Factors affecting the probability of bacteriological cure

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Review Article

Factors affecting the probability of bacteriological cure of bovine mastitis S. Degen1,2; J.-H. Paduch1; M. Hoedemaker2; V. Krömker1 1 Microbiology, 2Clinic

Department of Bioprocess Engineering, Faculty II, University of Applied Sciences and Arts, Hannover, Germany; for Cattle, University of Veterinary Medicine, Hannover, Germany

Keywords

Schlüsselwörter

Udder health, bacteriological cure, antibiotic therapy, somatic cell count

Eutergesundheit, bakteriologische Heilung, Antibiose, somatische Zellzahl

Summary

Zusammenfassung

The aim of this study was to review factors affecting the probability of cure of bovine mastitis and thereby establish criteria for deciding whether to treat or cull individual animals. A further objective was to avoid redundant treatment with antibiotics so as to reduce the risk of pathogen resistance and enhance economic benefit. In evaluating success of therapy, bacteriological cure is the standard type of cure and is defined as elimination of mastitis-causing pathogens from the mammary gland. Administration of antibiotics is considered reasonable only when there is a prospect of bacteriological cure. In addition to age of the affected cow, the history of mastitis, number of infected quarters and somatic cell count affect the probability of bacteriological cure. Identifying and characterising chronic mastitis, which causes enormous production losses, are especially important to prevent unnecessary treatment and to decide whether or not to cull. To our knowledge, this is the first work providing a complete list of factors that have been confirmed in scientific literature to influence the probability of cure. This review should support farmers and veterinarians in deciding between culling and administering appropriate therapy to an affected animal.

Ziel dieser Übersichtsarbeit war, Einflussfaktoren auf die Heilungswahrscheinlichkeit boviner Mastitiden zu erarbeiten und dadurch Kriterien für die Entscheidung zwischen Behandlung und Merzung einzelner Tiere festzulegen. Hierdurch sollen überflüssige antibiotische Behandlungen vermieden und das Risiko der Resistenzbildung minimiert werden, um den ökonomischen Nutzen zu optimieren. Bei der Beurteilung des Therapieerfolgs ist die bakteriologische Heilung die Standardform der Heilung und definiert durch die Elimination von Mastitiserregern aus dem Euter. Die Anwendung antibiotischer Präparate wird nur als sinnvoll betrachtet, wenn eine Chance auf bakteriologische Heilung besteht. Zusätzlich zum Alter der betroffenen Kuh beeinflussen die Anamnese hinsichtlich Mastitiden, die Anzahl infizierter Viertel und die somatische Zellzahl die bakteriologische Heilungswahrscheinlichkeit. Die Identifizierung und Charakterisierung chronischer Mastitiden, die enorme Produktionsverluste verursachen, sind besonders wichtig für die Vermeidung unnötiger Behandlungen und für die Entscheidung für oder gegen eine Merzung. Nach unserem Wissen ist dies die erste Arbeit, die eine vollständige Auflistung aller Faktoren bietet, die in der wissenschaftlichen Literatur als Einflussfaktoren auf die Heilungswahrscheinlichkeit bestätigt wurden. Diese Übersichtsarbeit sollte Landwirten und Tierärzten Hilfestellung geben, wenn Entscheidungen zwischen Merzung und angemessener Behandlung betroffener Tiere anstehen.

Correspondence to Prof. Dr. Volker Krömker Mikrobiologie der Fakultät II Maschinenbau und Bioverfahrenstechnik Hochschule Hannover Heisterbergallee 12 30453 Hannover E-Mail: [email protected]

Einflussfaktoren auf die bakteriologische Heilung boviner Mastitiden Tierärztl Prax 2015; 43 (G): ■■■ http://dx.doi.org/10.15653/TPG-141082 Received: December 11, 2014 Accepted after revision: February 16, 2015 Epub ahead of print: May 11, 2015

