Preventive Veterinary Medicine 54 (2002) 179–190

Risk factors for metritis in Danish dairy cows

J. Bruuna,b,*, A.K. Ersbølla,b, L. Albana,b,1
a
Department of Animal Science and Animal Health, The Royal Veterinary and Agricultural University,
Grønnegårdsvej 8,1870 Frederiksberg C, Denmark
b
Research Centre for the Management of Animal Production and Health,
Foulum, P.O. Box 50, 8830 Tjele, Denmark
Received 5 July 2001; accepted 30 March 2002

Abstract

A retrospective longitudinal study of metritis was conducted in Denmark on data collected during
1993–1994. Data on herd size, breed, parity, and treatment of disease were obtained from the Danish
Cattle Database. Management and production-facility data were collected using a questionnaire,
conducted as a telephone interview in 1994. The study included 2144 herds from three regions in
Denmark (102,060 cows). Herd-level variables included were: herd size, housing, flooring, grazing,
calving measures, and calving supervision. Cow-level variables were: parity, breed, calving season
and whether the cow had been treated by a veterinarian for dystocia or the diseases: retained placenta,
reproductive disease, ketosis, milk fever, or dry cow mastitis.
Marginal multivariable logistic-regression analyses were performed. The cow with highest odds of
metritis was a first or greater than or equal to third parity cow, of large breed, that calved during
November–April, in a zero-grazing herd. The cow had been treated for dystocia, retained placenta,
and at least one other reproductive disease, but not for ketosis. # 2002 Elsevier Science B.V. All
rights reserved.

Keywords: Dairy cows; Reproductive diseases; Metritis; Risk factors; Epidemiology

1. Introduction

Metritis in dairy cows is an important disease, because it can increase the calving-to-
conception interval (Erb et al., 1981; Bartlett et al., 1986; Fourichon et al., 2000) and

*
Corresponding author. Present address: Department of Animal Science and Animal Health, The Royal
Veterinary and Agricultural University, Grønnegårdsvej 8,1870 Frederiksberg C, Denmark.
Tel.: þ45-3528-3011; fax: þ45-3528-3022.
E-mail address: jbr@kvl.dk (J. Bruun).
1
Present address: The Danish Bacon and Meat Council, Axelborg, Axel Torv 3, 1609 København V,
Denmark.

0167-5877/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 7 - 5 8 7 7 ( 0 2 ) 0 0 0 2 6 - 0
180 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190

decrease milk yield (Coleman et al., 1985). The occurrence of metritis might be decreased
by manipulating risk factors for it.
Different incidence risks of metritis have been reported in the past. The range in
incidence risks varied from 0.2% in a Finnish study (Roine and Saloniemi, 1978) to 39% in
a French study (Martinez and Thibier, 1984).
Various risk factors for metritis have been identified: some are controversial, while
others are consistent in the literature. The ones which consistently have been identified are
dystocia and retained placenta (Dohoo and Martin, 1984a; Coleman et al., 1985; Curtis
et al., 1985; Etherington et al., 1985; Saloniemi et al., 1986; Kaneene and Miller, 1995).
Other suggested risk factors are: herd size (Roine and Saloniemi, 1978; Kaneene and
Miller, 1995), age (Erb and Martin, 1980a; Erb et al., 1981; Dohoo and Martin, 1984a;
Dohoo et al., 1984; Etherington et al., 1985), parity (Markusfeld, 1984, 1987; Saloniemi
et al., 1986; Gröhn et al., 1990; Rajala and Gröhn, 1998a), ketosis (Curtis et al., 1985;
Markusfeld, 1987; Kaneene and Miller, 1995), milk fever (Roine and Saloniemi, 1978;
Saloniemi et al., 1986; Kaneene and Miller, 1995), housing (Coleman et al., 1985) and
calving season (Erb and Martin, 1980a; Markusfeld, 1984, 1987; Martinez and Thibier,
1984; Etherington et al., 1985; Gröhn et al., 1990). However, the herd-management factors
grazing, farmer supervision at night for calving cows, and farmer intervention at calving
and their influence on metritis have not been investigated previously.
Our purpose was to investigate the risk factors for metritis among Danish dairy cows,
including these management factors.

