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alckenierquarter-levelestimationoftheimPactofnon-aureusstaPhylococcalinfectiononudderhealthandmilkyieldindairyheifers Dimitri Valckenier 2021
Precise Quarter-Level Estimation of the Impact of Non-Aureus Staphylococcal Intramammary
Infection on Udder Health and Milk Yield in Dairy Heifers
Dimitri Valckenier
Merelbeke, 2021
“A pessimist sees difficulty in every opportunity;
an optimist sees opportunity in every difficulty.”
Winston Churchill
“The pessimist complains about the wind; the optimist expects it to change;
the realist adjusts the sails.”
William Arthur Ward
Intramammary Infection on Udder Health and Milk Yield in Dairy Heifers Dimitri Valckenier
Cover design: Creativision, Erpe-Mere Printing: University Press, Wachtebeke
ISBN number: 9789464202434
Department of Reproduction, Obstetrics, and Herd Health Faculty of Veterinary Medicine
Ghent University
Precise Quarter-Level Estimation of the Impact of Non-Aureus Staphylococcal Intramammary
Infection on Udder Health and Milk Yield in Dairy Heifers
Dimitri Valckenier
Dissertation submitted to Ghent University in the fulfillment of the requirements for the degree of Doctor in Veterinary Sciences (PhD)
June 18, 2021
Faculty of Veterinary Medicine, Ghent University, Belgium Prof. dr. Sofie Piepers
Faculty of Veterinary Medicine, Ghent University, Belgium
Members of the Examination Committee Prof. dr. Edwin Claerebout, chairman
Faculty of Veterinary Medicine, Ghent University, Belgium Dr. Anneleen De Visscher
Flanders Research Institute for Agriculture, Fisheries, and Food (ILVO), Belgium Prof. dr. Marie Joossens
Faculty of Sciences, Ghent University, Belgium Prof. dr. Gerrit Koop
Department Population Health Sciences, Utrecht University, the Netherlands Prof. dr. Bart Pardon
Faculty of Veterinary Medicine, Ghent University, Belgium Prof. dr. Ynte H. Schukken
GD Animal Health, the Netherlands – Department of Animal Sciences, Wageningen University, the Netherlands – Department of Population Health Sciences, Utrecht University, the Netherlands
Chapter 1 General introduction 1
Chapter 2 Scope and aims of the thesis 29
Chapter 3 Effect of intramammary infection with non-aureus staphylococci in early lactation in dairy heifers on quarter somatic cell count and quarter milk yield during the first 4 months of lactation
33
Chapter 4 The effect of intramammary infection in early lactation with non- aureus staphylococci in general and Staphylococcus chromogenes specifically on quarter milk somatic cell count and quarter milk yield
65
Chapter 5 Longitudinal study on the effects of intramammary infection with non-aureus staphylococci on udder health and milk production in dairy heifers
103
Chapter 6 General discussion 143
Summary 191
Samenvatting 197
Curriculum vitae and publications 205
Dankwoord 213
AMS Automatic milking system
AS Ali and Schaeffer
BMSCC Bulk milk somatic cell count CFU Colony forming units
cIMI Cured intramammary infection CM Clinical mastitis
d Days
DCC Direct cell counter DHI Dairy herd improvement
DHIA Dairy Herd Improvement Association
DIM Days in milk
IMI Intramammary infection
LnSCC Natural log-transformed somatic cell count LSM Least squared means
MALDI-TOF Matrix-assisted laser desorption/ionization time of flight MLST Multilocus sequence typing
Mo Months
MS Mass spectrometry
MY Milk yield
NAGase N-acetyl-β-D-glucosaminidase NAS Non-aureus staphylococci nIMI New intramammary infection PCR Polymerase chain reaction PFGE Pulsed-field gel electrophoresis pIMI Persistent intramammary infection PMNL Polymorphonuclear leukocytes
PRL Prolactin
q Quarter
qMY Quarter milk yield qPRL Quarter milk prolactin
qSCC Quarter milk somatic cell count
RAPD-PCR Random amplification of polymorphic DNA - polymerase chain reaction
RIA Radioimmunoassay
S. Staphylococcus
SCC Somatic cell count SCM Subclinical mastitis
SD Sampling day
SE Standard error
tDNA-PCR Transfer RNA intergenic spacer - polymerase chain reaction tIMI Transient intramammary infection
G eneral introduction
D. Valckenier
Department of Reproduction, Obstetrics, and Herd Health Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
