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Incidence of Clinical Mastitis in Dairy Herds Grouped in Three Categories by Bulk Milk Somatic Cell Counts H. W. BARKEMA,*,1 Y. H. SCHUKKEN,† T.J.G.M. LAM,‡ M. L. BEIBOER,§ H. WILMINK,‚ G. BENEDICTUS,* and A. BRAND† *Animal Health Service, PO Box 361, 9200 AJ Drachten, The Netherlands †Department of Herd Health and Reproduction, Utrecht University, PO Box 80151, 3508 TD Utrecht, The Netherlands ‡Department of Infectious Diseases and Immunology, Utrecht University, PO Box 80165, 3508 TD Utrecht, The Netherlands §Veterinary Clinic Ureterp, Weibuorren 1/aa, 9247 AX Ureterp, The Netherlands ‚Royal Dutch Cattle Syndicate, PO Box 454, 6800 AL Arnhem, The Netherlands

ABSTRACT Incidence of clinical mastitis was studied in 274 herds grouped in three categories by bulk milk somatic cell count (SCC). Mean incidence rate of clinical mastitis was 0.278, 0.257, and 0.252 cases per 365 cow-days at risk in herds with low ( ≤150,000), medium (150,000 to 250,000), and high (250,000 to 400,000 cells/ml) bulk milk SCC, respectively. The incidence rate of clinical mastitis was not different among the three categories. Variance in the incidence of clinical mastitis among herds increased as bulk milk SCC decreased. Clinical mastitis caused by Gram-negative pathogens, such as Escherichia coli, Klebsiella spp., or Pseudomonas spp., occurred more often in herds with a low bulk milk SCC. Clinical mastitis caused by Staphylococcus aureus, Streptococcus dysgalactiae, and Streptococcus agalactiae occurred more often in herds with a high bulk milk SCC. Systemic signs of illness caused by clinical mastitis occurred more often in herds with a low bulk milk SCC. Both overall culling rate and culling rate for clinical mastitis were not different among groups catergorized by bulk milk SCC. In herds with a high bulk milk SCC, however, more cows that produced milk with a high SCC were culled. In herds with a low bulk milk SCC, more cows were culled for teat lesions, milkability, udder shape, fertility, and character than were cows in herds with a high bulk milk SCC. In herds with a low bulk milk SCC, cows were also culled more for export and production reasons. ( Key words: somatic cell count, clinical mastitis, bulk milk, culling)

Received March 31, 1997. Accepted August 25, 1997. 1Corresponding author. 1998 J Dairy Sci 81:411–419

Abbreviation key: BMSCC = bulk milk SCC, IRCM = incidence rate of clinical mastitis. INTRODUCTION A decrease in the regulatory limit for bulk milk SCC ( BMSCC) in the last decade has resulted in a decrease in the mean BMSCC in The Netherlands from 310,000/ml in 1985 to 221,000/ml in 1995. This decrease indicates that the prevalence of subclinical mastitis was reduced during those years. However, clinical mastitis continues to be a significant problem. The incidence rate of clinical mastitis ( IRCM) in herds with a low BMSCC ( ≤150,000/ml) ranges from 5.16 to 13.9/10,000 cow-days at risk (2, 9, 16). Erskine et al. ( 3 ) compared 6 herds with a very high BMSCC ( ≥700,000/ml) with 12 herds with a low BMSCC ( ≤150,000/ml) and found a higher IRCM in herds with the low BMSCC ( 3 ) . Although herds with a low BMSCC may manifest a high IRCM caused by Staphylococcus aureus (9, 16), the IRCM from which contagious pathogens, such as Streptococcus agalactiae and Staph. aureus, were isolated is lower in herds with a low BMSCC than in herds with a high BMSCC ( 3 ) . With regard to the IRCM caused by environmental pathogens, such as Escherichia coli and streptococci other than Strep. agalactiae, the opposite is true (3). The relationship between BMSCC and the IRCM is of interest. The milk quality of milk with a high BMSCC is not acceptable, but some researchers (6, 7, 11, 12, 16) have suggested that cows in herds with a low BMSCC might have an increased susceptibility to clinical mastitis. This theory could mean that there is an optimal BMSCC that is low but not necessarily the lowest BMSCC possible. However, no convincing evidence is available that indicates that clinical mastitis increases when a herd has a low BMSCC (17).

