Effects of disease on milk production in the dairy cow: a review

Preventive Veterinary Medicine 41 (1999) 1±35

Review

Effects of disease on milk production in the dairy cow: a review C. Fourichon*, H. Seegers, N. Bareille, F. Beaudeau Unit of Animal Health Management, Veterinary School-INRA, BP 40706, F44307, Nantes Cedex 03, France Received 20 July 1998

Abstract Estimates of milk losses consequent to dystocia, stillbirth, milk fever, retained placenta, metritis, cystic ovaries, ketosis, displaced abomasum and locomotor disorders were reviewed. Papers were selected if they provided quantitative estimates of losses based on data collected after 1965, with a sample size resulting in a minimum number of disease cases of 25. Thirty-five papers fulfilled the selection criteria. Milk losses were expressed in kg/day over the period under study to allow comparison of results. Milk fever and cystic ovaries were not associated with yield losses (six studies for each disease). Less than half of the studies found losses associated with dystocia, retained placenta, and metritis, with, respectively, five studies out of 13 (0.3±2.3 kg/day across the lactation), five studies out of 13 (0.8 kg/day across the lactation to 2.5 kg/day across 100 days in milk), and two studies out of 10 (0.4 kg/day across the lactation, and 2.3 kg/day across 119 days in milk). More than half of the studies found losses associated with stillbirth, clinical ketosis, ketosis evidenced by a diagnostic test, and locomotor disorders, with, respectively, three studies out of five (0.7±1.3 kg/day across the lactation), seven studies out of 11 (2.6±5.7 kg/day short-term, and 1.2 kg/day across the lactation), five studies out of seven (1±7 kg/day on the day of diagnosis, and around 1 kg/day across 200 days in milk), and six studies out of 11 (0.3±3.3 kg/day across the lactation). All the five studies, investigating effects of displaced abomasum, found losses (3.5± 10.9 kg/day across 80 days in milk, or 0.8±2.5 kg/day across the lactation). # 1999 Elsevier Science B.V. All rights reserved. Keywords: Cattle-milk production; Diseases; Milk yield; Milk loss

* Corresponding author. Tel.: +33-240-68-77-86; fax: +33-240-68-77-68; e-mail: [email protected] 0167-5877/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 5 8 7 7 ( 9 9 ) 0 0 0 3 5 - 5

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C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

1. Introduction Assessment of the profitability of disease-control actions at the herd level relies on characterization of relationships between losses consequent to disease and expenditures for disease control (McInerney et al., 1992). At the herd level, losses are defined as a reduction of the output/input ratio of the production process (Dijkhuizen, 1983). To quantify economic losses, herd simulation models are needed. Simulation of disease consequences in a herd relies on knowledge of both, the disease effects at the cow level and decision rules of the farmer (regarding, e.g. culling) (Seegers et al., 1994). At the cow level, the occurrence of disease might result in mortality, or might decrease milk yield, impair fertility and, subsequently, lead to culling. For simulation purpose, these effects need to be quantified. Regarding effect of disease on milk yield, the relevant information is the difference in milk yield of a diseased cow, compared to the expected yield of that cow, had there been no disease. A review of the relationships between diseases and milk yield by Erb (1987) reported that milk losses were associated with dystocia, retained placenta, metritis, cystic ovaries, milk fever, displaced abomasum and mastitis, but not with ketosis. Considering each disease separately, only one-to-four source papers were available, and quantitative estimates of the losses were issued from one or two studies, evidencing a significant effect. Since then, several studies have aimed at quantifying milk losses and further results have been given regarding the main diseases of dairy cows. Study designs used to quantify these effects can influence the estimates. Particular attention should be paid to potential confounding when the risk of disease varies according to production level. For example, some diseases of the dairy cow have been described as more frequent in high-yielding cows: e.g. milk fever (Dohoo and Martin, 1984a); metritis (PoÈsoÈ and MaÈntysaari, 1996); cystic ovaries (Erb et al., 1981b); ketosis (Detilleux et al., 1994); and displaced abomasum (Martin et al., 1978). When comparing the yields of diseased and nondiseased animals, without control for this circumstance, the analysis underestimates losses and may result incorrectly in a positive estimate of the disease effect. The objectives of this paper were to summarize the reported effects of diseases on milk yield in the dairy cow, and to provide a detailed description of study-design components which can lead to biased estimates. This review only considered health disorders which are frequently met in current dairy production systems, and for which quantification of milk losses were studied by several authors in field conditions. The milk losses consequent to clinical and subclinical mastitis were recently reviewed by Hortet and Seegers (1998a, b) and are, therefore, not presented here. Moreover, single-agent infectious diseases or parasitic diseases were not considered. 2. Material and methods 2.1. Selection of papers Papers providing quantitative estimates of variation in milk yield were selected for a detailed description of study design and results whereas papers reporting only trends or

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

3

direction of relationship were not included. Papers which failed to describe the method used to quantify losses were not selected, either. To be able to generalize the results to current production systems, this investigation focused on results issued from data collected as recently as possible. On account of the small numbers of available studies, the date threshold for source data had to be set to 1965, except in Simerl et al. (1992) where most of the data recorded from 1959 to 1979 fulfilled this criteria. The reason for setting a date threshold is that, in older papers, the management systems under study and the production level would differ from current standards. Furthermore, older studies could include time periods when disease patterns differed from current patterns, with, for instance, a higher prevalence of single-agent infectious diseases with strong effects on milk yield. Sample size was considered to check for power of the analysis. Numbers of case records were either read directly in source papers, or calculated by us according to disease incidence and sample size. When the disease risk was only known in a total sample larger than the study sample used to quantify milk loss, the number of cases in the study sample was estimated by multiplying the total-sample incidence risk by the studysample size. All the papers in which the number of case records was below 25 were a priori excluded because of possible lack of power. With a significance level of 0.05, this threshold resulted in 80% chance to detect losses equal to 0.4±0.6 times the standard deviation of the milk-yield parameter considered for proportions of cases in the sample from 0.01 to 0.5. For Lean et al. (1994), a smaller sample size was accepted because few reports on short-term losses exist. Moreover, Lean et al. (1994) found short-term losses based on every 3-day measurement of milk yield, in spite of a low a priori power (nine cases). In most papers, standard errors of the milk±loss estimates were not available. Thirty-five papers were selected. 2.2. Description of study designs used to quantify disease effect 2.2.1. Source of data Data mainly originated from commercial Holstein herds in North America or northern Europe (Table 1). Only six studies were based on data from the last decade. Therefore, average milk-production level was often low compared to current production systems. Four data sets were analyzed in several papers with different statistical designs, and provided different estimates based on the same source (Erb et al., 1981a, b; Dohoo and Martin, 1984b, c; Lucey et al., 1986 and Rowlands and Lucey, 1986; Gustafsson et al., 1993 and Gustafsson and Emanuelson, 1996). Fourteen papers were based on data originating from <10 herds. The main source of information for cow milk yield was official recording schemes (Dairy Herd Improvement, cattle-breeders associations, Record Of Performance). In such cases, available data were monthly milk records. In a few studies (mainly in research herds), data were collected on a weekly or daily basis. Disease information was generally drawn from farm records; few large-scale disease-information systems were available. Case definitions are provided in the tables in Section 3 and should be considered when comparing estimates of losses. Especially in commercial herds, the ability to detect disease varies widely between farmers. Many studies relied on herds involved in a herd-

4

Table 1 Source of data, sampling and data collection Study period

Country

Breed a

ArgaÁez-Rodriguez et al., 1997 Barkema et al., 1992

1993/1994

Mexico

H

1982/1990

Netherlands

Barkema et al., 1994

1988/1991

Netherlands

Bigras-Poulin et al., 1990 Cobo-Abreu et al., 1979 Coulon et al., 1996

Herds Cows

Lactations

Herd type b

Diseases recording c

Milk recording d

Average milk yield e (kg)

C

FR

FR

6388 LY

FVR 3-week MR visit FVR 3-week MR visit FR MR FR MR FR FR weekly

1

591

591

DF,DFH

35

Ð

1029

CU

DF,DFH,MRY

13

Ð

2435

CU

1980/1983 Canada 1970/1976 Canada 10±20 years France

H Ð MO,H,FF,cross

34 1 3

1588 26±52 1179

1588 Ð 3851

C R R

Deluyker et al., 1991

1986/1987

USA

H

1

408

408

C

Dematawewa and Berger, 1997 Detilleux et al., 1994 Detilleux et al., 1997 Djemali et al., 1987 Dohoo and Martin, 1984b Dohoo and Martin, 1984c Enting et al., 1997

1980/1991

USA

H

Ð

71 618

122 715

C

FR 3-day check FR

1985/1988 1992/1994 1982/1984 1979/1981 1979/1981 Ð

Finland USA USA Canada Canada Netherlands

A H H H H H,DF

Ð 21 Ð 32 32 21

60 851 12 572 Ð Ð 2008 2183

76 190 Ð 141 655 1315 2875 6273

C CD C CV CV CU

RS FVR FR FVR FVR FVR

Erb et al., 1981a, b Erb et al., 1985

1970/1975 1981/1983

Canada USA

H H

20 33

Ð 2569

810 2850

RS MR

Gustafsson et al., 1993, 1996 Kauppinen, 1984 Kay, 1978 King, 1979 Lean et al., 1994

1985/1988

Sweden

SRW,SF

474

22 334

38 624

CU CU,35 cows C

Ð 1965/1975 10 years Ð

Finland UK UK USA

F,A Ð A,BF H

Ð 3 Ð 1

570 34 53 24

Ð 224 53 24

C R C C,BST trial

sampling FR ± FVR daily

sampling

Ð 8611 L3Y

FR daily

Ð Ð 20 kg/day*DY (dpp 4±6) 10 900 HY

MR

Ð

MR 5710 L3Y MR monthly 9782 L3M MR Ð MR 7500 L3M MR 7500 L3M Ð 24.6 kg/day* DM MR 7006m BCM MR 8094 L3M MR monthly 25.4 kg/day* DFC (dpp  200) MR 5819 AY FR 4382* LY SR 10.6 kg/dayr DY every 3±6 40 kg/day* DY days

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Reference

Table 1 (Continued ) 1977/1982 1979/1980 1991/1992 1984 1970/1977 1968/1972 1967/1970 1977/1982 1984/1985

