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Spontaneous recovery or persistence of postpartum endometritis and
risk factors for its persistence in Holstein cows
G. Gautam, T. Nakao *, K. Koike, S.T. Long, M. Yusuf,R.M.S.B.K. Ranasinghe, A. Hayashi
Laboratory of Theriogenology, Department of Veterinary Medicine, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Japan
Received 3 July 2009; received in revised form 8 August 2009; accepted 24 August 2009
Abstract
It has been stated that postpartum endometritis in dairy cows has a tendency to cure without intervention. The objectives of this
field study, therefore, were to determine the proportions of cows with spontaneous clinical recovery or persistence of postpartum
endometritis and to determine some risk factors for its persistency in dairy cows (Bos taurus). Holstein-Friesian cows (n = 441
lactations) from seven dairy herds were examined monthly by vaginoscopy and transrectal palpation. A cow was considered to have
‘‘postpartum endometritis’’ if it had pus in the cervico-vaginal discharge at the first postpartum examination during Days 15 to 60
(Day 0 = day of calving); this was classified as mild, mucopurulent, or purulent endometritis, or endometritis with fluid in uterus.
Furthermore, a cow with evidence of endometritis at least once during Days 61 to 150 was considered to have ‘‘persistence (or
recurrence) of endometritis.’’ A total of 104 (23.6%) lactations had postpartum endometritis, of which 25.3% had persistence or
recurrence of clinical endometritis. Cows with persistence or recurrence of endometritis became pregnant at a slower rate (hazard
ratio [HR] = 0.28; P < 0.001) than those with no endometritis until Day 150. Calving in summer (odds ratio [OR] = 7.00; P = 0.04),
early postpartum complications (OR = 6.58; P = 0.05), moderate (OR = 4.03; P = 0.08) and severe (OR = 30.99; P = 004) degrees
of urovagina, and mucopurulent (OR = 9.54; P = 0.02) and purulent (OR = 5.70; P = 0.04) endometritis were risk factors for the
persistence or recurrence of endometritis. Furthermore, 10.6% of cows that had not shown signs of postpartum endometritis had a
new diagnosis of endometritis during Days 61 to 150. Some risk factors for the new diagnosis of endometritis beyond Day 60 were
early postpartum complications (OR = 2.82; P = 0.03) and moderate (OR = 5.00; P = 0.001) or severe (OR = 12.63; P < 0.001)
degrees of urovagina. In conclusion, approximately one quarter of cows with postpartum endometritis had persistence of
endometritis until or beyond the breeding period. Risk factors for the persistence of clinical endometritis were summer calving,
early postpartum complications, clinically relevant urovagina, and clinically relevant endometritis within 2 mo postpartum.
# 2010 Elsevier Inc. All rights reserved.
Keywords: Endometritis; Holstein cows; Spontaneous recovery; Urovagina; Vaginoscopy
www.theriojournal.com
Available online at www.sciencedirect.com
Theriogenology 73 (2010) 168–179
1. Introduction
Postpartum uterine diseases have been described as a
leading cause of reproductive inefficiency in dairy cattle
* Corresponding author. Tel.: +81 83 933 5935;
fax: +81 83 933 5935.
E-mail address: tnakao@yamaguchi-u.ac.jp (T. Nakao).
0093-691X/$ – see front matter # 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2009.08.010
[1–17]. Uterine diseases, postpartum endometritis in
particular, reduce the reproductive efficiency of cows by
extending the calving to conception interval, increasing
the number of inseminations per conception [5,7–
9,15,16], and increasing culling rates [5,7,8]. The
prevalence of endometritis in 43 studies ranged from
2.2% to 37.3%, with a median of 10.1% [18]. In some
herds, 40% of postpartum cows may be diagnosed and
treated for uterine infections [17].
G. Gautam et al. / Theriogenology 73 (2010) 168–179 169
Although the prevalence of postpartum endometritis
and its impact on subsequent fertility has been widely
reported, the follow-up clinical examination regarding
its fate has not been well documented. Many published
reports failed to document an overall significant
improvement in reproductive performance after treat-
ment of endometritis [19–25], suggesting that a high
proportion of endometritis cases have a tendency to
recover spontaneously. Some previous studies sup-
ported the likelihood that a high proportion of cows
have spontaneous resolution of endometritis until at
least 4 wk postpartum [5,19]. However, others demon-
strated that the clinical examination of vaginal contents
even before 3 wk postpartum predicted reduced
reproductive performance in dairy cows [7,13,14,20].
Therefore, it is necessary to determine whether the
postpartum period at a diagnosis of endometritis
influences its recovery or persistence. The central
question is how some postpartum cows can resolve
uterine infections spontaneously without intervention,
whereas others in the same herd, with presumably the
same general management, have persistent infection. It
is also not known what proportion of cows resolve
uterine infection spontaneously and what proportions
have persistent infection. Therefore, the objectives of
this field study were to determine the proportions of
cows with spontaneous clinical recovery or persistence
of postpartum endometritis and to determine some risk
factors for its persistency in Holstein cows in a
subtropical area of Japan.
2. Materials and methods
2.1. Animals and management
This study was conducted in 291 Holstein-Friesian
cows (Bos taurus) and used 441 lactations for cows
calving between October 2005 and December 2008.
