Risk factors of clinical endometritis in an Iranian dairy farm
Abstract
Clinical endometritis is one of the most common causes of declining reproductive performance in dairy cows. The purpose of this study was to investigate the effects of some factors including cow’s parity, milk yield, dystocia, retained placenta, calf sex, calving season, abortion, and stillbirth on the incidence of clinical endometritis and the effect of clinical endometritis on open days in an Iranian dairy farm. Uterine health of 557 dairy cows was evaluated by rectal palpation and ultrasonography during 30-35 days after calving. The presence of mucopurulent secretions in the vagina and vulva as well as the ultrasonographic observation of echogenic secretions in the uterine lumen were considered endometritis. The effect of the mentioned factors on the incidence of clinical endometritis was then analyzed in univariate and multivariate logistic regression models. The chance of developing clinical endometritis in the low-producing cows was 27.2% higher than that of the high-producing cows (p=0.06). Other parameters had no significant effect on the incidence of endometritis. The incidence of clinical endometritis in the studied herd was 49.5%. Based on the results of this study, the low milk yield may be a risk factor for developing clinical endometritis in the studied herd's condition, while parameters of the parity, dystocia, retained placenta, calf sex, calving season, abortion, and stillbirth was not effective in the occurrence rate of endometritis. There was no association between clinical endometritis and days open in the studied herd.
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Uterine disease is an intensely studied part of dairy cattle health management as it heavily affects many commercial dairy farms and has serious economic consequences. Forms of the disease, pathophysiology, pathogens involved and the effects of uterine disease on the health and performance of cows have already been well described by various authors. Lately, researchers' attention has shifted towards the healthy microbiome of the uterus and the vagina to put emphasis on prevention rather than treatment. This aligns with the growing demand to reduce the use of antibiotics or-whenever possible-replace them with alternative treatment options in farm animal medicine. This review provides a comprehensive summary of the last 20 years of uterine disease research and highlights promising new areas for future studies.
Transition period is a critical time for dairy cows because a large proportion of clinical and subclinical diseases are observed in the first month after parturition. Occurrence of negative energy balance is associated with depressed immunity and these conditions can affect oocyte quality and further embryonic development. The aim of this study was to assess the effects of negative energy balance-associated disorders on in vitro embryo production (IVP) in dairy cattle. We hypothesized that subclinical metabolic and/or inflammatory disorders have a negative effect on oocyte developmental competence and morphokinetic parameters of the resulting embryos. The study was conducted on 30 lactating Holstein-Friesian cows which were assigned into four groups: healthy (HEAL, n = 6), metabolic disease (META, n = 8), inflammatory disease (INFL, n = 8), or combined metabolic and inflammatory disease (COMB, n = 8). Ovum pick-up (OPU) was performed twice weekly on all cows over a period of four weeks (n = 8 OPU sessions/cow) starting on the fifth week postpartum, and the collected oocytes were subjected to routine IVP. Donor’s health status did not affect the number of oocytes/OPU or the recovery rate (p > 0.05). The number of quality 1 oocytes collected from INFL and COMB cows was lower compared to HEAL cows (p < 0.05). Also, the percentage of quality 1 embryos was reduced in META and COMB compared to HEAL cows (p < 0.05). Cleavage, blastocyst and hatching rates were similar among groups (p > 0.05). Presence of disease did not affect the time required by zygotes to reach specific developmental stages, as recorded by means of time-lapse monitoring. Nevertheless, there was a higher probability of direct cleavage after IVF in oocytes of COMB cows compared to those of HEAL cows (p < 0.05). In conclusion, oocytes and embryos derived from dairy cows diagnosed with subclinical metabolic and/or inflammatory diseases during the transition period showed reduced quality but similar developmental potential and morphokinetics when compared to healthy cows. These results shed light on the consequences of subclinical disease on embryonic development in dairy cows which might be important for embryo transfer programs.
Background:
The aim of this study was to investigate the risk factors for and the impact of ultrasound-diagnosed endometritis (UDE) on lactating dairy cows' reproductive performance.
Methods:
Data were analysed from 1123 Holstein and Holstein-Friesian cows from two Scottish dairy farms. A reproductive ultrasound examination was conducted on two occasions, at 43 ± 3 and 50 ± 3 days in milk (DIM), to screen for hyperechoic fluid in the uterus. Statistical analyses were performed using multivariable logistic regression modelling and Cox proportional hazards models.
Results:
The overall incidence of UDE was 8.8% (99/1123). Risk factors for UDE included calving during autumn/winter seasons, increased parity and the presence of two or more diseases in the first 50 ± 3 days postpartum. The presence of UDE was associated with a reduced odds of pregnancy after all artificial inseminations up to 150 DIM.