UK Canada Israel USA Canada USA Sweden UK Norway

BF,A,H,cross H H H H H SF BF,A,H,cross Ð

4 Ð 8 1 23 1 Ð 4 5

Simerl et al., 1992 Tranter and Morris, 1991 Van Werven et al., 1992

1959/1979 1989/1990 1988/1990

USA H,J,others 1 New Zealand Ð 3 Netherlands DF, DFH, MRY 21

732 Ð 839 339 Ð Ð 972 732 86 1144 838 Ð

1594 23 873 839 339 124 298 972 1594 86 1144 Ð 1087

C,R C CV C CU R C C,R C,ketosis

FVR FR FVR syst FR RS FVR FR FVR RS, sampling

FR weekly MR MR monthly MR MR MR MR FR weekly FR weekly

R CU CU

FR FVR FVR 4-week visit

MR Ð Ð

5060 L3Y 5687 L3Y 10 045 L3M 6317 L3Y 6156* L3Y 6370 L3M 4857 LY 5060 L3Y 24.0 kg/daym DY (dpp  42) 3494p LY 3500* LY 8054 HY

a A, Ayrshire; BF, British Friesian; DF, Dutch Friesian; F, Friesian; FF, French Friesian; H, Holstein; J, Jersey; MO, MontbeÂliarde; MRY, Meuse Rhine Yssel; SF, Swedish Friesian; and SRW, Swedish Red and White. b Type of herds and criteria for inclusion: C, commercial herd; CD, commercial herd in DHI health database; CU, commercial herd involved in a herd-health program with university; CV, commercial herd involved in a herd-health program with veterinary practitioner; and R, research herd. c FR, farm records; FVR, farmer and veterinary practitioner records; RS, diseases and/or treatments recording system based on veterinary practitioner; and syst, systematic veterinary examination postpartum. d FR, farm records; MR, milk-recording program (DHI, ROP, dairy syndicate, herd book,. . .), records assumed to be monthly when not stated; and SR, specific study recording at signs onset and after recovery. e AY, annual yield; BCM, yield estimated from breed-class-average for milk; DFC, daily 4%-fat-corrected yield; DM, daily mature-equivalent milk; DY, daily yield; HY, annual mean herd yield; LY, lactation yield; L3M, standardized 305-day mature-equivalent milk; L3Y, standardized 305-day lactation yield; *, yield of non-diseased cows; m, yield of multiparous cows; p, yield of primiparous cows; and r, yield of diseased cows after recovery; Ð, no information available in the paper; and dpp, days postpartum.

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Lucey et al., 1986 Mangurkar et al., 1984 Markusfeld and Ezra, 1993 Martin et al., 1986 Martin et al., 1978 Muller and Owens, 1974 Philipsson, 1976 Rowlands and Lucey, 1986 Simensen et al., 1990

5

6

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

health program (either with a veterinary practitioner or with a university). Disease cases were then recorded by both, the farmer and the veterinarian. Health programs usually included systematic veterinary visits and cow examination in the postparturient period whereas some recording systems considered only veterinary treatments. Studies based on farm records mainly considered dystocia and retained placenta (which are more easily detected than other diseases). For ketosis diagnosis, specific sampling was implemented in some studies. 2.2.2. Effects of disease on milk yield Effects were studied either for one disease, or for several simultaneously (Table 2). Quantification of yield reduction was done under existing management conditionsÐ implying that cows generally were treated at the time of diagnosis. Accuracy and effectiveness of treatment implemented by farmers or vets can be assumed to have been at a standard level. Consequently, estimates are the net losses remaining in spite of the (presumed-positive) effect of treatment. In a few studies (Rowlands and Lucey, 1986; Deluyker et al., 1991; Coulon et al., 1996), the stage of occurrence of disease was accounted for when estimating milk losses (assuming stage-specific variation in losses). When repeated occurrences of disease were recorded, generally only the first diagnosis was considered; however, Lucey et al. (1986) considered all occurrences as separate cases to estimate short-term reduction in yield. Lucey et al. (1986), Deluyker et al. (1991), and Detilleux et al. (1994, 1997) looked for possible decrease in milk yield prior to disease diagnosis. Besides quantification of milk-yield losses, Martin et al. (1986), Rowlands and Lucey (1986), Bigras-Poulin et al. (1990), Deluyker et al. (1991); Tranter and Morris (1991), and Markusfeld and Ezra (1993) investigated possible effect on the shape of the lactation curve (peak yield, month of peak yield, rate of decline at Week 25 or between peak and six months later, days in milk). A few papers reported effects on fat and protein yields or contents, and on lactose and mineral contents, but only effects on milk yield are reviewed here. Erb et al. (1981b, 1985) and Dohoo and Martin (1984b) investigated direct and indirect effects of disease on milk yield separately. Indirect effects resulted from an increased risk of occurrence of another disease after a first disease, or from the negative effect of some diseases on fertility. In other studies, when the study design controlled for these consequences of disease, the resulting estimate measured only the direct effectÐwhereas without any control the estimate included both, direct and indirect effects. Calculation of losses was based on comparison of yield of diseased cows with yield of reference cows. Generally, reference records were defined as all records (lactations or test-days) of cows without the disease under study, but a few authors restricted reference cows to cows without any disease. Some authors matched reference and case records. Only three studies considered a cow as its own reference (Table 3). Cobo-Abreu et al. (1979) and Dohoo and Martin (1984b) considered deviation from the herd average yield (expressed in breed-class-average units), instead of absolute yield. A further restriction was done by Coulon et al. (1996) who considered case cows only if they were free of mastitis, milk fever or retained placenta in the period of occurrence of the disease under study (lameness).

Table 2 Investigation of disease effects on milk yield Dystocia a

Retained placenta a

Milk fever a

Metritis a

Cystic ovary a

Ketosis a

Displaced abomasum a

Locomotor disorders a

Other diseases b

ArgaÁez-Rodriguez et al., 1997 Barkema et al., 1992 Barkema et al., 1994 Bigras-Poulin et al., 1990 Cobo-Abreu et al., 1979 Coulon et al., 1996 Deluyker et al., 1991 Dematawewa and Berger, 1997 Detilleux et al., 1994 Detilleux et al., 1997 Djemali et al., 1987 Dohoo and Martin, 1984b Dohoo and Martin, 1984b Dohoo and Martin, 1984c Enting et al., 1997 Erb et al., 1981a Erb et al., 1981b Erb et al., 1985 Gustafsson et al., 1993 Gustafsson and Emanuelson, 1996 Kauppinen, 1984 Kay, 1978 King, 1979 Lean et al., 1994 Lucey et al., 1986 Mangurkar et al., 1984 Markusfeld and Ezra, 1993 Martin et al., 1986 Martin et al., 1978 Muller and Owens, 1974

Ð ‡ Ð ‡ Ð Ð ‡ ‡ Ð Ð ‡ ‡ Ð Ð Ð ‡ ‡ ‡ Ð Ð Ð Ð Ð Ð ‡ ‡ Ð Ð Ð Ð

Ð Ð Ð ‡ ‡ Ð ‡ Ð Ð Ð Ð ‡ Ð Ð Ð ‡ ‡ ‡ Ð Ð Ð ‡ Ð Ð ‡ Ð Ð ‡ Ð ‡

Ð Ð Ð ‡ ‡ Ð ‡ Ð Ð Ð Ð ‡ Ð Ð Ð Ð Ð ‡ Ð Ð Ð Ð Ð Ð ‡ Ð Ð Ð Ð Ð

Ð Ð Ð ‡ ‡ Ð ‡ Ð Ð Ð Ð ‡ Ð Ð Ð ‡ ‡ ‡ Ð Ð Ð Ð Ð Ð ‡ Ð ‡ Ð Ð Ð

Ð Ð Ð ‡ ‡ Ð Ð Ð Ð Ð Ð ‡ Ð Ð Ð ‡ ‡ ‡ Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð

Ð Ð Ð ‡ ‡ Ð ‡ Ð ‡ Ð Ð ‡ ‡ ‡ Ð Ð Ð Ð ‡ ‡ ‡ Ð ‡ ‡ ‡ Ð Ð Ð Ð Ð

Ð Ð Ð Ð ‡ Ð ‡ Ð Ð ‡ Ð ‡ Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð ‡ Ð

‡ Ð ‡ ‡ ‡ ‡ ‡ Ð Ð Ð Ð ‡ Ð Ð ‡ Ð Ð Ð Ð Ð Ð Ð Ð Ð ‡ Ð Ð Ð Ð Ð

Ð Ð Ð A,S,M,U,V M,R Ð M,S Ð Ð Ð Ð A,D,M,R,TR SCC Ð Ð Ð Ð M Ð Ð Ð Ð Ð H,M Ð Ð Ð Ð Ð

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Reference

7

8

Reference

Dystocia a

Retained placenta a

Milk fever a

Metritis a

Cystic ovary a

Ketosis a

Displaced abomasum a

Locomotor disorders a

Other diseases b

Philipsson, 1976 Rowlands and Lucey, 1986 Simensen et al., 1990 Simerl et al., 1992 Tranter and Morris, 1991 Van Werven et al., 1992

‡ ‡ Ð ‡ Ð Ð

‡ ‡ Ð ‡ Ð ‡

Ð ‡ Ð Ð Ð Ð

Ð ‡ Ð ‡ Ð Ð

Ð Ð Ð Ð Ð Ð

Ð ‡ ‡ Ð Ð Ð

Ð Ð Ð Ð Ð Ð

Ð ‡ Ð Ð ‡ Ð

S H Ð S Ð Ð

a

‡, studied; Ð, not studied. A, abortion; D, digestive disorders; H, hypomagnesaemia; M, mastitis; R, respiratory disorders; S, stillbirth; SCC, somatic cell count; TR, traumatic reticuloperitonitis; U, udder disorders other than mastitis; and V, vaginitis. b

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Table 2 (Continued )

Table 3 Estimation of effects of diseases on milk yield: method and modeling Reference

Type d

(P > 1),DIM 200±360

Ð

LSR

LY

cesarean section

random selection

LSR

Ð Ð cow lifetime lactations no disease  dpp 245 Ð Ð

Barkema et al., 1994 (P > 1) Bigras-Poulin et al., 1990 DIM > 240 (BCM, X305) Cobo-Abreu et al., 1979 once diseased Coulon et al., 1996

no other disease

Deluyker et al., 1991 Dematawewa and Berger, 1997 Detilleux et al., 1994 Detilleux et al., 1997

DIM  119 P < 9, DIM  7

P<7 (P > 1),P < 6, d open  40 Djemali et al., 1987 Ð Dohoo and Martin, 1984b DIM > 150 Dohoo and Martin, 1984b (P > 1),DIM > 150 Dohoo and Martin, 1984c P > 1 Enting et al., 1997 (P > 1),no case in previous lactation Erb et al., 1981a P > 1,cow calving again Erb et al., 1981b P > 1,cow calving again Erb et al., 1985 Ð Gustafsson et al., 1993

Controlled effects e H

P

M

PMYf

D

Other variables adjusted for

4

1

‡

‡

PDY

ÿ

LL, cow origin

100dY,270dY

2

‡

‡

‡

ÿ

ÿ

LSR LSR

100dY,270dY LY,BCM,X305

2 4

‡ ‡

‡ ‡

‡ ÿ

PL100Y ÿ ÿ ‡

C Y, g e s t a t i o n length CY LL (for LY)