These cows were in seven commercial dairy herds in
Yamaguchi Prefecture, southwestern region of Japan,
under subtropical conditions. These herds were visited
monthly for reproductive examination by a team of
three or four persons including faculty members, as well
as graduate and undergraduate students from the
Laboratory of Theriogenology, Yamaguchi University
(headed by the senior author). The study population
consisted of cows used for our previous study [26], as
well as additional cows from the same herds. Cows were
kept in a loose housing system in a small paddock (zero-
grazing system) with wood shavings on the floor
throughout the year (Herds A and B), tie-stall barns with
rubber mattresses on the floor (Herds C, D, and E), or in
tie-stall barns with an open paddock (Herds F and G).
The herd size ranged from 20 to 60 lactating cows. The
cows were nonseasonal, year-round calvers, milked
twice daily with herd average 305-d milk yield between
8700 and 10,200 kg per cow. Parity ranged from one to
seven. Cows were artificially inseminated after detec-
tion of estrus by the herd owners, usually after 35 d
postpartum. In all herds, no estrus/ovulation synchro-
nization programs were used. Cows were observed for
signs of estrus in the morning, at noon, and in the late
afternoon. In Herds A, B, F, and G, standing to be
mounted was interpreted as a sign of estrus, and those
cows were inseminated 8 to14 h later. In Herds C, D,
and E, estrus was detected based on some secondary
estrous signs (swelling, relaxation, and congestion of
vulva, mucus discharge, bellowing, restlessness, or
decreased milk yield), and cows were inseminated 8 to
14 h later. In all herds, cows were inseminated with
frozen-thawed semen of proven sires (three or four sires
in total) from the Livestock Improvement Association
of Japan. In Herds F and G, embryo transfer was also
done in some cows (decided by the herd owners).
Pregnancy was diagnosed by transrectal palpation or
with ultrasonography (Tringa Linear Vet, equipped with
a dual frequency 5/7.5 MHz intrarectal transducer; Pie
Medical Equipment BV, Maastricht, The Netherlands),
usually �30 d after insemination (or embryo transfer).
2.2. Clinical examination
Each herd was visited once a month for regular
reproductive examinations, which included the detec-
tion and treatment of reproductive disorders, pregnancy
diagnosis, and recording of body condition score (BCS;
scale 1 to 5, with 0.25-point increments) [27]. Cows that
were more than 2 wk postpartum were examined by
vaginoscopy and transrectal palpation every month until
confirmation of pregnancy, a decision to cull, or at least
until 5 mo postpartum. Each time, all subjective
assessments were made by the same veterinarian (the
senior author). At each visit, if a cow was within 1 mo
after artificial insemination (AI) and did not return to
estrus, only vaginoscopy was performed. If the cow was
more than 1 mo after AI, pregnancy was diagnosed by
transrectal palpation or ultrasonography. All other cows
were examined vaginoscopically followed by transrec-
tal palpation of the genital tract.
For vaginoscopy, first the cow was restrained in a
feeding stanchion or a halter, the tail was held to one
side, the vulva washed with lukewarm water mixed with
benzylkonium chloride 10% (Osvan; Nihon Seiyaku
Co., Tokyo, Japan) at 1:1000 dilution, wiped with a
G. Gautam et al. / Theriogenology 73 (2010) 168–179170
clean paper towel, sprayed with 2% polyvinyl pyrrol-
iodine, and wiped with cotton soaked in 70% alcohol.
An autoclave-sterilized glass vaginoscope (35 cm long,
2 mm thick, and 4 cm external diameter; L.C.C. Co.
Ltd., Shunan Shi, Yamaguchi, Japan) was inserted into
the vagina up to the level of the external cervical os. A
separate vaginoscope was used for each cow. The
contents of the anterior vagina, if any, were viewed
using a torch light, and a portion was aspirated with a
25-mL or 50-mL syringe fitted to an AI gun sheath and
transferred into a Petri dish. Each time, the nature of the
recovered fluid was scored qualitatively as clear mucus,
predominately clear mucus with some flecks of pus,
mucopurulent (approximately 50% pus and 50%
mucus), or purulent (>50% pus). The recovered fluid
was also checked for its color (yellowish or no color),
consistency (watery or mucoid), smell (uremic or no
smell), and pH using a paper strip (Spezial-Indikator-
papier; Macherey-Nagel GmbH & Co. KG, Duren,
Germany).
After vaginoscopy, transrectal palpation of the
reproductive tract was performed to determine the
diameter of cervix, diameter, location (abdominal or
pelvic), consistency (contraction, elasticity and toni-
city), and symmetry of uterine horns (i.e., differences in
diameter), the presence of any fluid in the uterus (yes or
no), and the presence of any palpable ovarian structures
(follicle, corpus luteum, cystic ovarian follicle, etc.).
2.3. Case definition
Cases having any amount of purulent material in the
cervico-vaginal discharge without any signs of systemic
illness were defined as endometritis and classified into
the following categories, based on vaginoscopic and
transrectal palpation findings:
� Mild endometritis (E1): cows with predominately
clear mucus with some flecks of pus on vaginoscopy.
� Mucopurulent endometritis (E2): cows with muco-
purulent discharge on vaginoscopy.
� Purulent endometritis (E3): cows with purulent
discharge on vaginoscopy.
� Endometritis with fluid in uterus (E4): cows with
purulent or mucopurulent discharge on vaginoscopy
and appreciable amount of fluid in uterus detected by
transrectal palpation.