1. Bovine mastitis
1.1. What is bovine mastitis?
Bovine mastitis, defined as an inflammation of the mammary gland parenchyma (Fig. 1), is an immunological reaction to infectious or noninfectious injury (e.g., physical trauma or toxic agents). The majority of mastitis cases are associated with bacteria, with over 137 species, subspecies and serovars that have been isolated from the mammary gland (Watts, 1988). A minority of mastitis cases can be attributed to other organisms such as yeasts, fungi, algae (Watts, 1988) and viruses (Gourlay et al., 1974; Wellenberg et al., 2002; Çomakli and Özdemir, 2019). Intramammary infections (IMI) are usually caused by bacteria invading the bovine mammary gland through the teat canal by growth or propulsion (Blowey and Edmondson, 2010) and subsequently adhering to the mammary tissue.
Based on the clinical presentation, mastitis can be categorized as subclinical mastitis (SCM) or clinical mastitis (CM). In cases of SCM there are no visible changes to the milk, udder, and cow (Ruegg, 2011); however, there is an inflammatory reaction resulting in an influx of white blood cells, primarily polymorphonuclear neutrophil leukocytes. The most common method to detect this type of mastitis is by measuring the somatic cell count (SCC) in the milk.
Inflammation in the mammary gland combined with the potential adverse effects of invading bacterial pathogens in the udder parenchyma can result in suboptimal milk production in the affected quarter (Koldeweij et al., 1999; Seegers et al., 2003; Halasa et al., 2007). Conversely, in cases of CM, a variety of symptoms can be observed such as altered milk composition (e.g., flakes, watery milk, …), local symptoms in the udder (e.g., swelling, loss of the function of a quarter, …), systemic symptoms, and even death (Ruegg, 2011).
Figure 1: Schematic illustration of the anatomy of one udder quarter from the bovine mammary gland.
Adapted from http://www.ubrocare.com/content/udder-anatomy
1.2. Importance of bovine mastitis in general and heifer mastitis in specific
After more than 30 years, the dairy sector in the European Union entered a new economic context in 2015 with the termination of the milk quota system. As milk prices become more volatile and resources for milk production (e.g., nutrition, ground, labor, ...) more expensive, optimizing the milk production and management on dairy farms is more crucial than ever.
Additionally, an increasing trend in herd size and specialization in the dairy industry requires ever-increasing investments of the herd owner. The income of most dairy farms relies almost
production is of the utmost importance. Producing large quantities of milk requires a well- developed and healthy udder to meet the quality standards. For example, infection of the udder tissue in the developing udder (Trinidad et al., 1990a) or during the first lactation (De Vliegher et al., 2005b) could potentially threaten the milk production capacity of the developing udder and might impair the udder health for the duration of the productive life of the dairy cow (Rupp et al., 2000).
Heifers, i.e., cows in their first lactation, form the future of each dairy herd. They replace older cows at the end of their productive life, both for milking and breeding. On well-managed dairy farms, implementation of continuous genetic selection and well-considered breeding programs results in new generations of animals with higher genetic merit for milk production than previous generations. Therefore, the goal of each dairy herd should be to raise bred heifers in optimal conditions to maximize the expression of their genetic potential. The IMI status of pre-calving heifers is seldomly checked because pre-existing IMI before calving is unexpected (Nickerson, 2009) and it is less feasible to collect mammary secretion samples. Unfortunately, heifers often have IMI before their first calving. Depending on the herd and region, estimated IMI prevalences range from 12% to 75% of the quarters of heifers before and around calving (Oliver and Mitchell, 1983; Trinidad et al., 1990b; Roberson et al., 1994; Parker et al., 2007;
Fox, 2009). Infections of the udder in late gestation or in lactation form a threat to the genetic potential of heifers (De Vliegher et al., 2012).
