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. 2020 Aug 18;98(Suppl 1):S9–S14. doi: 10.1093/jas/skaa143

Antimicrobial use in dairy cattle in the Netherlands

Theo J G M Lam 1,2,✉, Annet E Heuvelink 1, Maaike A Gonggrijp 1, Inge M G A Santman-Berends 1
PMCID: PMC7433912  PMID: 32810248

Introduction

Since penicillin was discovered by Alexander Fleming (1929), the mortality of infectious diseases decreased and antimicrobials were widely applied in both human and veterinary medicine. As early as 1940, penicillinase-producing bacteria were described (Abraham and Chain, 1940). In that same decade, already epidemics of antimicrobial-resistant strains of Staphylococcus aureus occurred in U.S. hospitals. In those days, physicians heavily relied on antimicrobials, both for treatment and for prophylaxis. Outbreaks of resistant S. aureus forced the implementation of epidemiological studies and novel infection control measures, such as segregation, as has been described by Shaffer (2013). In veterinary medicine, antimicrobials were initially used therapeutically, but soon nontherapeutic use was also found to be attractive. Feeding low dosages of antimicrobials promoted growth and was considered to prophylactically protect against bacterial disease. After World War II, this type of use of antimicrobials through feed was rapidly adopted by farmers, eager to anticipate on the booming post-war demand for meat (Kirchhelle, 2018).

In dairy cattle, antimicrobials were initially mainly used for the treatment of bacteriological infections. That changed with the introduction of blanket dry cow treatment in the 1960s of the previous century (Neave et al., 1969) where it was recommended to treat all cows with antimicrobials at drying off, irrespective of their infection status. Since the beginning of this century, however, reduction of antimicrobial usage in farm animals became an important issue on the political agenda of several European countries. Where Scandinavian countries traditionally had a restricted approach on the usage of antimicrobials, the issue then also got full attention in other countries due to the presumed relation between antimicrobial use in farm animals and antimicrobial resistance in humans (Lowder et al., 2009; Spoor et al., 2013). In this paper, we discuss several aspects on antimicrobial use and resistance in dairy cattle that are potentially associated with antimicrobial resistance in humans. This work is based on experiences in the Netherlands during a period in which the political approach toward antimicrobial use in animal husbandry changed from indifferent to very demanding. General aspects of this changing approach are presented, while two types of resistant bacteria, methicillin-resistant S. aureus (MRSA) and extended-spectrum β-lactamase (ESBL)-producing bacteria, will be described in more detail.

Antimicrobial Use in Dairy Cattle in the Netherlands

Around the year 2008, the approach toward antimicrobial use in veterinary medicine in the Netherlands changed considerably. The background was a gradually increasing overuse of antimicrobials in veterinary medicine, a high prevalence of antimicrobial resistance in both human and animal pathogens, the fact that the same types of antimicrobials are used in humans and animals, and that pathogens, including those that are resistant to antimicrobials, can transfer from animals to humans. Several incidents, particularly on MRSA (Ekkelenkamp et al., 2006) and on ESBL-producing Escherichia coli (Smet et al., 2010), further increased the political pressure and made the parliament decide to target a stepwise decrease in the usage of antimicrobials in animal husbandry, with an ultimate goal of 70% reduction in 2015 as compared with 2009 (Speksnijder et al., 2015).

Even though antimicrobial usage in the dairy industry was already low compared with other animal husbandry sectors, the Dutch dairy sector managed to decrease the total antimicrobial usage by 47% in the period 2009 to 2015 (MARAN, 2012, 2016). Since then, antimicrobial usage remained more or less stable (MARAN, 2019). Additionally, during this period, the use of critically important antimicrobials decreased significantly to very low levels (Lam et al., 2017; MARAN, 2019). These changes were realized through an approach in which transparency of antimicrobial usage at the herd level, a ban on the preventive use of antimicrobials, a ban on the use of the WHO-defined critically important antimicrobials, and the introduction of herd health and herd treatment plans were crucial parts. An overview on measures to reduce antimicrobial usage in the dairy sector in the Netherlands has been described earlier by Lam et al. (2017). Simultaneously, extensive research was executed in order to find the best way to reduce antimicrobial usage without negative consequences for animal health and to understand the risk factors and epidemiological relations as well as the mindset of people involved, in order to smoothen the reduction in antimicrobial usage. Specific attention was given to reduction of the use of dry cow treatment, because that type of treatment attributed considerably to the usage of antimicrobials in dairy cattle and is partly prophylactic, which was no longer allowed. Extensive studies showed that introducing selective dry cow treatment, in which a limited number of cows in a herd are dried off with antimicrobials, did have a negative effect on udder health when compared with blanket dry cow treatment where all cows are dried off with antimicrobials. This probably is partly due to the removal of the preventive effect of dry cow antimicrobials (Scherpenzeel et al., 2016). In the same study, however, it was found that the negative consequences of selective dry cow treatment at herd level were very limited, while it led to a significant reduction in antimicrobial usage (Scherpenzeel et al., 2016). Further studies showed that application of blanket dry cow treatment was not the economic optimum in all dairy herds. If a herd has a low prevalence of subclinical mastitis and a low incidence of clinical mastitis, selective dry cow treatment is economically more beneficial compared with blanket dry cow treatment (Scherpenzeel et al., 2018). On the basis of these and other findings, selective dry cow treatment was introduced successfully in the Netherlands, with a significant decrease in the percentage of cows being dried off with antimicrobials (Figure 1), without a major deteriorating effect on udder health (Santman-Berends et al., 2016).

