Trop Anim Health Prod (2014) 46:1435–1439
DOI 10.1007/s11250-014-0661-y
REGULAR ARTICLES
Incidence of subclinical endometritis and its effects
on reproductive performance of crossbred dairy cows
Luisa Cunha Carneiro & Adolfo Firmo Ferreira &
Mariana Padua & João Paulo Saut &
Antonio Sergio Ferraudo & Ricarda Maria dos Santos
Received: 7 November 2013 / Accepted: 19 August 2014 / Published online: 4 September 2014
# Springer Science+Business Media Dordrecht 2014
Abstract In dairy cattle, uterine infections are not life threat-
ening and often unavoidable; however, they reduce fertility
and increase the production costs of properties. The aim of this
study was to evaluate the incidence of subclinical endometritis
from 32 to 70 days in milk (DIM) and its effects on the
reproductive performance of crossbred dairy cows. Lactating
cows (Holstein/Gir; n=172), with no history of retained pla-
centa, without clinical signs of uterine infection were used.
The body condition score (BCS) was evaluated on a scale
from 1 to 5. Ultrasound examination was performed to eval-
uate uterine lining and ovarian activity, while vaginal mucus
was analyzed by gloved hand. The diagnosis of subclinical
endometritis was performed by endometrial cytobrush tech-
nique. The samples were collected, stained, and examined
microscopically; positive cases for subclinical endometritis
were considered with the presence of ≥5 % of neutrophils.
Later, the cows were submitted to conventional artificial in-
semination or timed artificial insemination. The incidence of
subclinical endometritis in the herd was 26 %, and this was not
affected by the season of calving, presence of corpus luteum,
DIM, and parity. Cows with a BCS ≤2.50 had a higher
incidence of subclinical endometritis. The conception rate to
first insemination and pregnancy rate at 150 days postpartum
L. C. Carneiro (*)
Faculty of Agricultural Sciences and Veterinary, UNESP, 1270,
Machado de Assis St, Uberlândia, Minas Gerais 38400112, Brazil
e-mail: luisacunhacarneiro@hotmail.com
A. F. Ferreira : M. Padua : J. P. Saut : R. M. dos Santos
Faculty of Veterinary Medicine, Federal University of Uberlandia,
3637, República do Piratini St, Uberlândia, Minas Gerais 38402028,
Brazil
A. S. Ferraudo
Faculty of Agricultural Sciences and Veterinary, UNESP, Jaboticabal,
SP 14884-900, Brazil
were not influenced by the presence of subclinical endometri-
tis in crossbred dairy cows.
Keywords Cytobrush . Neutrophils . Uterine infection .
Reproduction
Introduction
In dairy cows, after the voluntary waiting period, the repro-
ductive performance depends on many factors, such as body
condition score (BCS), heat detection, insemination tech-
nique, semen quality, and uterine health (Noakes et al.
2002). The resumption of ovarian cyclicity is one of the most
important events for dairy cows to recover to their reproduc-
tive potential (Kaneko and Kawakami 2009).
Within the postpartum period, the uterus tolerates the
growth of lots of bacteria, such as aerobic and anaerobic.
The proportion of infected animals or uterine bacterial amount
usually increases between the seventh and 14th day postpar-
tum. This observation leads to the assumption that there is not
only a bacterial contamination during postpartum that is re-
sponsible for uterine problems (Sheldon 2004).
During 4 weeks after parturition, the cows immune system
is extremely challenged, most of the cows in the early post-
partum period develop a non-pathological endometritis, and
the lochia and placenta are usually eliminated by the second
week postpartum (Thatcher et al. 2006).
About 35 % of dairy cows may be clinically affect in the
first 21 days postpartum (metritis), and approximately 10–
20 % will remain infected or develop endometritis (Borsberry
and Dobson 1989; McDougall et al. 2007; Sheldon et al.
2009).
Inflammatory and endometrial cells can be collected by
swab, in order to diagnose the presence of a subclinical
endometritis, uterine biopsy (most common in mares), uterine
1436
lavage, or by cytobrush technique (Kasimanickam et al.
2005). Barlund et al. (2008) stated that cytobrush technique
is a useful tool and it is considered the most reliable test.
Subclinical endometritis is most commonly diagnosed by
uterine cytology and affects about 35–50 % of cows between
35 and 60 days in milk (DIM) and is associated with a
reduction in pregnancy rate, increase in time to conception
(30–88 days), and increase in 20 % of cows that are not
pregnant by 300 DIM (Kasimanickam et al. 2004; Gilbert
et al. 2005).
Some important economic losses are caused by uterine
infections in dairy farms, since they increase calving interval,
number of artificial insemination (AI) per conception, culling
rate and decrease milk production (Fourichon et al. 2000;
Drillich et al. 2005).
