Advertisement

Economic optimization of selective dry cow treatment

Open ArchivePublished:December 07, 2017DOI:https://doi.org/10.3168/jds.2017-13076

      ABSTRACT

      The objective of this study was to develop a mathematical model to identify a scenario with the lowest costs for mastitis associated with the dry period while restricting the percentage of cows to be dried off with dry cow antimicrobials. Costs of clinical and subclinical mastitis as well as antimicrobial use were quantified. Based on data from a large field trial, a linear programming model was built with the goal to minimize the costs associated with antimicrobial use at drying off. To enable calculations on minimizing costs of dry cow treatment on herd-level by drying-off decisions in an “average” herd, we created an example herd. Cows were projected on 3 different types of herds, based on bulk tank somatic cell count, and were categorized in groups based on parity and somatic cell count from the last test recording before drying-off. Economically optimal use of antimicrobials was determined while restricting the maximum percentage of cows dried off with antimicrobials from 100 to 0%. This restriction reveals the relationship between the maximum percentage of cows dried off with antibiotics and the economic consequences. A sensitivity analysis was performed to evaluate the effect of variation in the most important input variables, with the effect of dry cow antimicrobials resulting in a lower or higher percentage of clinical and subclinical mastitis depending on being dried off with or without dry cow antimicrobials, respectively, and the milk price. From an economic perspective, blanket dry cow treatment seems not to be the optimal approach of dry cow therapy, although differences between approaches were small. With lower bulk tank somatic cell counts, more dry cow antimicrobials can be omitted without economic consequences. The economic impact of reducing the percentage of clinical mastitis was found to be much larger than reducing the bulk tank somatic cell count. The optimal percentage of cows to be dried off with antimicrobials depends on the udder health situation, expressed as the bulk tank somatic cell count and the incidence of clinical mastitis. For all evaluated types of herds, selective dry cow treatment was economically more beneficial than blanket dry cow treatment. Economic profits of selective dry cow treatment are greater if bulk tank somatic cell count and clinical mastitis incidence are lower. Economics is not an argument against reduction of dry cow antimicrobials by applying selective dry cow treatment.

      Key words

      INTRODUCTION

      Control of mastitis is of major importance for the dairy sector. Apart from other consequences, mastitis leads to high monetary costs because of treatment, discarded milk, and major production losses (
      • Hogeveen H.
      • Huijps K.
      • Lam T.J.G.M.
      Economic aspects of mastitis: New developments.
      ). In the dairy industry, antimicrobials are mainly used for treatment of clinical mastitis (CM) and dry cow treatment (DCT). For many years, approximately 60% of the antimicrobial use (AMU) in dairy cows in the Netherlands was related to mastitis, of which roughly two-thirds related to DCT (
      • Kuipers A.
      • Koops W.J.
      • Wemmenhove H.
      Antibiotic use in dairy herds in the Netherlands from 2005 to 2012.
      ).
      One of the points recommended since the 1970s in the 5 Points Mastitis Control Plan (
      • Neave F.K.
      • Dodd F.H.
      • Kingwill R.G.
      • Westgarth D.R.
      Control of mastitis in the dairy herd by hygiene and management.
      ) was blanket dry cow treatment (BDCT) to control the risk of new IMI during the dry period (
      • Dodd F.H.
      • Westgarth D.R.
      • Neave F.K.
      • Kingwill R.G.
      Mastitis–The strategy of control.
      ). The main goal of DCT was to reduce the prevalence of IMI, both by eliminating IMI present at drying off and preventing new IMI from occurring during the dry period (
      • Bradley A.J.
      • Green M.J.
      An investigation of the impact of intramammary antibiotic dry cow therapy on clinical coliform mastitis.
      ). In many countries, more than 90% of all dairy cows were treated with antibiotics during the dry period [e.g., 94% in the Netherlands (
      • Lam T.J.G.M.
      • van den Borne B.H.P.
      • Jansen J.
      • Huijps K.
      • van Veersen J.C.
      • van Schaik G.
      • Hogeveen H.
      Improving bovine udder health: A national mastitis control program in the Netherlands.
      ) and 99% in the United Kingdom (
      • Berry E.A.
      • Hillerton J.E.
      The effect of selective dry cow treatment on new intramammary infections.
      )].
      Due to public health concerns and risk for antimicrobial resistance (AMR), prudent and restricted use of antimicrobials is promoted and preventive use of antimicrobials for all food animals has been prohibited since 2012 in the Netherlands (
      • Santman-Berends I.M.G.A.
      • Swinkels J.M.
      • Lam T.J.G.M.
      • Keurentjes J.
      • van Schaik G.
      Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy.
      ). Selective dry cow treatment (SDCT), not using DCT in cows that had a low SCC at the last milk recording before drying off, significantly increased the incidence rate of CM as well as SCC postpartum in a study in the Netherlands (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Olde Riekerink R.G.M.
      • Keurentjes J.M.
      • Lam T.J.G.M.
      Evaluation of the use of dry cow antibiotics in low somatic cell count cows.
      ).
      A meta-analysis done by
      • Halasa T.
      • Osteras O.
      • Hogeveen H.
      • van Werven T.
      • Nielen M.
      Meta-analysis of dry cow management for dairy cattle. Part 1. Protection against new intramammary infections.
      showed that BDCT seemed to protect better against new IMI than SDCT, which seemed to protect better than no DCT at all. It was also shown that the decrease in AMU due to SDCT was substantial and by no means compensated by an increase in AMU due to an increased incidence rate of CM (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ).
      The effect of SDCT compared with BDCT on udder health, AMU, and economics is influenced by the criteria used to select cows for DCT (
      • Cameron M.
      • McKenna S.L.
      • MacDonald K.A.
      • Dohoo I.R.
      • Roy J.P.
      • Keefe G.P.
      Evaluation of selective dry cow treatment following on-farm culture: Risk of postcalving intramammary infection and clinical mastitis in the subsequent lactation.
      ;
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ). The chosen criteria have an effect on quantifiable parameters, such as CM incidence, AMU, and economics, but also nonquantifiable parameters, such as welfare and practical feasibility. These effects can be contradictory; SDCT as compared with BDCT leads to more CM cases and a higher SCC, whereas it decreases AMU substantially (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Olde Riekerink R.G.M.
      • Keurentjes J.M.
      • Lam T.J.G.M.
      Evaluation of the use of dry cow antibiotics in low somatic cell count cows.
      ). Udder health, welfare, production losses, AMU, and economic consequences are all parameters that are influenced by decisions on DCT, but that potentially move in different directions. Additionally, although the relationship between AMU and development of AMR in mastitis pathogens is complex and unclear (
      • Oliver S.P.
      • Murinda S.E.
      • Jayarao B.M.
      Impact of antibiotic use in adult dairy cows on antimicrobial resistance of veterinary and human pathogens: A comprehensive review.
      ), there is a potential effect of AMU on the development of AMR (
      • Chantziaras I.
      • Boyen F.
      • Callens B.
      • Dewulf J.
      Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: A report on seven countries.
      ). In decision making of farmers, this can, however, be considered as an externality because these consequences are experienced by the environment or society while they are not necessarily directly experienced by the farmer. A common way to quantify different parameters, with the exception of animal welfare and public health, is in economic units. As such, economic consequences along with animal welfare, legislation, and public health concerns, may be helpful in making decisions on animal health strategies.
      A few studies describe the economic consequences of DCT. Most economic analyses have concluded that BDCT is financially beneficial, because of increased milk yield, lower SCC, or reduced CM cases, when compared with SDCT or no DCT (
      • McNab W.B.
      • Meek A.H.
      A benefit cost analysis of dry-cow mastitis therapy in Ontario dairy herds.
      ;
      • Berry S.L.
      • Maas J.
      • Kirk J.H.
      • Reynolds J.P.
      • Gardner I.A.
      • Ahmadi A.
      Effects of antimicrobial treatment at the end of lactation on milk yield, somatic cell count, and incidence of clinical mastitis during the subsequent lactation in a dairy herd with a low prevalence of contagious mastitis.
      ;
      • Yalcin C.
      • Stott A.W.
      Dynamic programming to investigate financial impacts of mastitis control decisions in milk production systems.
      ). Most of these calculations were, however, based on uncertain assumptions and the results had much variation. In a study done by
      • Huijps K.
      • Hogeveen H.
      Stochastic modeling to determine the economic effects of blanket, selective, and no dry cow therapy.
      , SDCT was economically most attractive. In that study, however, differences between BDCT and SDCT were small and with regard to selection of the appropriate animals, the assumptions for DCT were rough. None of the above studies described the level of reduction of AMU while practicing SDCT.
      The economic impact of SDCT likely varies for different types of herds and for different levels of DCT use. Studies describing and evaluating economic consequences of SDCT on the herd level can be used by dairy farmers and their advisors to help them to optimize decisions on DCT, thereby minimizing costs. Thus, the economic consequences of decisions on DCT need further attention. Therefore the objective of this study was to develop a mathematical model to minimize economic costs while restricting the percentage of cows to be dried off with DCT, accounting for effects of CM, subclinical mastitis (SCM), and AMU.