Figure 1.

Figure 1.

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Percentage of cows dried off with antimicrobials in the Netherlands (based on Scherpenzeel, 2017).

Product safety aspects related to human health, such as allergic reactions, as well as disadvantageous consequences for the production of, for example, yogurt and cheese are important reasons for tight regulations and monitoring on antimicrobial residues in milk. Thus, we assume that there always has been an intrinsic motivation for farmers to minimize the usage of antimicrobials in dairy cattle because of the economic consequences of being unable to deliver milk with antimicrobial residues to the dairy plant. For some of the critically important antimicrobials, however, this motivation could not exist because these had a zero withdrawal time for milk and were, therefore, extensively being used in the Netherlands in the first decade of the current century. Changing legislation and mindset led to an abrupt decrease in the usage of this type of antimicrobials from 2012 onwards (Lam et al., 2017). Another type of treatment in which this intrinsic motivation for limitation of antimicrobial usage likely was lacking is the treatment of young calves. Specifically in this group of animals, large differences between farms existed with a limited number of farmers using a lot of antimicrobials. Using large amounts of antimicrobials was found to be associated not only with reduced calf health, with respiratory disease, and with Salmonella status, but also with mindset. Whether a farmer is inclined to quickly treat with antimicrobials irrespective of the true infection status, or whether first supportive non-antimicrobial therapy is used, was found to have a significant effect on the usage of antimicrobials in young calves (Holstege et al., 2018).

Methicillin-Resistant Staphylococcus aureus

While trying to combat the antimicrobial resistance problem in the past 70 years, science and industry went through different phases evolving from relatively optimistic, via increasing concern to being publicly embedded in large concerns on global emerging infections (Podolsky, 2018). Serious problems are faced with MRSA, being a major cause of hospital-acquired infections that are very difficult to combat because of resistance to almost all available antibiotic classes. As early as 1961, S. aureus was found to be resistant to methicillin, a drug that was introduced in 1959 to treat infections caused by penicillin-resistant S. aureus (Enright et al., 2002).

In the Netherlands, the prevalence of MRSA in clinical samples from humans was described to be <1% (Voss et al., 2005), which was very low in comparison to other countries that were studied in the European Antimicrobial Resistance Surveillance System (Tiemersma et al., 2004). This result was considered to be best explained by the national policy that entails strict screening and isolation of all persons who are admitted to a hospital and are considered at high risk for MRSA. In a study in pig farmers, nasal MRSA prevalence was found to be as high as 23% (Voss et al., 2005), leading to questions with respect to infection risks in case of hospitalization of these people. A study in the same period in pig herds revealed a herd prevalence of 39%. Using Multi Locus Sequence Typing (MLST), the MRSA isolated from pigs all belonged to clonal complex 398 (CC398) (de Neeling et al., 2007). This confirmed that a high rate of strain exchange occurs between pigs and farmers, while these strains are hardly present in nonfarmers (Armand-Lefevre et al., 2005). In this period, it was decided that pig breeders, veterinarians, and slaughterhouse personnel, if admitted to a hospital, needed to be isolated until surveillance cultures were negative (Vandenbroucke-Grauls and Beaujean, 2006).

At the end of the previous century, the potential importance of MRSA in bovine mastitis was recognized, and it was emphasized that mastitis bacteriology laboratories need to identify MRSA accurately, because there is a problem in curing these intramammary infections (Watts and Salmon, 1997). Over the years, MRSA was also cultured from milk samples from dairy cattle in the Netherlands. During routine screening in Dutch dairy herds in the period from January to September 2008, 14 MRSA isolates were cultured out of approximately 35,000 quarter milk samples (Tavakol et al., 2012). These were all MRSA with MLST CC398, like the MRSA earlier cultured from clinical and subclinical mastitis cases in Belgium (Vanderhaeghen et al., 2010) and those isolated from pigs (de Neeling et al., 2007).