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Because of a lack of published data on a sufficient number of herds, the purpose of the present study was to examine the relationship between BMSCC and the IRCM. MATERIALS AND METHODS Herds Based on mean BMSCC, three categories of 100 dairy herds each were selected. For participating herds, 10 of 13 times in the last year and the last three times that BMSCC was evaluated, the BMSCC had to be in one of the following categories: ≤150,000 (low), 151,000 to 250,000 (medium), or 251,000 to 400,000/ml (high). These three categories were selected to include relevant ranges of BMSCC under current farming conditions in The Netherlands. Herds were selected that housed lactating cows in a freestall barn during winter, participated in a three or four weekly milk recording system, had an annual production quota between 300,000 and 900,000 kg, and had cows of the Holstein-Friesian or Dutch Friesian breeds. Three hundred four herds that matched these criteria were randomly selected and invited to participate. Four farmers refused; the remaining 300 herds, 100 per BMSCC category, participated in the study for 1.5 yr, entering the study between December 1992 and June 1994. Eight herds did not complete the study because farming activities ceased. Sampling Farmers collected milk samples from every quarter that had visible signs of clinical mastitis before treatment. Aseptic sampling procedures were discussed with the farmers before the start of the project. For all cases of clinical mastitis, farmers recorded the date of occurrence, identification of the cow, affected quarter, treatment, and whether the cow was systemically ill or not. The samples were stored in a freezer on the farms (at approximately –20°C ) and were collected for bacteriological examination at intervals of 6 to 8 wk. At that time, data recording was verified. At the end of the data collection period, farmers were asked to estimate how many cases of clinical mastitis were not sampled and not recorded. If this number exceeded 10 and was >25% compared with the number of cases sampled, the herd was excluded from analysis of the clinical mastitis data. Eighteen herds were excluded from the analyses for this reason. Of these 18 herds, 4 were from the low BMSCC Journal of Dairy Science Vol. 81, No. 2, 1998

category, 4 were from the middle BMSCC category, and 10 were from the high BMSCC category. Culling dates and the reason for culling of all cows were recorded by the farmer. At the end of the data collection period, the culling list of the farmer was checked with registration of culling via the Dutch Identification and Registration system (13). Cows that were not present on the list provided by the farmer were added, and the farmer was asked for the reason for culling. Calving and drying off dates and three or four weekly milk recordings were available for all herds [Royal Dutch Cattle Syndicate, Arnhem, The Netherlands]. Bulk Milk SCC was determined 13 times/yr by a milk quality laboratory using a Fossomatic cell counter (Foss Electric, Hillerød, Denmark). As the basis for comparison of herds in the three BMSCC categories, geometric BMSCC during the study, and not BMSCC before the study, was used (18). Laboratory Analysis Bacteriological culturing of milk samples was performed according to standards of the National Mastitis Council ( 8 ) . An aliquot of 0.01 ml was cultured from all milk samples. In each of the cultures, the number of colony-forming units of each of the bacterial species was counted. The contagious pathogens Staph. aureus and Strep. agalactiae were considered to cause IMI if one colony (100 cfu/ml) was isolated. Isolation of ≥200 cfu/ml of environmental mastitis pathogens ( E. coli, streptococci other than Strep. agalactiae, Klebsiella spp., and Pseudomonas spp.) or ≥1000 cfu/ml of Corynebacterium bovis or coagulasenegative staphylococci were considered significant. If three or more bacterial species were cultured from a sample, the sample was considered to be contaminated ( 5 ) . IRCM The cow IRCM was expressed as the number of quarter cases per 365 cow-days at risk when data were analyzed at the herd level. In all other situations (i.e., parity groups and stages of lactation), IRCM was expressed as the number of quarter cases per 10,000 cow-days at risk. Intervals between cases of clinical mastitis in the same quarter had to be ≥14 d for a case to be included in the analysis. Cow-days at risk were calculated as the total number of days during the study that a cow was present in the herd, starting 7 d before the first parturition, minus 14 d after each case of clinical mastitis. Calculations of clinical mastitis included the total number of cases