The impact of IMI depends on, amongst others, the form of mastitis (subclinical versus clinical), the pathogenicity and virulence of the invading bacteria (major versus minor pathogens), the time and duration of the infection relative to calving, and the host’s immunity (De Vliegher et al., 2012). Heifer mastitis results in extra costs and/or financial losses that can be ascribed to milk production losses, additional labor, use of drugs, veterinary needs, premature culling, production of nonsaleable milk and risk of residues. The combined costs of an elevated SCC in early lactation that decreased again, an elevated SCC at calving that evolved in SCM, and a clinical heifer mastitis case associated with an elevated SCC at calving, resulted in an average total cost of €31 per heifer present on a farm (range: €0 - €220) (Huijps et al., 2009). However, not all reports on IMI in early lactating heifers show a negative effect. When compared to noninfected heifers, IMI caused by non-aureus staphylococci (NAS) in early
lactation results in a higher milk yield (MY), a lower risk of culling, and fewer cases of clinical mastitis (Piepers et al., 2009, 2010, 2013).
In many countries and regions, raw bovine milk must meet the high quality standards described by legislation to be fit for human consumption. Regarding these legal requirements in the European Union, Council Directive 92/46/EEC states that raw milk may not originate from cows whose general state of health is impaired or have a recognizable inflammation of the udder, and that the bulk tank milk’s geometric average SCC of 4 measurements per month over a period of 3 months must be lower than 400,000 cells/mL milk. In the United States of America, the legislation is based on the federal Pasteurized Milk Ordinance and implemented by a series of rules and regulations by the different states.
Globally, the general bovine udder health has improved greatly by implementing diverse control programs and preventive measures (e.g., the 10 point plan of the National Mastitis Council) (National Mastitis Council, 2011), with a significant reduction in the incidence of IMI by Staphylococcus (S.) aureus, streptococci and coliforms. However, mastitis remains the most important disease in the dairy sector worldwide. And in a context of a continuously increasing worldwide concern regarding the usage of antibiotics and the emergence of antimicrobial resistance, the importance of animal health should not be overlooked as 50% of the total amount of antibiotics used in the European Union were administered to animals (van den Bogaard and Stobberingh, 2000). All animal production systems are currently contributing to lower their usage of antibiotics. A good udder health management is of utmost importance because IMI are one of the most frequent reasons for antimicrobial therapy in dairy herds worldwide (Pol and Ruegg, 2007; Brunton et al., 2012; Stevens et al., 2016a). In a cohort of Flemish dairy herds, about 29% of the total amount of antibiotics were used for the intramammary treatment of subclinical and clinical mastitis cases and 33% for dry cow therapy via long acting antimicrobial preparations (Stevens et al., 2016a). However, the finding that a better udder health management and implementation of preventive measures is not always associated with a lower antimicrobial usage, and vice versa, was quit strikingly (Stevens et al., 2016b).
2. Role of non-aureus staphylococci in bovine mastitis
Non-aureus staphylococci, consisting of more than 50 (sub)species, form a heterogeneous group of Gram-positive bacteria (Piessens et al., 2011). Until recently, NAS were generally termed coagulase-negative staphylococci. In most clinical laboratories the differentiation of staphylococci was performed by the tube coagulase test in which the ability to clot plasma by converting fibrinogen to fibrin was tested. At the time, all Staphylococcus species other than S.
aureus were often regarded as coagulase-negative. However, some Staphylococcus species have the (variable) ability to clot plasma such as S. delphini, S. agnetis, S. lutrae, S.
pseudintermedius, S. schleiferi subsp. coagulans, S. hyicus, S. intermedius, and S. chromogenes (Roberson et al., 1996; Vanderhaeghen et al., 2015; Santos et al., 2016).