In a prospective study performed in the Netherlands in 2008, all quarters of heifers and cows with an elevated somatic cell count (SCC) (>150,000, respectively, >250,000 cells/mL) in 200 randomly selected dairy herds were sampled. Of 16,355 head of cattle, 2,873 had an elevated SCC, of which milk of all quarters with SCC > 200,000 cells/mL (n = 4,813) was cultured. From 1,897 of these samples, bacteria were cultured, of which S. aureus was identified in 419 cases. A total of 71 S. aureus isolates from 26 herds were β-lactamase positive, of which 7 (from 6 cows) were identified as MRSA, corresponding to a prevalence of 0.2% of the sampled cows and of 0.04% of all cows in the sampled herds (Olde Riekerink et al., 2009). In the same period, between March 2006 and December 2008, the prospective monitoring in the service laboratory of GD Animal Health identified 60 dairy farms being MRSA-positive, based on bacteriological culture of milk from one or more cows with (sub)clinical mastitis. Further analysis showed an association between the presence of MRSA in the milk samples and the presence of pigs on these farms. Dairy farms that also housed pigs had higher odds of being MRSA-positive compared with herds without pigs (odds ratio 6.3; 95% CI 3.1 to 12.8). Most of the MRSA-positive dairy herds, with or without pigs, were found to be located in the eastern part of the country, a region with high pig-herd concentrations (Figure 2) as was earlier described by Olde Riekerink et al. (2009).

Figure 2.

Figure 2.

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Dairy herds with at least one MRSA-positive quarter milk sample, projected over swine herd density in the Netherlands. Each dot represents a dairy herd, where blue dots are herds without and red dots are herds with swine on the same farm. The darker the yellow background color of the (postal code) areas is, the more swine herds are present (based on Olde Riekerink et al., 2009).

Overall, we found that the prevalence of intramammary infections with MRSA was very low in the Netherlands and that it was likely associated with the high prevalence of MRSA in pigs as described by de Neeling et al. (2007). Given the high MRSA prevalence among pig farmers (Voss et al., 2005), transmission of MRSA from pigs through farmers to dairy cows is possible, because the relation between MRSA in farmers and dairy cows has been described before (Juhász-Kaszanyitzky et al., 2007). Transmission through dust, however, is also possible, because MRSA was also cultured from dust samples in pig barns (van den Broek et al., 2009). Ultimately, all MRSA isolates from both pigs and dairy cattle were found to belong to MLST CC398, the livestock-associated lineage, which is a different lineage of MRSA than the typical lineages of the more virulent hospital-associated strains generally found in hospitalized people. MRSA CC398 has only incidentally been described as the cause of infection in human patients (Ekkelenkamp et al., 2006), suggesting that there is no indication of substantial cross-over of MRSA between farm animals and the general population or hospitalized people specifically.

Extended-Spectrum β-Lactamase-Producing Bacteria

Due to their multi-resistant character, their capacity to inactivate β-lactam antimicrobials including third- and fourth-generation cephalosporins, and the potential horizontal transmission of ESBL genes within and between bacterial species, ESBL-producing bacteria are a serious health threat (Peirano and Pitout, 2019). Genes encoding for ESBL production such as CTX-M, TEM-1, SHV, AmpC, and others are based on chromosomal DNA or on plasmids that can transmit resistance horizontally within and between bacterial species. ESBL-producing bacteria are often co-resistant or multi-resistant, exhibiting resistance to antibiotics of other antimicrobial classes (Jacoby and Munoz-Price, 2005). The relation between the occurrence of ESBL-producing bacteria in animals and humans acquired extra attention after the finding of a high prevalence of ESBL-producing E. coli in retail chicken meat, which partly carried the same genes, plasmids, and strain genotypes as E. coli obtained from human clinical isolates. This finding suggested that ESBL genes, plasmids, and E. coli isolates from poultry could potentially, most likely through the food chain, be transmitted to humans (Leverstein-van Hall et al., 2011).

Because ESBL-producing bacteria can be found widespread (Liakopoulos et al., 2016), we also studied the prevalence of these bacteria in manure samples of dairy herds in 2011 and evaluated its association with antimicrobial usage. Conventional dairy herds were compared with organic dairy herds which used a relatively small amount of antimicrobials. Regardless of herd type, the herd-level prevalence of ESBL-producing E. coli varied in time, with infections in individual cows that did not seem to persist. The prevalence of ESBL-producing E. coli was found to be not associated with the total usage of antimicrobials, whereas a significant association was found with the usage of critically important antimicrobials, possibly explaining the higher prevalence of ESBL-producing E. coli in conventional than in organic herds (Gonggrijp et al., 2016; Santman-Berends et al., 2017). The strongly decreased usage of critically important antimicrobials from 2012 onwards (Lam et al., 2017) may have been the cause of the decreased prevalence of ESBL-producing E. coli that was found in 2013, when the 2011 study in conventional dairy herds was repeated (Heuvelink et al., 2019).