Based on this information, the aim of this study was to
evaluate the incidence of subclinical endometritis between 32
and 70 days postpartum and their effects on the reproductive
performance of crossbred dairy cows.
Materials and methods
The study was submitted to the Ethics Committee on Animal
Use at the Federal University of Uberlandia and subsequently
approved (082/11) for this experiment.
All data were collected on a commercial dairy farm, located
in Centralina, Minas Gerais, Brazil, from April 2010 to June
2011. For this experiment, 172 crossbred dairy cows (Hol-
stein/Gir) were used. All the cows were lactating milked twice
daily (average 17 kg milk/day). During winter, the cows were
fed with corn or sorghum silage, and during summer, they
were managed in rotational grazing system, properly sup-
plemented with concentrate, mineral salt, and access to
water ad libitum. The cows were not subjected to any type
of environmental control (ventilation, heating, cooling, or
others). The animal zoonotic calendar was regularly
followed to all the state laws for dairy herd (recommended
vaccination and vermifugation in accordance to the state
law was performed).
Only animals that did not have a history of retained pla-
centa, puerperal metritis, or other diseases that required anti-
biotic treatment before collecting uterine material were select-
ed. All animals with clinical uterine infection were excluded
from the study, based on the presence of a muco-purulent
vaginal discharge or the presence of echogenic contents in
the uterus during ultrasound examination (Emperor-Vet ®
820) (adapted from LeBlanc et al. 2002a).
Reproductive data and endometrial cytology samples were
collected between 32 and 70 days postpartum. The BCS was
evaluated (scale of 1—very thin to 5—obese; Ferguson et al.
1994). To evaluate the characteristics of the uterine wall,
Trop Anim Health Prod (2014) 46:1435–1439
ovarian activity, follicles and/or corpus luteum (CL), an ultra-
sound examination was performed.
The uterine mucus was evaluated by gloved hand accord-
ing to Pleticha et al. (2009) and classified as follows: grade 0
(no discharge), grade 1 (clear mucus), grade 2 (mucus with
pus flakes), grade 3 (mucopurulent discharge), grade 4 (puru-
lent discharge), and grade 5 (fetid purulent discharge)
(adapted from McDougall et al. 2007).
The method selected to diagnose subclinical endometritis
was the cytobrush technique, where a gynecologic modified
sterile brush was introduced into the uterine body through the
vagina then turned approximately one quarter turn to obtain
cellular material from the endometrium. This method was
used only in animals with clear mucus (without clinical uter-
ine infection).
After sample collection, the slides were identified (animal
number, date of collection, and property) and prepared by
rolling the cytobrush with the collected material on a clean
microscope slide. The slides were air-dried and transported to
the laboratory to be stained by May-Grunwald-Giemsa meth-
od (Vallada 1999) and subsequently subjected to a microscop-
ic evaluation.
The microscopic evaluation was based on the number of
neutrophils present in each slide. Two independent observers
counted 200 cells under a microscope (Olympus®, CHT-2
Optical Co. Ltd, Japan) by ×400 magnification in each blade.
The cells were classified into epithelial cells, polymorphonu-
clear cells (neutrophils), large mononuclear cells (presumed to
be macrophages), and small mononuclear cells (presumed to
be lymphocytes). Subclinical endometritis was defined as
being positive in all those animals that had more than 5 % of
neutrophils in each slide (Gilbert et al. 2005).
After evaluation and material collection, the cows were
submitted to a reproductive management program. This
consisted in a conventional artificial insemination (AI) or
timed artificial insemination (TAI). The TAI protocol
consisted of the following: day (D) 0: intramuscular injection
of 2.0 mg estradiol benzoate (2.0 mL Estrogin®, Farmavet)
and insertion of a progesterone (P4) device with 1.9 g of P4
(CIDR®, Zoetis Animal Health); D7: intramuscular injection
of 12.5 mg diniprost tromethamine, PGF2a analog (2.5 mL
Lutalyse®, Zoetis Animal Health); D9: P4 device removal and
muscular injection of 0.5 mg of estradiol cypionate (0.5 mL of
ECP®, Zoetis Animal Health); D11: TAI (adapted from
Meneghetti et al. 2006). All animals were inseminated with
previously analyzed semen.
Pregnancy diagnosis was performed by ultrasound (Emperor
820-Vet®) 28 days after artificial insemination technique was
fulfilled. All cows that showed embryo with heartbeat was
considered to be pregnant. Forty five days after insemination,
pregnancy diagnosis was confirmed by rectal palpation.
