Prevalence of Cervicitis in Dairy Cows and Its Eff
Prevalence of Cervicitis in Dairy Cows and Its Eff
Prevalence of Cervicitis in Dairy Cows and Its Eff
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Theriogenology
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Article history: The objective of this study was to determine whether cervicitis in dairy cows is an inde-
Received 16 February 2015 pendent disease or occurs concomitantly with inflammation of the uterus, and to clarify
Received in revised form 9 September 2015 possible effects of cervicitis on reproductive performance. Dairy cows (n ¼ 416) from 33
Accepted 14 September 2015
dairy farms were examined by rectal palpation and vaginoscopy between 42 and 50 days
postpartum. Inclusion criteria for this study were absence of abnormal vaginal discharge
Keywords:
and abnormalities of the uterus (fluctuation) at rectal palpation. Cervicitis was diagnosed
Cervix uterus
when the second cervical fold was swollen and prolapsed with (C2) or without (C1)
Endometritis
Cattle reddening. Cytobrush samples from the uterus (n ¼ 370) and the cervix (n ¼ 402) were
collected, and the percentage of neutrophils in the uterus (PMNU) and the cervix as in-
dicators of inflammation (threshold: 5%) was determined. In addition, endometrial bi-
opsies for histology were collected, 300 of which were suitable for evaluation. Cervicitis
(C1/C2) was diagnosed in 253 of 416 (60.8%) of cows. Of these, the prolapsed cervical
mucosa was hyperemic (C2) in 29.1% of cases. Of 370 available uterine cytology samples,
221 cows had a clinical cervicitis; however, 170 (76.9%) had PMNU less than 5%. Of 300
uterine histologic examinations, 82 (27.3%) did not reveal any abnormalities; the
remaining cows either had uterine inflammation and/or degenerative uterine changes
such as endometriosis and angiosclerosis. Furthermore, of 300 biopsied animals, 184
revealed a cervicitis (C1/C2); however, 30.4% of these animals had no histopathologic
uterine findings. For further analysis, only animals either without histopathologic findings
and normal uterine cytology or with solely endometritis (defined as PMNU 5% and/or
positive histopathology of the uterine tissue) were evaluated (n ¼ 157). Of these, 95 cows
had cervicitis. Unexpectedly, 63 of 95 (66.3%) cows had cervicitis without endometritis.
With regard to reproductive performance, days to first service were not affected by
cervicitis. Number of days open in animals with cervicitis but without endometritis tended
to be lower than in cows with cervicitis plus endometritis (P ¼ 0.092). Also, number of
days open relative to percentage of neutrophils greater than 5% was lower when the
cervical compared to the uterine mucosa was affected (P < 0.05). Total conception and
pregnancy rates of animals 200 days into lactation decreased significantly in cows with
severe cervical inflammation (C2). In conclusion, the results of this study suggested that
cervicitis occurs independent of endometritis, and a higher degree of cervicitis is associ-
ated with poorer reproductive performance.
Ó 2015 Elsevier Inc. All rights reserved.
* Corresponding author. Tel.: þ44 7721 127522; fax: þ44 1296 340017.
E-mail address: desireehartmann@hampdenvets.co.uk (D. Hartmann).
0093-691X/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.theriogenology.2015.09.029
2 D. Hartmann et al. / Theriogenology xxx (2015) 1–7
Fig. 1. (A) Cervix without abnormality of the Portio vaginalis cervicis (C0). (B) Cervix in which the second cervical fold of the Portio vaginalis cervicis was swollen
and prolapsed without reddening (C1). (C) The second cervical fold of the Portio vaginalis cervicis was swollen and prolapsed with reddening (C2).
pregnant cows after first insemination: number of first Breslow–Gehan–Wilcoxon test. Differences were consid-
inseminations 100), total conception rate (number of ered statistically significant when P values were less than
pregnant animals: number of total insemination 100), or equal to 0.05. A value of P greater than 0.05 and less than
and total pregnancy rate up to 200 days into lactation 0.10 was considered a trend toward significance.