No treatment was indicated for endometritis within 2
mo postpartum, except for 10 cows, which were
excluded from the analysis. Similarly, after 2 mo
postpartum, no treatment was indicated for endometritis
(except six cows treated for persistent endometritis,
which were excluded from the analyses of reproductive
performance).
Cases having vaginal contents with the presence of
urine or urine mixed mucus (characterized by at least
any two of yellowish in color, watery in consistency,
uremic in smell, and/or pH >7.4) were defined as
urovagina. Cases of urovagina were further classified
into the following different degrees based on the extent
of covering of external cervical os by the urine or urine-
mixed mucus [26]:
� Mild degree of urovagina: small amount of urine or
urine mixed mucus (approximately 10 to 100 mL)
only on the floor of vagina, but not covering the
external cervical os.
� Moderate degree of urovagina: appreciable amount of
urine or urine mixed mucus (approximately 100 to
500 mL) covering almost half or less than half of the
external cervical os (with some risk of urine entering
the uterus).
� Severe degree of urovagina: large amount of urine or
urine mixed mucus (approximately >500 mL) cover-
ing more than half or the whole external cervical os
(high risk of urine entering the uterus).
The vagina of cows with urovagina (except that of
those not returning to estrus after AI) was flushed with 2
L 3% aluminum potassium sulfate (Myouban; Nipro
Farm Co., Osaka, Japan) using an autoclaved glass
vaginoscope and a hose (2 cm in diameter) fitted to a
funnel, and the fluid was removed from the vagina.
2.4. Data collection and management
Data were collected from 441 lactations, which
included herd, parity (1, 2, 3, or �4), season of calving
(autumn: September through November; winter:
December through February; spring: March through
May; summer: June through August), type of calving
(normal, or abnormal [dystocia, abortion or fetal
death]), retention of fetal membranes >24 h (RFM),
early postpartum complications (any one or more of
puerperal metritis, hypocalcemia, abomasal displace-
ment, ketosis, lameness, or clinical mastitis before or at
first postpartum examination), BCS at first postpartum
examination, BCS at first examination beyond Day 60
(Day 0 = day of calving), degree of endometritis, and
degree of urovagina. Cows treated for endometritis
within Day 60 (n = 10) and those culled before having
two examinations beyond Day 60 (culled too early,
n = 9) were excluded from the analysis.
G. Gautam et al. / Theriogenology 73 (2010) 168–179 171
During scheduled monthly herd visits, all postpartum
cows were examined for the first time during Days 15 to
60. Therefore, a cow was considered to have ‘‘post-
partum endometritis’’ if it showed any degree of
endometritis (defined as above) at first postpartum
examination. During Days 61 to 150, a cow with any
amount of pus in the cervico-vaginal discharge at least
once (out of two or more examinations) was considered
to have endometritis (considering that any pus discharge
during the breeding period is abnormal, all degrees of
endometritis beyond Day 60 were simply considered as
‘‘endometritis’’ without any classification).
Based on these criteria, a cow that had postpartum
endometritis but showed no more clinical endometritis
beyond Day 60 (out of two or more examinations) or
conceived within Day 60 was considered to have
‘‘spontaneous clinical recovery of endometritis,’’
whereas a cow that had postpartum endometritis and
was still showing clinical endometritis during Days 61
to 150 was considered to have ‘‘persistence or
recurrence of clinical endometritis.’’ To avoid confu-
sion, hereafter the terms ‘‘spontaneous recovery’’ and
‘‘persistence’’ are used. Likewise, a cow that had no
signs of postpartum endometritis but showed clinical
endometritis at least once during Days 61 to 150 was
considered to have ‘‘new diagnosis of endometritis.’’
2.5. Statistical analysis
The prevalence of different degree of ‘‘postpartum
endometritis’’ was expressed as a percentage of total
examined lactations within Day 60. During Days 15 to
60, the uterine conditions were expected to be dynamic
over the enrollment period. Therefore, for the analysis,
the findings were stratified into three stages, 15 to 20 d
(early), 21 to 28 d (intermediate), and 29 to 60 d (late),
as well as overall. Spontaneous recovery (%) or
persistence (%) of endometritis was expressed as a
proportion of cows with ‘‘postpartum endometritis’’
that had spontaneous clinical recovery or that had
persistence of clinical endometritis during Days 61 to
150, respectively. All analyses were performed with
SPSS software [28], with lactation as the unit of
concern. The reproductive performance of cows
diagnosed with endometritis before 3 wk postpartum
was compared with that of those with no endometritis
during this period by Cox’s proportional hazards
regression models of time to conception and by logistic
regression models of pregnancy proportions by 210 d
postpartum. The variables describing endometritis
during Days 15 to 20 (yes or no), herd, season of
calving, parity group, and BCS (continuous) were
included in a proportional hazards regression model of
time to conception. Models were built by manual
reverse stepwise elimination, using likelihood-ratio test
statistics. At each step, the variable with highest P value
was removed, and the model was run until all the
remaining independent variables and covariates were
significant (P < 0.05). Multiple logistic regression
analysis was used to analyze variables with dichot-
omous outcomes. Risk factors were tested against each
outcome variable in a univariate analysis. All variables
that were associated with an outcome of interest
(P < 0.25) were included in a full model, and a reverse
stepwise procedure using a likelihood-ratio test
statistics was used to arrive at a final model, with a
threshold P value for inclusion being < 0.05 and >0.1
for exclusion. The final models were assessed using
Hosmer-Lemeshow goodness of fit test. For analysis of
pregnancy proportion by 210 d postpartum in cows
examined within 3 wk postpartum, the model included
endometritis status during Days 15 to 20 (yes or no),
herd, season of calving, parity group, and BCS at first
postpartum examination (continuous).