      MATERIALS AND METHODS

      A randomized controlled field trial was carried out between June 2011 and March 2012 in the Netherlands in which the effect of DCT on CM, bacteriological status, SCC, and AMU was evaluated (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Olde Riekerink R.G.M.
      • Keurentjes J.M.
      • Lam T.J.G.M.
      Evaluation of the use of dry cow antibiotics in low somatic cell count cows.
      ). Based on these data, data from literature for high-SCC cows dried off with antimicrobials (
      • Barkema H.W.
      • Schukken Y.H.
      • Lam T.J.G.M.
      • Beiboer M.L.
      • Wilmink H.
      • Benedictus G.
      • Brand A.
      Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts.
      ) and smoothed data based on regression analysis for high-SCC cows dried off without antimicrobials (data not shown) a linear programming (LP) model was built with the goal to minimize the costs associated with AMU at drying off. In this model different approaches of selecting cows for DCT were compared based on the SCC at the last milk recording before drying off (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ). A timeframe of 1 yr was used to take seasonal differences into account and to represent the financial planning horizon of dairy farmers. The general purpose of an LP approach is to maximize or minimize a goal variable (e.g., maximize profit or minimize costs) by finding the optimal combination of different parameters with respect to a set of fixed constraints. Microsoft Excel (Microsoft Corp., Redmond, WA) was used to develop and run the LP model, using the Simplex Algorithm for optimization.

      Definition of the Herd

      To enable calculations on minimizing costs of DCT on herd-level by drying-off decisions in an “average” herd, we created an example herd. Cows that were dried off at the end of their first lactation were referred to as first dry period (FDP) cows at drying off, during the dry period and the first 100 DIM of the subsequent lactation. Cows that were dried off for the second or later time were referred to as multiple dry period (MDP) cows at drying off, during their dry period and the first 100 DIM of the subsequent lactation.
      Nine cow groups (i = 1–9) were considered, consisting of 4 classes of FDP cows (0–50,000 cells/mL; 51,000–100,000 cells/mL; 101,000–150,000 cells/mL; and >150,000 cells/mL) and 5 classes of MDP cows (0–50,000 cells/mL; 51,000–100,000 cells/mL; 101,000–150,000 cells/mL; 151,000–250,000 cells/mL; and >250,000 cells/mL). For each of these cow groups there were 2 options regarding DCT (j = 1,2), either dried off with (1) or without (2) dry cow antimicrobials. Thus, in total 18 units of activity were included in the model.
      Three different types of herds with respect to bulk tank SCC (BTSCC) were defined. One with a low BTSCC <150,000 cells/mL (BTL), one with an average BTSCC ≥150,000 cells/mL and <250,000 cells/mL (BTA), and one with a high BTSCC ≥250,000 cells/mL but <400,000 cells/mL (BTH), based on
      • Barkema H.W.
      • Schukken Y.H.
      • Lam T.J.G.M.
      • Beiboer M.L.
      • Wilmink H.
      • Benedictus G.
      • Brand A.
      Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts.
      . The distribution of cows over the 9 cow groups (1–9) for a BTL, BTA, and BTH herd (Table 1) was based on the approach of
      • Huijps K.
      • Lam T.J.G.M.
      • Hogeveen H.
      Costs of mastitis: Facts and perception.
      and on Dutch averages.
      Table 1Distribution of cows at drying-off in groups (1–9) in a 75-cow example herd, based on their SCC (×103 cells/mL) and parity at the last milk recording before drying off for a low-bulk tank SCC (BTSCC) herd (BTL), an average-BTSCC herd (BTA), and a high-BTSCC herd (BTH), and cow-level incidence of clinical mastitis (ICM) and subclinical mastitis (ISCM) when dried off with (j = 1) or without (j = 2) dry cow antimicrobials
      GroupSCCParity
      FDP = first dry period cows; MDP = multiple dry period cows.
      Number of cows included in the modelICM (%)ISCM (%)
      BTLBTABTHj = 1j = 2j = 1j = 2
      10–50FDP141049.911.84.87.2
      251–100FDP6749.110.810.619.0
      3101–150FDP23313.518.28.217.7
      4>150FDP351414.420.011.325.0
      50–50MDP287812.820.17.317.3
      651–100MDP1310915.226.813.618.8
      7101–150MDP4959.019.115.724.8
      8151–250MDP410516.524.118.431.7
      9>250MDP1142316.624.422.637.4
      1 FDP = first dry period cows; MDP = multiple dry period cows.