Introduction Within the dairy industry, the greatest economic losses are caused by bovine mastitis (13). Inflammation of the mammary gland not only leads to changes in milk composition but also decreases the quantity of milk (33). Veterinary fees, costs for additional labour, and the value of discarded milk also need to be considered (14). A © Schattauer 2015

fundamental aim of mastitis research is minimizing use of antibiotics to protect the consumer and prohibit development of resistant pathogens (9). First, a reduction in use of antibiotics can be achieved by lowering the new infection rate (16). Improving management and hygiene and introducing prevention programs, thus lowering the risk of infection, are the most effective ways to reduce antibiotic usage. Tierärztliche Praxis Großtiere 3/2015

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S. Degen et al.: Bacteriological cure of bovine mastitis

However, some mastitis cases cannot be prevented and should be treated carefully. In these cases, evidence-based therapy should be used to improve results of antibiotic treatment. Cows with a lower possibility of cure despite the best possible therapy can either be treated symptomatically or be removed from the herd. Treating such cows with antibiotics is unnecessary and does not conform to responsible usage of antibiotics. Second, a substantial percentage of all mastitis cases are recurrences. According to a recent study (39), nearly half of all clinical mastitis cases (43%) have precedent cases. These findings stress the importance of recurrent mastitis as a major trigger for unsuccessful treatment with antimicrobials. Therefore, unnecessary usage of antibiotics can also be prevented by removing animals with incurable mastitis from the herd (16). Treatment should be avoided if the probability of cure appears very low (2). This review aims to outline and merge essential knowledge about the probability of curing mastitis. The study concentrates on animal related factors because in the case of mastitis in a single cow, they are easiest and quickest to obtain. For collecting relevant literature, the PubMed search engine was used (30). The keywords ‘bovine mastitis’, ‘antibiotic therapy/treatment’, ‘risk factors’ and ‘(probability of) cure’ were employed most frequently for identifying appropriate papers. Similarly, ‘somatic cell count’, ‘success of therapy’, ‘culling’ and ‘monitoring’ led to various applicable papers. Useful articles were scanned for secondary literature in order to cover the topic completely. This search was repeated regularly between June 2012 and August 2014. In all, 38 articles (including one conference proceeding) published between 1994 and 2013 were reviewed. These studies permitted an exhaustive overview of factors affecting the probability of cure.

Subclinical and chronic mastitis After mastitis pathogens have invaded the bovine mammary gland, infection becomes either clinical with visible signs of inflammation or subclinical with no visible symptoms. Ineffective treatment of clinical mastitis can result in chronic mastitis. For example, mastitis-causing pathogens that are not eliminated completely due to under-dosing or insufficient duration of treatment can persist within the udder without triggering clinical symptoms (9). Furthermore, cases of severe acute infections of the udder often result in permanent tissue damage, preventing the mammary gland from recovering its full functional efficiency. Risk of recurrence in the affected quarter increases considerably (9). In the case of subclinical mastitis, antibiotic treatment that would favour bacteriological cure is generally not initiated, leaving persistent proliferating pathogens in the mammary gland under ideal circumstances. This condition can also lead to chronicity, causing alterations in the amount and composition of milk that may last for weeks or months (9). By then, udder tissue is generally partially or irrevocably damaged (38), causing additional economic losses. Lack of visible signs of inflammation hinders deTierärztliche Praxis Großtiere 3/2015

tection of subclinical mastitis; therefore, analytical methods are required to determine udder health (26). These methods include bacteriological analysis of milk samples and determining the somatic cell count (SCC).