For analysis of risk factors for ‘‘postpartum
endometritis,’’ the model included herd (1 to 7), parity
(1, 2, 3, or �4), season of calving (autumn, winter,
spring, or summer), type of calving (normal or
abnormal), RFM (no or yes), early postpartum
complications (no or yes), BCS at first postpartum
examination (continuous), urovagina within Day 60 (no,
mild, moderate, or severe), and postpartum interval at
examination (15 to 20, 21 to 28, or 29 to 60 d).
For analysis of persistence of endometritis, a model
was constructed for cattle in which the ‘‘postpartum
endometritis’’ (i.e., endometritis within Day 60) was
diagnosed; the model included herd, parity, season of
calving, RFM, early postpartum complications, BCS at
first postpartum examination, BCS at first examination
beyond Day 60, BCS change between first postpartum
examination and first examination beyond Day 60
(increased, unchanged, or decreased), degree of
urovagina until Day 150, degree of postpartum
endometritis, postpartum interval at examination, and
terms of interactions between degree of endometritis
and postpartum interval at examination.
Likewise, a model was constructed for cattle that did
not show the postpartum endometritis to analyze the
risk factors for ‘‘new diagnosis of endometritis’’; the
model included the same explanatory variables
described for the persistence of endometritis except
the degree of postpartum endometritis.
The pregnancy rates among cows with no endome-
tritis until Day 150, those with spontaneous recovery of
G. Gautam et al. / Theriogenology 73 (2010) 168–179172
Table 1
Prevalence of degrees of postpartum endometritis in Holstein cows examined for the first time between Days 15 and 60.
Finding Interval postpartum at examination
15–20 d (Early) 21–28 d (Intermediate) 29–60 d (Late) Overall
Number of cows examined 89 114 238 441
Postpartum endometritis, n (%)* 40 (44.9) 29 (25.4) 35 (14.7) 104 (23.6)
Mild (E1), n (%) 11 (12.4) 10 (8.8) 19 (8.0) 40 (9.1)
Mucopurulent (E2), n (%) 7 (7.7) 7 (6.1) 6 (2.5) 20 (4.5)
Purulent (E3), n (%) 16 (18.0) 8 (7.0) 7 (2.9) 31 (7.0)
Endometritis with fluid in uterus (E4), n (%) 6 (6.7) 4 (3.5) 3 (1.3) 13 (3.0)
E1, almost clear mucus with some flecks of pus; E2, mucopurulent discharge; E3, purulent discharge; and E4, purulent or mucopurulent discharge on
vaginoscopy and fluid in uterus detected by transrectal palpation.* Postpartum endometritis was diagnosed based on vaginoscopic and transrectal palpation findings at first postpartum examination.
endometritis, those with persistence of endometritis,
and those with new diagnosis of endometritis were
compared by Cox’s proportional hazards regression
analysis as above, accounting (if significant) for the
effects of herd, season of calving, parity, and BCS at
first postpartum examination. Likewise, the odds ratios
of pregnancy proportions by 210 d postpartum among
these four categories were compared by multiple
logistic regression model as above, accounting (if
significant) for the effects of herd, season of calving,
parity, and BCS at first postpartum examination.
3. Results
In total, 441 lactations were examined for endome-
tritis, of which 104 (23.6%) had postpartum endome-
tritis (i.e., endometritis within Day 60), with 9.1% mild
(E1), 4.5% mucopurulent (E2), 7.0% purulent (E3)
endometritis, and 3.0% endometritis with fluid in the
uterus (E4). The prevalence of endometritis during the
early (15 to 20 d), intermediate (21 to 28 d), and late (29
Table 2
Odds ratios of the variables included in the final logistic regression model for
cows.
Factor Class Endometriti
n
Herd
Type of calving Normal 82/381
Abnormal 22/60
Retention of fetal membranes No 83/398
Yes 21/43
Early postpartum complications* No 84/387
Yes 20/54
Postpartum interval at examination, d 15 to 20 40/89
21 to 28 29/114
29 to 60 35/238
*Early postpartum complications included any one or more of the followin
lameness, or clinical mastitis before or at the first postpartum examination
to 60 d) postpartum periods was 44.9%, 25.4%, and
14.7%, respectively (Table 1). Cows diagnosed with
clinical endometritis during Days 15 to 20 became
pregnant at a slower rate (HR = 0.60; 95% CI 0.36 to
0.98; P = 0.04) compared with that of those with no
clinical endometritis during this period. When the
endometritis status during Days 15 to 20 was substituted
by the degrees of endometritis in the model, the
respective HRs for pregnancy were 1.33 (95% CI, 0.64
to 2.77; P = 0.44), 0.29 (95% CI, 0.10 to 0.98; P = 0.05),
0.59 (95% CI, 0.31 to 1.12; P = 0.10), and 0.27 (95% CI,
0.10 to 0.91; P = 0.03) for E1, E2, E3, and E4,
respectively. No other factors remained in the final
model. Likewise, cows diagnosed with clinical endo-
metritis during Days 15 to 20 were 0.32 times less likely
to become pregnant by 210 d postpartum (66.7% vs.