      Model Description

      Total economic costs of mastitis are the sum of preventive costs and failure costs. The preventive costs were the costs for use of DCT, where other preventive costs were not evaluated in this paper because they were assumed to be the same for the different approaches. Failure costs are the economic values of the losses and the economic values of the expenditures related to the occurrence of mastitis. Losses are costs associated with a cow being affected by CM or SCM (e.g., production losses, culling, discarded milk). Expenditures are the payments made by the farmer to treat mastitis.
      Calculation of the total economic costs of mastitis (TCM) for the example herd was done by summing the total costs of mastitis per unit of activity (TCMij), multiplied by the number of cows in each unit of activity (Nij):
      TCM=i=19j=12TCMij×Nij,
      [1]


      where TCM = total economic costs of mastitis, i = cow group 1 to 9, j = treatment with (1) or without (2) dry cow antimicrobials, TCMij = total costs of mastitis per unit of activity, and Nij = the number of cows in each unit of activity.
      The total economic costs of mastitis per unit of activity (TCMij) are the sum of the total costs of CM, SCM, and DCT per unit of activity:
      TCMij=TCCMij+TCSCMij+TCDCTij.
      [2]


      The total costs of CM in each unit of activity (TCCMij) are the incidence of CM in this unit of activity (ICMij) multiplied with the number of cows in this unit of activity (Nij) and the costs of a case of CM (CCM):
      TCCMij=ICMij×Nij×CCM.


      The total costs of SCM in each unit of activity (TCSCMij) are derived equally by multiplying the incidence of SCM in this unit of activity (ICMij) with the number of cows in this unit of activity (Nij) and the costs of a case of SCM (CSCM):
      TCCMij=ICMij×Nij×CCM.
      [4]


      The total costs of DCT in each unit of activity (TCSCMij) are the number of cows to be dried off in this unit of activity (ISCMij) times the costs per cow for dry cow treatment (CDCT):
      TCDCTij=NDCTij×CDCTj.
      [5]


      For cows dried off without antimicrobials (j = 2), there are no costs of DCT (TCDCTij=0).
      Data on all individual antimicrobial treatments regarding CM and DCT were collected during the field trial, consisting of active compound, application route, dosage, frequency, and duration of treatment. Antimicrobial usage for DCT and CM treatments was expressed as the calculated number of animal defined daily dosage (ADDD; i.e., the average number of days a cow receives antimicrobial treatment). One ADDD is defined as a standardized 1-d treatment, being the average dose for a 1-d treatment of a registered veterinary drug for its main indication. A cow dried off with antimicrobials was calculated as 4.0 ADDD (
      • Santman-Berends I.M.G.A.
      • Swinkels J.M.
      • Lam T.J.G.M.
      • Keurentjes J.
      • van Schaik G.
      Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy.
      ), and a case of CM as 3.0 ADDD, including both intramammary and parenteral treatment (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ). Antimicrobial treatment of SCM during lactation was not taken into account.

      Parameterization

      The example herd had a herd size of 100 dairy cows with an average age distribution of Dutch dairy herds (
      CRV
      ), in which 33% of animals had calved once and 67% had calved twice or more. Given a calving interval of 412 d (
      CRV
      ), an average culling rate of lactating cows in Dutch dairy herds of 30% (
      • Mohd Nor N.
      • Steeneveld W.
      • Hogeveen H.
      The average culling rate of Dutch dairy herds over the years 2007 to 2010 and its association with herd reproduction, performance and health.
      ), and 90% of cows to be culled that were not dried off, the total number of cows for drying-off during a year in the example herd was 75, of which 25 were FDP cows and 50 were MDP cows. The distribution of high-SCC and low-SCC animals was based on cow-level SCC data from the last milk recording before drying off of all animals of 97 herds included in a previously described field trial (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ). Cows that were dried off were grouped based on parity (FDP/MDP) and SCC at the last milk recording before drying off.
      The failure costs for a case of CM were calculated based on the average costs for CM cases during the first 3 mo of lactation and were adapted from
      • Huijps K.
      • Lam T.J.G.M.
      • Hogeveen H.
      Costs of mastitis: Facts and perception.
      . In that study, all cost categories, such as milk production losses, discarded milk, veterinary support, drugs, labor, and culling were included, but were based on a quotum situation. In our study, the average costs for a CM case were recalculated based on the calculation method of
      • Huijps K.
      • Lam T.J.G.M.
      • Hogeveen H.
      Costs of mastitis: Facts and perception.
      and using an average milk price levels in the post-quotum era of €0.35/kg and an average price level of concentrate feed costs of €0.13/kg of milk, making the net costs of milk production losses €0.22/kg of milk. Based on that, the costs of a case of CM in the first 100 DIM were set at €242.
      The failure costs for a case of SCM were calculated as milk production losses due to SCM multiplied by the related costs per kilogram of milk loss.
      • Halasa T.
      • Nielen M.
      • De Roos A.P.W.
      • Van Hoorne R.
      • de Jong G.
      • Lam T.J.G.M.
      • van Werven T.
      • Hogeveen H.
      Production loss due to new subclinical mastitis in Dutch dairy cows estimated with a test-day model.
      estimated milk production losses for different levels of increased SCC without differentiating parities and calculated that the average milk production loss of all cows with cow-level SCC >200,000 cells/mL was 0.87 kg/d. We set the average duration of an SCM case, irrespective of the causative pathogen at 85 d, based on
      • Lam T.J.G.M.
      • Schukken Y.H.
      • van Vliet J.H.
      • Grommers F.J.
      • Tielen M.J.
      • Brand A.
      Effect of natural infection with minor pathogens on susceptibility to natural infection with major pathogens in the bovine mammary gland.
      . The costs of production losses due to SCM were calculated as above, and were €0.22/kg. Thus, the economic losses for a case of SCM were €16.27 per case.
      The preventive costs of DCT consisted of AMU and labor of the farmer. It was estimated that it took on average 15 min to correctly dry-off a cow, at an hourly rate of €18, leading to €4.50 per cow (
      • Halasa T.
      • Nielen M.
      • De Roos A.P.W.
      • Van Hoorne R.
      • de Jong G.
      • Lam T.J.G.M.
      • van Werven T.
      • Hogeveen H.
      Production loss due to new subclinical mastitis in Dutch dairy cows estimated with a test-day model.
      ). The costs for dry-cow antimicrobials were assumed to be €11.00/cow, which makes CDCT1 €15.50. The milk price was calculated by taking the average prices over the last 5 yr from the Agrimatie database (
      Agrimatie
      ).
      Cow-level incidences of CM and SCM (Table 1) were based on quarter-level incidences from the field study for low-SCC cows, assuming that on average 1.3 CM quarters were affected per cow. For high-SCC cows, assumptions were based on literature from
      • Barkema H.W.
      • Schukken Y.H.
      • Lam T.J.G.M.
      • Beiboer M.L.
      • Wilmink H.
      • Benedictus G.
      • Brand A.
      Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts.
      , as is described in more detail in
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      .

