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1 Animal Epidemiology Research Unit, INRA, 63122 Saint Genès Champanelle, France
2 France Contrôle Laitier, 167 rue du Chevaleret, 75013 Paris, France
3 Département de Génétique Animale, INRA, 78352 Jouy en Josas Cedex, France
Corresponding author: J. Barnouin; e-mail: barnouin{at}clermont.inra.fr.
| ABSTRACT |
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Key Words: somatic cell score management practice
Abbreviation key: 36-mo SCS = mean somatic cell score for the 36 mo preceding the beginning of the survey, BMCC = bulk milk somatic cell count, INRA = Institut National de la Recherche Agronomique, LOW = very low SCS herds, MED = medium SCS herds, PRIM = primary final logistic model, SEC = secondary final logistic model, ZMP = Zero Mastitis Objective Program.
| INTRODUCTION |
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The aim of the present epidemiological work, conducted between February 1999 and August 2001 in French dairy herds selected on a national basis through the Zero Mastitis Objective Program (ZMP), was to highlight from questionnaire surveys management practices and characteristics discriminating between herds with a very low SCC for at least 5 yr (considered as going beyond the objective concerning the degree of control of herd SCC) and herds with a medium SCC for at least 5 yr (considered as reaching the current objective concerning herd SCC).
| MATERIALS AND METHODS |
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Two samples of herds were constituted according to the herds previous 36-mo history of somatic cell score (36-mo SCS), because SCS (SCS = log2[SCC/100.000] + 3) is a criterion not biased by milk discarding. Herd 36-mo SCS was the arithmetic mean of all monthly cow SCS values determined in a herd during the 36 mo preceding the beginning of the study.
Herd samples were stratified on department and breed. The first sample included very low SCS herds (LOW herds) belonging to the first 5 percentiles of herds regarding 36-mo SCS. LOW herds had scores
1.99 for Montbéliarde,
2.38 for Holstein, and
2.76 for Normande herds. The second sample included herds belonging to the 50 to 55th percentiles of herds (MED herds). The MED herds had 36-mo SCS greater than, but close to, the median breed value (i.e., 2.78 for Montbéliarde, 3.22 for Holstein, and 3.32 for Normande herds). In each department, the herds were chosen in the ratio of 3 LOW to 2 MED herds, as another ZMP objective (not concerned by the present article) was to highlight practices linked with clinical mastitis risk in LOW herds. Finally, the number of herds in a department depended on: (1) the number of herds that each local DHIA could survey; (2) the number of available LOW and MED herds; and (3) the percentage of herds per breed in the department. When the numbers of available herds were greater than requested, the herds with the lowest SCS were chosen. Herds (n = 586) that matched the criteria were enrolled in the program. Three selected farmers quit the survey before starting. Seven herds were not used because of bovine spongi-form encephalopathy. Forty-two farmers quit the program before it ended for various reasons (DHIA resignation, health, lack of time, personal, and unknown reasons) or were discarded for incomplete data. Finally, 326 LOW and 208 MED herds that did not change from one SCS category to another during the survey were compared, representing 91.1% of the initially enrolled herds.
Data Collection
The DHIA technicians collected questionnaire data concerning characteristics and management practices of the selected farms by interviewing dairy farmers. Milk samples were collected to determine milk yield, SCC (through Fossomatic cell counters), and other milk-quality parameters. Bacteriological analyses of milk were not available in the study.
The questionnaire was validated by the consensus of an expert working group and pilot interviews of 10 farmers outside ZMP to check its feasibility and comprehensiveness. Questions not easily understood were not included in the questionnaire. In total, the final version of the questionnaire consisted of 1,055 herd characteristics and practices, of which 188 were determined by the technician from preexisting information (farm general descriptors, monthly numbers of calvings, milking machine characteristics, milk production, and quality data). The interviewees did not have to answer all questions because some did not apply to their farm (e.g., cubicle characteristics could not be described when the cows were loose-housed in a straw yard). Some information could be quickly collected; for example, 135 characteristics of the feeding system (presence or absence of 45 foodstuffs in the diet of heifers, milking cows, and dry cows) could be collected in 15 to 20 min. Nevertheless, to collect all the questionnaire data, 7 to 8 h were necessary. Consequently, 2 complementary questionnaires were carried out. The first questionnaire, which concerned basic characteristics of the dairy, cowshed, and milking parlor description, personal characteristics of the herdsman, and milk-quality traits, was administered from October to December 1999. The second questionnaire, which concerned herd housing conditions, feeding system, udder and calving hygiene, and herd health, was administered from October to December 2000. As the farmers declared that their dairy management system would not change during ZMP, we assumed that herd characteristics and practices were fairly stable between the time of the 2 questionnaires. Moreover, we checked that herds did not change from one SCS category to another during the survey period.