Limitations:
The retrospective design of this study led to some inherent limitations with the quality and quantity of data collected.
Conclusions:
The findings of this study indicate which risk factors should be monitored in postpartum dairy cows to limit the impact of UDE on future reproductive performance.
A certain level of endometrial bacterial infection and inflammation is involved in bovine uterine involution during the puerperal period. Factors that hamper normal uterine involution expose the uterine environment to pathological conditions, causing different endometritis levels. The lack of proper diagnostic tools extends the time to conception. Efforts have been made to elucidate the postpartum uterine environment, including bacterial flora, changes in transient endometrial inflammation, and the pathophysiology of endometritis, to improve bovine reproductive performance. E. coli and Trueperella pyogenes in the uterus are likely to cause persistent infection, and Mycoplasma bovigenitalium infection is associated with dystocia and cytological endometritis in postpartum dairy cows. Due to the widespread use of cytobrush as a diagnostic tool for bovine subclinical endometritis (SE) that enables quantification of the degree of inflammation, we found that endometritis at week 5 postpartum was associated with delayed first ovulation. Approximately 30% of open cows have SE during the postpartum period, and cows with low blood glucose during prepartum have a high risk of developing SE. Additionally, cows with purulent vaginal discharge do not always have endometritis but only vaginitis and/or cervicitis. Intrauterine infusion of polyvinylpyrrolidone-iodine (PVP-I) improves fertility and promotes endometrial epithelial cell regeneration after inducing transient uterine inflammation, suggesting that PVP-I could be a good alternative to antibiotics. In conclusion, prepartum management to prevent glucose deficiency, prompt diagnosis to identify causative agents and intrauterine inflammation levels, and appropriate treatment to minimize antimicrobial resistance is beneficial for tackling endometritis and improving reproductive performance in bovine herds.
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Uterine diseases are some of the most prevalent and costly diseases for the dairy industry. It has been reported that an exacerbated and prolonged inflammatory response around calving can increase the risk of developing metritis, which subsequently can impair production and fertility in dairy cows. The objective of this study was to assess the effects of 2 oral administrations of acetylsalicylic acid 24 h apart on the incidence of uterine diseases [i.e., retained fetal membranes, clinical metritis, clinical endometritis) and reproductive performance [i.e., days in milk to conception, number of services to conception, proportion of cows pregnant at first service, proportion of abortion at first service (ABRT)] in dairy cows after calving. Cows from one dairy farm (n = 246) located in central Pennsylvania were included in this study. Animals were blocked by parity and randomly assigned to 1 of 2 groups: (1) ASA (n = 121): within ~12 h after parturition, cows received 2 treatments with acetylsalicylic acid (ASA; 200 mg/kg, 4 boluses) 24 h apart; or (2) UNT (n = 125): cows remained untreated. Clinical metritis was assessed at 7 ± 3 and 14 ± 3 d in milk (DIM) using a Metricheck device (Simcro Tech Ltd., Hamilton, New Zealand). Cows that presented a fetid, red-brownish, watery vaginal discharge were classified as having clinical metritis. Clinical endometritis was assessed through ultrasonography and defined as presence of hyperechoic fluid (>3 mm) in the uterus lumen at 50 ± 10 DIM. The incidence of retained fetal membranes was defined as the failure of expulsion of the placenta within 24 h after calving and recorded by farm personnel. The data were analyzed using the MIXED and GLIMMIX procedures of SAS (SAS Institute Inc., Cary, NC) as a randomized complete block design. A lower proportion of cows treated with acetylsalicylic acid developed clinical metritis at 7 ± 3 DIM (ASA = 34.97 ± 5.57%; UNT = 57.21 ± 5.80%) and tended to develop clinical endometritis at 50 ± 10 DIM (ASA = 3.84 ± 2.67%; UNT = 13.61 ± 5.23%) compared with cows that remained untreated. Cows treated with acetylsalicylic acid tended to require 18 d less to conceive compared with UNT cows (ASA = 125.63 ± 8.21 d; UNT = 143.44 ± 6.28 d). Furthermore, there was a tendency for a treatment × ABRT interaction, whereby ASA cows that aborted at first service tended to conceive 35 d sooner compared with UNT cows that aborted at first service (ASA = 151.42 ± 15.90 d; UNT = 186.38 ± 11.84 d). Although there was no difference in pregnancy per AI at first service between treatment groups (ASA = 23.88 ± 7.92%; UNT = 17.93 ± 6.31%), the proportion of cows aborting at first service in the ASA group tended to be lower than that in the UNT group (ASA = 1.03 ± 1.06%; UNT = 6.04 ± 2.62%). Results from this study suggest that a short-duration acetylsalicylic acid treatment after calving may decrease the incidence of uterine diseases and improve reproductive success in cows that aborted at first service in dairy cattle.