UNI

DBCM

4

1

m

m

m

ÿ

Ð

CURV

LY

3

ÿ

‡

ÿ

REFY

ÿ

LS,SEA,BR

LSR BLUE

119dY,ndY,PY X305

3 4

1 ‡

‡ ‡

‡ ‡

EBV ÿ

‡ ÿ

Ð no disease

REPEAT REPEAT

TDY (305) TDY (250)

3 3

‡ ‡

‡ ‡

‡ ‡

AR PLY

ÿ ‡

Ð Ð Ð Ð Ð

LSR PATH LSR LSR LSR

305ME DBCM TDY TDY DLY

4 4 3 3 3

‡ ‡ ‡ ‡ ‡

‡ ‡ ‡ ‡ ‡

‡ ‡ ÿ ÿ ‡

ÿ ÿ PBCM PLY PDY

ÿ ‡ ÿ ÿ ‡

Ð HYS,SX,AC in P,CO SEA,YS,LS LS,CY,AC,LD,SEA,YS,SCC HYS,SX AC,CI LS,SCC LS,SCC HYS,AC

Ð Ð Ð

LSR PATH PATH

BCM BCM 305ME

4 4 4

ÿ ÿ ‡

‡ ‡ ‡

‡ ‡ ÿ

LSR

TDY, 100dY, 200dY

2,3

‡

‡

‡

PBCM ‡ PBCM ‡ E B V, ‡ PMEY ITD ÿ

AC,LD,CI,PBCF AC,LD,CI CI,BW (heifers), LD(cows) Region-herd, BR,CO,CY

9

Statistical Dependent method b yield variable c

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

ArgaÁez-Rodriguez et al., 1997 Barkema et al., 1992

Reference records (if other than all non-cases)

Selection of cows or lactations a

initial test day 14 dpp Ð

10

Table 3 (Continued ) Reference

King, 1979 Lean et al., 1994 Lucey et al., 1986 Mangurkar et al., 1984 Markusfeld and Ezra, 1993 Martin et al., 1986 Martin et al., 1978 Muller and Owens, 1974 Philipsson, 1976 Rowlands and Lucey, 1986 Simensen et al., 1990

Statistical Dependent method b yield variable c

Type d

Ð

Ð

LSR

TDY

Ð

Ð

LSR

Ð 3 lactations,no RP with twins ketotic cows

matched Ð after recovery (7±10 days) Ð Ð Ð

Controlled effects e H

P

M

PMYf

D

Other variables adjusted for

3

‡

‡

‡

ÿ

ÿ

BR,CO,LS,CY

100dY, 200dY

2

‡

‡

‡

ITD

ÿ

BR,CO

UNI LSR

AMY LY,DLY

1 1,3

m ‡

m ‡

m ÿ

ÿ ÿ

ÿ ÿ

Ð CO

UNI

TDY

4

m

m

m

m

ÿ

Ð

REPEAT CURV BLUE

TDY TDY 90dY,X305

3 3 4

1 ÿ ‡

‡ ÿ ‡

ÿ ‡ ‡

ÿ ÿ ÿ

ÿ ÿ ÿ

CO SEA SIR,CI (305dY)

Ð

LSR

305ME,PY

4

‡

‡

‡

ÿ

ÿ

Ð P > 1,DIM  240 (BCM) Ð

Ð lactation before, and after Ð

LSR UNI

305dY,PY 305dY,BCM

4 2,3,4

1 m

‡ m

‡ ÿ

ÿ ÿ or m

ÿ ÿ

SIR,BW,AC,CI, height LS,SX,SEA*RP CY(m)

UNI

305ME

4

ÿ

‡

ÿ

ÿ

ÿ

Ð

P ˆ 1,DIM > 45

Ð

LSR

X305

4

ÿ

‡

‡

ÿ

‡

(P > 1),P < 6, DIM  105 cows observed 28 days

Ð

CURV

2,4

‡

‡

‡

m

ÿ

Ð

LSR

X305,305dY, PY TDY

CY, AC, herd yield, CI CY

3

‡

‡

ÿ

ÿ

ÿ

CO,LS

P>1 DIM > 105 normal calf presentation Pˆ1

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Gustafsson and Emanuelson, 1996 Gustafsson and Emanuelson, 1996 Kauppinen, 1984 Kay, 1978

Reference records (if other than all non-cases)

Selection of cows or lactations a

Simerl et al., 1992 Tranter and Morris, 1991 Van Werven et al., 1992 a

P ˆ 1, DIM  30,no twins or abortion lame cows Ð

Ð

LSR

LY

1

1

‡

‡

ÿ

‡

BR,SIR,CY,AC

matched Ð

UNI LSR

LY,ndY 100dY

1,3 1

m ‡

m ‡

m ÿ

ÿ ÿ

ÿ ÿ

Ð Ð

P, parity; (P > 1), previous lactation yield needed; DIM, lactations with specified length only; dpp, days postpartum; and RP, retained placenta. UNI, univariable analysis; LSR, multiple least-squares regression; PATH, path analysis; BLUE, best linear unbiased estimation; REPEAT, repeated-measures model; and CURV, modeled lactation curves. c AMY, annual milk yield; BCM, breed-class-average for milk; DBCM, breed-class-average in deviation from herd average; DLY, daily yield across the lactation; LY, entire-lactation milk yield; PY, peak yield; TDY, test-day milk yield; ndY, cumulative milk yield up to n days in milk or in specified interval; X305, standardized extrapolated 305-day milk yield; and 305ME, 305-day mature-equivalent milk. d Type of long-term effect estimate: 1, whole-lactation (whatever length); 2, lactation truncated at a threshold day-in-milk; 3, lactation truncated at end of lactation of diseased cows; and 4, extrapolated yield (see text). e m, matching, ‡, adjustment, ÿ, no control; H, herd; P, parity; age; M, calving season; month; D, other diseases; AC, age at calving; BR, breed; BW, weight; CO, cow; CI, conception interval; CY, calving year; HYS, herd-year-season; LS, lactation stage; LL, lactation length; LD, dry period length; PBCF, previous fat yield; RP, retained placenta; SCC, somatic-cell count; SEA, season of milk sampling; SIR, sire; SX, sex of calf; and YS, year of milk sampling. f PMY, previous milk yield or potential milk; EBV, estimated breeding value; PBCM, previous BCM; PMEY, previous mature-equivalent milk; PDY, previous-lactation daily yield; PLY, previous-lactation yield; PLnY: previous-lactation yield to n days in milk; AR, autoregressive model; ITD, initial test-day yield; and REFY, reference yield (mean yield of DIM 4±6, or weeks 4 and 3 prior to disease occurrence). b

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Table 3 (Continued )

11

12

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Time periods over which the effect on milk yield was assessed were either short-term periods (e.g. yield at test-day of diagnosis, yield in the weeks following diagnosis, cumulative yield in the first part of lactation) or long-term periods (e.g. cumulative yield across 6 months, or whole-lactation yield). Rowlands and Lucey (1986) and BigrasPoulin et al. (1990) considered carry-over effects in the lactation following the lactation of disease occurrence. Dohoo and Martin (1984b) investigated effect on average daily milk yield at the cow-lifespan level (effects resulting from combined effects on yield, reproduction and longevity). Effects of disease on milk yield after the lactation of occurrence are not reported here. Quantification of short-term losses required either records measured daily or weekly, or statistical-model designs accounting for the interval between disease occurrence and test-day, as for example those developed by Detilleux et al. (1994, 1997). The former approach required either specific milk-yield recording for research purpose or automatic yield recording and, therefore, was limited to a few herds, whereas the latter was possible (due to the model specifications) only in very large data sets. Depending on the study design (Table 3), estimates of long-term effect (within a lactation) accounted differently for the fact that diseased cows may have a shorter lactation than non-diseased ones, because they are either dried off earlier or are culled, or die. Four different types of situations were found, which could result in a wide variation in loss estimates, especially for diseases inducing a long-term decrease in yield and an increased culling risk (Fig. 1): 1. The difference in yield between non-diseased and diseased cows was calculated across the whole lactation of the non-diseased cows, including a period after the end of the lactation of the diseased cows. After the end of lactation of the diseased cows, the difference in yield was equal to the yield of reference cows which contributed to the

Fig. 1. Definition of milk loss according to areas between diseased± and reference±lactation curves included in the estimate. Type 1: loss ˆ A ‡ B ‡ C ‡ D; type 2: loss ˆ A ‡ B ‡ C; type 3: loss ˆ A; type 4: loss ˆ A ‡ B.

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

13

loss estimate until the end of their own lactation. This type of estimate (type 1) was calculated when comparing lactation yield or annual yield. 2. The difference in yield of non-diseased and diseased cows was calculated across a lactation duration truncated at a threshold day-in-milk, which could last more than the lactation length of the diseased cows. In the period from the end of the lactation of the diseased cows to the threshold day, the difference in yield was the yield of reference cows, as in type 1. This type of estimate (type 2) was calculated when comparing lactations recorded in 305 days, for instance. The lower the threshold day-in-milk, the smaller was the impact of the decreased days-in-milk of the diseased cows in the estimate. 3. The difference in yield of non-diseased and diseased cows was calculated across a period when both, diseased and reference cows were in milk. This type of estimate (type 3) was calculated when comparing lactation yield of only complete lactations, lactations truncated to the duration of diseased cows lactation, daily yields, or when lactation curves were modeled from observed test-day records. 4. In case of missing values, due to shorter lactation length, milk yield was extrapolated to a standardized duration of lactation. This type of estimate (type 4) included estimates based on comparisons of breed-class-average for milk, mature-equivalent milk, 305-day extrapolated milk, and models of lactation yield adjusted for the lactation length. In estimates of types 1 and 2, the contribution of shortened lactations to the calculated losses was limited when records included in the analysis were selected based on a minimum lactation length. 2.2.3. Control for other effects on milk yield Factors (besides the disease under study) influencing milk yield were sometimes controlled, depending on the study design (Table 3). Matching while selecting the reference records or adjustment in the statistical modeling were used, and some authors expressed yield in breed-class-average units, or in mature-equivalent milk to control for some potential confounders. Effects of parity, calving season and herd were most often controlled (all studies but 1, 11 and 6, respectively). Only 18 analyses considered the cow's previous milk yield or milk-production potential, whereas others did not account for possible higher risk of disease incidence in higher yielding cows. Ten studies considered possible confounding effects of other diseases. Seven studies adjusted for the effect of reproductive status on milk yield. For diseases impairing cow fertility, the positive indirect effect of disease on milk yield due to poorer reproductive performance (higher persistency and longer lactation length) was not accounted for in the estimate. Adjustment for other variables and criteria for selection of records, which can influence loss estimates, are described in Table 3. 2.2.4. Methods for comparison and statistical modeling In six studies, univariable methods were used to assess milk losses. Three of them compared the yield of the same cows at the time of disease occurrence, and before or after (Martin et al., 1978; Cobo-Abreu et al., 1979; King, 1979), whereas in two of them,