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and the number of cases per species of pathogenic bacteria. Separate calculations were performed per parity and per day of lactation.

Statistical Analysis Prior to statistical analyses, observations were checked for unlikely values; no data were excluded for this reason. Missing values routinely caused a record to be excluded if the analysis included that variable. Statistical significance was defined at P = 0.05. Change in BMSCC classification before the study and geometric mean BMSCC during the study was modeled with a state transition model (15). The distribution of cases of clinical mastitis across quarters was determined using the frequency procedure of SAS (14). Differences between observed and expected distributions were tested using chi-square analysis (18). Statistical analyses to compare the estimated number of cases of mastitis not sampled and not recorded per herd and the number of cows per herd per BMSCC category, as well as to compare mean herd milk production among the BMSCC categories, were done using a Student’s t test (18). The relationship between geometric mean BMSCC during the study period and IRCM per herd was tested using Poisson regression with a log link [PROC GENMOD; (14)]. The linearized model used was as follows:

RESULTS Description of the Data Mean herd size of the 274 farms evaluated in this study was 76 adult cows (SD = 21.1), varying from 40 to 143. Median herd size was 71.5 cows. Herds with a low BMSCC in this study had fewer cows than did herds with a high BMSCC (Table 1). Mean daily production at the start of the study was 24.0 kg (SD = 7.4 kg) for the 274 herds. BMSCC Bulk milk SCC for the 274 herds during the study was on average 204,000/ml. Arithmetic mean BMSCC per herd during the study ranged from 67,000 to 422,000/ml; the geometric mean ranged from 62,000 to 401,000/ml. The geometric mean BMSCC of the herds selected for the low and medium BMSCC categories before the study did not change during the study (Figure 1). The medium BMSCC category was the most stable category. Geometric mean BMSCC of the herds selected for the high BMSCC category before the study decreased (Figure 1). Forty herds (45%) changed from the high to the medium BMSCC

TABLE 1. Incidence rate of clinical mastitis (IRCM; cases per 365 cow-days at risk) in herds with different bulk milk SCC (BMSCC) ( ×1000 cells/ml). BMSCC

NCASES = a + ln CDi + BMSCCCj + eij where NCASES = number of cases of clinical mastitis during the study period in herd i, a = intercept, ln CDi = natural logarithm of number of cow-days at risk for herd i (used as an offset variable in the model), BMSCCCj = BMSCC category during the study (low, medium, or high), and eij = residual random error (Poisson distributed). This model was also used to model pathogen-specific IRCM and IRCM of systemically ill cows per BMSCC category. The number of cases of clinical mastitis during the study period was then restricted to cases of clinical mastitis caused by that specific pathogen and cases of clinical mastitis in systemically ill cows. The prediction part of the Poisson regression model for culling rate was equal to the IRCM model. In this culling model, the dependent variable was the number of cows culled during the study period. This model was also used to model culling rates for specific reasons per BMSCC category.