(number of pregnant animals 200 days into lactation:
number of inseminated animals) [13]. 3. Results
Statistical analysis was carried out using SAS (SAS Inst. Uterine size ranged between scores 1 and 4. In 32 of 416
Inc., version 9.1; Cary, NC, USA) and applying routine sta- (7.7%) cows, the uterus was retractable and horn diameter
tistical procedures [14]. Correlation coefficients were less than 2 cm (score 1), 247 of 416 (59.4%) had a uterine horn
determined with Pearson’s correlation coefficient (r). Re- diameter of 2 to 5 cm (score 2), and in 135 of 416 (32.4%), horn
sults with positive or negative correlation coefficients of diameter was greater than 5 cm (score 3). Two animals (0.5%)
less than or equal to 0.20 were interpreted as low or no had a uterus that was not retractable but with the greater
correlation; between 0.21 and 0.50 as weak correlation; curvature palpable (score 4). Of 416 cows, 242 (58.2%) had a
between 0.51 and 0.80 as moderate correlation; and greater symmetrical uterus, whereas in 166 of 416 (39.9%) cows, a
than or equal to 0.81 as good correlation. Days to first slight uterine asymmetry and in 8 of 416 (1.9%), a medium to
service and number of days open with regard to cervicitis high asymmetry were found. No significant differences
were compared using Kruskal–Wallis one-way ANOVA. among the cervicitis groups relating to uterine size and
Frequencies of occurrence were calculated using the chi- symmetry of the uterine horns could be found.
square test. In cases of a small number of observations,
Fisher’s exact test was used. Number of days open related to 3.2. Vaginoscopy
cervical and uterine polymorphonuclear cells (PMN), as
well as cytology and histologic findings of the uterus In total, 163 of 416 (39.2%) cows had a cervix without
related to cervicitis, was plotted using Kaplan–Meier abnormality (C0). Cervicitis without reddening (C1) was
curves, and curves were compared using the Mantel–Cox or diagnosed in 132 of 416 (31.7%), and 121 of 416 (29.1%) cows
4 D. Hartmann et al. / Theriogenology xxx (2015) 1–7
Table 1
Frequency of polymorphonuclear leukocytes greater than or equal to 5% and less than 5% with regard to cervicitis rating.
Cervicitis rating Endometrial cytology (in %, n ¼ 370) Cervical cytology (in %, n ¼ 402)
Abbreviations: C0, cervix without abnormality; C1, swollen and prolapsed Portio vaginalis cervicis without reddening; C2, swollen and prolapsed Portio
vaginalis cervicis with reddening.
displayed cervicitis with reddening of the second cervical (Table 2). However, no significant associations could be
fold of the Portio vaginalis cervicis (C2). Six animals showed found between the occurrence of cervicitis and histopath-
reddening of the Portio vaginalis cervicis without a pro- ologic abnormalities of the uterine tissue, nor between
lapsed second cervical fold. These cases were assigned to endometritis and degenerative uterine diseases such as
group C2. Vaginal urine pooling was found in 10 cows; of endometriosis and angiosclerosis. Of 300 biopsied cows,
these, two had a normal cervix, two were evaluated as C1, 184 had cervicitis (C1/C2); remarkably, among these 184
and six as C2. animals, 56 (30.4%) had no uterine histopathologic
abnormalities.
3.3. Endometrial and cervical cytology
3.5. Uterine cytology and histology in relation to cervicitis
In all, 370 endometrial and 402 cervical cytology slides
were assessed successfully (Table 1). Altogether, 92 of 370 To analyze the relationship between uterine cytology
(24.9%) cows had PMN greater than or equal to 5%, and 278 and histology in relation to cervicitis, only animals with no
of 370 (75.1%) had PMN less than 5% in the uterus. In histopathologic findings and with solely histologic endo-
comparison, 46 of 402 (11.4%) had PMN greater than or metritis (without other pathologic endometrium findings)
equal to 5%, and 356 of 402 (88.6%) had PMN less than 5% in were evaluated. The number of cows where uterine
the cervix. No significant differences among the cervicitis cytology was also available amounted to n ¼ 157. Of these,
groups and PMN could be found. Of 370 cows with available 95 cows had cervicitis (Table 3). Furthermore, 29 of 157
uterine cytology, 221 had cervicitis; however, 170 of these (18.5%) cows showed neither cervical (C0) nor uterine ab-
(76.9%) had percentage of neutrophils in the uterus less normalities and could, therefore, be designated as incon-
than 5%. spicuous animals. Among cows with cervicitis (C1/C2), 63
of 95 (66.3%) had no pathologic abnormalities and negative
3.4. Histology of uterine biopsy cytology of the uterine tissue. Therefore, these animals had
an isolated cervicitis without uterine involvement. Only 13
A total of 416 uterine biopsies were collected, and 300 of of 157 (8.3%) cows had both positive cytology of the uterine
them could be evaluated. Thus, the following diagnoses tissue and histologically diagnosed endometritis.