2. Materials and methods

Ours was a retrospective longitudinal study of data collected during 1993–1994. The
data were collected from three regions of Denmark: Funen and Ringkøbing county and an
area around the city of Brørup in the south-west of Jutland (all cows in these areas were
included). Production and disease data were extracted from the Danish Cattle Database
(Table 1), and management and production-facility data were collected using a ques-
tionnaire (Table 2). The questionnaire data were collected via telephone interviews
conducted during February and September 1994, and of the 2391 farmers contacted,
2148 (89.1%) agreed to participate. The questionnaire included mainly closed questions
and the telephone interviews were performed by 22 pre-trained students. The students were
instructed to ask the questions exactly the way they were written every time they conducted
an interview, each interview lasted 15–45 min. The questionnaire is described in detail in a
previous study (Alban and Agger, 1996).
The criteria used for inclusion of cows were: calving between 1 July 1993 and 30 June
1994, disease recording available from 30 days before and 30 days after calving, and
records of production available for the first 30 days after calving. Furthermore, for cows
with metritis, a case of metritis was recorded as veterinary treatment registered in the
Danish Cattle Database during the first 30 days postpartum, and only the first occurrence
was used. A period of 30 days postpartum was chosen to include mainly cases where
clinical symptoms are present, and not to include cows around their first insemination
which would be recorded due to vaginal discharge and infertility. Also, most treatments of
 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190 181

Table 1
Descriptive statistics of data from the Danish cattle database collected in 1993–1994, included in the analysis of
risk factors for metritis in 102,060 Danish dairy cattle

Variable name Level No.

Metritis þ Metritis 
Herd level
Herd size (number of cows) 40 173 23531
41–60 216 23343
61–80 197 32580
81 147 21873
Cow level
Parity 1 319 38796
2 140 27414
3 126 16468
4 148 18649
Breed Jersey 73 22863
Large breed 660 78464
Calving season May–October 264 40092
November–April 469 61235
Dystocia Yes 64 2188
No 669 99139
Retained placenta Yes 184 6527
No 549 94800
Reproductive disease Yes 50 1688
No 683 99639
Ketosis Yes 9 1524
No 724 99803
Milk fever Yes 43 4154
No 690 97173
Dry-cow mastitis Yes 9 1230
No 724 100097

metritis in the Danish Cattle Database occurred during 30 days postpartum. Applying these
criteria, a total of 2144 herds and a total of 102,060 cows were included.
The risk factors for the analyses were selected based on biological plausibility and are
shown in Tables 1 and 2. Disease risk factors were coded positive if treatment for disease
preceded the diagnosis of metritis, and only the first treatment of each disease was included.
‘Dry-cow mastitis’ was generated from codes in the Danish Cattle Database that
distinguish between different types of mastitis (e.g. acute mastitis, chronic mastitis and
mastitis due to teat lesions). It included recordings of any treatment of mastitis during the
30 days before calving.
‘Reproductive disease’ was generated by collapsing different original disease data
on reproduction (intrauterine therapy, prolapsed uterus, vaginitis, abortion, and induced
calving). This was done for three reasons: there was a low frequency of cows with both
182 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190

Table 2
Descriptive statistics of questionnaire herd level data from 2144 herds, conducted as a telephone interview in
1994, included in the analysis of risk factors for metritis in 102,060 Danish dairy cows

Variable name Level No.

Metritis þ Metritis 

Housing Deep bedding and cubicle 196 22196

Tie stall 537 79131
Flooring Concrete or slats without bedding 54 4395
Concrete/slats with bedding 637 92089
Deep bedding 42 4843
Grazing Zero grazing 221 23168
Only dry cows 47 5012
Exercise possibility 19 1534
Grazing 446 71613
Calving measure Yesa 592 80606
Nob 141 20721
Calving supervision Farmer supervises cows calving at night 626 85371
Farmer does not supervise cows calving at night 107 15956
a
Includes turning or pulling the calf, using a pulling machine or removing the placenta.
b
Includes calving box, extra bedding, wooden platform or straw bale behind tethered cow.

metritis and one of these diseases, they were all significant risk factors ðP < 0:15Þ in the
univariable analyses, and it is biologically meaningful.
‘Breed’ was divided into two categories Jersey cows (22.5%) and large-breed cows
(51% Holstein Friesians, 16% Red Holstein, 1.0% Danish Reds, and 9.5% Cross-breed).
The analyses were done with marginal logistic regression; this analysis takes the
hierarchical structure of data into account (cows are clustered within farms) without
actually estimating the coefficient of the random variation as in a random-effects model.
The software used was SAS (1999).
Correlation between the variables in the initial multivariable model was checked using
Spearman correlation coefficients.
The initial multivariable model included all risk factors; it was reduced using backward
elimination (P > 0:05 in the GEE score test was the elimination criterion). Changes in
parameter estimates >20% and biological relevance was evaluated between two models to
check for potential confounding. Likewise, the preliminary final model was rerun including
each eliminated variable one-at-a-time to check for changes in parameter estimates >20%,
which were of biological relevance.
Biologically meaningful interactions were tested between factors of the preliminary
final multivariable model. Initially, the interactions were included in this model, it then
was reduced by backward elimination (P > 0:05 as the elimination criterion). The
interactions tested were: retained placenta and breed; parity and breed; dystocia and
breed; grazing and calving season; retained placenta and calving season; and retained
placenta and parity.
 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190 183