Herds, no. Cows per herd, mean no. Cases per herd, mean no. Cases not sampled and not recorded per herd, mean no. IRCM Mean Median Minimal Maximal Of cows that were systemically ill

≤150

151 to 250

251 to 400

All herds

85

133

56

274

701,2

773

81

76

30 3.62,4

31 4.52

32 5.3

31 4.5

0.278 0.234 0 0.993 0.0442,4

0.257 0.236 0.042 0.921 0.036

0.252 0.214 0.013 0.673 0.029

0.262 0.233 0 0.993 0.037

1Tendency (0.05 ≤ P < 0.10) for difference from herds in the medium BMSCC category (151,000 to 250,000 cells/ml). 2Different ( P < 0.05) from herds in the high BMSCC category (251,0000 to 400,000 cells/ml). 3Tendency (0.05 ≤ P < 0.10) for difference from herds in the high BMSCC category (251,000 to 400,000 cells/ml). 4Different ( P < 0.05) from herds in the medium BMSCC category (151,000 to 250,000 cells/ml).

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Figure 1. Mean bulk milk SCC (BMSCC) per category from 1992 to 1995. Legends: low BMSCC ( ≤150,000 cells/ml; ÿ) , medium BMSCC (151,000 to 250,000 cells/ml; * ) , and high BMSCC (251,000 to 400,000 cells/ml; ⁄) . Figure 2. Distribution of the incidence rate of clinical mastitis (ICRM) per parity.

category (Table 2). Because a total of 85 herds (31%) changed BMSCC categories (Table 2), we decided to use the geometric mean BMSCC during the study in the analyses of the relationships between BMSCC categories and IRCM. Clinical Mastitis A total of 8429 cases of clinical mastitis in 7596 quarters in 6373 lactations of 5827 cows were reported by the farmers and included in the analysis, ranging from 2 to 131 cases per herd in a 1.5-yr period. In 286 of these cases, ≥2 quarters were affected at the same time. In 824 (9.8%) of the affected quarters, ≥1 case of clinical mastitis occurred during the same lactation. Recurrent cases of clinical mastitis from which the same pathogen was isolated from the same quarter during the same lactation were found in 290 quarters (3.5%). Heifers had the lowest IRCM, 4.38 quarter cases/ 10,000 cow-days at risk. The IRCM increased as parity increased (Figure 2). Cows that had calved eight

times had the highest IRCM, 13.88 quarter cases/ 10,000 cow-days at risk. The IRCM during lactation is presented in Figures 3 and 4. The highest IRCM was in early lactation. Peak incidence around calving was higher in heifers than in older cows: >30% of the cases of clinical mastitis in heifers occurred during the first 14 d of lactation, but, in cows, this prevalence was at 13%. After the 2nd wk of lactation, the IRCM was higher in cows than in heifers.

TABLE 2. State transition matrix for bulk milk SCC (BMSCC) ( ×1000 cells/ml) the last year before and during the 1.5-yr study period of the 274 herds. During study Before study

≤150

151 to 250

251 to 400

≤150 151 to 250 251 to 400

71 14 0

23 70 40

0 8 48


Figure 3. Distribution of the incidence rate of clinical mastitis (ICRM) per week after calving for heifers ( …) and older cows ( ⁄) .

BULK MILK SOMATIC CELL COUNT AND CLINICAL MASTITIS

Figure 4. Distribution of the incidence rate of clinical mastitis (IRCM) per DIM around calving for heifers ( …) and older cows ( ⁄) .

All herds had cases of clinical mastitis during the study period. The mean IRCM was 0.262 quarter cases/365 cow-days at risk (Table 1). Distribution of the IRCM per herd in the three BMSCC categories is presented in Figure 5. All herds with an IRCM that was >0.7 cases/365 cow-days at risk had a geometric mean BMSCC of ≤250,000/ml (Figure 5). However, the mean IRCM was approximately equal for herds in the low, medium, and high BMSCC categories (Table 1). No significant correlation between BMSCC and IRCM was found in the Poisson regression model ( x2 < 1.0; 1 df; P > 0.35; Table 1 and Figure 6). The number of cases of clinical mastitis that were not sampled and not recorded during the study period but were estimated by the farmer at the end of the study period was lower for herds in the low BMSCC category than for herds in the high BMSCC category (Table 1).