Definition of cure An objective evaluation of probability of cure of mastitis before implementing therapy could help reduce the use of antibiotics. For this purpose, it is essential to establish a clear definition of cure, parameters affecting cure, and subsequent rationality of antibiotic treatment. In various publications, the term ’cure’ connotes bacteriological cure. Bacteriological cure implies that microorganisms detected before treatment could not be found afterwards (7, 9, 28, 36, 37). Another form of cure is cytological cure, which only pertains to the presence or absence of high SCC (33). Additionally, clinical cure has been identified (23) and elaborated (9). According to these sources, an udder is classified as clinically cured when outer signs of inflammation and clots in the foremilk are absent, although milk may still be compositionally and quantitatively altered. Animals with clinically inconspicuous mammary glands, however, may be a threat to uninfected animals in the herd as they are reservoirs for pathogens (9). Since administration of antibiotics can only induce bacteriological cure, in the best circumstances clinical and cytological cure can be expected as a consequence of bacteriological cure. Therefore, evaluating the probability of bacteriological cure is crucial for decisions about how to proceed most reasonably.

Factors affecting the probability of bacteriological cure Once a cow becomes conspicuous due to long-term high SCCs or repeated clinical symptoms of mastitis, its chances of bacteriological cure need to be considered to minimize economic losses and prevent needless use of antibiotics. For this purpose, parameters influencing the probability of bacteriological cure need to be defined.

Animal related factors Table 1 provides an overview of animal related factors affecting bacteriological cure that have been reported in the literature. The likelihood that a mastitic cow can be cured using an antibiotic at drying off (i. e., cultured secretion is bacteriologically negative at the start of lactation) depends on its age (odds ratio [OR] of treatment failure for second lactation or higher = 2.4; 95% confidence interval [CI] = 1.1–5.0) and on position of the affected quarter (hind quarters incur treatment failure twice as often as front quarters) (28). It also depends on the cow’s clinical mastitis history; one or more cases of clinical mastitis during the previous lac© Schattauer 2015


tation period decrease the probability of bacteriological cure (OR of treatment failure for one or more clinical mastitis cases = 3.6) (28). Some papers also list stage of lactation and SCC prior to treatment as other risk factors that are positively correlated with treatment failure (OR of bacteriological cure for 101–200 days in milk compared to < 100 days in milk = 0.39 and for SCC > 1,000,000 cells/ml = 0.29, respectively; 95% CI = 0.12–1.21 and 0.09–0.90, respectively) (7, 37). According to one study (28), the probability of cure of Staphylococcus (S.) aureus infection decreases with an increasing number of affected quarters. An increasing duration of infection also decreases the probability of bacteriological cure (3, 5, 21). Another study (5) reported a non-significant but numerically higher cure rate following early treatment of S. aureus (65%) compared with later treatment (43%). Furthermore, the presence of palpable lumps in udder tissue is listed as a factor affecting the probability of cure (15). Palpation findings are divided into three grades. Grade I applies to the udder being fine-grained throughout, whereas grade II describes an udder that is altogether coarse-grained, with solitary small lumps. When the udder is indurate and infiltrated with multiple large lumps, the finding is grade III. According to this study (15), the probability of cure decreased by 43% when the whole udder was infiltrated with lumps as large as mandarin oranges (> grade III). When animals with palpation findings of grades I to III were compared to animals with normal findings, the probability of clinical cure decreased significantly (p < 0.05), but there was no difference in bacteriological cure.

Table 1 Factors affecting the probability of cure. Tab. 1 Einflussfaktoren auf die Heilungswahrscheinlichkeit Factor