were made: either no abnormalities, endometritis, bovine
endometriosis, perivasculitis, or angiosclerosis. 3.6. Cervicitis and reproductive performance
Angiosclerosis is characterized by perivascular and
intimal sclerosis [15]. To date, the diagnosis of bovine For analyses of reproductive performance with regard to
endometriosis is not established in buiatrics. It is equiva- degree of cervicitis, only animals with no histopathologic
lent to endometrial periglandular fibrosis in cattle and re- and cytologic findings as well as animals with solely
sembles endometriosis in the mare [16]. endometritis (positive histology and/or cytology) were
Although no palpable uterine or vaginal abnormalities evaluated (n ¼ 157, Table 4). Of these, 11 cows had left the
were detectable, histologically 72.7% of cows either had farm for an unknown reason and were not considered.
uterine inflammation and/or degenerative uterine changes Neither days from calving to first insemination nor number
Table 2
Association between histopathologic uterine diagnosis and degree of cervicitis.
n % n % n % n %
No histopathologic abnormalities 82 27.3 26 22.4 30 33.3 26 27.7
Endometritis 111 37.0 47 40.5 33 36.7 31 33.0
Bovine endometriosis 133 44.3 51 44.0 43 47.8 39 41.5
Intercaruncular angiosclerosis 50 16.7 20 17.2 16 17.8 14 15.0
Caruncular angiosclerosis 39 13.0 18 15.5 13 14.4 8 8.5
Perivasculitis 19 6.3 9 7.8 5 5.6 5 5.3
Table 3
Relationship between degree of cervicitis and cytologic and pathohistologic endometrial findings.
Abbreviations: C0, cervix without abnormality; C1, swollen and prolapsed Portio vaginalis cervicis without reddening; C2, swollen and prolapsed Portio
vaginalis cervicis with reddening; cytology ve, PMN < 5%; cytology þve, PMN 5%; pathohistology ve, uterine biopsy without histopathologic findings;
pathohistology þve, endometritis (without other pathologic endometrial findings); PMN, polymorphonuclear neutrophils.
of days open differed significantly among the cervicitis However, of the cows with cervicitis (n ¼ 221), 170 animals
groups. However, in consideration of survival analysis, (76.9%) were without positive cytology of the uterus.
there was a trend (P ¼ 0.092) toward a shortened interval of Comparison of the mean PMN content in the cervical and
days open in animals with cervicitis (C1/C2) but without uterine mucosa in the present study did not reveal any
endometritis compared with cows that had cervicitis as significant differences among cervicitis groups (data not
well as endometritis (Fig. 2). Also, with regard to poly- shown). However, a significant difference was detected
morphonuclear cells, a significantly shortened interval of between PMN content in the cervical and uterine mucosa
days open was found in cows that had increased PMN relative to number of days open (Fig. 3). This difference
content in the cervical mucosa but not in the uterus (Fig. 3). suggests that higher PMN content in the uterus is associ-
Cows with or without endometritis and a cervix rated as ated with extended days open, whereas increased cervical
C0 or C1 had a higher total conception rate than animals PMN content seems to play a minor role in this reproduc-
with C2 (P < 0.05). No differences were found within the tive measurement of reproductive performance.
cervicitis groups relative to animals with and without Histologically, 218 of 300 (72.7%) animals in the present
endometritis. Similarly, total pregnancy rate at 200 days study displayed one or more pathologic findings in the
into lactation was significantly lower in cows with C2 than uterine tissue with predominantly degenerative changes
in animals with C0 or C1; this result was independent of (bovine endometriosis and angiosclerosis) or, less frequently,
cytologic and/or histologic findings in the uterus. inflammatory diseases (endometritis and perivasculitis).