Before genotypic methods were commonly available, a scale of phenotypic methods, such as API Staph ID 20 (Carretto et al., 2005) or 32 (Ieven et al., 1995), Vitek Gram-Positive Identification Card (Bannerman et al., 1993), and several others, were used for the identification of NAS species. However, these tests were mainly validated for human NAS species, depend on the variable expression of certain phenotypic characteristics of the bacteria, and were rather subjective to interpret, making them less accurate than genotypic methods such as gene sequencing (Ruegg, 2009). One of the more recent developments in identification methods is the matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry, which has proven to be a reliable assay for identification of NAS species from ruminants when using a database of spectra of bovine mastitis pathogens (Cameron et al., 2018; Gosselin et al., 2018; Mahmmod et al., 2018b).
2.1. Prevalence of non-aureus staphylococci
According to studies carried out in 100 Belgian dairy herds (De Visscher et al., 2017) and in all 4,258 Danish dairy herds (Katholm et al., 2012), it is estimated that NAS species are present in practically all dairy herds. In the last 2 decades, NAS have become the most isolated bacteria from cases of SCM on well-managed dairy farms that have controlled contagious major mastitis pathogens and have a low bulk milk SCC (BMSCC) (Pitkälä et al., 2004; Bradley et al., 2007; Piepers et al., 2007; Pyörälä and Taponen, 2009; Reyher et al., 2011). In a meta-
analysis of studies published between 1971 and 2000, the prevalence of IMI caused by NAS varied between 5.5% and 27.1% at the quarter level (Djabri et al., 2002). At least 26 different NAS species have been isolated from bovine milk samples: S. agnetis, S. arlettae, S.
auricularis, S. capitis, S. caprae, S. chromogenes, S. cohnii, S. devriesei, S. epidermidis, S.
equorum, S. fleurettii, S. gallinarum, S. haemolyticus, S. hominis, S. hyicus, S. lentus, S.
nepalensis, S. pasteuri, S. pseudintermedius, S. saprophyticus, S. sciuri, S. simulans, S.
succinus, S. vitulinus, S. warneri, and S. xylosus (Persson Waller et al., 2011; Piessens et al., 2011; Taponen et al., 2011; Youn et al., 2011; De Visscher et al., 2014, 2016; Fry et al., 2014;
Mahmmod et al., 2018a).
Although the prevalence and distribution of the different species is herd- and regional- dependent, the 5 NAS species that have been most frequently isolated from bovine mastitis cases and identified by molecular identification techniques are S. chromogenes, S. simulans, S.
haemolyticus, S. xylosus and S. epidermidis (Vanderhaeghen et al., 2014). However, studies using the more reliable genotypic identification methods and reporting NAS species-specific prevalence data are scarce. Staphylococcus chromogenes appears to be the predominant species amongst the group of NAS, with more than 40% of the isolates belonging to this species in heifers and multiparous cows (Supré et al., 2011; Fry et al., 2014; Tomazi et al., 2015; De Visscher et al., 2016; Condas et al., 2017a).
Risk factors at the herd, cow, and quarter level for NAS IMI have been identified for multiple species (Piessens et al., 2011; Bexiga et al., 2014; De Visscher et al., 2016). For example, heifers were shown to be more prone to NAS IMI than multiparous cows, especially in early lactation (Matthews et al., 1992; Bradley, 2002; Tenhagen et al., 2006; Sampimon et al., 2009; De Vliegher et al., 2012). Previous studies reported a proportion of SCM caused by NAS of 21.8% to 39.0% at first calving (Roberson et al., 1994; Fox et al., 1995; Nickerson et al., 1995) and of 19.3% to 35.3% in early lactation (Aarestrup and Jensen, 1997; Piepers et al., 2010) in heifers.