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Figure 5. Distribution of the incidence rate of clinical mastitis (IRCM) of the 274 herds stratified per bulk milk SCC (BMSCC) category. Legend: low BMSCC ( ≤150,000 cells/ml; open bar), medium BMSCC (151,000 to 250,000 cells/ml; solid bar), and high BMSCC (251,000 to 400,000 cells/ml; cross-hatched bar).

low BMSCC category than for herds in the medium or high BMSCC categories (Table 3). Mixed cultures and contaminated samples were also found less often in herds in the low BMSCC category than in herds in the high BMSCC category. Herds in the low BMSCC category had higher IRCM associated with E. coli, Klebsiella spp., Pseudomonas spp., and culturenegative samples than did herds in the medium or high BMSCC categories.

Pathogens Staphylococcus aureus was the major pathogen that was most frequently cultured (Table 3). For 498 cases (5.9%), no milk sample was collected for bacteriological culturing. This tendency occurred more frequently in herds in the low BMSCC category than in herds in the high BMSCC category (Table 3). The percentage of mixed cultures was 18.8%. In 50.6% of these samples, Staph. aureus was cultured; in 35.0% of these samples, Streptococcus dysgalactiae was cultured. The IRCM caused by Strep. agalactiae, Strep. dysgalactiae, or Staph. aureus was lower for herds in the

Figure 6. Scatter plot of the incidence rate of clinical mastitis (IRCM) versus bulk milk SCC (BMSCC). Journal of Dairy Science Vol. 81, No. 2, 1998

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BARKEMA ET AL. TABLE 3. Incidence rate of clinical mastitis (cases per 365 cow-days at risk) per pathogen of 8429 cases within three bulk milk SCC (BMSCC; ×1000 cells/ml) categories.1 BMSCC Pathogen

≤150

151 to 250

251 to 400

All herds

Streptococcus dysgalactiae Streptococcus agalactiae Streptococcus uberis Other streptococci Staphylococcus aureus Coagulase-negative staphylococci Escherichia coli Corynebacterium bovis Arcanobacterium pyogenes Klebsiella spp. Pseudomonas spp. Mixed culture Negative Contaminated Not sampled but recorded

0.02792,3 0.00082,4 0.0178 0.0250 0.04804,5 0.0182 0.06054 0.0146 0.0018 0.00542 0.00322,4 0.04094,5 0.05902,4 0.01292,4 0.01994,5

0.0375 0.0040 0.0176 0.0206 0.06254 0.0185 0.0520 0.0146 0.0028 0.0028 0.0009 0.0503 0.03623 0.0191 0.01453

0.0361 0.0059 0.0197 0.0205 0.0827 0.0150 0.0441 0.0190 0.0025 0.0040 0.0011 0.0574 0.0261 0.0203 0.0093

0.0344 0.0035 0.0182 0.0218 0.0628 0.0176 0.0527 0.0156 0.0024 0.0038 0.0016 0.0492 0.0406 0.0176 0.0149

1If

two pathogens were isolated, they were treated as a case of either pathogen. ( P < 0.05) from herds in the medium BMSCC category (151,000 to 250,000 cells/ml). 3Tendency (0.05 ≤ P < 0.10) for difference from herds in the high BMSCC category (251,000 to 400,000 cells/ml). 4Different ( P < 0.05) from herds in the high BMSCC category (251,000 to 400,000 cells/ml). 5Tendency (0.05 ≤ P < 0.10) for difference from herds in the medium BMSCC category (151,000 to 250,000 cells/ml). 2Different