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reference cows were matched on case cows according to herd, age and calving date (Kauppinen, 1984; Tranter and Morris, 1991). Multiple-least-squares regression was the method most often used, with various dependent and independent variables for adjustment (Table 3). Three studies relied on path analysis, with multiple-least-squares analysis for milk yield as the dependent variable, and could estimate direct and indirect effects of disease on lactation yield separately (Erb et al., 1981b, 1985; Dohoo and Martin, 1984b). Mangurkar et al. (1984) and Dematawewa and Berger (1997) used mixed models with random effects. In Lean et al. (1994) and Detilleux et al. (1994, 1997), models of test-day yield were elaborated by repeated-measures analysis, and estimates of milk loss were calculated as the difference between modeled lactation curves. Three other papers relied on comparison of lactation curves elaborated in a first step. Lucey et al. (1986) and Rowlands and Lucey (1986) first fitted Wood models based on observed data issued from the same data set. The former then modeled residuals between observed data and predicted yield nine weeks prior to disease through 10 weeks after the occurrence of disease, whereas the latter compared relationships between two consecutive lactations of cows with or without the disease in the second lactation of the pair. Coulon et al. (1996) described average lactation curves in separate groups (defined by parity and calving season) of case cows and reference cows and compared the resulting lactation curves. 2.3. Expression of estimates and additional calculations for this review In the selected papers, loss estimates were expressed in different units (e.g. kg/day, kg/lactation, kg across a stated period), according to the time period of effect under study, and to the unit of interest in the statistical analysis. To facilitate comparisons, all were transformed by us to kg/day across the period of concern. When losses across a lactation were given without the duration of lactation, a standard duration of 305 days was assumed. A quantitative estimate was assessed from the difference between curves measured on figures when results were provided graphically (Lucey et al., 1986; Lean et al., 1994). Available information about average milk yield was heterogeneous (Table 1). In some papers, average yield was provided for reference cows, whereas, in others, it was given for all cows, including a proportion of diseased cows which varied as shown by incidence rates. Therefore, we could not express losses as a proportion of yield in a standardized way. 3. Results Effects on yield reported in Tables 4±14 were significant at p  0.05, except when otherwise stated. When available, indirect effects on milk yield and effects on the lactation-curve shape (peak, persistency) are reported in the text. Seven data sets with very large sample size (several thousand lactations) had high case numbers (>400, for most diseases), 14 had between 100 and 400 cases and 10 <100 cases. With a power of 80% and assuming a 1000 kg residual SD (after adjustments) of lactation yield, losses could be demonstrated if they reached 110±160, 160±220, 220±310, and 440±630 kg with

Table 4 Effect of dystocia on milk yield of dairy cows Reference

Case definition

LIR% a

caesarean section difficult calving

1.3 na

Deluyker et al., 1991

assistance needed

6.9

Dematawewa and Berger, 1997

dystocia score -assistance needed -considerable force needed -extreme difficulty veterinary assistance needed dystocia or assisted delivery farmer-or vet-assisted dystocia veterinary assistance needed calving ease and calf survival -hard pull and calf alive -hard pull and calf dead -surgical and calf alive -surgical and calf dead difficult calving veterinary assistance needed assistance needed

Dohoo and Martin, 1984b Erb et al., 1981a Erb et al., 1985 Lucey et al., 1986 Mangurkar et al., 1984

Philipsson, 1976 Rowlands and Lucey, 1986 Simerl et al., 1992

198 na 28 b

8.7 3.6 1.7 4.2 4.1 14.0d 4.0

10 615 b 4430 b 2037 b 55 c 33 b 110 b 64 b

4.8 1.8 0.4 0.2 15.9 d 4.0 3.9

1157 423 87 51 162 23 45 b

Short-term effect

Long-term effect

time period

kg/day

time period

kg/day

100 days Ð

ÿ0.80 Ð

119 days short-term

NS NS

270 days2 lactation4 305 days4 Ð Ð

NS NS NS Ð Ð

Ð Ð Ð Ð Ð Ð 70 days

Ð Ð Ð Ð Ð Ð NS

305 305 305 305 305 305 Ð

90 90 90 90 Ð Ð Ð

ÿ0.50 ÿ1.02 NS ÿ1.89 Ð Ð Ð

305 days4 305 days4 305 days4 305 days4 305 days4 305 days2,4 lactation1 (262 days)

days days days days

days4 days4 days4 days4 days4 days4

ÿ0.54 ÿ0.62 ÿ2.31 NS NS NS Ð ÿ0.30 ÿ0.66 ‡0.33 ÿ1.32 NS NS ÿ0.66

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Barkema et al., 1992 Bigras-Poulin et al., 1990

Cases

a

LIR, lactational incidence risk; days, days in milk or specified interval; and na, not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. Number of cases estimated from incidence risk in total sample and study sample size. d Primiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b c

15

16

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Table 5 Effect of dystocia on 305-day milk yield of dairy cows in different parities Reference

Dystocia score

Parity 1

Parity 2

a

a

LIR%

kg/day

LIR%

Parity  3 kg/day

LIR% a

kg/day

Dematawewa and Berger, 1997

assistance needed considerable force needed extreme difficulty

11.6 5.1 2.3

ÿ0.46 ÿ0.53 ÿ2.24

4.7 1.6 0.8

NS ÿ0.72 ÿ1.47

4.5 1.4 0.7

NS NS ÿ1.07

Djemali et al., 1987

assistance needed considerable force needed extreme difficulty

11 5 3

‡0.30 ÿ0.37 ÿ1.52

4 1 1

ÿ0.46 ÿ0.31 ÿ1.89

4 1 1

ÿ0.57 ÿ1.38 ÿ2.38

a

Lactational incidence risk.

case numbers of 400, 200, 100 and 25, respectively (range of effect for cases representing 1±50% of the sample). 3.1. Dystocia and stillbirth Eight studies out of 13 reported no effect of dystocia on milk yield whereas five found losses (Tables 4 and 5). A small reduction in milk yield after assisted calving with slight Table 6 Effect of stillbirth on milk yield of dairy cows Reference

Case definition

LIR% a Cases

Bigras-Poulin et al., 1990

na

Deluyker et al., 1991

na

Mangurkar et al., 1984

calving ease x calf survival -unassisted and calf dead 2.3 -easy pull and calf dead 0.9 -hard pull and calf dead 1.8 -surgical and calf dead 0.2 na 6.7 calf not alive 24 h 11.5 c postpartum

Philipsson, 1976 Simerl et al., 1992 a

na 6.3

Short-term effect Long-term effect time period (days)

kg/day

time period (days)

na

Ð

Ð

26 b

1±5 1±21 22±49 50±119 119

ÿ2.4 ÿ1.80 NS NS NS

lactation1 NS 3054 NS Ð Ð

90 90 90 90 Ð Ð

ÿ1.80 ÿ0.53 ÿ1.02 ÿ1.89 Ð Ð

556 222 423 51 73 132 b

kg/day

3054 ÿ1.35 3054 ÿ0.56 3054 ÿ0.66 ÿ1.32 3054 3054 NS lactation1 ÿ0.69 (262 days)

LIR, lactational incidence risk; days, days in milk or specified interval; na, not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. c Primiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

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17

Table 7 Effect of milk fever on milk yield of dairy cows Reference

Case definition

LIR% a

Bigras-Poulin et al., 1990

na

5.6

Cobo-Abreu et al., 1979 Deluyker et al., 1991

na inability to rise with response to intravenous calcium treatment, five days prior to two days after calving

4.9 6.7

89 c 69 c 29 27 b

Dohoo and Martin, 1984b Lucey et al., 1986

milk fever with cow down clinical signs confirmed by blood analysis clinical signs confirmed by blood analysis

2.9 7.6 7.6

Rowlands and Lucey, 1986

Cases

Time period (days)

Effect kg/day

lactation4 3054 3054 119 short-term

‡0.93 NS NS NS NS

38 c 121 b

3054 70

NS NS

48

3052,4

NS

a

LIR, lactational incidence risk; na, not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. c Number of cases estimated from incidence risk in total sample and study sample size. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

assistance was reported by Djemali et al. (1987) and Dematawewa and Berger (1997) but not by Mangurkar et al. (1984) (not shown). Most of the estimates of losses across the lactation were in a range from 100±200 kg for needed assistance with hard pull, and up to 500±700 kg for calvings with extreme difficulty. Losses were higher when both dystocia and stillbirth occurred (see below). Absence of significant losses was found in studies relying on only 20±160 cases. Two studies with small samples, but where disorders of concern were more severe, identified significant losses: Barkema et al. (1992) considered only caesarean section and found a mid-term negative effect, but no long-term loss. In Simerl et al. (1992), the low frequency of dystocia in primiparous cows (3.9%) suggested that only very difficult calvings were recorded. Except for Simerl et al. (1992), who adjusted for possible effects of retained placenta and metritis, losses were identified in studies where the effect of dystocia was investigated without adjusting for effects of other diseasesÐwhereas studies with such an adjustment were unable to identify loss. Therefore, the observed effect could be indirect and might result from an increased risk of postpartum diseases after dystocia. Impaired reproduction following dystocia resulted in higher milk yield as shown by the path analysis by Erb et al. (1985), and by adjustment for days open by Mangurkar et al. (1984). Djemali et al. (1987) associated increasing losses with increasing parity, whereas Dematawewa and Berger (1997) showed an opposite trend even though part of the data was common in the two analyses (Table 5). Two papers out of five reported no effect of stillbirth on milk yield. In Mangurkar et al. (1984), losses after stillbirth depended on calving ease: losses were reduced by half after a normal or surgical calving, compared to non-surgically assisted calving. Given intervals between milk tests, cows with very severe reduction in yield after a calving disorder and which, therefore, were culled in early lactation before any milk

18

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Table 8 Effect of retained placenta on milk yield of dairy cows Reference

Bigras-Poulin et al., 1990

Case definition: retention after calving >48 h

LIR% a

7.7

Cases

122 c c

Cobo-Abreu et al., 1979 Deluyker et al., 1991

na >24 h

Dohoo and Martin, 1984b Erb et al., 1981a Erb et al., 1985 Kay, 1978 Lucey et al., 1986