      Optimization

      The LP model in the optimization phase will select cows within the groups (i = 1–9) for being dried off with (j = 1) or without (j = 2) dry cow antibiotics. The optimal situation for the example herd is the situation in which TCM is lowest. To calculate this, the LP model will give the minimal TCM related to mastitis in the dry period and first 100 DIM, based on the number of cows affected by CM and SCM and the amount of antimicrobials used for each unit of activity for different herd situations based on BTSCC.
      The restrictions for the groups in the model were
      i=19Ni1PDCT×N,
      [6]


      where PDCT = the maximum percentage of cows to be dried off with antimicrobials, and
      Ni1+Ni2=Nij,
      [7]


      where Nij = the number of cows per unit of activity.

      Simulation

      In the optimization part of the study, the LP model was used while restricting the maximum percentage of cows dried off with antimicrobials in SDCT from 100 to 0%. This restriction reveals the relationship between the percentage of cows dried off with antimicrobials and the economic consequences. The number of cows to be dried off with antimicrobials was reduced by steps of 5%, leading to 21 restriction levels, and for every level the LP model was run. Based on the restriction level, the LP model selected the cows in each group for being treated (j = 1) or not being treated (j = 2) with dry cow antimicrobials at drying off, to find the situation with the lowest TCM in the dry period and the first 100 DIM. Additionally, the average incidence of CM and SCM and the ADDD were calculated by the model for every restriction level.
      In the baseline level, all cows were allowed to be dried off with dry cow antimicrobials (100%). Drying off none of the cows with antimicrobials (0%) was the other extreme. All other levels applied SDCT, and cows were selected by the model for being treated with (j = 1) or without (j = 2) dry cow antimicrobials, depending on their parity (FDP or MDP) and their SCC at the last milk recording before drying off.

      Variation in Herd Level CM Incidence

      Clinical mastitis is an expensive disease (
      • Hogeveen H.
      • Huijps K.
      • Lam T.J.G.M.
      Economic aspects of mastitis: New developments.
      ) and strongly influences TCM. Because CM incidence can vary in herds with the same BTSCC (
      • Barkema H.W.
      • Schukken Y.H.
      • Lam T.J.G.M.
      • Beiboer M.L.
      • Wilmink H.
      • Benedictus G.
      • Brand A.
      Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts.
      ), we varied the initial incidence of CM per unit of activity as input parameter within the 3 types of herds. Thus, we modeled BTL, BTA, and BTH herds with low (BTLCL, BTACL, BTHCL), average (BTLCA, BTACA, BTHCA), and high (BTLCH, BTACH, BTHCH) incidence of CM as the initial situation. These incidences per type of herd were calculated by summing the multiplications of doubled (for high incidence) or halved (for low incidence) ICMij per unit of activity multiplied with Nij, and divided by 75 animals (formulas [8] and [9]).
      CH=i=19ICMij×2.0×Nij/75cows,
      [8]


      CL=i=19ICMij×0.5×Nij/75cows,
      [9]


      where ICMij = the incidence of CM in this unit of activity.
      Variation in the initial situation of the incidence of CM per unit of activity led to variance in the dependent output variable, being the mean herd-level incidence of CM.

      Sensitivity Analysis

      A sensitivity analysis was performed to evaluate the effect of variation in the most important input variables, being the effect of dry cow antimicrobials (ΔDCT) resulting in a lower or higher incidence of CM and SCM and the effect of milk price. Both these parameters directly affect the most important output variable in this study, TCM. To evaluate the effect of the use of dry cow antimicrobials, ΔDCT was varied per group by multiplying the difference between ICMil and ICMi2 per group with 0.5 as the lower limit and with 2.0 as the upper limit. The incidences of CM and SCM in the treated groups were the constant baseline and the incidences of CM and SCM in the untreated groups were varied, to analyze the sensitivity of the model. We expected that assumptions about milk price would have a substantial effect on TCM. Therefore we multiplied the average milk price of €35/100 kg by 0.775 as the lower limit and by 1.225 as the upper limit. This resulted in €27/100 kg of milk for a low milk price and €43/100 kg of milk for a high milk price. The sensitivity analysis was carried out for all 21 restriction levels in the BTL, BTA, and BTH herds to determine the effect on the minimal TCM.