2.2. Impact of intramammary infections caused by non-aureus staphylococci on udder health
Due to variations in study design and in identification methods (i.e. phenotypic methods vs.
genotypic methods), many studies reported contradictory conclusions regarding the relevance of NAS for udder health (Vanderhaeghen et al., 2015). In general, NAS were considered to be minor mastitis pathogens or even harmless commensals (Piepers et al., 2009; Schukken et al., 2009; Vanderhaeghen et al., 2014), and their clinical relevance was under debate (Compton et al., 2007). However, in most studies published in the past 10-15 years, NAS are generally considered minor pathogens that cause a moderate increase of the SCC, and to a lesser extent able to cause mild cases of CM (Schukken et al., 2009; Fry et al., 2014; Tomazi et al., 2015).
More ambiguity exists on the potential species differences in impact for udder health. In 2 Finnish studies, one reported that clinical symptoms were related to the NAS species involved and were most severe when caused by S. hyicus (Honkanen-Buzalski et al., 1994), whereas the other study showed no such relation (Taponen et al., 2006). Some studies found no significant differences in quarter milk SCC (qSCC) between the different NAS species (Hogan et al., 1987;
Bexiga et al., 2014), whereas others reported relevant species differences (Supré et al., 2011;
Fry et al., 2014). Staphylococcus chromogenes, S. simulans, and S. xylosus were called the species “more relevant for udder health” due to their ability to raise the qSCC to a level comparable to that of S. aureus (Supré et al., 2011), although the power in that study was low.
This is however a common issue in many studies investigating the impact of NAS IMI, especially because many different NAS species occur and the differences in SCC and MY compared with noninfected animals or quarters are relatively small, thus resulting in the need for huge numbers of animals to have sufficient IMI cases with the different NAS species in order to have sufficient power in the analysis. Staphylococcus chromogenes was also amongst the NAS species that resulted in a significantly higher qSCC compared with noninfected quarters and was more prevalent in high than in low SCC quarters (Fry et al., 2014; Condas et al., 2017b). Heifers were at greater risk to be infected with the “more relevant” species when compared with multiparous cows (Taponen et al., 2007; De Visscher et al., 2015). Although heifers with an elevated SCC in early lactation had a higher culling risk (De Vliegher et al., 2005a), heifers having an IMI caused by NAS (as a group) had a significantly lower incidence
of CM (Piepers et al., 2010), leaving the question open whether control programs should also focus on NAS prevention or not. Still, the number of studies identifying the NAS isolates at the species level and determining the IMI status and milk SCC at the quarter level are limited, and most of them lack a longitudinal follow-up.
2.3. Impact of intramammary infections caused by non-aureus staphylococci on milk yield
The effect of IMI caused by NAS on MY is the subject of controversy and conflicting conclusions in the past 40 years (Table 1 and 2), and has yet to be unequivocally clarified. Most remarkable is the finding that IMI with NAS had a positive association with MY, despite an increased SCC (Wilson et al., 1997; Compton et al., 2007; Schukken et al., 2009; Piepers et al., 2010, 2013). This suggests that NAS are capable of causing IMI resulting in an elevated SCC yet not in less milk; on the contrary (Piepers et al., 2009, 2010). One of the potential explanations for this higher MY is that NAS IMI might lead to a higher local production of prolactin, the main lactogenic hormone in ruminants (Lacasse et al., 2016), in the udder. Indeed, the bovine mammary gland is able to synthesize prolactin (Piccart, 2016), but despite a trend towards a higher milk prolactin level in NAS-infected quarters, the prolactin gene expression is not different compared with noninfected quarters, thus leaving many questions about the prolactin level and its potential role in the higher MY of NAS-infected quarters. However, it might also be possible that high-yielding animals were more prone to NAS IMI, although it has been shown that a higher MY was no significant risk factor (Dolder et al., 2017; Piepers et al., 2011). On the other hand, a plethora of studies have found no association between IMI with NAS and MY (Eberhart et al., 1982; Kirk et al., 1996; Paradis et al., 2010; Pearson et al., 2013;
Tomazi et al., 2015; Heikkilä et al., 2018), as can be expected taking into account the status of NAS as minor pathogens. This would also confirm that not all NAS isolated from the udder cause IMI but rather act as commensals (Isaac et al., 2017). Other studies, however, detected a slight decrease in milk production due to IMI with NAS (Timms and Schultz, 1987; Gröhn et al., 2004; Thorberg et al., 2009; Simojoki et al., 2011). These findings are likely explained by the fact that an increased SCC caused by NAS IMI results in a proportional decrease in MY (Koldeweij et al., 1999; De Vliegher et al., 2005b).