>48 h na >24 h na >24 h

Van Werven et al., 1992

a

8.6 7.7 3.6 d 3.7 3.1

95 40 66 b

113 c 62 b 110 b 34 49 b

Long-term effect

time period (days)

kg/day

time period (days)

kg/day

Ð

Ð

lactation4

NS

Ð Ð 1±5 1±21 22±49 50±119 119 Ð Ð Ð Ð 1±28 29±35 36±70 Ð Ð Ð

Ð Ð ÿ2.4 NS NS NS NS Ð Ð Ð Ð ÿ0.54 NS ‡0.74 Ð Ð Ð Ð

na 9.1 3.1

173 c 25 25

>24 h

3.6

41 b

Ð

>6 h >8 h >12 h >23 h

27.1 16.1 10.1 7.6

75 45 28 21

100 100 100 100

>6 h >8 h >12 h >23 h

32.9 25.6 19.5 17.0

130 101 77 67

100 100 100 100

>6 h >8 h >12 h >23 h

41.3 30.1 28.1 18.3

140 102 95 62

100 100 100 100

Martin et al., 1986 >12 h Muller and Owens, 1974 >24 h Rowlands and Lucey, 1986 >24 h Simerl et al., 1992

5.9 16.2

Short-term effect

parity 1 (ÿ0.91) NS ÿ1.67 ÿ2.37 ÿ1.98 parity 2±3 ÿ1.44 ÿ2 ÿ1.88 ÿ1.70 parity > 3 ÿ1.31 ÿ2.21 ÿ2.5 (ÿ1.26)NS

4

305 3054 Ð

NS NS Ð

3054 3054 3054 lactation1,3 Ð

NS NS NS NS Ð

3054 3054 3052 3054 lactation1 (262 days)

‡ ‡1.23 ÿ1.18 ÿ0.85 ÿ0.91

Ð Ð Ð Ð

Ð Ð Ð Ð

Ð Ð Ð Ð

Ð Ð Ð Ð

Ð Ð Ð Ð

Ð Ð Ð Ð

LIR, lactational incidence risk; na, not available in source paper; ‡, higher yield in diseased cows. Number of cases calculated from incidence risk in study sample and sample size. c Number of cases estimated from incidence risk in total sample and study sample size. d Primiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

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19

Table 9 Effect of metritis on milk yield of dairy cows Reference

Case definition

LIR% a Cases

Bigras-Poulin et al., 1990

metritis at any dpp

10.7

Cobo-Abreu et al., 1979 Deluyker et al., 1991

metritis, endometritis or pyometritis early metritis: clinical signs or detection at routine veterinary examination within 21 dpp

Dohoo and Martin, 1984b Erb et al., 1981a Erb et al., 1985 Lucey et al., 1986

7.9 5.6

late metritis: clinical signs 9.7 or detection at routine veterinary examination within 22 to 119 dpp first diagnosis in 1 to 21 dpp 9.0 first diagnosis in 22 to 60 dpp 4.6 first diagnosis after 60 dpp 4.6 na 14.2 metritis, endometritis or pyometra 10.2 d secretions or discharges at the vulva 4.7

Markusfeld and Ezra, 1993 foul smelling colored discharge 48.6 removed from cervix during routine postparturient examination, without previous retained placenta Rowlands and Lucey, 1986 secretions or discharges at the vulva 4.7 Simerl et al., 1992 treatment of infection of reproductive 10.5 tract or abnormal vaginal discharge within 60 dpp

Time period (days)

Effect (kg/day)

170 c 132 c 52 23 b

lactation4 3054 3054 1±5 1±21 22±49 50±119 119

NS NS NS ÿ2.6 ÿ2.39 ÿ2.21 NS ÿ2.26

40 b

short-term 119

NS NS

3054 3054 3054 3054 3054 70 days after diagnosis 3054

NS NS NS NS NS NS

3052,4 lactation1 (262 days)

NS ÿ0.37

118 c 60 c 60 c 115 b 80 b 75 b 315 c

26 120

NS

a

LIR, lactational incidence risk; dpp, days postpartum; na, not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. Number of cases estimated from incidence risk in total sample and study sample size. d Primiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b c

record, were excluded from the analysis. Moreover, records selected for analysis were often from lactations with a minimum lactation length (Table 3). Philipsson (1976) excluded all lactations shorter than 46 days in milk and reported a higher proportion of such short lactations in cows with dystocia or stillbirth. 3.2. Milk fever No author identified any loss in milk yield after milk fever, and one found a higher lactation yield (Table 7). Samples included only 20±120 cases (resulting in low power to detect small reductions). Only cows with successful treatment are kept in the herd;

20

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Table 10 Effect of cystic ovaries and luteal cysts on milk yield of dairy cows Reference

Case definition

Bigras-Poulin et al., 1990

ovarian cyst

Cobo-Abreu et al., 1979

cystic Graafian follicles ovarian hypofunction cystic ovary cystic follicle luteal cyst cystic follicle ovarian structure at any single veterinary rectal palpation excluding cystic corpora lutea and luteal cyst

Dohoo and Martin, 1984b Erb et al., 1981a Erb et al., 1981b Erb et al., 1985

LIR% a

5.0 8.1 5.1 10.4 16.0 3.7 16.0 5.1 d 9.2 e

Cases

Time period (days)

Effect (kg/day)

79 c 62 c 46 26 137 c 130 b 30 b 130 b 40 b 190 b

3051 3054 3054 3054 3054 3054 3054 3054 3054 3054

NS ‡1.08 NS NS NS ‡0.96 NS ‡0.97 ‡1.04 d ‡0.46 e (p ˆ 0.12)

a

LIR, lactational incidence risk; dpp, days postpartum. Number of cases calculated from incidence risk in study sample and sample size. c Number of cases estimated from incidence risk in total sample and study sample size. d Primiparous cows. e Multiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

therefore, cows with a severe drop in milk yield and no recovery after treatment are culled before recording of milk yield. In cows which recover, milk yield quickly returns to normal, or losses (if any) are limited. Dohoo and Martin (1984b), Erb et al. (1985), and Bigras-Poulin et al. (1990) reported poorer reproductive performance after milk fever, and, consequently, a significant positive indirect effect on the lactation yield. Only the latter had adjusted for previous milk yield which can be a confounder because high-yielding cows are at higher risk for milk fever (Dohoo and Martin, 1984a). 3.3. Retained placenta In eight studies out of 13, no milk loss was identified after retained placenta (Table 8). Two studies identified a small negative short-term effect (12±15 kg), but no mid-term effect. In three studies, mid- or long-term losses averaged 200±250 kg. Studies identifying no loss were based on only 25±170 disease cases. Two of the three studies with disease effects across the lactation did not adjust for other diseases. Rowlands and Lucey (1986) suspected an odd farm-specific disease effect in the four herds they studied, because duration of retention cases averaged four days. Simerl et al. (1992) included only cases in heifers and excluded twin birth and short gestationlengthÐprobably selecting cases with an infectious etiology. Two analyses based on the same initial data set resulted in inconsistent conclusions for short-term and long-term effects (Lucey et al., 1986; Rowlands and Lucey, 1986). In the former, absence of adjustment on previous or potential milk yield may have resulted in

Table 11 Effect of clinical ketosis on milk yield of dairy cows Case definition

Bigras-Poulin et al., 1990

na

Cobo-Abreu et al., 1979 Deluyker et al., 1991

na depressed feed intake, drop in milk yield, and response to ketosis treatment, with no concurrent disease

Detilleux et al., 1994 Dohoo and Martin, 1984b Kauppinen, 1984 King, 1979 Lean et al., 1994 Lucey et al., 1986

LIR% a 3.3

Cases

4.5 18.3

52 41 28 75 b

veterinary treatment for ketosis

6.0

4571 b

ketosis with no concurrent disease the same day clinical signs loss of appetite and positive test on milk clinical signs clinical signs and positive test on milk or urine

7.4

97 c

Time period (days)

Effect (kg/day)

lactation4 3054 3054 1±21 22±49 50±119 119 1±21 22±49 50±119 119 1±21 22±49 50±110 119 17 days after diagnosis 3053 3054

NS NS ÿ1.20 ÿ3.1 ÿ3.3 NS ÿ2.1 ÿ2.6 ÿ5.6 NS ÿ2.2 NS NS ÿ4.1 ÿ2.8 ÿ2.6 ‡0.5 NS

31.8 na

181 53

lactation1 at diagnosis/after recovery

NS ÿ2.74

37.5 3.6

9 91

69 7 days before/7 days after 28 days before diagnosis 28 days after diagnosis

ÿ5.7 ÿ5.1 ÿ2.8 ‡2.0

Comment

diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed diagnosed

on on on on on on on on on on on on

day day day day day day day day day day day day

1±21 1±21 1±21 1±21 22±49 22±49 22±49 22±49 50±119 50±119 50±119 50±119

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Reference

21

22

Reference

Case definition

Rowlands and Lucey, 1986

clinical signs and positive test on milk or urine treatment for ketosis

Simensen et al., 1990 a

LIR% a

Cases

Time period (days)

Effect (kg/day)

3.6

27

41.9

21

3052 3054 week with max. acetoacetate/week before

‡0.7 ‡0.6 ÿ3.6

LIR, lactational incidence risk; dpp, days postpartum; na, not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. c Number of cases estimated from incidence risk in total sample and study sample size. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

Comment

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Table 11 (Continued )

Table 12 Effect of ketosis diagnosed by milk or blood analysis on milk yield of dairy cows Reference

Classification of test results

Dohoo and Martin, 1984b

milk ketone bodies

qualitative test

Dohoo and Martin, 1984c

milk ketone bodies

Gustafsson et al., 1993

milk acetone

Gustafsson and Emanuelson, 1996 Kauppinen, 1984 Lean et al., 1994

milk acetone

Simensen et al., 1990

a

blood acetoacetate blood parameters (several) milk acetoacetate

Value or threshold (mM)

score 1 score 2 qualitative test score 1 score 2 maximum cow value 1.01±2.00 >2.00 maximum cow value >1.4

LIR% a

5.7 3.9 7.0t65 5.1t65 na 1 c, 3 d

maximum cow value 0.36±1.05 cluster analysis ketonaemic

17.9 20.8

test-day value

15.9t42 5.7t42 46.1

0.1±0.3 >0.3 maximum cow value >0.1

Cases

Clinically Short-term effect ketotic time period kg/day cows (days) included

Long-term effect

yes

test-day

3054

yes

test-day

yes

100

yes

102 5 53 19 12

75e 51e 176 131 na na na

time period (days)