Agreement between the responses of the farmers and the observations of DHIA technicians during a milking-parlor visit carried out 13 mo on average after the farmers interview was evaluated using the Kappa statistic. For hygiene milking practices, recorded through interviews and milking parlor visits, the Kappa coefficient value ranged between 0.66 and 0.79. It is reasonable to expect that ZMP farmers, as good managers, gave reliable information concerning their management procedures (Schukken et al., 1989b). Nevertheless, as the interviewers were the DHIA technicians of the surveyed farms and had a thorough knowledge of the herd management system, they checked the farmers answers by requesting confirmation at the end of the interview of any information that seemed erroneous. Finally, questions concerning 15 herd characteristics and practices that involved some inconsistent answers regarding our knowledge of dairy farm management in France were removed from data analyses.
Database
All data were transmitted to the Institut National de la Recherche Agronomique (INRA) Animal Epidemiology Research Unit and stored in an Access 2000 relational database organized through 34 tables. Herd identification number, breed, SCC data, and other milk traits were extracted from the national DHIA database. Checking procedures for data validity were conducted. They consisted of controlling the missing answers and checking with the herd surveyor if such answers were normal or had to be completed. A set of automatic logical procedures also was implemented through the database to detect erroneous entries (e.g., absence of response concerning free stalls if the cows were housed in a straw yard or yearly number of weeks in which the herd was outdoors <53 wk). Moreover, a double data keyboarding was performed independently by 2 INRA technicians to check keyboarding errors.
Statistical Analyses
Statistical procedures were conducted using SAS/STAT 8.1 (SAS Institute Inc., Cary, NC). The dependent variable was the group of herds based on SCS (LOW vs. MED). Herd characteristics and management variables shared by the whole sample were analyzed through 3 main steps.
First,
2 and Wilcoxon tests were performed through PROC FREQ and PROC NPAR1WAY to screen the univariate relationships between hypothesized explanatory variables and SCS group. Then, the results of the univariate analysis were discussed by the ZMP collaborators (INRA, France Contrôle Laitier, Etablissements Départementaux de lElevage, Institut de lElevage, Schering Plough Vétérinaire) through a preliminary report (Barnouin et al., 2002). In a second step, significant variables (P < 0.25; n = 126) through the univariate analysis were selected within 10 categories of management characteristics and practices (Table 1
), and 10 multiple regression logistic models were performed by PROC LOGISTIC. In all the logistic models, PROC LOGISTIC modeled the probability that a herd belonged to the LOW group. Moreover, the correlations between selected variables were analyzed (PROC REG and PROC CORR), and if variables were correlated (condition index >30 or correlation coefficient >0.15), only the variable with the best fit was included in the final model. As these selection criteria were more severe than those that were generally used, it was reasonable to expect that within the final models of the present study, the multicolinearity among variables was notably weak. Logistic model building used a backward algorithm that assessed 2-way interaction at each step. Assessment of how the models fitted the data was determined using HosmerLemeshow test (Hosmer and Lemeshow, 1989), residual distribution, and deviance analysis. In a last step, the category models were first combined and those variables (n = 47) selected (P < 0.10) from the 10 models were offered to a primary final logistic model (PRIM). Those 18 variables selected (P < 0.05) by the PRIM best explained the SCS grouping and were considered to be the primary variables to define a mastitis control program. Then, the variables removed from PRIM were included in a second logistic model (Barkema et al., 1998a) and the 8 variables selected (P < 0.05) by the secondary final logistic model (SEC) were considered as secondary explanatory variables for the SCS grouping. As for the 22 significant variables from the univariate analysis that were not selected in the final logistic models, they consisted mainly of calving hygiene and mastitis prevention (n = 6), milking (n = 4), and mastitis management (n = 3) category models (Table 1
).
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| RESULTS |
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Univariate Analysis
Table 3
displays the univariate analysis of the explanatory variables offered to PRIM and SEC logistic models. The most discriminating variables (P < 0.001) that characterized LOW herds through univariate analysis were teat spraying (23.1% of LOW vs. 9.1% of MED herds) and herdsman considering himself precise in his techniques (82.5% of LOW vs. 68.5% of MED herds). The most discriminating variables characterizing MED herds were udder checking for mastitis beginning <2 wk before the first calving (21.1% of MED vs. 10.4% of LOW herds), no mastitis treatment when only one clot was detected in the milk at successive milkings (72.1% of MED vs. 57.4% of LOW herds), and dairy cows housed in a straw yard (62.0% of MED vs. 37.4% of LOW herds).