3. Results

Descriptive statistics for the risk factors included in the initial multivariable model are
given in Tables 1 and 2. A total of 733 cases of metritis were included, giving an overall
incidence risk (Kleinbaum et al., 1982) in the present study of 0.7%. However, the
distribution across herds was uneven. The incidence risk ranged from 1 to 21% in the 391
herds where at least one treatment of metritis was reported during the study period (Fig. 1).
The distribution of metritis treatments within the 30 days after calving is shown in Fig. 2.
The risk factors significantly associated with metritis in the multivariable model were:
parity, grazing, calving season, dystocia, reproductive disease, ketosis, and the interaction
between retained placenta and breed (Table 3). The significance of risk factors was
evaluated using a score test which is a good approximation of the log likelihood-ratio test.
However, the confidence limits were generated using Wald’s approximation. Therefore, a
risk factor could be significant in the score test, even though the Wald’s confidence limits
include 1.0 (as is the case for ketosis).

Fig. 1. Herd prevalence of metritis in 2144 herds in a study on risk factors for metritis on data collected during
1993–1994 from 102,060 Danish dairy cows.
 184
J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190
Fig. 2. The distribution of day of metritis treatments within the 30 days after calving, in a study on risk factors for metritis on data collected during 1993–1994 from
102,060 Danish dairy cows.
 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190 185

Table 3
Results of a multivariable analysis of risk factors for metritis on data, from 102,060 Danish dairy cows, collected
during 1993–1994

Risk factor Level b S.E. Pa Odds ratiob Confidence

interval

Parity 1 0.017 0.11 <0.001 1.0 b 0.8–1.2

2 0.506 0.12 0.6 c 0.5–0.8
3 0.058 0.12 0.9 b 0.7–1.2
4 0.000 0.00 1.0 b
Grazing No 0.478 0.13 <0.001 1.6 b 1.3–2.1
Dry cows 0.762 0.24 2.1 b 1.4–3.4
Exercise area 0.627 0.34 1.9 bc 1.0–3.6
Yes 0.000 0.00 1.0 c
Calving season November–April 0.204 0.08 0.010 1.2 b 1.0–1.4
May–October 0.000 1.0 c
Dystocia Yes 1.101 0.15 <0.001 3.0 b 2.3–4.0
No 0.000 1.0 c
Reproductive disease Yes 0.903 0.18 <0.001 2.5 b 1.8–3.5
No 0.000 1.0 c
Ketosis Yes 0.755 0.51 0.013 0.5 b 0.2–1.3
No 0.000 1.0 c
Breed  retained placenta Large, yes 2.288 0.18 0.005 9.9 b 6.9–14.1
Jersey, yes 2.380 0.27 10.8 b 6.4–18.3
Large, no 1.047 0.16 2.9 c 2.1–3.9
Jersey, no 0.000 0.00 1.0 d
a
P-value for each factor in the overall GEE score test.
b
Levels within a variable with different letters were significant ðP  5%Þ.

There was no important 2-way correlation between the variables in the initial multi-
variable model; the highest correlation coefficient was 0.53 (between housing type and
herd size).

4. Discussion

4.1. Data quality

The recording of treatment of animal disease in dairy cows is mandatory in Denmark.

Veterinarians mostly report the diagnoses and treatments in the Danish Cattle Database.
However, farmers also may report the occurrence of disease. The sensitivity of disease
recordings in central databases is uncertain, and depends on the properties of the disease,
and the consequences of having it. Different factors influence the sensitivity:
1. The farmer must recognize the disease and find it severe enough to call for a
veterinarian.
186 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190

2. The veterinarian must make a correct diagnosis and recording of the disease.
3. The entering of the record into the database must be correct.

The sensitivity of metritis in the present study is expected to be reasonable because: The
follow-up period of 30 days mainly includes metritis, for which the disease symptoms are
relatively severe (so the farmer will recognize the disease and call the veterinarian). This
disease does affect production—which also will motivate the call for a veterinarian.
Models including routine clinical reproductive examinations might have higher sensi-
tivity—but could be modeling a different spectrum of the disease depending on how
stringent the definition of a case was (often include cows whose only symptom is
discharge).