Applicable for the following microorganisms

References

Age

S. aureus S. aureus, Sc. dysgalactiae Major/minor pathogens1 Major/minor pathogens2

37 28 33 7

Position of the quarter

S. aureus S. aureus, Sc. dysgalactiae Major/minor pathogens2

37 28 7

Mastitis history

S. aureus, Sc. dysgalactiae Major/minor pathogens1

28 33

Stage of lactation

S. aureus Major/minor pathogens1 Major/minor pathogens2

37 33 7

Number of the affected quarters

S. aureus, Sc. dysgalactiae

28

Duration of infection

Major pathogens3 Major pathogens3, S. chromogenes Major pathogens4, CNS

3 21 5

Palpation findings

Major/minor pathogens4

15

Somatic cell count

S. aureus Major/minor pathogens2 Major/minor pathogens4

22, 37 7 6

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Somatic cell count As a diseased mammary gland activates the body’s defences, immune cells from the blood migrate into the milk. Hence, the state of health at the level of the quarter, cow or herd can be derived from the SCC in quarter foremilk, composite, or bulk milk samples, respectively. For this purpose, an upper threshold in a quarter of 100,000 cells/ml of milk was defined as the absence of mastitis (10). Internationally, a threshold of 200,000 cells/ml is used to distinguish between healthy and diseased quarters because it provides the highest sensitivity and specificity (74.5% and 89.6%, respectively) (32). In addition to the presence or absence of infection, somatic cell count in milk is also affected by factors that have a proven impact on the probability of bacteriological cure (7, 28). These factors include the species and strain of mastitis-causing microorganism, stage of lactation, age of the affected cow, and position of the affected quarter. Furthermore, one study (7) noted that the level of SCC prior to treatment significantly affects posttreatment SCC. These associations suggest that there is a correlation between the SCC prior to treatment and the probability of bacteriological cure. The connection between the SCC and probability of bacteriological cure was investigated in several studies. Sol et al. (36, 37) showed that during S. aureus infection, in addition to important © Schattauer 2015

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3 4

Major pathogens: Streptococcus (Sc.) agalactiae, Staphylococcus (S.) aureus, environmental streptococci, Mycoplasma spp., Escherichia (E.) coli, Klebsiella spp., Serratia spp., Trueperella pyogenes; minor pathogens: Corynebacterium bovis, coagulase-negative staphylococci (CNS) Major pathogens: S. aureus, Sc. uberis, other streptococci; minor pathogens: Corynebacterium bovis, CNS Sc. dysgalactiae, Sc. uberis, S. aureus Major pathogens: S. aureus, Sc. agalactiae, Sc. dysgalactiae, Sc. uberis, E. coli, Trueperella pyogenes; minor pathogens: Enterococcus spp., CNS

factors identified above in individual cows, the SCC (at the time of occurrence or beginning of treatment) affected the probability of curing mastitis. With an increase in SCC in both the quarter (37) as well as composite milk samples (36), the probability of bacteriological cure decreased (OR of cure for SCC > 1,000,000 cells/ml = 0.29; 95% CI = 0.09–0.90). The SCC prior to treatment has been defined as a factor affecting cyto-bacteriological cure (OR of cytobacteriological cure for SCC < 100,000 cells/ml = 2.69 compared to SCC > 100,000 cells/ml; 95% CI = 1.25–5.77) (22). Other authors have described comparable results with regard to other pathogens (6, 7). The impact of chronic infections of the mammary gland on SCC has been described (24, 35). After quarters were infected with S. aureus, a delayed but extended increase in SCC was observed when compared to effects on SCC of acute Escherichia (E.) coli inTierärztliche Praxis Großtiere 3/2015

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fection. However, correlations between SCC and characteristics of inflammation should be verified using additional parameters, such as electrical conductivity or bacteriological analysis, because exclusive consideration of SCC in milk of mastitic cows does not allow an accurate characterisation of the progress and prognosis of the disease (33, 34).

Treatment, microorganisms and herd specific factors In addition to animal related factors influencing the probability of cure, some other factors should not be overlooked. Method of treatment (active agent, duration of treatment) has also been described as having a significant impact on cure (17, 18, 37). Moreover, mastitis-causing microorganisms (species; strain; resistance; bacterial counts; ability to adhere, invade and form biofilms) (7, 25, 27, 36, 37) and herd-specific factors such as housing, vitamin supplementation, stock density, and new infection rate influence the probability of cure (3, 4, 11, 29, 31). Although this study focusses on animal related factors, these additional factors need to be considered when veterinarians and farmers determine treatment choice or modifications to farm management.