Systemically Ill Cows The IRCM for cows that were reported by the farmer to be systemically ill was higher for herds in the low BMSCC category than for herds in the medium and high BMSCC categories, 0.044, 0.036, and 0.029 cases/365 cow-days at risk, respectively ( P < 0.05; Table 1). Culling Rate The overall mean culling rate for clinical mastitis was not different among herds in low, medium, and high BMSCC categories (Table 4). The distribution of reasons for culling, however, was different (Table 4). Culling rate for clinical mastitis was not different among the BMSCC categories. Farmers of herds in the high BMSCC category culled more cows because of high SCC than did farmers of herds in the low and medium BMSCC categories. Farmers of herds with a low BMSCC culled more cows because of teat lesions, milkability, udder shape, fertility, and character than did farmers of herds with a high BMSCC. Farmers of herds with a low BMSCC also culled more adult cows for export and had to cull more cows without problems than did farmers of herds with a high BMSCC so as not to exceed their milk production Journal of Dairy Science Vol. 81, No. 2, 1998

quotas. Farmers of herds with a high BMSCC forgot more often to record culling and remembered less often the reason for culling compared with farmers of herds with a low BMSCC (Table 4). DISCUSSION The mean IRCM of 0.26/365 cow-days at risk in our study was lower than that suggested by Wilesmith et al. ( 1 9 ) in a study of approximately 200 dairy herds in the United Kingdom. Contrary to Erskine et al. ( 3 ) , we did not find a significantly different IRCM in herds with a low and high BMSCC. However, those researchers ( 3 ) compared 12 herds with a low BMSCC ( ≤150,000/ml) with 6 herds with a BMSCC that was >700,000 cells/ml. The maximum BMSCC for herds in our high BMSCC category was 401,000 cells/ml. The IRCM was higher for herds in our low BMSCC category than that reported by Schukken et al. ( 1 6 ) (5.2/10,000 cow-days at risk) but lower than that reported by Hogan et al. ( 1 0 ) when those researchers studied nine dairy herds. The ability to find a possible difference in IRCM among the three BMSCC categories was high in our study. Our inability to find a difference in the data suggested that, if a difference in IRCM existed among the BMSCC categories, it could not be large.

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BULK MILK SOMATIC CELL COUNT AND CLINICAL MASTITIS TABLE 4. Culling rate per reason for culling (cows culled per 365 cow-days at risk) in the 274 herds with different bulk milk SCC (BMSCC; ×1000 cells/ml). BMSCC Reason for culling

≤150

151 to 250

251 to 400

All herds

Clinical mastitis High SCC Teat lesions Milkability Udder shape Fertility Lameness Low milk production Calving problems Mortality Other health problems Age Export Milk quota Meat cattle Character No reason remembered All reasons for culling

0.0268 0.01191,2 0.01322,3 0.01123,4 0.01212 0.09071,2 0.0283 0.03523 0.00583 0.0088 0.0276 0.0112 0.00642 0.03201,2 0.0014 0.00202 0.00452 0.2867

0.0232 0.02372 0.0097 0.0080 0.01102 0.0754 0.0312 0.0448 0.00852 0.0076 0.0333 0.0106 0.00622 0.02132 0.0018 0.0013 0.00342 0.2767

0.0247 0.0433 0.0073 0.0069 0.0048 0.0718 0.0312 0.0363 0.0047 0.0095 0.0340 0.0102 0.0025 0.0062 0.0011 0.0008 0.0106 0.2666

0.0246 0.0246 0.0102 0.0087 0.0100 0.0790 0.0304 0.0401 0.0069 0.0084 0.0318 0.0106 0.0055 0.0211 0.0015 0.0014 0.0053 0.2774

1Different

( P < 0.05) from herds in the medium BMSCC category (151,000 to 250,000 cells/ml). ( P < 0.05) from herds in the high BMSCC category (251,000 to 400,000 cells/ml). 3Tendency (0.05 ≤ P < 0.10) for difference from herds in the medium BMSCC category (151,000 to 250,000 cells/ml). 4Tendency (0.05 ≤ P < 0.10) for difference from herds in the high BMSCC category (251,000 to 400,000 cells/ml). 2Different