4.2. Incidence risk

The use of the terminology ‘incidence risk’ and ‘incidence rate’ is not always
standardized. In the present study, incidence risk was calculated using the simple
cumulative method (Kleinbaum et al., 1982). Many studies use the term lactational
incidence rate (Erb and Martin, 1980b; Dohoo et al., 1983; Gröhn et al., 1990); however,
the definition used, especially for metritis, makes incidence rates calculated in this way
comparable to incidence risk (Bendixen, 1987).
In studies that use treatment of disease voluntarily registered in a central database,
incidence risks of metritis often are reported as 0.2–7.8% (Roine and Saloniemi, 1978). In
contrast, the reported incidence risk in studies that use routine clinical examination of
calving cows is higher (between 13 and 39%) (Coleman et al., 1985).

4.3. Parity

The u-shaped association between parity and metritis is supported in the literature
(Markusfeld, 1984, 1987; Saloniemi et al., 1986). However, ‘no association’ between
metritis and parity also has been found (Gröhn et al., 1990). There was a tendency for a
u-shaped relationship between parity and metritis in a study by Rajala and Gröhn (1998a,b),
even though it was not tested.
Biologically, the u-shaped association between parity and metritis makes sense. The
heifers could have a greater odds of metritis than second-parity cows, because damage to
the uterus is more common in heifers. Also, heifers that are unsuccessful in calving are
likely to be culled. The third-parity cows could have a higher odds of metritis compared to
second-parity cows due to delayed involution of the uterus (Etherington et al., 1985;
Fishwick, 1997), with increased risk of infection.
Parity and age are closely related, but it depends on the categorization of both. Some
studies have shown an association between age at calving (Erb and Martin, 1980a; Dohoo
and Martin, 1984a; Dohoo et al., 1984), while other studies have shown no association
between metritis and age (Erb et al., 1981; Dohoo and Martin, 1984a; Etherington et al.,
1985; Bartlett et al., 1986). However, the u-shaped association between parity and metritis
has not been reflected in the age-metritis association by these authors, though an age-
tendency could be seen from Table 1 in the study by Bartlett et al. (1986). A reason for this
 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190 187

could be that most studies categorize 2- and 3-year-old cows into one category, which
might include a mix of heifers and second-parity cows, and thereby the u-shaped
association is blurred.

4.4. Grazing

The odds of metritis were lower for cows in herds with grazing, relative to cows in zero-
grazing herds and where only dry cows grazed. There could be two biological reasons for
this finding. Cows that graze during the summer months regain good health in general
(because of the grass and the sun), but also their musculature and condition could be
increased—thereby making calving easier. The last reason also could be in effect for cows
in herds with exercise areas.

4.5. Calving season

The odds of metritis increased in cows calving during the period November and April in the
present study, and this is supported in the literature (Erb and Martin, 1980a; Markusfeld,
1984; Martinez and Thibier, 1984; Etherington et al., 1985; Gröhn et al., 1990). During the
winter months, the general health of cows is lowered making them more prone to infections.

4.6. Reproductive diseases

Dystocia and reproductive diseases both increased the odds of metritis. Dystocia can
increase the risk of trauma to the uterine wall and thereby increase the odds of metritis.
Also, calving assistance can increase the risk of introducing infection. Reproductive
disease could increase the risk of infection (and thereby the odds of metritis), so this finding
was not surprising and is supported by the literature (Erb et al., 1981; Coleman et al., 1985;
Curtis et al., 1985; Etherington et al., 1985; Gröhn et al., 1990; Kaneene and Miller, 1995).

4.7. Metabolic disorders

Unexpectedly to us, ketosis seemed to be protective for metritis in our study. This might
arise from inaccurate reporting dates of disease; also, for cows with both diseases on the
same day, it could be that only ketosis gets reported because it is probably considered the
more important of the two.
In the literature, some studies found ketosis to be a risk factor for metritis (Markusfeld,
1987; Kaneene and Miller, 1995), whereas others have found no association (Markusfeld,
1984; Curtis et al., 1985; Kaneene and Miller, 1995). Kaneene and Miller (1995) found that
there was an association between metritis and ketosis in their cow-based model and a weak
association ðP ¼ 0:06Þ in the herd-based model. However, in their study, the specific dates
for metritis were not recorded (the recording used was whether a cow had metritis within a
month or not).
In one study with positive association between ketosis and metritis, the measure for
ketosis was ketonuria which means that subclinical cases of ketosis were included
(Markusfeld, 1987). This could change the relationship to metritis.
188 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190

There was no association between milk fever and metritis, which is supported in the
literature (Kaneene and Miller, 1995). However, a positive association between metritis
and milk fever also has been seen (Saloniemi et al., 1986; Markusfeld, 1987; Gröhn et al.,
1990). The time ordering of the disease variables was probably good in the study by
Markusfeld (1987), because cows were monitored daily by veterinarians and no treatment
was performed by farmers; therefore these results could be the most reliable.