100

ÿ0.99 ÿ1.98 ÿ1.03 ÿ1.4 ÿ0.64 ÿ2.33 ÿ1.92

2002

no no

Ð 70

± NS

lactation1 ‡ Ð Ð

yes yes no

test-day ÿ1.8 test-day ÿ7 week of ÿ2.8 detection/ previous week

Ð 2002

Ð Ð Ð

LIR, lactational incidence risk; ‡, higher yield in diseased cows; tn, proportion of test days within n days postpartum; na, not available in source paper. Number of cases estimated from incidence risk in total sample and study sample size. c Primiparous cows. d Multiparous cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

kg/day

NS Ð ÿ0.04 ÿ1.14 ÿ0.95

Ð Ð Ð

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Diagnostic test

23

24

Reference

Case definition

LIR% a

Cases

Cobo-Abreu et al., 1979 Deluyker et al., 1991

na veterinary diagnosis

4.4 2.0

27 8b

Detilleux et al., 1997

veterinary examination and surgery

5.5

691 c

Dohoo and Martin, 1984b Martin et al., 1978

na surgically corrected cases

1.2 na

16 c 61 41 41

a

LIR, lactational incidence risk; na: not available in source paper. Number of cases calculated from incidence risk in study sample and sample size. c Number of cases estimated from incidence risk in total sample and study sample size. d Lower yielding cows. e Higher yielding cows. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

Time period (days) 4

305 1±5 1±21 22±49 50±119 119 80.6 (calving to 60 days after diagnosis) 3054 3052 3054 3053

Effect (kg/days) ÿ1.55 NS ÿ9.62 ÿ7.14 NS ÿ3.18 ÿ6.91 ÿ4.50 ÿ5.24 d to ÿ9.65 e ÿ3.49 d to ÿ10.87 e ÿ1.85 ÿ2.49 ÿ1.40 ÿ0.78 to 1.82

Comment

(p ˆ 0.18) all parity 1 parity 2 parity 3

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Table 13 Effect of displaced abomasum on milk yield of dairy cows

Table 14 Effect of locomotor disorders on milk yield of dairy cows Reference

Case definition

LIR% a

Cases

Time period (days)

Effect (kg/day)

Comment

ArgaÁez-Rodriguez et al., 1997 Barkema et al., 1994

papillomatous digital dermatitis farmer or veterinarian diagnosis -sole ulcer -digital dermatitis -interdigital phlegmon -arthritis, periarthritis -interdigital dermatitis -laminitis -other lameness or no diagnosis musculo-skeletal problem related to the limb

34.0 26.0 9.8 b 6.4 b 3.9 b 1.7 b 1.5 b 0.5 b 7.3 b 3.6

190

lactation4 (274 days)

NS

ÿ0.45 kg/day, p ˆ 0.35

foot problem: any abnormality distal to the carpal or tarsal joint clinical cases detected through cow behavior and foot examination limping due to signs of inflammation within the foot

5.6

201 d 131 d 79 d 35 d 31 d 10 d 149 d 57 d 44 d 29

100,2702 100,2702 100,2702 100,2702 100,2702 100,2702 100,2702 lactation4 3054 3054

‡ NS NS NS NS NS NS NS NS NS

lactation3*

15.2

121 307 62 c

5.0 21.2 NS

66 d 958 d 372 d

ÿ0.41 ÿ0.27 ‡ ‡ -1.68e ‡ NS NS NS NS ÿ3.3

first diagnosed 35 dpp first diagnosed >35 dpp diagnosed on day 1±49 diagnosed on day 1±49 diagnosed on day 1±49 diagnosed on day 1±49 diagnosed on day 50±119 diagnosed on day 50±119 cows not culled (72%) cows culled (28%)

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11.6

241

ÿ1.1

sole and white line lesions: -0.25 kg/day during 56 days before diagnosis and ‡0.4 kg/day during 28 days after, other: NS in the period

25

Bigras-Poulin et al., 1990 Cobo-Abreu et al., 1979 Coulon et al., 1996 Deluyker et al., 1991

Dohoo and Martin, 1984b Enting et al., 1997 Lucey et al., 1986

clinical digital diseases predominant lesions: -interdigital lesions

33.3 b

1±5 1±21 22±49 50±119 short-term 119 3054 lactation3 7 days before/7 days after diagnosis

26

Reference

Rowlands and Lucey, 1986

Tranter and Morris, 1991 a

Case definition

LIR% a

-sole and white line lesions -wall and coronary band lesions -heel lesions Predominant lesions: -interdigital cleft lesions -sole and white line lesions -wall and coronary band lesions -heel lesions lameness

10.2 2.1 3.2

224 44 72

11.6 10.2 2.1 3.2 14.3

95 82 18 32 120

Cases

Time period (days)

Comment

ÿ1.1 ÿ1.1 NS 3052,4 3052,4 3052,4 3052 lactation1 (251 days) lactation3 (237 days)

LIR, lactational incidence risk; dpp, days postpartum; na: not available in source paper; ‡, higher yield in diseased cows. Cumulative incidence risk. c Number of cases calculated from incidence risk in study sample and sample size. d Number of cases estimated from incidence risk in total sample and study sample size. e Estimate extrapolated from the positive difference with control cows before and after the period. * Assumed standard duration of 305 days. 1, 2, 3, 4 Type of long-term effect estimate (for definition see text). b

Effect (kg/day)

‡ NS NS ÿ1.15 ÿ1.23 ÿ0.97

NS on 305 days4 (p < 0.1)

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Table 14 (Continued )

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27

underestimation of the short-term effect. On the contrary, in the latter, where lactation yield was adjusted for previous-lactation yield, a significant effect was found across the lactation. Decreased yield across the lactation was interpreted as a consequence of lower peak yield (ÿ2 kg/day), with no change in persistency. In four studies, cows with retained placenta produced more than controls across the lactation. In Martin et al. (1986) and Muller and Owens (1974), the disease effect was assessed without adjusting for milk production potential, hence the identified relationship could be related to higher risk in higher producing cows. In Erb et al. (1981a, 1985), the positive relationship was indirect and attributable to impaired reproduction in diseased cows (not shown). 3.4. Metritis Eight studies out of 10 reported no effect of metritis on milk yield whereas two found milk losses (Table 9) of 100 kg, for any case, to 270 kg for early metritis. Absence of loss was found even in the study with the largest number of cases (315). In studies without adjustment for previous or potential milk yield, confounding could mask an existing negative relationship because metritis is more frequent in high-yielding cows. Nevertheless, five studies showing no effect had controlled for that possible confusion. No effects were shown on peak yield and persistency (Rowlands and Lucey, 1986; Deluyker et al., 1991; Markusfeld and Ezra, 1993). A higher yield in lactations with metritis was reported by Dohoo and Martin (1984b) and Erb et al. (1981b, 1985), due to the indirect positive effect on yield of impaired reproduction in cows with metritis. Markusfeld and Ezra (1993) identified this trend only in tall and heavy cows. Typically, no milk loss was associated with metritis. Further assessment is needed with better distinction between acute and chronic metritis. 3.5. Cystic ovaries In the six studies investigating possible effect of cystic ovaries on milk yield, no loss was found. On the contrary, a positive effect was shown in four of them (Table 10). The effect was either direct, or indirect through impaired reproduction of cows diagnosed with cystic ovaries. Possible confounding by previous or potential milk yield was controlled for except in one analysis (Dohoo and Martin, 1984b). 3.6. Ketosis Seven studies found short- or long-term reduction in milk yield associated with clinical ketosis, whereas four reported no loss (Table 11). Five studies found losses associated with ketotic status according to a diagnostic test, whereas two reported no loss (Table 12). Reduction in yield on the day of diagnosis reached 4±10 kg/day for clinical ketosis, 1±7 kg/day for ketotic status (including some clinically ketotic cows), and 3 kg/day for subclinical ketosis. Over short-term periods, losses following clinical cases averaged

28

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3±6 kg/day. Detilleux et al. (1994) found higher short-term losses in multiparous cows than in primiparous cows. Duration of losses was short (17±28 days) in Detilleux et al. (1994) and Lucey et al. (1986), but lasted more than 50 days in Deluyker et al. (1991) and Lean et al. (1994). Peak yield was 2±2.7 kg lower in clinically ketotic cows as was the rate of decline after the peakÐresulting in a flattened lactation curve (Rowlands and Lucey, 1986; Deluyker et al., 1991). Gustafsson et al. (1993) and Gustafsson and Emanuelson (1996) found a flattened lactation curve in cows reaching a maximum milk-acetone value between 0.4 and 1.0 mmol/l, and yield reduction above 0.7 mmol/l in postpartum 2±10 weeks or more. At the lactation level, no long-term losses were evidenced for clinical ketosis and subclinical ketosis but a yield reduction of 200±230 kg was associated with ketotic status (including clinical cases). Studies finding no loss included the study with the most cases (180). Only eight studies controlled for higher risk of ketosis in high-producing cows. 3.7. Displaced abomasum The five studies investigating effect of displaced abomasum found milk losses (Table 13). Average losses varied from 400 to 800 kg overall. Losses were higher in multiparous cows than in heifers and (within parity) more than proportionally higher in high-producing cows than in low-producing cows (Detilleux et al., 1997). In Detilleux et al. (1997), 30% of the losses occurred before diagnosis, and milk yield returned to normal between 20 and 45 days after diagnosis. In Deluyker et al. (1991), all the losses resulted from drop in milk yield within 50 day postpartum. In Detilleux et al. (1997), 5% of the cows with displaced abomasum were culled before being milk tested and, therefore, were not included in the analysis. This was probably similar in all studies although not reported by other authors. Selection of lactations with a minimum length of 119±150 days also resulted in an underestimation of milk losses (Dohoo and Martin, 1984b; Deluyker et al., 1991). Martin et al. (1978) reported that 80% of the cows with displaced abomasum had a complete lactation and experienced milk losses between 239 and 555 kg, whereas losses on observed 305-day yield reached 760 kg when incomplete lactations in the analysis were included. 3.8. Locomotor disorders Six of 11 studies found losses due to lameness (Table 14). Across the lactation, loss estimates averaged 80±350 kg. Studies finding no effect on milk yield included 30±190 cases. In Deluyker et al. (1991), cows lame in early lactation had a drop in yield in the fourweek period around diagnosis, whereas no effect was found in cows lame after 50 days postpartum. In Lucey et al. (1986), short-term milk losses occurred before diagnosis but in the weeks following diagnosis (and treatment), yield was higher than expected (partly compensating for earlier losses). Coulon et al. (1996) identified three patterns of milk losses following lameness: 45±55% of the cows had no decrease in yield, 19±30% had a