The denominator of the IRCM was chosen as 365 cow-days at risk. A period of 365 d is not necessarily contributed by one cow. Heifers calved during the study and entered the period at risk, and cows were culled during the study and left the period at risk. Mean BMSCC has decreased on Dutch dairy farms in the last decade. The BMSCC was more stable than that suggested by Schukken et al. ( 1 5 ) in a study conducted using data from 1982 to 1987. This stability was likely due to our selection of herds. We only selected herds that already had a stable BMSCC. Data collection of cases of clinical mastitis depends heavily on the willingness of farmers to collect milk samples. We tried to encourage the farmers by visiting them as frequently as possible, sending them results of bacteriological analyses of milk samples between visits, and organizing a meeting every year. Farmers of herds in the low BMSCC category were the most accurate collectors of milk samples from cows with cases of clinical mastitis and recorded culling data better than did farmers of herds in the high BMSCC category. Farmers of herds in the low BMSCC category forgot less frequently to take a milk sample than did farmers of herds in the high BMSCC category, and, if they forgot to sample before treatment, the event was recorded more often than it was by farmers of herds in the high BMSCC category.

Therefore, the mean IRCM of herds in the high BMSCC category in our study may be underestimated. The predominant microorganism that caused clinical mastitis in herds in the low BMSCC category was E. coli. However, pathogens like Staph. aureus and Strep. dysgalactiae were also important on these farms. The distribution of pathogens was comparable with that suggested by Schukken et al. ( 1 6 ) for 125 herds with a low BMSCC. The higher percentage of negative cultures in herds with a low BMSCC was comparable with other reports (3, 16) and might have been associated with IMI caused by E. coli (20). As expected, Staph. aureus was cultured most often in herds with a high BMSCC. Other important pathogens in these herds were E. coli and Strep. dysgalactiae. Compared with the results reported by Erskine et al. ( 3 ) , on farms with a high BMSCC, the incidence of clinical mastitis caused by Strep. agalactiae was low. However, the mean BMSCC of herds in the high BMSCC category in our study was lower than that in the study of Erskine et al. ( 3 ) . Approximately 89% of the herds in our study were free of Strep. agalactiae ( 1 ) . The correlation between BMSCC and pathogenspecific IRCM might have been due to farm management practices. Further studies to evaluate simulJournal of Dairy Science Vol. 81, No. 2, 1998

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taneously the risk factors associated with a lower BMSCC and factors associated with a lower or higher rate of clinical mastitis are necessary. Both the mean culling rate and the distribution of the reasons for culling were similar to those suggested by Esslemont and Kossaibati ( 4 ) for 50 dairy herds in the United Kingdom. Farmers of herds with a low BMSCC did not cull or infrequently culled cows with a high SCC in their milk. However, these farmers culled more frequently because of teat lesions, milkability, and udder shape. These culling reasons might indicate a more preventive culling strategy compared with farmers of herds with a high BMSCC. Furthermore, herds with a low BMSCC were able to sell more adult cows for export. Several researchers (6, 7, 12, 16) have suggested that the risk for clinical mastitis increases as individual cow SCC decreases. The level of BMSCC, however, does not reflect the mean SCC of cows with a low SCC in that herd. The question as to whether or not a low SCC at the cow level implicates an increased risk of clinical mastitis was not answered in this report. To study the risk of cows that acquired clinical mastitis in relation to SCC, SCC at the cow level should be evaluated instead of BMSCC. Clearly, at herd level, a low SCC does not contribute to a significant increase in clinical mastitis, which is important when advising farmers to decrease BMSCC. Apparently, there is no associated risk of a higher incidence of clinical mastitis when the BMSCC is decreased. However, variance in the incidence of clinical mastitis does appear to increase; mean incidence is not affected, but the highest and lowest incidence rates were those for cows in the low BMSCC category. Additionally, the incidence of systemic signs that accompanied clinical mastitis was higher for herds in the low BMSCC category. Therefore, overall incidence of mastitis was not affected, but its variance and the severity of disease were higher at the lowest BMSCC. Whether the increased severity of disease outweighs the increased milk production and the decreased prevalence of subclinical mastitis has to be analyzed further using economic analyses. CONCLUSIONS Herds with low BMSCC did not have significantly higher IRCM than did herds with medium or high BMSCC. The variance in the IRCM among herds was higher for herds in the low BMSCC category than for herds in the high BMSCC category; the highest and lowest incidence rates occurred for herds in the low BMSCC category. Clinical mastitis caused by GramJournal of Dairy Science Vol. 81, No. 2, 1998