4.8. Retained placenta and breed interaction

The effect of retained placenta has in the previous studies been shown to largely increase
the odds of metritis (Erb and Martin, 1980a; Erb et al., 1981; Dohoo and Martin, 1984a;
Coleman et al., 1985; Curtis et al., 1985; Etherington et al., 1985; Saloniemi et al., 1986;
Kaneene and Miller, 1995). However, because most studies include mainly one breed of
cows (e.g. Holstein Friesian (Erb et al., 1981; Dohoo et al., 1983; Curtis et al., 1985) and
Finnish Ayrshire (Gröhn et al., 1986; Saloniemi et al., 1986; Rajala and Gröhn, 1998b)), the
retained placenta–breed interaction has not been tested. This interaction was significant in
our final multivariable model.
Cows with retained placenta had higher odds of metritis irrespective of breed. Retained
placenta as a risk factor for metritis is very much supported in the literature, and a probable
biological explanation could be that retained placental membranes pose a perfect media for
bacterial growth. However, when retained placenta was not present, large-breed cows had
significantly higher odds of metritis than Jersey cows. This would be expected, because
Jersey cows generally have an easier calving (less exposed to farmer-assisted calving), and
thereby are less prone to trauma to the uterus. Because trauma to the uterine wall can be a
source of infection (Fishwick, 1997), this could explain the difference in odds of metritis
between the breeds when retained placenta was not present.
Coleman et al. (1985) found no association between metritis and breed. The breeds in
their study were, however, different from ours and their analysis was conducted at the herd
level.

4.9. Herd size

We found no association between metritis and herd size. This contrasts with Roine and
Saloniemi (1978) and Kaneene and Miller (1995). However, the herd-size categories in the
study by Roine and Saloniemi (1978) were very small, and in the study by Kaneene and
Miller (1995) the categories were different than in the present study and the significance
was borderline ðP ¼ 0:053Þ.

4.10. Housing

We found no association between housing and metritis, similar to the study by

Coleman et al. (1985). Most studies includes no variation in the housing of the cows.
Cows were housed in stanchion barns in the study by Erb and Martin (1980b) and in tie
stalls in the study by Dohoo et al. (1983) and therefore, housing could not be included as a
risk factor.
 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190 189

4.11. Flooring

This variable was included as a measure of cleanliness around the cows. It was expected
that the environment on concrete or slats without bedding would be less clean than on
concrete or slats with bedding, this could affect the odds of metritis but it was not the case
in our study. However, only few farmers in the present study used concrete or slats without
bedding, which could be one reason for not finding a significant association between
metritis and flooring. Another reason could be that the variable does not describe the
cleanliness of the environment adequately. A barn with bedding could be more dirty than a
barn with only concrete, depending on the management of the barn. The effect of different
types of bedding on metritis was investigated in a study by Kaneene and Miller (1995) and
no effect was found in that study, either.

4.12. Calving measures and calving supervision

These data were collected using a questionnaire on each farm and were therefore, not
cow specific.
A farmer could have an intention to have special measures and calving supervision for
calving cows, but this would be a management ‘policy’ and would not necessarily be
applied on the animal level. The management might be applied differently to different cows
depending on their calving status and history. This could be a reason for not finding the
expected association between calving measures and calving supervision and metritis. The
effect on reproductive tract infection of heifers and cows supervised at calving was
investigated with no association found (Dohoo and Martin, 1984b).

4.13. Dry-cow mastitis

The hypothesis tested here was whether mastitis in the dry period could suppress the
immune response of a cow, thereby increasing the odds of metritis. In our study there was
no such association and no literature could confirm or contrast this finding.

5. Conclusion

Metritis is influenced by management factors. Having cows on summer pasture

decreased the odds of metritis, as did having cows calve during the summer months.
The complex of problems occurring around calving is also very important in reducing the
incidence of metritis. Problems such as dystocia and retained placenta greatly increased the
odds of metritis. Jerseys have a lower odds for metritis than large breed cows, provided they
do not have retained placenta postpartum.

Acknowledgements

We acknowledge The Research Centre for the Management of Animal Production and
Health, Foulum, P.O. Box 50, 8830 Tjele, Denmark for funding.
190 J. Bruun et al. / Preventive Veterinary Medicine 54 (2002) 179–190

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