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According to the SEC, the probability for a herd to belong to the LOW group was maximized when: (1) cows were housed in a calving pen at parturition; (2) the herdsman asserted that at least 2 cows reacted to their name; (3) a teat disinfection before intramammary infusion was performed to treat a clinical mastitis (variables 1 to 3; P < 0.01); (4) udder scores were checked by herd-book organization; (5) dry cows were not housed in a separate cowshed; (6) high SCC and mastitic cows were milked last; (7) painful udder was not considered to be a symptom of mastitis; and (8) milking-cow exercise area was scraped more than once daily (variable 4 to 8; P < 0.05). Figure 1
displays 4 practice boxes summarizing herd factors associated with a high degree of SCC control: (1) specialized and attentive herdsman (Box 1); (2) hygienic living conditions (Box 2); (3) optimized calving conditions (Box 3); and (4) strict teat and udder hygiene (Box 4).
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| DISCUSSION |
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The ZMP is the first epidemiological work on bovine mastitis conducted on a national basis using SCS to compare stratified groups of herds with very low and medium somatic cell levels by using multivariate procedures on a large set of characteristics. Somatic cell score is considered to be a better indicator of subclinical mastitis than the more imperfect bulk milk somatic cell count (BMCC; Sargeant et al., 2001). Bulk milk somatic cell count usually is poorly correlated with subclinical infection status (Noordhuizen et al., 1987). Eliminating milk practices that interfere with BMCC could explain unexpected results concerning the relationship between farm hygiene practices and BMCC (Agabriel et al., 1997). Reviewing common factors highlighted in studies comparing groups of herds on the basis of BMCC with those displayed in the final PRIM and SEC logistic models can be informative. But, such a comparison is difficult because BMCC categories, collected variables, and statistical procedures (univariate or multivariate models studying confounding factors by several procedures) differed among surveys.
As in the present work, the univariate study of Hutton et al. (1990) demonstrated that cow milking order and teat disinfection before antibiotic infusion characterized low SCC herds. Cows having a dry bedding, a characteristic which was highlighted as a protection factor by Hutton et al. (1991), would correspond in ZMP to cows not housed in a straw yard, a characteristic inducing a smaller risk of damp bedding. In Erskine et al. (1987), the risk factors were different, but low SCC herds (<150,000 cells/mL) were compared with very high SCC herds (>700,000 cells/mL), implicating different risk attitudes compared with MED herds. For Barkema et al. (1998a), the variables which discriminated low and medium BMCC differed from those discriminating LOW and MED herds, except regular mastitis checking before calving and cows locked up at the feed-line, 2 practices tending to be used more often in low BMCC herds than medium herds. According to Barkema et al. (1998b), cows were more frequently culled for teat lesions in low BMCC herds. As in the ZMP study, Barkema et al. (1999) found that farmers having low BMCC herds worked more precisely and were more familiar with each cow (a concept close to the cows react to their name variable in our study). Using study designs other than comparisons between stratified groups of herds, management practices decreasing milk SCC have been extensively studied. Nevertheless, some ZMP significant factors were not investigated in any previous work: prepartum Ca restriction in the diet, distance from the farmers house to the cowshed, mastitis treatment when one milk clot was observed at successive milkings, painful udder not considered as a symptom of mastitis, heifers in a nondamp pasture, and no pasture free access during bad weather.
From the first box of Figure 1
, the LOW herdsman had the following characteristics: (1) specialized in dairy farming; (2) lived near the cowshed; (3) considered to be precise in his management techniques (e.g., meticulous and tidy); (4) integrated animal welfare in his management (cows reacting to their names); and (5) had a positive udder checking attitude (in the heifer, at milking, and via herd-book). Such an attitude involved culling of cows with damaged teats to reduce mastitis recurrence (Bendixen et al., 1988) and mastitis treatments implemented just after observation of clinical signs. A frequent udder checking for mastitis before calving characterized low BMCC herds (Barkema et al., 1998b). The influence of dairy producers personal characteristics on SCC has been investigated (Tarabla and Dodd, 1990; Barkema et al., 1999). According to these authors, a positive attitude toward animal and milking may influence milk quality by correct application of management practices. Moreover, farmers considered to be clean and accurate know their cows better. Interactivity between the herdsman and his cows would qualify a competent dairy farmer (Albright and Stricklin, 1989). Finally, frequent contacts between herdsmen, technicians, and cows would promote appropriate observations and quick therapeutic decisions at any change in udder or milk appearance (one clot observed in the milk at successive milkings).