86.1%; OR, 0.32; 95% CI, 0.11 to 1.00; P = 0.05)
compared with those with no clinical endometritis
during this period.
Logistic regression analysis for the risk of post-
partum endometritis indicated no significant effects of
the risk of postpartum endometritis (during Days 15 to 60) in Holstein
s (15–60 d) OR 95% CI P value
Percentage, %
0.01
21.5 Reference
36.4 2.20 1.08–4.46 0.03
20.8 Reference
48.8 3.48 1.65–7.37 0.001
21.7 Reference
37.0 2.29 1.08–4.46 0.02
44.9 6.33 3.47–11.57 <0.001
25.4 2.21 1.23–3.98 0.008
14.7 Reference
g: puerperal metritis, hypocalcemia, abomasal displacement, ketosis,
.
G. Gautam et al. / Theriogenology 73 (2010) 168–179 173
Table 3
Frequency distribution for varying degrees of postpartum endometritis diagnosed during various periods in dairy cows and their spontaneous
recovery or persistency during the latter (Days 61 to 150) postpartum period.
Diagnosis at first postpartum examination Endometritis status during
Days 61 to 150, n (%)
Postpartum interval at
first examination (d)
Degree of postpartum
endometritis*
Number of
cowsyNo Yes
15–20 (Early) E1 10 9 1
E2 6 4 2
E3 16 12 4
E4 5 5 0
Total 37 30 (81.0) 7 (19.0)
21–28 (Intermediate) E1 10 8 2
E2 5 3 2
E3 5 4 1
E4 2 1 1
Total 22 16 (72.7) 6 (27.3)
29–60 (Late) E1 19 16 3
E2 5 3 2
E3 6 2 4
E4 2 1 1
Total 32 22 (68.8) 10 (31.2)
Overall 91 68 (74.7) 23 (25.3)
*For definition, see Table 1.yCows treated for endometritis (n = 10) and those culled before having two examinations beyond Day 60 (n = 3) were not included.
parity, season of calving, BCS at first postpartum
examination, and urovagina within Day 60. Variables
that significantly increased the risk of diagnosing
postpartum endometritis were herd, type of calving,
RFM, early postpartum complications, and postpartum
interval at examination (Table 2). There were no
significant interactions (P > 0.1).
Table 4
Odds ratios of the variables included in the final logistic regression model fo
Holstein cows.
Factor Class Persistence o
n*
Season of calving Autumn 3/21
Winter 7/23
Spring 1/18
Summer 12/29
Early postpartum complications No 15/72
Yes 8/19
Urovagina No 8/54
Mild 3/15
Moderate 7/14
Severe 5/8
Endometritis during Days 15 to 60y E1 6/39
E2 6/16
E3 9/27
E4 2/9
*Cows treated for endometritis (n = 10) and those culled before having twoyFor definition, see Table 1.
Of 104 cattle with postpartum endometritis, 10 were
treated for endometritis within Day 60, and three were
culled before having two examinations beyond Day 60.
Thus, 91 cattle remained for the analysis of persistence
or spontaneous recovery of endometritis. Of 91 cows
with postpartum endometritis, 68 (74.7%) recovered
spontaneously, and 23 (25.3%) had persistence of
r the risk of persistence or recurrence of postpartum endometritis in 91
f endometritis OR 95% CI P value
Percentage, %
14.3 Reference
30.4 1.69 0.22–13.03 0.61
5.6 0.08 0.03–1.83 0.11
41.4 7.00 1.05–46.93 0.04
20.8 Reference
42.1 6.58 0.90–48.46 0.05
14.8 Reference
20.0 1.65 0.26–10.30 0.59
50.0 4.03 0.83–19.69 0.08
62.5 30.99 2.91–330.09 0.004
15.4 Reference
37.5 9.54 1.33–67.02 0.02
33.3 5.70 1.11–30.78 0.04
22.2 0.70 0.05–9.66 0.78
examinations beyond Day 60 (n = 3) were not included in the model.
G. Gautam et al. / Theriogenology 73 (2010) 168–179174
Table 5
Odds ratios of the variables included in the final logistic regression model for the risk of new diagnosis of endometritis (during Days 61 to 150)
among cows that had no endometritis within 60 d postpartum.
Factor Class New diagnosis of endometritis
(61–150 d)
OR 95% CI P value
n* Percentage, %
Early postpartum complications No 26/297 8.8 Reference
Yes 9/34 26.5 2.82 1.11–7.18 0.03
Urovagina No 18/263 6.8 Reference
Mild 4/32 12.5 1.84 0.57–5.90 0.30
Moderate 8/26 30.8 5.00 1.85–13.49 0.001
Severe 5/10 50.0 12.63 3.26–48.86 <0.001
*Cows having postpartum endometritis during Days 15 to 60 (n = 104), and those culled before having two examinations beyond Day 60 (n = 6)
were not included in the model.