The association between NAS IMI and MY is influenced by a whole complex of other factors, e.g. type of infection (clinical vs. subclinical mastitis), parity and stage of lactation of the studied animals, … Differences and even some flaws in the design of the aforementioned studies might explain why no general conclusions could be drawn about the association between NAS IMI and MY. First of all, most studies have considered NAS as a group rather than scrutinizing the individual NAS species, or at least the most prevalent species, separately. Due to the diversity of this group of bacteria with species that differ in pathogenicity and virulence and have a species-dependent effect on (q)SCC (Vanderhaeghen et al., 2014, 2015), the association with MY could have depended on the type of NAS species. If the predominant NAS species was different between the studies, and these species had not the same effect on milk production, this may explain why a negative association with MY was found in some studies, whereas no association or a positive association was observed in other studies. However, when multiple species had a similar prevalence within a study, the effects could be just averaged out, thus resulting no overall association between MY and NAS IMI. Several studies have also included both heifers and multiparous cows, whereas it has been shown that the odds of being infected with the “more relevant species” S. chromogenes, S. simulans and S. xylosus is higher in heifers (De Visscher et al., 2016). However, the conclusions of studies including only heifers were not unambiguous either. Also, most of the previous studies, except 2, were observational studies that did not allow to determine the causal relationship between NAS IMI and MY. Thus it could also have been possible that the cows with the highest MY were more susceptible to NAS IMI. The fact that in 2 experimental challenge studies (Piccart et al., 2015; Simojoki et al., 2011) a negative association was found, albeit with a small study group, may have complicated the interpretations of the results even more. If more high-yielding animals were having NAS IMI, and these infections resulted in a lower MY, these animals could have had a MY that was no longer different from that of uninfected herd mates, as was observed in the study by Gröhn et al. (2004). Furthermore, in almost all studies, MY was measured at the cow level (e.g., via Dairy Herd Improvement data). The total production of an animal measured in those studies is the result of the combined production of 4 separate mammary quarters. This could lead to distorted results because it has been shown that a reduced or absent milk production in one quarter can be partially compensated by a higher production of milk in the
Table 1. List of publications studying the association between IMI caused by NAS and milk yield in dairy cows: overview of the study designs. (continued on next page) Study Design No.1 of herds No. of animals No. of quartersParity of included animals Stage of lactation Clinical or subclinical
Quarter or composite milk samplesNAS2 species identification
Most prevelant NAS species Eberhart 1982 Observational 29Not available Not available All paritiesAll stagesSubclinicalQuarterNo / Timms and Schultz 1987Observational 2 139 554 All paritiesAll stages Subclinical and clinicalQuarterNo / Kirk 1996Observational1 339 / HeifersPeripartumSubclinical CompositeNo / Wilson 1997 Observational1,601 108,312 / All paritiesAll stages SubclinicalCompositeNo / Gröhn 2004 Observational2 3,071 692 cases
Heifers and multiparous cows analyzed separately