The second box corresponds to characteristics of the cows life cycle. Regarding housing cows in a straw yard compared with free stalls, our results agree with those of Peeler at al. (2000), who demonstrated that straw yards induce more clinical mastitis cases in low SCC herds. Less mastitis cases are detected in cows housed in free stalls compared with those housed in straw yards (Berry, 1990). Free stalls are linked with fewer SCC (Goodger et al., 1988). Larger SCC and dirtier cows are reported when cows were housed in a straw yard than in free stalls (Fregonesi and Leaver, 2001). Straw bedding promotes rapid growth of various udder pathogens, particularly in humid weather conditions (Zehner et al., 1986). Hutton et al. (1990) reported that DM content of bedding for lactating cows was higher in low SCC herds. Other box 2 variables (heifers in a nondamp pasture and heifers not drinking water from a river, no free access of cows to pasture during bad weather, frequently cleaned exercise area) correspond to living and bedding conditions including a less damp and cleaner environment. Drinking water from sources other than public water increased risk for mastitis (Schukken et al., 1990). Moreover, drinking from a river involves consumption of mud, manure, and water splashes unfavorable to udder hygiene. Bartlett et al. (1992) found lower BMCC in herds having a clean and dry cow exercise area and less risk for mastitis is associated with twice-daily scraping of cow lots (Peeler et al., 2000). Moreover, the fact that nonlactating cows are often housed in poor facilities (Khaitsa et al., 2000) may be associated with greater risks for mastitis in herds in which dry cows and replacement heifers are housed in a separate facilities from lactating cows.
The third box includes variables related to calving conditions. Prepartum dietary Ca restriction, a protective factor against milk fever (Barnouin, 1990), prevents increased lying time after calving and loss of muscle tone in the teat sphincter (Goff, 2003), and subsequent less risk for mastitis. In addition, statistical associations were detected between milk fever and mastitis occurrence (Faye et al., 1986; Schukken, 1990). Menzies and Mackie (2001) indicated that preventive actions minimizing downer cow syndrome would reduce toxic mastitis occurrence. Moreover, longer standing than lying periods were observed in healthy vs. mastitic cows (Vavak, 1990). Calving in a calving pen enables better hygiene at parturition. This practice is an important protective factor against environmental mastitis, and calving pen cleanliness is better in low vs. high BMCC herds (Barkema et al., 1998a). In agreement with this result, the univariate analysis showed that more (P < 0.05) LOW herds (51%) than MED herds (40%) cleaned the calving pen after each calving. Because calving is often more stressful for heifers than for cows, use of a calving pen could decrease stress and subsequent attenuated phagocytosis (Barnouin and Chassagne, 2001). Spring calvings (March to May) were associated with a dry off period between January and March, which is less favorable for bedding hygiene. Moreover, spring is the most rainy season in France and is associated with increased mastitis risk (Barnouin et al., 1986).
The early postpartum period is a critical time for mastitis susceptibility (Peeler et al., 2000) via the impairment of the immune system (Burvenich et al., 2003), especially altering the functional capacity of peripheral blood leukocytes (Nonnecke et al., 2003). The greater proportion of polymorphonuclear leukocytes in the milk of spring-calved cows with moderate and high SCC (Kelly et al., 2000) could indicate more frequent mammary infections during spring because of poorer environmental and nutrition conditions during the winter precalving period.
Box 4 highlights the importance of strict udder hygiene for a total control of mastitis risk. The protective effect of teat disinfection before intramammary treatments (preventive/curative) was emphasized by Hutton et al. (1990). Such a practice characterized the low SCC herds in their study. Moreover, as herdsmen in LOW herds also dipped teat more frequently after intramammary infusion, their cows should be well protected against new IMI. Washing only the teats before milking was associated with a lower prevalence of high SCC (Hueston et al., 1990). Nevertheless, no previous study demonstrated the protective effect of a systematic washing of the teats even if they appeared clean. To decrease new IMI, other strategies could be developed, as implemented in LOW herds, such as locking up cows at the feed-line after milking, a practice that forces cows to remain standing while the ducts are patent and vulnerable to environmental pathogens (Tyler et al., 1998; Peeler et al., 2000). Consequently, clean and accurate farmers prevented cows from lying down after milking (Barkema et al., 1998b). Cows with clinical mastitis were milked last 3.5 times more frequently in low SCC vs. high SCC herds (Hutton et al., 1990). Hueston et al. (1990) reported that milking last cows with clinical mastitis and those being treated for mastitis, an old management recommendation (Minett et al., 1933), was associated with lower SCC. Milking potentially infected cows last is an effective way to reduce IMI (Wilson et al., 1995). Teat spraying, a practice characterizing LOW herds, was generally considered to be equally effective to teat dipping for IMI control (Meaney, 1974; Pankey and Watts, 1983). Teat spraying is becoming commonplace (Hogan and Smith, 2001) for herdsmen particularly careful in animal hygiene. Teat dipping efficiency may depend on effects of temperature on germicidal activity of dipping solutions (Pankey, 1984). Regular cleansing of teat dip cups with a strong disinfectant is recommended to eliminate possible infection transfer from one cow to another (Van Damme, 1982). Because in our study the univariate statistical analysis indicated that the teat cups were more frequently cleaned in LOW herds, it could be hypothesized that teat dipping is not less effective per se, but through less teat-cup hygiene.
| CONCLUSIONS |
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Received for publication March 1, 2004. Accepted for publication August 4, 2004.
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