Fig. 1. Survival curves derived from final Cox’s proportional hazards
regression analysis (adjusted for the effects of herd, season of calving,
and BCS at first postpartum examination) for proportion of nonpreg-
nant dairy cows against days postpartum in cows with no endometritis
until Day 150, cows with spontaneous recovery of endometritis, cows
with persistence or recurrence of endometritis, and cows with a new
diagnosis of endometritis during Days 61 to 150.
endometritis during Days 61 to 150 (Table 3). Among
91 cows with postpartum endometritis, 76 (83.5%) cows
had no abnormal vaginal discharge on the second
postpartum examination. However, 8 of these 76 cows
had an abnormal discharge again on subsequent
examinations.
Logistic regression analysis for the risk of persis-
tence of endometritis during Days 61 to 150 indicated
no significant effects of herd, parity, type of calving,
RFM, BCS at first postpartum examination, BCS at first
examination beyond Day 60, BCS change, postpartum
interval at examination, and the terms of interactions
between degree of endometritis and postpartum interval
at examination. Calving in summer season, early
postpartum complications, moderate and severe degrees
of urovagina, and mucopurulent and purulent endome-
tritis within Day 60 were significant risk factors for the
persistence of endometritis (Table 4). No significant
interactions were found between significant covariates
and degree of endometritis within Day 60 (P> 0.1). The
proportion of persistency was not influenced by the
periods postpartum at diagnosis of endometritis; that is,
whether postpartum endometritis was diagnosed during
Days 15 to 20, during Days 21 to 28, or during Days 29
to 60 (19.0%, 27.3%, and 31.2%, respectively; P = 0.49;
Table 3).
Likewise, among 337 lactations with no signs of
postpartum endometritis, six were culled before having
two examinations beyond Day 60. Of the remaining 331
lactations with no postpartum endometritis, 35 (10.6%)
had a new diagnosis of endometritis during Days 61 to
150. Logistic regression analysis for the risk of new
diagnosis of endometritis beyond Day 60 indicated no
significant effects of herd, season of calving, parity, type
of calving, RFM, BCS at first postpartum examination,
BCS at first examination beyond Day 60, and BCS
change. Early postpartum complications and the
moderate and the severe degrees of urovagina were
the significant risk factors for the new diagnosis of
endometritis during Days 61 to 150 (Table 5). There was
no significant interaction between postpartum compli-
cations and urovagina (P > 0.1).
Accounting for the effects of herd, season of calving,
and BCS at first postpartum examination (parity did not
remain in the final model), cows with the persistence of
endometritis and those with new diagnosis of endome-
tritis but not those recovered spontaneously became
pregnant at a slower rate compared with cows with no
clinical endometritis until Day 150 (Fig. 1 and Table 6).
Likewise, the pregnancy proportions by 210 d post-
partum in cows with persistence of endometritis
(40.0%; OR, 0.10; 95% CI, 0.05 to 0.22; P < 0.001)
G. Gautam et al. / Theriogenology 73 (2010) 168–179 175
Table 6
Final Cox’s proportional hazards regression models of clinical findings that were associated with time to conception (relative pregnancy rate) in
Holstein cows.
Categories n* HR pregnancyy 95% CI P value
No endometritis until Day 150 296 Reference
Spontaneous recovery of endometritis 68 0.89 0.66–1.20 0.43
Persistence or recurrence of endometritis 17 0.28 0.14– 0.53 <0.001
New diagnosis of endometritis (61–150 d) 35 0.44 0.28–0.70 <0.001
*Cows treated for endometritis (n = 16), and those culled before having two examinations beyond Day 60 (n = 9) were excluded from the analysis.yHazard ratio of pregnancy adjusted for the effects of herd, season of calving, and BCS at first postpartum examination.
and in those with a new diagnosis of endometritis during
Days 61 to 150 (53.1%; OR, 0.31; 95% CI, 0.14 to 0.68;
P = 0.004) but not in those that recovered spontaneously
(70.3%; OR, 0.65; 95% CI, 0.34 to 1.24; P = 0.19) were
lower compared with that in cows with no clinical
endometritis until Day 150 (78.3%).
4. Discussion
This study is one of the few reported trials that
conducted follow-up examinations of cows with
postpartum endometritis to determine the subsequent
fate of endometritis until or beyond the breeding period.
Although there are several reports on the prevalence of
postpartum endometritis, its impact on reproductive
performance, and risk factors for postpartum endome-
tritis [5,7–16], to our knowledge, the current study was
the first to investigate risk factors for persistence of
endometritis in Holstein cows. It is difficult to compare
the prevalence of postpartum endometritis with other
reports, due to differences in the methods of diagnosis,
postpartum periods at examination, and lack of
description of diagnostic methods in some studies
[29–31]. When comparing the prevalence rate with
other studies that examined the contents of vagina for
the presence of pus, the prevalence of postpartum
endometritis in this study seemed similar to those
reported by McDougall et al. [13] and Runciman et al.
[14] but slightly lower than some previously reported
rates [5,7,15,32] and higher than that reported by others
[24,33]. There are very few reported trials that
examined the cows prior to 3 wk postpartum using
vaginoscopy, due to concerns regarding diagnosing self-
resolving uterine infection. However, in the current
study, cows diagnosed with endometritis (but not mild
cases) even before 3 wk postpartum had detrimental
effects on future reproductive performance, which was
in agreement with our previous findings [7] and also
with some other reports [13,14,20]. This demonstrated
the usefulness of performing vaginoscopy even prior to
3 wk postpartum. Furthermore, it was also of interest to
determine whether the endometritis diagnosed before 3
wk postpartum had a greater tendency to recover
spontaneously than that diagnosed during later post-
partum periods; however, it was not verified from this
study. It was the degree of endometritis rather than the
postpartum interval at diagnosis of endometritis that
influenced the recovery or persistency of endometritis.