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decreased yield returning to normal within five weeks after diagnosis, and 25±26% experienced losses during more than five weeks; moreover, a few cows were dried off early. Enting et al. (1997) separately quantified losses in lactations ending or not by a cull. No milk loss was found in cows not culled, whereas culled cows produced on average 3.3 kg/day milk less than non-lame cows before being culled. In Tranter and Morris (1991), lactations with lameness were on average 12 days shorter than reference lactations. Yield across the lactating period was decreased by 229 kg, and, considering the whole lactation of reference cows, a further 79-kg loss was associated with shortened lactations in diseased cows. In Rowlands and Lucey (1986), cows with heel lesions produced 350 kg less milk in a 305-day lactation, and losses resulted from shortened lactations, not from lower yields. Almost all authors accounted for the higher risk of lameness in higher-yielding cows and adjusted for previous lactation or milk-production potential while estimating disease effects (Table 3). An existing negative effect could be masked by the absence of this adjustment in Dohoo and Martin (1984b), or underestimated in Lucey et al. (1986) and Tranter and Morris (1991). 4. Discussion 4.1. Main sources of estimate bias Among the potential biases in study designs, some would systematically result either in underestimating or in overestimating milk loss due to disease. Risk of underestimation of milk loss could result from: ± incomplete detection of case cows (resulting in a reduced yield in the cows misclassified as reference cows); ± not accounting for possible yield reduction before detection of disease (as evidenced by Detilleux et al. (1997) for displaced abomasum, and by Lucey et al. (1986) for several diseases); ± absence of control of factors potentially increasing milk yield in case cows, including milk-production potential and impaired reproduction; and ± for periparturient diseases, exclusion of cows with a dramatic drop in milk yield in early lactation, resulting in very early culls. Cows that happened to be culled very early in lactation could have been excluded from the analysis either because of a recordselection criterion based on minimum days in milk, or because the cow was culled prior to any test-day, as found by Beaudeau et al. (1994) for dystocia, milk fever and ketosis, Philipsson (1976) for dystocia and stillbirth, and Detilleux et al. (1997) for displaced abomasum. Available estimates quantified losses only for the cows kept in the herd. Also (depending on the expected use of milk-loss estimates), calculation of losses across a period truncated at the end of diseased-cow lactation (type 3) or extrapolation of yield of diseased cows with a short lactation (type 4) could be considered as an underestimation of milk loss.

30

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Risk of overestimation of milk loss could result from: ± selection of severe cases, particularly if the case definition was imprecise or when the farmer called the veterinarian to examine suspect cows only (e.g. for displaced abomasum or ketosis) although some undetected cases would then be considered as reference (resulting in a reduction of the reference-population yield); ± lack of effective treatments implemented at disease occurrence (assuming that the objective is to assess milk losses with correct treatment); and ± poor control of confounding (e.g. for diseases biologically linked to the disease under study). Also (depending on the expected use of milk-loss estimates), inclusion in losses of the yield reduction resulting from a shorter lactation in diseased cows (types 1 and 2) could be considered as an overestimation of losses. 4.2. Disease definition Disease definition varied widely and could result in variations in loss estimates (especially for metritis, ketosis, and locomotor disorders). Two authors separately considered early (within 21 days postpartum) and late metritis (Dohoo and Martin, 1984b; Deluyker et al., 1991) whereas others considered all cases together. Erb et al. (1985), Lucey et al. (1986) and Rowlands and Lucey (1986) reported that most of the cases they considered occurred early (76% within 28 days postpartum and 88% within 25 days postpartum, respectively). No distinction was made between acute metritis with systemic signs and chronic metritis. As the latter usually occur later in lactation, it may be assumed that a higher proportion of cases defined as early (within three weeks postpartum) were acute metritis. A drop in milk yield is often considered a sign of clinical ketosis, and would result `by definition' in significant short-term milk loss. Authors considered either clinical signs and response to treatment, or diagnostic tests (Tables 11 and 12). Diagnostic tests were used either on cows with clinical signs in order to confirm the diagnosis (King, 1979; Lucey et al., 1986; Rowlands and Lucey, 1986), or in cows systematically sampled, with various sampling designs: two or three times in a lactation in Dohoo and Martin (1984b), at each milk record within 60 days postpartum in Gustafsson et al. (1993) and Gustafsson and Emanuelson (1996) two or three times within a month before 72 days postpartum in Kauppinen (1984), weekly during the first six weeks of lactation in Simensen et al. (1990), and 19 times within 70 days postpartum in Lean et al. (1994). Testing on blood, milk or urine was based on various methods, and controversy exists in the literature on thresholds to determine that a cow is ketotic or not. Simensen et al. (1990); Gustafsson et al. (1993), and Gustafsson and Emanuelson (1996) suggested defining threshold values to diagnose subclinical ketosis according to the effect on milk yield. Ketosis cases detected by a diagnostic test generally included clinically ketotic cows. Dohoo and Martin (1984b) and Deluyker et al. (1991) excluded ketosis with a concurrent disease on the same day.

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Diagnosis of locomotor disorders either considered all cases of lameness due to foot lesions or investigated separately effects of different lesions. The most frequent lesions varied between studies. 4.3. Control for confounding factors Possible confounding due to higher risk of disease in high-yielding cows was controlled for in most studies assessing effect of cystic ovaries, displaced abomasum and locomotor disorders but only in half of the studies dealing with effects of milk fever, metritis and ketosis, and in almost none of the studies on dystocia, stillbirth and retained placenta. Because milk fever, metritis and ketosis are more frequent in high-yielding cows, losses may be underestimated. However, GroÈhn et al. (1995) found no significant association between previous milk yield and risk of retained placenta, metritis, cystic ovaries, milk fever and ketosis, after adjusting for parity, season and herd. An indirect positive effect on milk yield associated with poor reproductive performance may be observed while assessing the long-term effect of disease, as a consequence of higher persistency in non-pregnant cows. Impaired reproduction associated with occurrence of disease was reported for dystocia (Philipsson, 1976; Mangurkar et al., 1984; Djemali et al., 1987; Barkema et al., 1992; Simerl et al., 1992; Dematawewa and Berger, 1997), stillbirth (Philipsson, 1976), retained placenta (Philipsson, 1976; Martin et al., 1986; Simerl et al., 1992; Van Werven et al., 1992), metritis (Erb et al., 1981a, b, 1985; Dohoo and Martin, 1984b; Simerl et al., 1992), cystic ovaries (Erb et al., 1981a, b, 1985; Dohoo and Martin, 1984b), ketosis (Gustafsson and Emanuelson, 1996), and locomotor disorders (Tranter and Morris, 1991; Enting et al., 1997)Ðbut not for displaced abomasum. Yet, most often, this effect was not controlled for (except in studies addressing cystic ovaries, and in half of the long-term effect studies addressing dystocia, stillbirth, and metritis). For the other diseases impairing reproduction, this may have resulted in underestimating milk loss. The yield reduction due to pregnancy ranged from 90 kg in primiparous cows (81 days open) to 200 kg in high producing multiparous cows (88 days open), compared to non-pregnant cows, and was significant after 20 weeks of pregnancy in Coulon et al. (1995). In Oltenacu et al. (1980), cows open 120 and 180 days produced, respectively, 240 and 400 kg more in a 300-day lactation than cows open 80 days. Thus, the range of effect of the reproductive status is comparable to, or higher than, the range of milk losses evidenced for most of the diseases. Possible confounding effects of other diseases were controlled for in all but one study for stillbirth and cystic ovaries, in about half of the studies for dystocia, milk fever, retained placenta, metritis, and displaced abomasum, and in less than half of the studies for ketosis and locomotor disorders. Absence of control may have resulted in overestimating milk loss particularly for periparturient diseases which occur as part of a complex, as reported by Curtis et al. (1985) and Correa et al. (1993). For example, the effect of retained placenta depends probably on both, the etiology of the disease and the occurrence of other peripartum diseases. Cases following a difficult calving, twins or a short gestation, and not followed by another disease, seem to have no effect on milk yield.

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4.4. Type of effect In most studies, yield after the end of incomplete lactations was extrapolated, therefore, quantification of milk loss took no account for reduction in lactation length. The example of lameness illustrates the impact of reducing lactation length on the milk-loss estimate. In Tranter and Morris (1991), when comparing records of whole lactations, 26% of the loss was associated with lactation shortening in diseased cows. In Rowlands and Lucey (1986), loss associated with heel lesions only resulted from shortened lactation, and not from a lower yield when in milkÐas evidenced by the absence of difference in lactations extrapolated from existing records, to 305 days. To allow comparison between estimates, it would be preferable to consider effects on lactation length (due to culling or early drying off) and on yield when in milk separately. 4.5. Effect modifiers In most studies, milk losses were assumed not to vary in relation with cow characteristics. The influence of parity on the effect on milk yield was inconsistent for dystocia, according to Djemali et al. (1987) and Dematawewa and Berger (1997), but no explanation could be found. The effect of retained placenta was investigated separately in different parities by Van Werven et al. (1992), with no systematic trend being observed. A higher increase of yield was associated with cystic ovaries in primiparous vs. multiparous cows in Erb et al. (1985). Higher losses associated with displaced abomasum were found in parity 2 or 3 than in parity 1 by Detilleux et al. (1997). Previous milk yield influenced the effect of displaced abomasum, with higher loss in higher producing cows (Detilleux et al., 1997). A positive relationship between metritis and milk yield was observed in large cows (tall and heavy), whereas an opposite trend seemed to exist in small cowsÐ suggesting that height and weight could be effect modifiers (Markusfeld and Ezra, 1993). The stage of lactation at disease occurrence was investigated as a possible effect modifier. Deluyker et al. (1991) found significant losses associated with early metritis but not with late metritis. In contrast, Dohoo and Martin (1984b) found no effect of metritis, whatever the day of diagnosis. Milk losses associated with clinical ketosis increased with increasing lactation stage at diagnosis (Deluyker et al., 1991). Milk losses associated with locomotor disorders were higher for cases diagnosed in early lactation (Deluyker et al., 1991; Coulon et al., 1996). 4.6. Definition of summary patterns of milk losses To define a pattern of milk losses for each disease, short- and long-term effects can be combined and checked for consistency. For example, loss patterns can be defined on the basis of monthly variations, considering the average effect at the test-day level for the successive monthly tests. Four patterns are proposed by the present authors: ± no losses occur after milk fever, chronic metritis and cystic ovaries; ± small short-term losses and no long-term loss occur most often after retained placenta (from 0.3 to 0.7 kg/day during the first month or less);