Possibilities of evaluating the probability of bacteriological cure In evaluating the probability of bacteriological cure, many factors should be considered. At the level of the individual cow, age of the animal is of particular importance because immune systems of young cows can eliminate or reduce consequences of infection

Conclusion and clinical relevance In order to avoid redundant administration of antibiotics and further economic losses due to mastitis, determination of the probability of bacteriological cure before treatment is necessary. Animals should be removed from the herd if they have no chance of a short-term return to effective and economic milk production. This study summarizes animal factors influencing the probability of bacteriological cure. However, a combination of unmodified factors for an exact calculation of the probability of bacteriological cure is impossible, as various studies involve different reference values. For example, some studies describe only factors influencing bacteriological cure in mastitis cases caused by particular microorganisms. Nevertheless, some factors are confirmed several times to influence treatment outcome considerably. Therefore, it is possible to say that the most important factors are age of the mastitis cow, mastitis history of the udder, number of affected quarters, and SCC. Identifying chronic mastitis is particularly helpful for deciding between treatment and culling. Factors described in this review can assist farmers and veterinarians with evaluation of the probability of bacteriological cure and thus help to improve bovine health, milk quality, and food safety. Tierärztliche Praxis Großtiere 3/2015

more effectively than can immune systems of elderly cows (37). One explanation for older cows having lower chances of bacteriological cure can be larger sizes of their mammary glands. A larger mammary gland results in a larger volume of tissue that needs to be infiltrated by antibiotic drugs and to be cleared from infection (1). Another reason might be a pathogen associated effect: Higher prevalence of penicillin-resistant microorganisms has been found in older cows than in younger cows (36). Furthermore, medical history of the affected cow should be taken into account. If an animal has already had a single case of mastitis or recurrent mastitis in the current or previous lactation period, the probability of bacteriological cure is notably lower (33). Mastitis-causing microorganisms have been determined and thoroughly described (e. g. virulence factors like biofilm formation) in various studies aimed at evaluating the probability of cure (7, 25, 27, 36, 37). However, bacteriological culturing of milk samples is relatively labour-, time- and cost-intensive (19), and investigating other parameters is both too complex to be suitable for mass analyses and impractical for a quick evaluation of the probability of bacteriological cure. Instead, the particular mastitis of the affected cow must be characterised precisely to guide recommendations concerning further procedures. The SCC is an easily obtainable parameter that is routinely determined in the course of Dairy Herd Improvement programs on many farms, and the effect of SCC on the probability of bacteriological cure has been emphasized in many publications. The higher the SCC and the longer this high level persists, the less likely the cure (7, 20, 33). Using mathematical models, SCC can indicate mastitis before the appearance of clinical or subclinical signs (8), but although SCC is currently the most important tool for evaluating udder health, it does not allow conclusions about the bacteriological status of the mammary gland (34). Nonetheless, it can serve as an indicator of the probability of cure at the level of the individual cow (OR of bacteriological cure for SCC > 1,000,000 cells/ml pre-intervention = 0.81; 95% CI = 0.70–0.93) (5). The probability of bacteriological cure is especially important in cases of chronic mastitis because this is the most frequent cause of needless administration of antibiotics. Thus, the duration and progress of the disease are of outstanding importance. Absence of visible symptoms of inflammation impedes recognition of chronic mastitis. Solely counting immune cells in the milk is not sufficient either because chronic (often subclinical) mastitis is not necessarily accompanied by long term high SCC (12). At this stage of advancement, it is impossible to calculate the precise probability of cure using the parameters indicated above, even though their influence has proven useful. A reliable prognosis would require the inclusion of additional diagnostic parameters (19); nonetheless, an approximation to the real probability of bacteriological cure is possible and can support decision making (15). Acknowledgements

The project was supported by funds from the Federal Ministry of Food, Agriculture and Consumer Protection (BMELV) based on a © Schattauer 2015


decision of the Parliament of the Federal Republic of Germany through the Federal Office for Agriculture and Food (BLE) under the innovation support program. Conflict of interest

The authors declare no conflict of interest.

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