All stages Clinical QuarterNo / Compton 2007Observational 30708 2,664 HeifersPeripartumSubclinical and clinicalQuarterNo / Schukken 2009Observational 4,200 352,614 / Separate analyses for heifers and cows All stages SubclinicalCompositeNo / Thorberg 2009Observational 11587 2,303 All paritiesAll stages SubclinicalQuarterYes (via biochemical tests)
S.3 epidermidis, S. simulans, S. chromogenes Piepers 2010Observational20191
764 (of which 56 with unknown IMI4 status)
HeifersPeripartumSubclinical QuarterNo /
Table 1continued. List of publications studying the association between IMI caused by NAS and milk yield in dairy cows: overview of the study designs. Study Design No. of herds No. of animals No. of quarters
Parity of included animals Stage of lactation Clinical or subclinical
Quarter or composite milk samplesNAS species identification
Most prevelant NAS species Paradis 2010Observational501,691 / HeifersPeripartumSubclinical CompositeNo / Simojoki 2011Experimental challenge 1 8 16 (2 quarters per animal) HeifersMid- lactation
Mild to moderate clinical signs in all animal
Quarter/ / Piepers 2013Observational30344 1,354 HeifersPeripartumSubclinical QuarterNo / Pearson 2013Observational1 38 (19 monozygo- tic twins)154 HeifersPeripartumSubclinical QuarterNo / Tomazi 2015 Observational21285 1,140 All parities All stages SubclinicalQuarterYes (via PCR- RFLP5) S. chromogenes Piccart 2015 Experimental challenge 1 8
24 (3 quarters per animal, and every fourth quarter served as control quarter)
HeifersMid- lactation
No visual signs of clinical mastitis
Quarter/ / Heikkilä 2018 Observational 3,953 20,234Not available All paritiesAll stages
Subclinical and clinical (separate analyses) QuarterNo / 1 Number.2 Non-aureus staphylococci. 3 Staphylococcus. 4 Intramammary infection.5 Polymerase chain reaction - restriction fragment length polymorphism.
Table 2. List of publications studying the association between IMI caused by NAS and milk yield in dairy cows: overview of the results and conclusions.Continued on next page) Study
MY1 measured at animal or quarter level Period of MY measurements
Association between NAS2 IMI3 and MY Difference in MY between NAS-infected and noninfected quarters/animals Eberhart 1982 Animal1 DHIA4 record No association (not available). Timms and Schultz 1987AnimalEvery 28 d5 during entire lactation Negative -821 kg over 305 d period (P-value < 0.05) for all parities. Decreases of 776, 940, and 658 kg milk in 305 d for first, second, and third or greater lactation animals compared with uninfected animals (P-value < 0.05). Kirk 1996Animal5 months via DHIA recordsNo association 0 kg/d. Wilson 1997 AnimalDHIA from 1991 to 1995 Positive+41 kg on 305 d. Gröhn 2004 AnimalWeekly milk yield dataNegative
Heifers with NAS CM6 at a median DIM7 of 2: lactation curve was slightly lower. Largest drop (3.2 kg/d) in the week immediately following diagnosis (95% CI8: -6.6, 0.2 kg/d). After that, daily losses fluctuated between 1 and 3 kg/d. Multiparous cows with NAS CM significantly outproduced their healthy herdmates (2.5 kg/d) before diagnosis of CM. After diagnosis, they dropped down to the same level as healthy cows. Therefore, milk loss in such cases is greater than might at first be supposed. If the cows had not contracted CM, their milk yield would have been even higher. Compton 2007AnimalWhole lactation Positive+0.6 kg/d at first DHIA recording and 0.7 kg/d over entire lactation. Schukken 2009AnimalWhole lactation Positive+0.45 kg/d. Thorberg 2009Animal2 DHIA records with 4 week intervalNegative Cows with nonpersistent SCM9 had significantly (P-value < 0.01) lower production than healthy cows. When comparing all cows with nonpersistent or persistent SCM, significantly (P-value < 0.01) higher milk production was observed among persistently infected cows. Piepers 2010AnimalUntil 285 DIMPositive+2.9 kg/d.