The effects of season of calving (spring/summer versus
fall/winter), BCS, presence of CL, DIM at the time of
Trop Anim Health Prod (2014) 46:1435–1439 1437

collection, and parity (first versus second versus third or more
lactations) on the incidence of subclinical endometritis were
analyzed by logistic regression (Proc Logistic of SAS). The
effect of subclinical endometritis on conception rate to first AI
and pregnancy rate at 150 days postpartum was analyzed by
log-rank test by Statistic program, where survival analyses
curves were made. Differences detected at P≤0.05 were con-
sidered significant.
The presence of subclinical endometritis did not affect
conception rate at first AI (P > 0.05). Pregnancy rate at
150 days postpartum was analyzed, and there was no signif-
icant difference (P>0.05) between cows with subclinical en-
dometritis and those without subclinical endometritis (Fig. 1).
Discussion

The prevalence of subclinical endometritis is quite variable

among herds. The diagnosis of endometritis is herd-specific
Results and depends on the sensitivity and specificity of the diagnostic
method. The average of subclinical endometritis in this study
The prevalence of subclinical endometritis in crossbred dairy was 26 %, while Madoz et al. (2013) studied the prevalence of
cows at 32 and 70 DIM in this experiment was 26 % (44/172), subclinical endometritis in grazing dairy cows at 21 to
and the results are summarized in Table 1. Season (spring/ 62 DIM, with 5 % of PMN, and found an average around
autumn versus summer/winter) had no effect on the incidence 17 %. Although a shorter prevalence of subclinical endome-
of subclinical endometritis (P>0.05). Cows with BCS ≤2.50 tritis was reported by these researchers, endometritis diagnosis
showed a higher incidence of subclinical endometritis was performed in the same method (cytobrush technique).
(32.43 %) compared with those with BCS ≥2.75 (16.39 %) Barlund et al. (2008) also found a lower incidence than
(P<0.05). In this work, the presence or absence of CL had no observed in this study. They evaluated 189 dairy cows at 28–
effect on the incidence of subclinical endometritis (P>0.05). 41 days postpartum using the cytobrush technique and ob-
In this experiment, the interval between calving and material served that only 11.1 % had more than 8 % of polymorpho-
collection had no effect on the incidence of subclinical endo- nuclear cells as classified positive for subclinical endometritis.
metritis, even if these evaluations ranged from 32 to 70 days Still, a lower incidence was reported by Dubuc et al. (2010)
postpartum (fifth and tenth week). Parity (first versus second that evaluated 1,295 dairy cows at 35 days postpartum and
versus third or more) did not affect the incidence of subclinical found 18.7 % of cows positive for subclinical endometritis
endometritis (P>0.05). (considering positive those with ≥6 % neutrophils on endo-
metrial samples).
Kasimanickam et al. (2004) also used the cytobrush meth-
Table 1 Effects of season, body condition score, presence of corpus
luteum, days postpartum, and parity on the incidence of subclinical od as a diagnostic in cows around 20–33 days postpartum.
endometritis in crossbred dairy cows, Centralina-MG They found 37 % of cows positive for cytology endometritis;
however, they considered those cows with more than 18 % of
Variable Incidence of subclinical P value
endometritis %
neutrophils in each sample positive. They also related that the
incidence of subclinical endometritis at 20–33 and 34–47 days
Season postpartum in 228 dairy cows was not influenced by season,
Spring/summer 32.35 (22/68) 0.176 as in this study.
Fall/winter 23.08 (24/104) It was expected that those cows that calved in summer had
Body condition score a higher rate of subclinical endometritis than those that calved
≤2.50 32.43 (36/111) 0.025 in winter, due to increased stress and greater challenge of
≥2.75 16.39 (10/61)
environmental contamination; however, no effect of season
Presence of corpus luteum on the incidence of subclinical endometritis was reported in
Without corpus luteum 33.33 (21/63) 0.146 this experiment (P>0.05). On a study conducted by Senosy
With corpus luteum 22.94 (25/109)
and Osawa (2013), no influence of season on the incidence of
Days postpartum
subclinical endometritis was reported, while there was an
30–39 days 27.59 (08/29) 0.560
40–49 days 28.00 (21/75) effect on the PMN% on positive animals diagnosed between
50–59 days 27.66 (13/47)
the hot season and the temperate season.
More than 60 days 19.05 (04/21)
In this study, it was observed that cows with a BCS ≤2.50
Parity
showed higher prevalence of subclinical endometritis
(P<0.05) than those cows with BCS ≥2.75. In a study con-
First 33.33 (13/39) 0.097
Second 33.33 (14/42) ducted by Priest et al. (2013), they also found a lower BCS in
Third or more 20.88 (19/91) cows with subclinical endometritis, when compared to those
without it. In some studies conducted by Bacha and Regassa
1438
Fig. 1 Survival curves for non-
pregnant cows (%) related to days
after parturition, in a dairy herd of
172 Holstein cows, according to
NON-PREGNANT COWS
the presence (POSITIVE) or ab-
sence (NEGATIVE) of subclinical
endometritis
(2009), the BCS also had an effect on the occurrence of sub-
clinical endometritis when evaluated during 4 weeks after par-
turition. They found that 64.5 % of the cows with a BCS ≤2.50
had subclinical endometritis, and in those cows with a BCS
≥2.50, only 28.6 % was positive for subclinical endometritis.