      RESULTS

      Simulation

      All 21 DCT restriction levels were evaluated to study the effect of reducing the maximum percentage of cows to be dried off with antimicrobials on mastitis, AMU, and TCM during the dry period and the first 100 DIM. Results for CM, SCM, ADDD, and economics for the 21 restriction levels for the 3 types of herds (BTL, BTA, BTH) are presented in Table 2. Costs per cow to be dried off per year varied from €45 on a BTL herd where 100% of the cows were allowed to be dried off with antimicrobials to €56 on a BTH herd where no dry cow antimicrobials were allowed (Table 2). Clinical and subclinicial mastitis incidence in the different types of herds varied from 9.9 to 16.1% and from 8.2 to 19.6%, respectively. Antimicrobial use varied from 0.6 ADDD when no dry cow antimicrobials were allowed (0%) in BTL, BTA, and BTH herds to 3.9 ADDD when 100% of cows were allowed to be dried off with antimicrobials in a BTH herd.
      Table 2Mean incidence of clinical mastitis (ICM), mean incidence of subclinical mastitis (ISCM), animal defined daily dosage of antimicrobials per year (ADDD), and total economic costs of mastitis per cow per year (€)
      Calculations were done using the maximum percentage of dry cow antimicrobials (% AMU) as restriction level, which was reduced in steps of 5% from 100 to 0%, for a low-bulk tank SCC (BTSCC) herd (BTL), an average-BTSCC herd (BTA), and a high-BTSCC herd (BTH).
      % AMUBTLBTABTH
      ICMISCMADDDICMISCMADDDICMISCMADDD
      1009.98.23.244.5210.411.43.347.4211.011.93.951.17
      959.98.23.244.5210.411.43.347.4211.011.93.951.17
      909.98.23.244.5210.411.43.347.4211.011.93.951.17
      859.98.23.244.5210.411.43.347.4211.011.93.951.17
      809.98.23.244.5210.411.43.347.4211.212.43.651.18
      759.98.23.244.5210.411.43.347.4211.413.03.451.19
      709.98.23.244.5210.511.73.247.4311.613.43.351.20
      6510.18.73.044.5710.812.23.047.4911.813.93.151.26
      6010.49.12.844.7711.112.62.847.6812.114.32.951.45
      5510.79.52.644.9711.313.12.647.9112.414.72.751.66
      5010.99.82.545.1111.613.52.548.1112.615.12.551.86
      4511.210.22.345.3111.914.02.348.3712.915.72.352.16
      4011.510.62.145.5112.214.62.148.6713.316.32.152.47
      3511.811.11.945.7012.515.21.948.9813.616.91.952.78
      3012.011.41.745.8512.715.61.749.2113.817.31.853.01
      2512.311.91.546.1013.016.21.549.5214.117.91.653.32
      2012.612.31.346.5213.516.61.350.0814.418.51.453.63
      1513.112.61.147.1613.916.91.150.6414.818.91.254.13
      1013.412.81.047.6914.217.11.051.1315.119.21.054.59
      513.913.00.848.4114.717.30.851.8515.619.40.855.31
      014.313.20.649.1315.117.60.652.5716.119.60.656.02
      1 Calculations were done using the maximum percentage of dry cow antimicrobials (% AMU) as restriction level, which was reduced in steps of 5% from 100 to 0%, for a low-bulk tank SCC (BTSCC) herd (BTL), an average-BTSCC herd (BTA), and a high-BTSCC herd (BTH).

      Variation in Herd-Level CM Incidence

      Results of variation in the initial herd level CM incidence on the effect of a SDCT approach on TCM and the comparison with a BDCT approach for different types of herds are presented in Table 3 and Figure 1. If a BDCT approach was applied, 100% of the cows had to be dried off with dry cow antimicrobials and therefore the units of activity were forced in DCT group j = 1. If a SDCT approach was applied, a maximum of 100% of dry cow antimicrobials was allowed, which does not mean that 100% of the cows were placed in the DCT group (j = 1).
      Table 3Total economic costs (€) of mastitis in a blanket dry cow treatment (BDCT) approach and minimized total economic costs of mastitis when 100 and 0% dry cow antimicrobials are allowed for a 100-cow dairy herd with 75 cows to be dried off
      Calculations were done for a high-bulk tank SCC (BTSCC) herd (BTH), an average-BTSCC herd (BTA), and a low-BTSCC herd (BTL), each with a low (CL), an average (CA), and a high (CH) incidence of clinical mastitis and the difference between 100% and BDCT and between 0% and BDCT.
      Herd typeBDCT100% dry cow antimicrobials allowedDifference 100% − BDCT0% dry cow antimicrobials allowedDifference 0% − BDCT
      BTHCH6,5126,464−488,0851,573
      BTACH6,1526,049−1037,6011,449
      BTLCH5,8285,705−1237,1551,327
      BTHCA3,9283,838−904,202274
      BTACA3,7413,557−1843,943202
      BTLCA3,5543,339−2153,685131
      BTHCL2,6362,260−3762,260−376
      BTACL2,5382,114−4242,114−424
      BTLCL2,4171,949−4681,949−468
      1 Calculations were done for a high-bulk tank SCC (BTSCC) herd (BTH), an average-BTSCC herd (BTA), and a low-BTSCC herd (BTL), each with a low (CL), an average (CA), and a high (CH) incidence of clinical mastitis and the difference between 100% and BDCT and between 0% and BDCT.
      Figure thumbnail gr1
      Figure 1Minimized total economic costs of mastitis for a 100-cow dairy herd with 75 cows to be dried off applying selective dry cow treatment (dashed lines) and reducing the maximum percentage of dry cow antimicrobials from 100 to 0% for a low-bulk tank SCC (BTSCC) herd (BTL), an average-BTSCC herd (BTA), and a high-BTSCC herd (BTH), each with a low (BTLCL, BTACL, BTHCL), an average (BTLCA, BTACA, BTHCA), and a high (BTLCH, BTACH, BTHCH) incidence of clinical mastitis (selective dry cow treatment; SDCT) and for blanket dry cow treatment (BDCT; solid lines) in these 9 types of herds. Color version available online.
      Table 3 shows that the effect of CM is greater than the effect of BTSCC, with BDCT being always more expensive than SDCT and no dry cow antimicrobials (0%) being cheaper than BDCT if the incidence of CM is low.
      When the maximum percentage of cows to be dried off with antimicrobials decreased from 100 to 0%, TCM of an SDCT approach remained lower than the TCM for a BDCT approach, until a certain point where the TCM of SDCT becomes higher than the TCM of BDCT (Figure 1). For the BTHCH herd, this point was 80%, for the BTACH herd 65%, and for the BTLCH herd 60%. For the BTHCA herd, this point was 40%, for the BTACA herd 20%, and for the BTLCA herd 10%. When the incidence of CM was low (BTLCL, BTACL, BTHCL), in all 21 situations a SDCT approach was more beneficial than a BDCT approach.

      Sensitivity Analysis

      Minimal TCM was influenced by changes in ΔDCT and changes in milk price, as presented in Table 4. If the effect of DCT is smaller (ΔDCT × 0.5), incidence of CM in dry cow treated cows will be lower than in the baseline situation, as will be the TCM. The effect of a decreased ΔDCT is substantial (up to 9%), whereas it is limited for an increased ΔDCT (maximal 3%). The sensitivity analysis showed that the variability in milk price has a substantial effect on the minimal TCM for SDCT in both directions. If the milk price was €27/100 kg, BDCT was not beneficial for any type of herd (data not presented). Changing milk prices had a greater effect on minimal TCM than changing ΔDCT, up to 16% in both directions. The lowest minimal TCM was €2,809 per year for a BTLCA herd when the milk price was €27/100 kg. The highest minimal TCM was €4,422 per year for a BTHCA herd when the milk price was €43/100 kg.
      Table 4Results of the sensitivity analysis by halving and doubling the effect of dry cow treatment (ΔDCT) and variation in milk price on the calculated minimal total economic costs of mastitis (TCM)
      Calculations were done for a low-bulk tank SCC (BTSCC) herd (BTLCA), an average-BTSCC herd (BTACA), and a high-BTSCC herd (BTHCA) with an average incidence of clinical mastitis when 100% of cows are allowed to be dried off with antimicrobials.
      Sensitivity analysisMinimal TCM
      BTLCABTACABTHCA
      €/yr per herd%€/yr per herd%€/yr per herd%
      Baseline, 100% SDCT
      SDCT = selective dry cow treatment.
      3,3393,5573,838
      ΔDCT × 0.53,038−93,261−83,484−9
      ΔDCT × 2.03,445+33,665+33,887+1
      Milk price, €27/100 kg2,809−162,982−163,205−16
      Milk price, €43/100 kg3,850+154,113+164,422+15
      1 Calculations were done for a low-bulk tank SCC (BTSCC) herd (BTLCA), an average-BTSCC herd (BTACA), and a high-BTSCC herd (BTHCA) with an average incidence of clinical mastitis when 100% of cows are allowed to be dried off with antimicrobials.
      2 SDCT = selective dry cow treatment.