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± moderate to large short- or mid-term losses, and no long-term loss occur after acute metritis (from 2 to 2.5 kg/day during the first month, decreasing to 0.7±1.3 kg/day the following month and no loss thereafter), clinical ketosis and displaced abomasum (for these two latter diseases, yield reduction starts before diagnosis). One month before clinical ketosis, losses from 1.3 to 2 kg/day occur, then increase to 2.5±3.5 kg/day in the month following diagnosis, return to 0.3±0.7 kg/day the following month and no loss thereafter. One month before displaced abomasum, losses from 3.5 to 6.5 kg/day occur, then increase to >6.5 kg/day in the month following diagnosis, return to 3.5± 6.5 kg/day the following month and no loss thereafter; and ± moderate short-term losses and small long-term losses occur after dystocia (from 0.7 to 1.3 kg/day during the first month, and from 0.3 to 0.7 kg/day thereafter, until the end of the lactation), lameness (from 1.3 to 2 kg/day during the first month, and from 0.3 to 0.4 kg/day thereafter, until the end of the lactation) and contagious cases of retained placenta (from 2 to 2.5 kg/day during one month, decreasing to 1.3±2 kg during the following month, and then to 0.3±0.4 kg/day, until the end of the lactation). In view of discrepancies in the results, and differences in study designs, it is not possible to summarize available estimates in a unique result, applicable whatever the context. Rather, summary estimates should be calculated for a given purpose, weighing the results according to sample size and external validity. References ArgaÁez-Rodriguez, F.J., Hird, D.W., HernaÁndez de Anda, J., Read, D.H., Rodriguez-Lainz, A., 1997. Papillomatous digital dermatitis on a commercial dairy farm in Mexicali, Mexico: incidence and effect on reproduction and milk production. Prev. Vet. Med. 32, 275±286. Barkema, H.W., Westrik, J.D., Van Keulen, K.A.S., Schukken, Y.H., Brand, A., 1994. The effects of lameness on reproductive performance, milk production and culling in Dutch dairy farms. Prev. Vet. Med. 20, 249±259. Barkema, H.W., Schukken, Y.H., Guard, C.L., Brand, A., Van der Weyden, G.C., 1992. Fertility, production and culling following cesarean section in dairy cattle. Theriogenol. 38, 589±599. Beaudeau, F., Frankena, K., Fourichon, C., Seegers, H., Faye, B., Noordhuizen, J.P.T.M., 1994. Associations between health disorders of French dairy cows and early and late culling within the lactation. Prev. Vet. Med. 19, 213±231. Bigras-Poulin, M., Meek, A.H., Martin, S.W., 1990. Interrelationships of health problems and age on milk production in selected Ontario Holstein cows. Prev. Vet. Med. 8, 3±13. Cobo-Abreu, R., Martin, S.W., Willoughby, R.A., Stone, J.B., 1979. The association between disease, production and culling in a university dairy herd. Can. Vet. J. 20, 191±195. Correa, M.T., Erb, H.N., Scarlett, J., 1993. Path analysis for seven postpartum disorders of Holstein cows. J. Dairy Sci. 76, 1305±1312. Coulon, J.B., Lescourret, F., Fonty, A., 1996. Effect of foot lesions on milk production by dairy cows. J. Dairy Sci. 79, 44±49. Coulon, J.B., PeÂrochon, L., Lescourret, F., 1995. Modelling the effect of the stage of pregnancy on dairy cow's milk yield. Anim. Sci. 60, 401±408. Curtis, C.R., Erb, H.N., Sniffen, C.J., Smith, R.D., Kronfeld, D.S., 1985. Path analysis of dry period nutrition, postpartum metabolic and reproductive disorders, and mastitis in Holstein cows. J. Dairy Sci. 68, 2347± 2360. Deluyker, H.A., Gay, J.M., Weaver, L.D., Azari, A.S., 1991. Change of milk yield with clinical diseases for a high producing dairy herd. J. Dairy Sci. 74, 436±445.

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C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

Dematawewa, C.M.B., Berger, P.J., 1997. Effect of dystocia on yield, fertility, and cow losses and an economic evaluation of dystocia scores for Holsteins. J. Dairy Sci. 80, 754±761. Detilleux, J.C., GroÈhn, Y.T., Eicker, S.W., Quaas, R.L., 1997. Effects of left displaced abomasum on test day milk yields of Holstein cows. J. Dairy Sci. 80, 121±126. Detilleux, J.C., GroÈhn, Y.T., Quaas, R.L., 1994. Effects of clinical ketosis on test day milk yields in Finnish Ayrshire cattle. J. Dairy Sci. 77, 3316±3323. Dijkhuizen, A.A., 1983. Economic aspects of diseases and disease control. Ph.D. Thesis, University of Utrecht. pp. 155. Djemali, M., Freeman, A.E., Berger, P.J., 1987. Reporting of dystocia scores and effects of dystocia on production, days open, and days dry from dairy herd improvement data. J. Dairy Sci. 70, 2127±2131. Dohoo, I.R., Martin, S.W., 1984a. Disease, production and culling in Holstein±Friesian cows. III. Disease and production as determinant of diseases. Prev. Vet. Med. 2, 671±690. Dohoo, I.R., Martin, S.W., 1984b. Disease, production and culling in Holstein-Friesian cows. IV. Effects of disease on production. Prev. Vet. Med. 2, 755±770. Dohoo, I.R., Martin, S.W., 1984c. Subclinical ketosis: prevalence and associations with production and disease. Can. J. Comp. Med. 48, 1±5. Enting, H., Kooij, D., Dijkhuizen, A.A., Huirne, R.B.M., Noordhuizen-Stassen, E.N., 1997. Economic losses due to clinical lameness in dairy cattle. Livest. Prod. Sci. 49, 259±267. Erb, H.N., Martin, S.W., Ison, N., 1981a. Swaminathan, S. Interrelationships between production and reproductive diseases in Holstein cows. Conditional relationships between production and disease. J. Dairy Sci. 64, 272±281. Erb, H.N., Martin, S.W., Ison, N., Swaminathan, S., 1981b. Interrelationships between production and reproductive diseases in Holstein cows. Path analysis. J. Dairy Sci. 64, 282±289. Erb, H.N., Smith, R.D., Oltenacu, P.A., Guard, C.L., Hillman, R.B., Powers, P.A., Smith, M.C., White, M.E., 1985. Path model of reproductive disorders and performance, milk fever, mastitis, milk yield, and culling in Holstein cows. J. Dairy Sci. 68, 3337±3349. Erb, H.N., 1987. Interrelationships among production and clinical disease in dairy cattle: a review. Can. Vet. J. 28, 326±329. GroÈhn, Y.T., Eicker, S.W., Hertl, J.A., 1995. The association between previous 305 day milk yield and disease in New York State dairy cows. J. Dairy Sci. 78, 1693±1702. Gustafsson, A.H., Andersson, L., Emanuelson, U., 1993. Effect of hyperketonaemia, feeding frequency and intake of concentrate and energy on milk yield in dairy cows. Anim. Prod. 56, 51±60. Gustafsson, A.H., Emanuelson, U., 1996. Milk acetone concentration as an indicator of hyperketonaemia in dairy cows: the critical value revised. Anim. Sci. 63, 183±188. Hortet, P., Seegers, H., 1998a. Calculated milk yield loss and related composition changes associated with elevated somatic cell counts in dairy cows: review and critical discussion. Vet. Res. 29, 497±510. Hortet, P., Seegers, H., 1998b. Loss in milk yield and related composition changes resulting from clinical mastitis in dairy cows: a review. Prev. Vet. Med. 37, 1±20. Kauppinen, K., 1984. Annual milk yield and reproductive performance of ketotic and non-ketotic dairy cows. Zbl. Vet. Med. A. 31, 694±704. Kay, R.M., 1978. Changes in milk production, fertility and calf mortality associated with retained placentae or the birth of twins. Vet. Rec. 102, 477±479. King, J.O.L., 1979. The effects of ketosis in dairy cows on body weight, milk yield and milk composition. Br. Vet. J. 135, 40±43. Lean, I.J., Bruss, M.L., Troutt, H.F., Galland, J.C., Farver, T.B., Rostami, J., Holmberg, C.A., Weaver, L.D., 1994. Bovine ketosis and somatotrophin: risk factors for ketosis and effects of ketosis on health and production. Res. Vet. Sci. 57, 200±209. Lucey, S., Rowlands, G.J., Russel, A.M., 1986. Short-term associations between disease and milk yield of dairy cows. J. Dairy Res. 53, 7±15. Mangurkar, B.R., Hayes, J.F., Moxley, J.E., 1984. Effects of calving ease-calf survival on production and reproduction in Holsteins. J. Dairy Sci. 67, 1496±1509. Markusfeld, O., Ezra, E., 1993. Body measurements, metritis, and postpartum performance of first lactation cows. J. Dairy Sci. 76, 3771±3777.

C. Fourichon et al. / Preventive Veterinary Medicine 41 (1999) 1±35

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Martin, J.M., Wilcox, C.J., Moya, J., Klebanow, E.W., 1986. Effects of retained fetal membranes on milk yield and reproductive performance. J. Dairy Sci. 69, 1166±1168. Martin, S.W., Kirby, K.L., Curtis, R.A., 1978. Left abomasal displacement in dairy cows: its relationship to production. Can. Vet. J. 19, 250±253. McInerney, J.P., Howe, K.S., Schepers, J.A., 1992. A framework for the economic analysis of disease in farm livestock. Prev. Vet. Med. 13, 137±154. Muller, L.D., Owens, M.J., 1974. Factors associated with the incidence of retained placentas. J. Dairy Sci. 57, 725±728. Oltenacu, P.A., Rounsaville, T.R., Milligan, R.A., Hintz, R.L., 1980. Relationship between days open and cumulative milk yield at various intervals from parturition for high and low producing cows. J. Dairy Sci. 63, 1317±1327. Philipsson, J., 1976. Studies on calving difficulty, stillbirth and associated factors in swedish cattle breeds. V. Effects of calving performance and stillbirth in Swedish Friesian heifers on productivity in the subsequent lactation. Acta Agric. Scand. 26, 230±234. PoÈsoÈ, J., MaÈntysaari, E.A., 1996. Genetic relationships between reproductive disorders, operational days open and milk yield. Livestock Prod. Sci. 46, 41±48. Rowlands, G.J., Lucey, S., 1986. Changes in milk yield in dairy cows associated with metabolic and reproductive disease and lameness. Prev. Vet. Med. 4, 205±221. Seegers, H., Fourichon, C., Malher, X., L'Hostis, M., 1994. A framework for animal health management. Vet. Res. 25, 165±173. Simensen, E., Halse, K., Gillund, P., Lutnoes, B., 1990. Ketosis treatment and milk yield in dairy cows related to milk acetoacetate levels. Acta Vet. Scand. 31, 433±440. Simerl, N.A., Wilcox, C.J., Thatcher, W.W., 1992. Postpartum performance of dairy heifers freshening at young ages. J. Dairy Sci. 75, 590±595. Tranter, W.P., Morris, R.S., 1991. A case study of lameness in three dairy herds N. Z. Vet. J. 39, 88±96. Van Werven, T., Schukken, Y.H., Lloyd, J., Brand, A., Heeringa, H.T.J., Shea, M., 1992. The effects of duration of retained placenta on reproduction milk production, postpartum disease and culling rate. Theriogenol. 37, 1191±1203.