According to Dubuc et al. (2010), more cows had subclin-
ical endometritis when their BCS was lower than 2.75. Also,
Dubuc et al. (2011) in another study observed that cows with a
BCS less than 2.75 were more likely to develop any kind
of uterine disease.
Roche et al. (2013) in their studies about BCS during
calving, observed that cows with low and medium BCS had
proportionately more polymorphonucleated cells in their uter-
ine secretions at 3 and 5 weeks postpartum than those with
high BCS, indicating that both low and medium BCS at
calving will increase the risk of uterine disease.
Williams et al. (2005) concluded that uterine infection also
affects ovarian function; however, in this work, the presence
or absence of CL had no effect on the incidence of subclinical
endometritis. In a study conducted by Burke et al. (2010),
using the endometrial cytobrush technique, noticed that cyclic
cows diagnosed with low amounts of PMN cells ovulated
early (between 63 and 70 days postpartum) when compared
with those with high levels of these cells, which took longer to
ovulate. It is important to notice that the presence of CL affects
the recovery of the uterus after parturition, directly interfering
in the future reproductive performance.
According to Gilbert et al. (2005), cows parity did not
influence the prevalence of endometritis, as showed in this
study. However, LeBlanc et al. (2002b) reported that endo-
metritis was more prevalent in mature cows (in their third or
more lactations) than in those in the first and second lactation.
Bacha and Regassa (2009) observed that the number of
cows with subclinical endometritis decreased in the eighth
week postpartum when compared with the fourth week post-
partum. They found a total of 18 positive cows in the fourth
week postpartum and 13 of them remained being positive in
the eighth week. This indicated that cows that had uterine
infection during the fourth week postpartum had twice risk of
Trop Anim Health Prod (2014) 46:1435–1439
Cumulative Proportion Surviving (Kaplan-Meier)
100%
90%
80%
70%
60%
50%
40%
30%
20%
10% NEGATIVE
POSITIVE
0%
20 40 60 80 100 120 140
DAYS AFTER PARTURITION
uterine infection during the eighth week after parturition when
compared to those cows with a healthy uterus.
In a study with 201 milk cows, Kaufmann et al. (2009)
considered positive for subclinical endometritis cows with
more than 15 % of PMN cells in samples collected after AI
around 65 days postpartum and reported a conception rate at
first AI of 43.3 % for all cows examined by cytobrush tech-
nique; also, those cows with 0–15 % of neutrophils in endo-
metrial samples or those negative for subclinical endometritis
had higher conception rate at first service when compared to
those with more than 15 % of neutrophils (positive for endo-
metrial cytological).
Madoz et al. (2013) found that subclinical endometritis
diagnosed at 21 to 62 DIM decreased the hazard for pregnan-
cy and increased the calving-to-conception interval by 30 days
compared with normal cows; also, Galvao et al. (2009) re-
ported that cows with subclinical endometritis had a reduction
of 26 % in pregnancy rate at 300 days of lactation, when
compared with those without subclinical endometritis, al-
though, in this study, the presence of subclinical endometritis
did not influence the pregnancy rate.
Furthermore, Gilbert et al. (2005) certified that the positive
diagnosis for subclinical endometritis decreased the propor-
tion of pregnant cows at 300 days postpartum when compared
with those cows negative for subclinical endometritis (63.0
versus 89.0 %, respectively). Also, Dubuc et al. (2011) dem-
onstrated that the presence of subclinical endometritis was a
key factor in pregnancy rate, with an increase up to 16 days in
days open.
The incidence of subclinical endometritis in crossbred
dairy cows in this study was 26 %. Calving season, presence
of corpus luteum, DIM, and parity did not affect the incidence
of subclinical endometritis, while cows with BCS ≤2.50 had a
higher incidence. The presence of subclinical endometritis did
not affect conception rate at first AI and pregnancy rate at
150 days postpartum in crossbred dairy cows.
Acknowledgments The authors acknowledge the Research Support
Foundation of Minas Gerais state, Brazil, for the financial support.
Trop Anim Health Prod (2014) 46:1435–1439
Conflict of interest The authors declare that they have no conflict of
interest. All authors gave their informed consent prior to their inclusion in
the study.
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