The prevalence of postpartum endometritis in this
study was significantly associated with herd, abnormal
calving, RFM, early postpartum complications, and the
postpartum interval at examination. The increased
incidence of postpartum endometritis with abnormal
calving was consistent with some previous studies
[14,29,30,34,35] but in contrast with others [5,7,16].
Likewise, the increased risk of postpartum endometritis
in cows with RFM was consistent with most previous
studies [5,7,14,16,34]. Abnormal calving and RFM may
serve as a perfect medium for bacterial growth and
thereby increase the susceptibility for uterine diseases.
In the current study, early postpartum complications
increased the risk of postpartum endometritis, which
was consistent with the findings of previous studies that
demonstrated the increased risk of endometritis in cows
with postpartum metabolic disorders [16,29,30,36].
Because of the small number of cows with each
complication, and assuming that each might interfere
with immunity, and therefore ability of the animal to
clear uterine contamination, we combined all these
complications to form ‘‘early postpartum complica-
tions.’’ Similarly, the risk of diagnosing postpartum
endometritis decreased with the time postpartum, which
was in agreement with McDougall et al. [13] and also in
agreement with previous bacteriologic studies demon-
strating that the prevalence of uterine infection declines
with the time postpartum [12,37–40].
Approximately three quarters of the cows with
postpartum endometritis in this study had spontaneous
clinical recovery, whereas the remainder had persis-
tence or recurrence of infection until or beyond the
breeding period. It was not known whether these cases
were the persistence or recurrence of endometritis.
G. Gautam et al. / Theriogenology 73 (2010) 168–179176
Therefore, we simply used the term ‘‘persistence’’ to
include both cases. If clinical resolution had been
considered only on the basis of second examination,
83.5% of cows with postpartum endometritis would
have been classified as spontaneously recovered.
However, 8 (9%) of 91 cows with postpartum
endometritis that had no abnormal discharge on second
examination showed signs of clinical endometritis again
on subsequent examinations. Therefore, we decided to
define spontaneous recovery based on at least two
examinations during the breeding period. The diagnosis
of endometritis in this study was based only on clinical
findings. In the absence of clinical signs of endometritis,
a substantial proportion (up to 50%) of cows had
subclinical endometritis during the postpartum period
that impaired the subsequent reproductive performance
[8–10]. The cytologic criteria for diagnosis of
subclinical endometritis continue to be refined
[10,11,41]. Although the endometrial histology or
cytology for the diagnosis of endometritis was beyond
the scope of this study, we inferred that several
vaginoscopic examinations increased the accuracy of
our criteria of classifying cows into spontaneous
recovery or no endometritis until Day 150. Moreover,
the spontaneous recovery defined here was later
validated by the lack of difference in pregnancy rates
between cows with spontaneous recovery and those
with no endometritis until Day 150. Conversely, cows
with persistence of endometritis had poorer reproduc-
tive performance compared with those with no
endometritis until Day 150. Therefore, we inferred
that cows failing to resolve uterine infection suffer more
detrimental reproductive consequences than those that
resolve uterine infection. It can be assumed that the
persistence of endometritis left alternations in the
uterine lining and decreased the ability of cows to
conceive, and thus reduced reproductive performance.
Cows calving in summer were seven times more likely
to persist with endometritis beyond Day 60 than those
calving in autumn. Roman-Ponce et al. [42] reported that
uterine blood flow was reduced in cows exposed to heat
stress. Because of less blood flow to the uterus, fewer
leukocytes are moved to the endometrium; this may
compromise the clearance of uterine infection, leading to
the persistence of endometritis. Moreover, overall
immune status of cows decreased by the stress of calving
might be further exacerbated during heat stress and could
contribute to the persistence of endometritis. Postpartum
complications continued to be the risk factor for the
persistence of endometritis. Early postpartum complica-
tions might have interfered with immunity and therefore
the ability to clear a uterine infection and thus might have
contributed to its persistence for a prolonged period.
Likewise, cows with moderate and severe degrees of
urovagina were 4 and 31 times more likely, respectively,
to have persistence of endometritis compared with cows
with no urovagina. Cows with signs of postpartum
endometritis (a purulent cervical discharge) usually have
a relaxed cervix, which may allow the entry of
contaminated urine into the uterus in cows with
‘‘moderate’’ and ‘‘severe’’ degrees of urovagina, and
this may lead to the persistence of endometritis.
Similarly, persistence of postpartum endometritis
depended on its severity. Mucopurulent and purulent
endometritis were nine and six times, respectively, more
likely to persist compared with mild endometritis.