Surprisingly, 56 of 82 (68.3%) cows without histopathologic
4. Discussion findings of the uterus had cervicitis. A previous study simi-
larly found that purulent vaginal discharge did not neces-
After clinical, cytologic, and histologic examinations, we sarily indicate metritis or endometritis, but could be a
concluded that cervicitis in dairy cows is an independent separate inflammatory disease of the cervix [9]. Conversely,
disease and could have negative effects on reproductive the high prevalence of cervicitis and uterine pathologic al-
performance. terations of cows in the present study without abnormal
Clinically, cervicitis was diagnosed when the second vaginal discharge was unexpected. A previous study found
cervical fold was swollen and prolapsed with (C2) or that vaginal urine pooling caused severe pathologic conges-
without (C1) reddening of the Portio vaginalis cervicis [10]. tion of the external cervical os, indicating vaginitis and
Based on this classification, 60.8% of cows examined had a cervicitis [24]. In the present study, just a small number of
cervicitis between 42 and 50 days postpartum. Previous animals were found with urovagina (n ¼ 10); but of these,
studies have estimated the prevalence of cervicitis as eight had a cervicitis. Therefore, vaginal urine pooling seems
ranging from 15.6% to 56.9% [9,17–20]. However, the defi- to play a crucial role in the development of cervicitis.
nitions of cervicitis were different. Kumbhar et al. [19] It is generally accepted that inflammation of the endo-
examined the cervices of slaughtered animals for a pro- metrium has negative effects on reproductive measure-
lapse of cervical rings and inside contents. Other studies ments [2,25–27]. However, little is known about cervicitis
defined an inflammation of the cervix via PMN content [9] and its effects on reproductive performance. In the present
or by edema of the cervical os with mucosal congestion, study, no significant relationship could be observed be-
enlargement and hardening of the cervix, and presence of tween cervicitis and the number of days to first service as
flecks of pus in the vagina [18]. well as between days open and first service conception
It is known that an inflammatory process in the uterus rate. However, analyses revealed a trend (P ¼ 0.092) toward
causes migration of PMNs into the endometrial tissue a shortened interval of days open in animals with cervicitis
[1,21,22]. In previous studies, a threshold of greater than or (C1/C2) and without endometritis compared with cows
equal to 5% PMN was used to define endometritis that had cervicitis and endometritis (Fig. 2). Also, with re-
[1,9,17,23]. In the present study, we adopted the threshold gard to polymorphonuclear cells, cows with increased PMN
to define an endometrial inflammation. Therefore, of 370 content in the cervical mucosa had a significantly shorter
endometrial cytology slides, 92 (24.9%) had a PMN interval of days open than animals with high PMN content
content greater than or equal to 5%, and 278 (75.1%) were in the uterus (Fig. 3). Thus, we inferred that inflammation
negative. With regard to cervicitis, no significant differ- of the uterus has a marked negative effect on the success of
ences among the cervicitis groups and PMN could be found. insemination.
6 D. Hartmann et al. / Theriogenology xxx (2015) 1–7
Abbreviations: C0, cervix without abnormality; C1, swollen and prolapsed Portio vaginalis cervicis without reddening; C2, swollen and prolapsed Portio vaginalis cervicis with reddening; PMNU, percentage of
(15/52)2
(15/23)3
(23/46)
(15/31)
(8/23)
84.9 35.7
117.1 44.0
34.8
28.8
65.2
þve
Cytology þ pathohistolgoy
(16/47)B
(16/23)B
(23/46)
(16/31)
(11/23)
86.7 28.8
105.6 40.1
47.8
34.0
69.6
Fig. 2. Survival curves for days open up to 200 days postpartum based on
cervicitis with either positive (þ) or negative () cytology and pathohis-
tology of the endometrium. C0, cervices without abnormality; C1, the
ve
C2
Relationship between reproductive performance and degree of cervicitis without (ve) and with (þve) endometritis (defined as PMNU 5% or pathohistology).
second cervical fold was swollen and prolapsed without reddening; C2, the
second cervical fold was swollen and prolapsed with reddening. C1/2,
Cytology and Pathohistology (d) and C1/2, Cytology and
(7/7)b,2
(7/15)1
Values with different capital letters in a row differ significantly between the cervicitis groups (P < 0.05).
% Pregnant/1st service
% Pregnant/200
Fig. 3. Survival curves for days open up to 200 days postpartum, based on
Reproductive
(P < 0.05).
D. Hartmann et al. / Theriogenology xxx (2015) 1–7 7
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