negative pathogens, such as E. coli, Klebsiella spp., or Pseudomonas spp., occurred more often in herds in the low BMSCC category. Clinical mastitis caused by Staph. aureus, Strep. dysgalactiae, and Strep. agalactiae occurred more often in herds in the high BMSCC category. The IRCM of cows that were reported by the farmer to be systemically ill was higher for herds in the low BMSCC category than for herds in the medium and high BMSCC categories. Both overall culling rate and culling rate for clinical mastitis were not affected by BMSCC category. Farmers of herds with a high BMSCC, however, culled more cows with a high SCC. ACKNOWLEDGMENTS The authors thank Hendrika Brouwer, Simone Hollander, and Roelke Nieweg for performing the bacteriological analyses of the samples. Hink Jan Stel is acknowledged for collecting a large part of the milk samples from the farms, and Janneke van der Veen is acknowledged for coordinating the data collection. We also thank Michael Collins and Jan Grommers for their suggestions regarding the manuscript. This research was partially funded by the J. Mesdag Foundation (The Netherlands). REFERENCES 1 Barkema, H. W., Y. H. Schukken, T.J.G.M. Lam, D. T. Galligan, M. L. Beiboer, and A. Brand. 1997. Estimation of interdependence of subclinical mastitis among quarters of the bovine udder, and implications for analysis. J. Dairy Sci. 80: 1592–1599. 2 Erskine, R. J., R. J. Eberhart, L. J. Hutchinson, S. B. Spencer, and M. A. Campbell. 1987. Herd management and prevalence of mastitis in dairy herds with high and low somatic cell counts. JAVMA 190:1411–1416. 3 Erskine, R. J., R. J. Eberhart, L. J. Hutchinson, S. B. Spencer, and M. A. Campbell. 1988. Incidence and types of clinical mastitis in dairy herds with high and low somatic cell counts. JAVMA 192:761–765. 4 Esslemont, R. J., and M. A. Kossaibati. 1997. Culling in 50 dairy herds in England. Vet. Rec. 140:36–39. 5 Fox, L. K., S. T. Chester, J. W. Hallberg, S. C. Nickerson, J. W. Pankey, and L. D. Weaver. 1995. Survey of intramammary infections in dairy heifers at breeding age and first parturition. J. Dairy Sci. 78:1619–1628. 6 Green, M. J., L. E. Green, and P. J. Cripps. 1996. Low bulk milk somatic cell counts and endotoxin-associated (toxic) mastitis. Vet. Rec. 138:305–306. 7 Grommers, F. J. 1988. Host resistance mechanisms of the bovine mammary gland: an analysis and discussion. Neth. Milk Dairy J. 42:43–56. 8 Harmon, R. J., R. J. Eberhart, D. E. Jasper, B. E. Langlois, and R. A. Wilson. 1990. Microbiological Procedures for the Diagnosis of Bovine Udder Infection. Natl. Mastitis Counc., Inc., Arlington, VA. 9 Hoblet, K. H., J. S. Bailey, and D. E. Pritchard. 1988. Coagulase positive staphylococcal mastitis in a herd with low somatic cell counts. JAVMA 192:777–780. 10 Hogan, J. S., K. L. Smith, K. H. Hoblet, P. S. Schoenberger,

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