Further studies on the dynamics of ESBL in dairy herds learned that the prevalence of ESBL-producing E. coli in feces of calves up to 21 d of age is much higher than in feces of older animals, with a prevalence of up to 33% in these young calves. This prevalence decreased over time, leading to prevalences of 2% in older young stock and 1% in heifers and cows (M. Gonggrijp and A. Heuvelink, unpublished data). The presence of ESBL-producing E. coli in young calves was found not to be associated with the presence of residues of dry cow antimicrobials in colostrum that was consumed by these calves (Ricci et al., 2016). The opposite was found with respect to residues in waste milk fed to calves in a study in England and Wales (Randall et al., 2014). They found, in concordance with our results (Gonggrijp et al., 2016; Santman-Berends et al., 2017), that not the total amount of antimicrobials but specifically the use of cefquinome on a farm, as well as the amount of its residues in waste milk, were associated with the occurrence of ESBL-producing E. coli in calves.

Because of the potential association between antimicrobial use in animals and antimicrobial resistance in humans, as earlier described by, for example, Leverstein–van Hall et al. (2011), a study was initiated in the Netherlands evaluating all possible sources of ESBL/AmpC-producing E. coli for the human population. The aim was to study the relatedness of human, animal, food, and environmental isolates of ESBL/AmpC-producing E. coli. In this study, distinguishable transmission cycles of ESBL/AmpC-producing E. coli were found for different types of hosts and in different types of environments, such as humans in the general and clinical population and humans in farming communities and their animals, both broilers and pigs. No epidemiological linkage of ESBL/AmpC genes and plasmid replicon types detected both in farms and in people in the general population could be found. These findings suggest that direct contact is the most important route of exchange of ESBL genes between reservoirs (Dorado-Garcia et al., 2017).

Discussion

In this paper, an overview was provided of the activities with respect to antimicrobial use and resistance in dairy cattle in the Netherlands. MRSA and ESBL-producing bacteria were described in more detail, because these are the most prominent bacteria with respect to the threat of transmission of antimicrobial-resistant bacteria from animals to humans. Although, for both types of bacteria, no direct relation between their occurrence in dairy cattle and antimicrobial resistance in the general human population could be found, prudent antimicrobial use both in humans and in dairy cattle and other animals is of utmost importance. First of all, because of the precautionary principle, we know that transmission of bacteria from animals to humans and vice-versa is definitely possible and that collateral transfer of antimicrobial resistance cannot be excluded (Aarestrup et al., 1997; Hendriksen et al., 2004). In order to minimize antimicrobial resistance in human pathogens, we also ought to act prudently when we use antimicrobials in animals. Because farmworkers were found to be at higher risk to become infected with certain types of bacteria (Juhász-Kaszanyitzky et al., 2007; Dorado-Garcia et al., 2017) and direct contact with animals seems to play an important role in that transmission (Dorado-Garcia et al., 2017), this group of people asks for specific attention.

Another important reason for prudent antimicrobial use in animals is animal health itself. We know that there is an association between antimicrobial use and resistance in animals, as has been described at the national level (Chantziaras et al., 2014) and at the herd level (Checkley et al., 2010, Saini et al., 2012). More specifically, as presented in this paper, the use of antimicrobials that are considered as critically important for human medicine also has its effect on antimicrobial resistance in animal pathogens. Thus, we should not forget that prudent antimicrobial use in animals is not only important from the perspective of transmission of antimicrobial resistance to humans but also for animal health itself.

To implement prudent antimicrobial use, the mindset of people involved is crucial, which can be influenced by using several approaches at the same time, reaching different types of people to realize a tipping point in social pressure (Lam et al., 2017). In the Netherlands, this led to a significant decrease in the usage of antimicrobials in animal husbandry (Speksnijder et al., 2015), including dairy cattle (Lam et al., 2017), which was realized without major negative consequences for animal health and production (Santman-Berends et al., 2016) and, therefore, seems an attractive example for other countries wanting to implement similar strategies.

Glossary

Abbreviations

CC398

clonal complex 398

ESBL

extended-spectrum β-lactamase

MLST

multilocus sequence typing

MRSA

methicillin-resistant Staphylococcus aureus

SCC

somatic cell count

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.

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