforts to develop vaccines and to improve cow health through nutrition and stress reduction will continue to be important areas for research.
References
1. Anderson, N. 2001. Time-Lapse video opens our eyes to cow behaviour and comfort. Proc. Milk Quality Conference, National Mastitis Council/Professional Dairy Producers of Wisconsin, pp 21-32.
2. Angulo, F.J., R.V. Tauxe, and M.L. Cohen. 1999. The origins and consequences of antimicrobial-resistance nontyphoidal Salmonella: Implications for use of fluoroquinolones in food animals. Proc. 38th Annual Meeting of the National Mastitis Council, pp 16-30.
3. Booth, J.M. 1995. Progress in the control of mastitis. Proceedings II. The 3rd International Mastitis Seminar, Tel Aviv, Israel. S4:3-10.
4. Bramley, A.J., and Dodd, F.H., 1984. Reviews of the progress of dairy science: Mastitis control - progress and prospects. J. Dairy Res. 51:481-512.
5. Busato, A., P. Trachsel, M. Schallibaum, and J.W. Blum. 2000. Udder health and risk factors for subclinical mastitis in organic dairy farms in Switzerland. Preven. Vet. Med. 44:205-220.
6. DeGraves, F.J., and Fetrow, J., 1993. Economics of mastitis and mastitis control. Veterinary Clinics of North America: Food Animal Practice. 9:421-434.
7. Detilleux, J.C., M.E. Kehrli, J.R. Stabel, A.E. Freeman and D.H. Kelley. 1995. Study of immunological dysfunction in periparturient Holstein cattle selected for high and average milk production. Vet. Immunol. Immunopathol. 44:251-267.
8. Erskine, R.J., 1993. Nutrition and mastitis. Veterinary Clinics of North America: Food Animal Practice. 9:551-561.
9. Fox, L.K. and J.M. Gay. 1993 Contagious mastitis. Veterinary Clinics of North America: Food Animal Practice. 9:475-487.
10. Harmon, R.J. 1994. Physiology of mastitis and factors affecting somatic cell counts. J. Dairy Sci. 77:2103-2112.
11. Hillerton, J.E. 1996. Control of mastitis. In Progress in Dairy Science, Edited by C.J.C. Phillips, CAB International, Wallingford, Oxon, UK. Pp 171-190.
12. Hillerton, J.E. 1999. Redefining mastitis based on somatic cell count. Bulletin of the International Dairy Federation. No345, pp. 4-6.
13. Hillerton, J.E. 2000. Detecting mastitis cow-side. Proc. 39th Annual Meeting of the National Mastitis council, pp 48-53.
14. Hillerton, J.E. 2001. Meeting somatic cell count regulations in the European Union. Proc. 40th Annual Meeting of the National Mastitis Council, pp 47-53.
15. Hogan, J.S., Smith, K.L., Hoblet, K.H. Todhunter, D.A., Schoenberger, P.S., Hueston, W., Pritchard, D.E., Bowman, G.L., Heider, L.E., and Brockett, B.L., 1989. Bacterial counts in bedding materials used on nine commercial dairies. J. Dairy Sci. 72:250-258.
16. Hogan, J.S., Smith, K.L., Hoblet, K.H., Schoenberger, P.S., Todhunter, D.A., Hueston, W.D., Pritchard, D.E., Bowman, G.L., Heider, L.E., Brockett, B.L., and Conrad, H.R., 1989. Field survey of mastitis in low somatic cell count herds. J. Dairy Sci. 72:1547-1556.
17. Hogan, J.S., K.L. Smith, D.A. Todhunter, and P.S. Schoenberger. 1988. Rate of environmental mastitis in quarters infected with Corynebacterium bovis and Staphylococcus species. J. Dairy Sci. 71:2520-2525.
18. Hogan, J.S., Smith, K.L., Todhunter, D.A., and Schoenberger, P.S., 1992. Field trial to determine efficacy of an Escherichia coli J5 mastitis vaccine. J. Dairy Sci. 75:78-84.
19. Hogan, J.S., Weiss, W.P., and Smith, K.L., 1996. Nutrition and mammary host defenses against disease in dairy cattle. In: C.J.C. Phillips (Ed.) Progress in Dairy Science. CAB International, Wallingford, Oxon, UK. pp. 45-57.
20. Hogeveen, H., Y. van der Vorst, W. Ouweltjes, and B.A. Slaghuis. 2001. Automatic milking and milk quality: A European perspective. Proc. 40th Annual Meeting of the National Mastitis Council, pp 152-162.
21. Kehrli, M.E., B.J. Nonnecke and J.A. Roth. 1989. Alterations in bovine neutrophil function during the periparturient period. Am. J. Vet. Res. 50:207-214.