      DISCUSSION

      To control mastitis, much research has been done to evaluate the effects of DCT, generally indicating a positive effect of DCT on udder health (
      • Halasa T.
      • Osteras O.
      • Hogeveen H.
      • van Werven T.
      • Nielen M.
      Meta-analysis of dry cow management for dairy cattle. Part 1. Protection against new intramammary infections.
      ). Due to a changing view on AMU in the animal industry, preventive use of antimicrobials, including BDCT, is no longer allowed in several European countries, including the Netherlands (
      • Santman-Berends I.M.G.A.
      • Swinkels J.M.
      • Lam T.J.G.M.
      • Keurentjes J.
      • van Schaik G.
      Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy.
      ). Economic consequences likely contribute to farmers' decision-making on the use of dry cow antimicrobials and therefore are of interest with regard to SDCT as compared with BDCT.
      Our model compared different SDCT approaches based on monthly SCC. Some studies have used quarter-, cow-, and herd-level criteria to select cows for dry cow therapy. Decision-making to select cows for DCT can be based on bacteriological culture (
      • Browning J.W.
      • Mein G.A.
      • Barton M.
      • Nicholls T.J.
      • Brightling P.
      Effects of antibiotic therapy at drying off on mastitis in the dry period and early lactation.
      ;
      • Cameron M.
      • McKenna S.L.
      • MacDonald K.A.
      • Dohoo I.R.
      • Roy J.P.
      • Keefe G.P.
      Evaluation of selective dry cow treatment following on-farm culture: Risk of postcalving intramammary infection and clinical mastitis in the subsequent lactation.
      ), SCC and CM history (
      • Rindsig R.B.
      • Rodewald R.G.
      • Smith A.R.
      • Spahr S.L.
      Complete versus selective dry cow therapy for mastitis control.
      ;
      • Torres A.H.
      • Rajala-Schultz P.J.
      • Degraves F.J.
      • Hoblet K.H.
      Using dairy herd improvement records and clinical mastitis history to identify subclinical mastitis infections at dry-off.
      ;
      • Rajala-Schultz P.J.
      • Torres A.H.
      • Degraves F.J.
      Milk yield and somatic cell count during the following lactation after selective treatment of cows at dry-off.
      ), the California mastitis test (
      • Rindsig R.B.
      • Rodewald R.G.
      • Smith A.R.
      • Spahr S.L.
      Complete versus selective dry cow therapy for mastitis control.
      ;
      • Bhutto A.L.
      • Murray R.D.
      • Woldehiwet Z.
      California mastitis test scores as indicators of subclinical intra-mammary infections at the end of lactation in dairy cows.
      ), and N-acetyl-β-d-glucosaminidase (
      • Hassan Z.
      • Daniel R.C.
      • O'Boyle D.
      • Frost A.J.
      Effects of dry cow intramammary therapy on quarter infections in the dry period.
      ) with different accuracies in identification of infected cows. The most feasible selection method, however, is based on monthly SCC, which has a reported sensitivity of 70% and specificity of 63% to identify quarters with IMI at drying off (
      • Torres A.H.
      • Rajala-Schultz P.J.
      • Degraves F.J.
      • Hoblet K.H.
      Using dairy herd improvement records and clinical mastitis history to identify subclinical mastitis infections at dry-off.
      ). These are not ideal test characteristics, which may lead to false positive or false negatives in cow selection for DCT. This, however, was found not to lead to big problems when implemented in field studies (
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ).
      Although epidemiological consequences and effects of reducing DCT were extensively evaluated in the last 3 yr (
      • Cameron M.
      • McKenna S.L.
      • MacDonald K.A.
      • Dohoo I.R.
      • Roy J.P.
      • Keefe G.P.
      Evaluation of selective dry cow treatment following on-farm culture: Risk of postcalving intramammary infection and clinical mastitis in the subsequent lactation.
      ;
      • Santman-Berends I.M.G.A.
      • Swinkels J.M.
      • Lam T.J.G.M.
      • Keurentjes J.
      • van Schaik G.
      Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy.
      ;
      • Scherpenzeel C.G.M.
      • den Uijl I.E.M.
      • van Schaik G.
      • Riekerink R.G.M.
      • Hogeveen H.
      • Lam T.J.G.M.
      Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
      ), attention to economic consequences of different approaches of DCT was limited to a few studies in the last 10 yr (
      • Halasa T.
      • Huijps K.
      • Osteras O.
      • Hogeveen H.
      Economic effects of bovine mastitis and mastitis management: a review.
      ;
      • Huijps K.
      • Hogeveen H.
      Stochastic modeling to determine the economic effects of blanket, selective, and no dry cow therapy.
      ). In our study, our main finding was that from an economic perspective, although differences were small, BDCT seems not to be the optimal approach of DCT. The maximum percentage of cows to be dried off with dry cow antimicrobials in an SDCT approach could, in herds with different BTSCC and CM incidence levels, be decreased to a certain level without seeing an increase in TCM.
      We found that the maximum percentage of dry cow antimicrobials in SDCT, where the minimal TCM for SDCT equals TCM for BDCT, is influenced by the udder health situation of a herd, both by BTSCC as well as CM. The effect of the incidence of CM, as well as the BTSCC, were evaluated, showing that the effect of the incidence of CM on minimal TCM was much greater than the effect of BTSCC. This indicated that BDCT is not the economically optimal DCT approach as compared with 100% SDCT in all types of herds and as compared with 0% SDCT in all types of BTSCC herds with a low incidence of CM (BTLCL, BTACL, BTHCL).
      Comparison of the TCM for a BDCT approach and the minimal TCM for SDCT showed limited economic effects due to small differences between different approaches. This is in line with the findings of
      • Huijps K.
      • Hogeveen H.
      Stochastic modeling to determine the economic effects of blanket, selective, and no dry cow therapy.
      , who concluded that SDCT was economically the best approach to dry off cows, although the differences with BDCT were small. They concluded that a small change in the probabilities of the rate of infection and costs associated with mastitis moved the economically optimal decision toward BDCT. Assumptions on failure and preventive costs to estimate TCM, however, can differ per herd. We used the best available estimates for the Dutch situation to prevent potential bias as much as possible. The sensitivity analysis showed that the effect of variability in milk price and changes in ΔDCT has substantial effect on the TCM, although the conclusions do not change. This shows that the conclusions using our deterministic approach are robust.
      Evaluating the effect of the incidence of CM in a BTA herd showed a great effect on the minimized TCM (Figure 1). The minimized TCM was 3 times higher for a BTACH herd than for a BTACL herd. In a BTH herd, effects of the incidence of CM were similar to a BTL herd (Figure 1) as they were in a BTA herd (results not shown). In all types of herds, the minimal TCM for a low incidence of CM was always lower for SDCT than for BDCT (Figure 1). The largest difference in minimal TCM when applying 100% SDCT was between a BTH herd with a high incidence of CM (BTHCH) and a BTL herd with a low incidence of CM (BTLCL), being €4,515 per year per herd.
      In our optimization model, the relation between DCT and the incidence of CM and SCM was modeled in a straightforward manner. The limitation of the optimization approach is that some parameters and associations need to be assumed. We were, however, able to base the probabilities of mastitis on a large prospective field trial. In this field trial, no internal teat sealants were used, although the use of internal teat sealant is an important preventive tool. Usage of internal teat sealants was previously found to have a protective effect on the incidence of new CM cases because teat sealants help prevent colonization of quarters with bacteria during the dry period (
      • Rabiee A.R.
      • Lean I.J.
      The effect of internal teat sealant products (Teatseal and Orbeseal) on intramammary infection, clinical mastitis, and somatic cell counts in lactating dairy cows: A meta-analysis.
      ). A model including the effect of the use of internal teat sealants would be worthwhile, but was beyond the scope of this study.
      The economic effect of an improved udder health situation on the herd (e.g., having a lower BTSCC or a lower incidence of CM) is much greater than the economic effect of restricting the maximum percentage of dry cow antimicrobials used. For the minimal TCM on some types of herds (e.g., a BTHCA herd), economic benefits of SDCT were very small, as compared with a BDCT approach. From a risk avoidance approach, one could therefore choose for a BDCT approach. For reasons of prudent AMU, however, it is not desirable to use more dry cow antimicrobials than needed and there also seems to be no economic reason to do so. Thus, for several reasons investments and efforts should be made to reduce BTSCC and the incidence of CM, rather than using more dry cow antimicrobials.
      For all BTSCC levels, it was economically beneficial to reduce the incidence of CM to improve general udder health management. While searching for the economically optimal DCT approach, we compared udder health and AMU, because of opposite effects of limiting the use of dry cow antimicrobials on these parameters. When searching for optimal selection criteria for DCT, the incidence of mastitis, BTSCC, and AMU can be compared in an economic evaluation. This oversimplifies the potential effect of DCT, given the potential effect of AMR, the public opinion on preventive AMU, political issues, and animal welfare. This study, however, shows that economics is not an argument against reduction of the use of dry cow antimicrobials by applying SDCT.