Perhaps uterine inflammation in case of mucopurulent
and purulent endometritis may reach a level of severity
where spontaneous recovery of uterine tissue is less
likely. Conversely, most cases of mild endometritis
recovered spontaneously. We concluded that the self-
healing capacity of the uterus in case of mild
endometritis was very high. This might explain previous
reports in which severe degrees of endometritis, but not
mild endometritis, had a clear negative effect on fertility
[5,7,24,36]. However, due to the small number of cows
with endometritis with fluid in the uterus (E4), this
category might not have shown the significant effect on
persistence or recovery of the infection; and this needs
to be confirmed by further study using a large number of
cows. Thus, cows with purulent or mucopurulent
discharge on vaginoscopy during Days 15 to 60 may
be defined as ‘‘clinically relevant endometritis.’’ Based
on the outcome of the current and previous studies, we
concluded that cows with severe endometritis before the
breeding period need to be treated, provided the therapy
is known to improve the fertility of affected cows,
whereas in mild cases, the self-healing potential is very
high, and the affected cows show good reproductive
efficiency without treatment, as long as they do not have
postpartum complications or a moderate or severe
degree of urovagina.
There are very few ‘‘reported’’ trials that examined
cows vaginoscopically during the breeding period
(beyond Day 60). In this study, 10.6% of cows that
did not show the signs of postpartum endometritis had a
new diagnosis of endometritis during the breeding
period. Drillich et al. [43] also found that among the
cows that had no endometritis during 21 to 27 d
postpartum, approximately 5% of cows showed signs of
endometritis during 68 to 74 d postpartum. Cows with a
new diagnosis of endometritis clearly had poorer
reproductive performance compared with cows with
no endometritis until Day 150.
G. Gautam et al. / Theriogenology 73 (2010) 168–179 177
Among the cows without signs of clinical endome-
tritis within Day 60, early postpartum complications
and moderate and severe degrees of urovagina were risk
factors for the new diagnosis of endometritis beyond
Day 60. Perhaps cows with a new diagnosis of
endometritis had subclinical endometritis within Day
60, and because of poor immunity (due to early
postpartum complications and/or other factors) the
infection persisted and was clinically apparent during
the later postpartum period. However, the diagnosis of
subclinical endometritis was beyond the scope of this
study, and thus, these results should not be over-
estimated. Likewise, it was not fully known whether the
new diagnoses of endometritis were really new
infections or were the persistent cases that might not
have shown abnormal discharge within Day 60 because
of luteal phases of estrus cycle in some of the cows
during examination. Although assessment of vaginal
contents for the presence of pus is the most useful and
practical method for the diagnosis of endometritis [3], a
single vaginoscopic examination may miss up to 9% of
cows with uterine discharge [10]. Increased production
of cervical mucus and myometrial contractions during
estrus may increase the probability of observing
discharge externally or in the anterior vagina. Alter-
natively, uterine discharge may not be detected
externally or by vaginoscopy in cows in which the
cervix is closed. Therefore, it is recommended to
perform at least two vaginoscopic examinations at a 2-
to 4-wk interval before the breeding period to detect
cases of clinical endometritis.
Among cows without signs of endometritis within
Day 60, the prevalence of new endometritis (during Days
61 to 150) was significantly higher in cows with moderate
and severe degrees of urovagina but not in cows with mild
urovagina compared with that in cows with no urovagina,
which was similar to the findings of our previous study
[26]. Moderate and severe degrees of urovagina, defined
here, would have a higher risk of urine entering into the
uterus and might have caused chronic endometritis and
infertility [26,44,45]. Thus, similar to our previous study
[26], moderate and severe degrees of urovagina can be
considered as ‘‘clinically relevant urovagina.’’ The
prevalence of urovagina in this study (24%, 11%, 9%,
and 4% for overall, mild, moderate, and severe,
respectively) was consistent with our previous study
[26] that also used cows from the same herds. The reason
for the high prevalence of urovagina in these herds was
not known, although no other published reports were
available regarding the prevalence of urovagina in dairy
cows, and it was difficult to conclude whether this
prevalence rate was high.
The clinically relevant urovagina in this study
(prevalence, 13%) appeared to be one of the main
predisposing factors for the prevalence of endometritis
during the breeding period. Likewise, the competence
of the immune system may be one of the major
differences among cows that have spontaneous recov-
ery, persistence, or a new diagnosis of endometritis, and
postpartum complications might be one of the factors to
compromise the immune function of postpartum cows.
Neutrophil function was impaired in cows that develop
uterine infection [46–49]. However, it is still not known
whether there are any differences in neutrophil
functions between cows that recover uterine infection
spontaneously and those that have persistence of
infection, and therefore further study is recommended.
In conclusion, the prevalence of postpartum endo-
metritis in this study was 23.6%. Approximately three
quarters of cows with postpartum endometritis had
spontaneous clinical resolution, whereas the remainder
had persistence of clinical endometritis until or beyond
the breeding period, leading to poor reproductive
performance. Calving in summer season, early post-
partum complications, ‘‘clinically relevant urovagina,’’
and ‘‘clinically relevant endometritis’’ within 60 d
postpartum were risk factors for persistence of
endometritis. Furthermore, approximately 10% of cows
that did not show the signs of endometritis within 60 d
postpartum had a new diagnosis of endometritis beyond
60 d postpartum; some risk factors for the new diagnosis
of endometritis beyond 60 d postpartum were early
postpartum complications and ‘‘clinically relevant
urovagina.’’
Acknowledgments
The first author was supported by the Monbukaga-
kusho Scholarship of Japan for PhD study, and the
authors are thankful to the Ministry of Education,
Culture, Sports, Science and Technology of Japan for
financial support. The authors thank Mr. Nguyen Cong
Thinh and Ms. Naoko Mitsui for their help during
clinical examination and in collecting data. Our sincere
thanks are due to the herd owners involved in this study
for their cooperation.
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