22. Leigh, J.A. 1997. Progress in the development of vaccines against environmental streptococcal mastitis. Proc. Symposium on Udder Health Management for Environmental Streptococci, Ontario Veterinary College, Ontario, Canada, pp 59-74.
23. Leslie, K.E., T.F. Duffield, Y.H. Schukken, and S.J. LeBlanc. 2000. The influence of negative energy balance on udder health. Proc. Regional Meeting of the National Mastitis Council, pp 25-33.
24. Mein, G.A. and P.D. Thompson. 1993. Milking the 30,000-pound herd. J. Dairy Sci. 76:3294-3300.
25. Oliver, S.P., F.N. Schrick, M.E. Hockett and H.H. Dowlen. 2000. Clinical and subclinical mastitis during early lactation impairs reproductive performance of dairy cows. Proc. Regional Meeting of the National Mastitis Council, pp 34-51.
26. Pankey, J.W., and Drechsler, P.A., 1993. Evolution of udder hygiene: Premilking teat sanitation. Veterinary Clinics of North America: Food Animal Practice. 9:519-530.
27. Rainard, P., Ducelliez, M., and Poutrel, B., 1990 The contribution of mammary infections by coagulase-negative staphylococci to the herd bulk milk somatic cell count. Vet. Res. Commun. 14:193-198.
28. Rasmussen, M.D. 1999. Management , milking performance, and udder health. In K. Aagaard (ed): III Future Milk Farming, Proc. FIL-IDF 25th Int. Dairy Congress, 21-24 Sep. 1998, Aarhus. Danish Natl. Comm. IDF, Aarhus, Denmark. 174-178.
29. Schukken, Y. 2001. Can cell counts get too low? Proc. 40th Annual Meeting of the National Mastitis Council, pp 19-28.
30. Shook, G.E. 1993. Genetic improvement of mastitis through selection on somatic cell count. Veterinary Clinics of North America: Food Animal Practice. 9:563-577.
31. Smith, K.L., and Hogan, J.S., 1993. Environmental mastitis. Veterinary Clinics of North America: Food Animal Practice. 9:489-498.
32. Smith, K.L., and J.S. Hogan. 1995. The importance of coagulase-negative staphylococci. Mastitis Newsletter 20: Newsletter of the International Dairy Federation, No. 142 pp. 26-29.
33. Smith, K.L. and J.S. Hogan. 1995. Epidemiology of mastitis. Proceeding s Third IDF International Mastitis Seminar, Book II, Session 6. Tel-Aviv, IL. pp. 3-12.
34. Smith, K.L., and J.S. Hogan. 1996. Future prospects for mastitis control. Proceedings XIX World Buiatrics Congress, Edinburgh, Scotland. Vol1, pp. 263-269.
35. Smith, K.L. and J.S. Hogan. 1999. A world standard for milk somatic cell count: is it justified? Bulletin of the International Dairy Federation. No345, pp. 7-10.
36. Smith, K.L., and J.S. Hogan. 1999. An overview on mastitis - the year 2000. Proceedings International Conference on Mastitis and Machine Milking. Cork, Ireland. Pp 1-4.
37. Smith, K.L., K. Takemura, and J.S. Hogan. 2000. International progress in mastitis control. Proc. Pacific Congress on Milk Quality and Mastitis Control. Nagano, Japan. November 13-16, pp. 245-252.
38. Smith, K.L., Todhunter, D.A., and Schoenberger, P.S., 1985. Environmental pathogens and intramammary infection during the dry period. J. Dairy Sci. 68:402-408.
39. Smith, K.L., Todhunter, D.A., and Schoenberger, P.S., 1985. Environmental mastitis: cause, prevalence, and prevention. J. Dairy Sci. 68:1531-1553.
40. Tyler, J.W., J.S. Cullor, and D.C. Ruffin. 1993. Immunization and immunotherapy for mastitis. Veterinary Clinics of North America: Food Animal Practice. 9:537-549.
41. Vaarst, M. and C. Enevoldsen. 1997. Patterns of clinical mastitis manifestations in Danish organic dairy herds. J. Dairy Res. 64:23-37.
42. Williamson, J.H., M.W. Woolford, and A.M. Day. 1995. The prophylactic effect of a dry cow antibiotic against Streptococcus uberis. New Zealand Veterinary Journal 43:228-224.
43. Woolford, M.W., J.H. Williamson, A.M. Day, and P.J.A. Copeman. 1998. The prophylactic effect of a teat sealer on bovine mastitis during the dry period and the following lactation. New Zealand Veterinary Journal 46:12-19.