      CONCLUSIONS

      From an economic perspective, BDCT seems not to be the optimal approach of DCT, although differences between approaches were small. For all evaluated BTSCC levels, SDCT was economically more beneficial than BDCT with greater economic profits in herds with lower incidence of CM and lower BTSCC. In all types of herds, the use of dry cow antimicrobials can be reduced without economic consequences. In herds with low incidence of CM the use of no dry cow antimicrobials at all is cheaper than BDCT. The economic impact of improvement of the udder health situation, both the incidence of CM and BTSCC, however, is bigger than the effect of the DCT approach. Economics is not an argument against reduction of the use of dry cow antimicrobials by applying SDCT.

      ACKNOWLEDGMENTS

      This study was financially supported by the Dutch Dairy Board (PZ, Zoetermeer, the Netherlands). The authors appreciate the cooperation of the dairy producers who contributed to the field study the data used in this paper were based on.

      REFERENCES

        • Agrimatie
        Annual prices of the most important products and production equipment for the dairy sector as based on information from the Farm Accountancy Data Network. Vol. 2016.2016 (Accessed Apr. 25, 2016.)
        • Barkema H.W.
        • Schukken Y.H.
        • Lam T.J.G.M.
        • Beiboer M.L.
        • Wilmink H.
        • Benedictus G.
        • Brand A.
        Incidence of clinical mastitis in dairy herds grouped in three categories by bulk milk somatic cell counts.
        J. Dairy Sci. 1998; 81 (9532494): 411-419
        • Berry E.A.
        • Hillerton J.E.
        The effect of selective dry cow treatment on new intramammary infections.
        J. Dairy Sci. 2002; 85 (11860103): 112-121
        • Berry S.L.
        • Maas J.
        • Kirk J.H.
        • Reynolds J.P.
        • Gardner I.A.
        • Ahmadi A.
        Effects of antimicrobial treatment at the end of lactation on milk yield, somatic cell count, and incidence of clinical mastitis during the subsequent lactation in a dairy herd with a low prevalence of contagious mastitis.
        J. Am. Vet. Med. Assoc. 1997; 211 (9227753): 207-211
        • Bhutto A.L.
        • Murray R.D.
        • Woldehiwet Z.
        California mastitis test scores as indicators of subclinical intra-mammary infections at the end of lactation in dairy cows.
        Res. Vet. Sci. 2012; 92 (21074231): 13-17
        • Bradley A.J.
        • Green M.J.
        An investigation of the impact of intramammary antibiotic dry cow therapy on clinical coliform mastitis.
        J. Dairy Sci. 2001; 84 (11467813): 1632-1639
        • Browning J.W.
        • Mein G.A.
        • Barton M.
        • Nicholls T.J.
        • Brightling P.
        Effects of antibiotic therapy at drying off on mastitis in the dry period and early lactation.
        Aust. Vet. J. 1990; 67 (2076066): 440-442
        • Cameron M.
        • McKenna S.L.
        • MacDonald K.A.
        • Dohoo I.R.
        • Roy J.P.
        • Keefe G.P.
        Evaluation of selective dry cow treatment following on-farm culture: Risk of postcalving intramammary infection and clinical mastitis in the subsequent lactation.
        J. Dairy Sci. 2014; 97 (24183691): 270-284
        • Chantziaras I.
        • Boyen F.
        • Callens B.
        • Dewulf J.
        Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: A report on seven countries.
        J. Antimicrob. Chemother. 2014; 69 (24216767): 827-834
        • CRV
        Jaarstatistieken 2015: Dutch Royal Cattle Syndicate Annual Report (in Dutch). 2015 (Accessed Apr. 25, 2016.)
        • Dodd F.H.
        • Westgarth D.R.
        • Neave F.K.
        • Kingwill R.G.
        Mastitis–The strategy of control.
        J. Dairy Sci. 1969; 52 (5391702): 689-695
        • Halasa T.
        • Huijps K.
        • Osteras O.
        • Hogeveen H.
        Economic effects of bovine mastitis and mastitis management: a review.
        Vet. Q. 2007; 29 (17471788): 18-31
        • Halasa T.
        • Nielen M.
        • De Roos A.P.W.
        • Van Hoorne R.
        • de Jong G.
        • Lam T.J.G.M.
        • van Werven T.
        • Hogeveen H.
        Production loss due to new subclinical mastitis in Dutch dairy cows estimated with a test-day model.
        J. Dairy Sci. 2009; 92 (19164670): 599-606
        • Halasa T.
        • Osteras O.
        • Hogeveen H.
        • van Werven T.
        • Nielen M.
        Meta-analysis of dry cow management for dairy cattle. Part 1. Protection against new intramammary infections.
        J. Dairy Sci. 2009; 92 (19528591): 3134-3149
        • Hassan Z.
        • Daniel R.C.
        • O'Boyle D.
        • Frost A.J.
        Effects of dry cow intramammary therapy on quarter infections in the dry period.
        Vet. Rec. 1999; 145 (10619609): 635-639
        • Hogeveen H.
        • Huijps K.
        • Lam T.J.G.M.
        Economic aspects of mastitis: New developments.
        N. Z. Vet. J. 2011; 59 (21328153): 16-23
        • Huijps K.
        • Hogeveen H.
        Stochastic modeling to determine the economic effects of blanket, selective, and no dry cow therapy.
        J. Dairy Sci. 2007; 90 (17297099): 1225-1234
        • Huijps K.
        • Lam T.J.G.M.
        • Hogeveen H.
        Costs of mastitis: Facts and perception.
        J. Dairy Res. 2008; 75 (18226298): 113-120
        • Kuipers A.
        • Koops W.J.
        • Wemmenhove H.
        Antibiotic use in dairy herds in the Netherlands from 2005 to 2012.
        J. Dairy Sci. 2016; 99 (26709178): 1632-1648
        • Lam T.J.G.M.
        • Schukken Y.H.
        • van Vliet J.H.
        • Grommers F.J.
        • Tielen M.J.
        • Brand A.
        Effect of natural infection with minor pathogens on susceptibility to natural infection with major pathogens in the bovine mammary gland.
        Am. J. Vet. Res. 1997; 58 (8989490): 17-22
        • Lam T.J.G.M.
        • van den Borne B.H.P.
        • Jansen J.
        • Huijps K.
        • van Veersen J.C.
        • van Schaik G.
        • Hogeveen H.
        Improving bovine udder health: A national mastitis control program in the Netherlands.
        J. Dairy Sci. 2013; 96 (23245961): 1301-1311
        • McNab W.B.
        • Meek A.H.
        A benefit cost analysis of dry-cow mastitis therapy in Ontario dairy herds.
        Can. Vet. J. 1991; 32 (17423801): 347-353
        • Mohd Nor N.
        • Steeneveld W.
        • Hogeveen H.
        The average culling rate of Dutch dairy herds over the years 2007 to 2010 and its association with herd reproduction, performance and health.
        J. Dairy Res. 2014; 81 (24107585): 1-8
        • Neave F.K.
        • Dodd F.H.
        • Kingwill R.G.
        • Westgarth D.R.
        Control of mastitis in the dairy herd by hygiene and management.
        J. Dairy Sci. 1969; 52 (5391057): 696-707
        • Oliver S.P.
        • Murinda S.E.
        • Jayarao B.M.
        Impact of antibiotic use in adult dairy cows on antimicrobial resistance of veterinary and human pathogens: A comprehensive review.
        Foodborne Pathog. Dis. 2011; 8 (21133795): 337-355
        • Rabiee A.R.
        • Lean I.J.
        The effect of internal teat sealant products (Teatseal and Orbeseal) on intramammary infection, clinical mastitis, and somatic cell counts in lactating dairy cows: A meta-analysis.
        J. Dairy Sci. 2013; 96 (24054298): 6915-6931
        • Rajala-Schultz P.J.
        • Torres A.H.
        • Degraves F.J.
        Milk yield and somatic cell count during the following lactation after selective treatment of cows at dry-off.
        J. Dairy Res. 2011; 78 (21939576): 489-499
        • Rindsig R.B.
        • Rodewald R.G.
        • Smith A.R.
        • Spahr S.L.
        Complete versus selective dry cow therapy for mastitis control.
        J. Dairy Sci. 1978; 61 (81843): 1483-1497
        • Santman-Berends I.M.G.A.
        • Swinkels J.M.
        • Lam T.J.G.M.
        • Keurentjes J.
        • van Schaik G.
        Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy.
        J. Dairy Sci. 2016; 99 (26874413): 2930-2939
        • Scherpenzeel C.G.M.
        • den Uijl I.E.M.
        • van Schaik G.
        • Olde Riekerink R.G.M.
        • Keurentjes J.M.
        • Lam T.J.G.M.
        Evaluation of the use of dry cow antibiotics in low somatic cell count cows.
        J. Dairy Sci. 2014; 97 (24746132): 3606-3614
        • Scherpenzeel C.G.M.
        • den Uijl I.E.M.
        • van Schaik G.
        • Riekerink R.G.M.
        • Hogeveen H.
        • Lam T.J.G.M.
        Effect of different scenarios for selective dry-cow therapy on udder health, antimicrobial usage, and economics.
        J. Dairy Sci. 2016; 99 (26947289): 3753-3764
        • Torres A.H.
        • Rajala-Schultz P.J.
        • Degraves F.J.
        • Hoblet K.H.
        Using dairy herd improvement records and clinical mastitis history to identify subclinical mastitis infections at dry-off.
        J. Dairy Res. 2008; 75 (18474143): 240-247
        • Yalcin C.
        • Stott A.W.
        Dynamic programming to investigate financial impacts of mastitis control decisions in milk production systems.
        J. Dairy Res. 2000; 67 (11131065): 515-528