The objective of this study was to characterize incidences of health disorders during early lactation in a large population of Holstein cows calving in 2 seasons across multiple US dairy herds. In addition, cumulative effects of combinations of health-related events on fertility and survival by season of calving and parity number were tested. Data were prospectively collected from a total of 11,729 cows in 16 herds located in 2 regions in the United States [north (7,820 cows in 10 herds) and south (3,909 cows in 6 herds)]. Cows were enrolled at parturition and monitored weekly for disease occurrence, reproductive events, and survival. Health-related events were grouped into reproductive disorders (REP; dystocia, twins, retained fetal membranes, metritis, and clinical endometritis) and other disorders (OTH; subclinical ketosis, mastitis, displaced abomasum, and pneumonia). Counts of health events within 50 d postpartum were added into each of the groups and categorized as 0, 1, 2, 3, and ≥4 for REP and 0, 1, 2, and ≥3 for OTH. Multivariable logistic regression was used for testing potential associations between categories of disease occurrence and outcome variables, including resumption of ovarian cyclicity, pregnancy per artificial insemination (AI), pregnancy loss, and survival up to and after 50 DIM. The incidence of disease varied with season of calving and parity, and these 2 variables were associated with the reproductive and survival outcomes. The size of the detrimental effect of disease incidence on reproduction and survival depended on disease group and varied for each specific outcome. Resumption of ovarian cyclicity decreased as incidences of disorders increased in both REP and OTH categories. Pregnancy at first AI also was smaller in greater number of REP categories, but the effect of number of OTH categories on pregnancy at first AI was not consistent. Similarly, pregnancy loss at first AI was not affected consistently by REP or OTH. Survival was reduced by REP and OTH. The magnitude of these negative effects was variable, depending on season of calving and parity, but consistently increased with the number of health events during early lactation.
This paper reviews recent data and concepts on metritis, purulent vaginal discharge (PVD), and endometritis in dairy cows and the ways in which these diseases affect reproductive performance. Metritis is characterized by fetid discharge from the uterus, with or without fever. Purulent vaginal discharge describes exudate that is >50% pus that may be attributable to uterine infection or cervicitis. Endometritis is inflammation of the uterus diagnosed by endometrial cytology with a proportion of neutrophils (typically ≥5%) that is associated with impaired fertility. Metritis and PVD are associated with uterine bacterial dysbiosis: changes in the microbiota to lesser diversity and greater abundance of pathogens, especially Gram-negative anaerobic bacteria, and Trueperella pyogenes in the case of PVD. Metritis is justifiably treated with approved antibiotics but criteria for more selective treatment without loss of performance are emerging. Purulent vaginal discharge is not synonymous with clinical endometritis, and greater precision in terminology is warranted. PVD is likely under-diagnosed and represents an opportunity for improved management in many herds. Endometritis seems in many cases to reflect persistent, dysregulated inflammation, for which the inciting cause is unclear. Postpartum uterine infection and inflammation have harmful effects on oocytes, embryo development, and the endometrium for at least three months, even if the disease is apparently resolved. Emerging concepts of the resolution and regulation of inflammation are promising for the improvement of prevention and therapy of endometritis.
The detection of reproductive tract disease (RTD) 3 wk postpartum is important because of its effect on subsequent reproductive outcomes. Numerous methods for the diagnosis of RTD are described, some of which are more practical and instantaneous in terms of diagnosis. Two of these methods involve identification of purulent vaginal discharge (PVD) and evidence of ultrasonographic uterine changes indicative of endometritis (UE). The objectives of our retrospective observational study were (1) to assess the association of PVD or UE score at the prebreeding examination (PBE) with the hazard of pregnancy within the subsequent breeding season; (2) to determine the test sensitivity (Se) and specificity (Sp) at the point of sampling of both tests using a Bayesian latent class model; and (3) to determine the effect of varying positivity thresholds on test accuracy. To achieve these objectives, we analyzed an initial data set of 5,049 PBE from 2,460 spring-calved cows in 8 herds between 2014 and 2018. Each PBE was conducted once between 25 and 86 d in milk. At each PBE, vaginal discharge was obtained with a Metricheck device (Simcro) whereas uterine contents were assessed using transrectal ultrasonography. Purulent vaginal discharge was scored on a scale of 0 to 3 depending on discharge character, and UE was scored on a scale of 0 to 4 depending on the presence and consistency of intraluminal fluid. Cows with scores of ≥2 in either test had received treatment. Fertility data were available from 4,756 PBE after data exclusion. The association between PVD or UE score at the PBE and subsequent hazard of pregnancy was analyzed using a Cox proportional hazards model. Cows with a PVD score of 2 or 3 were less likely to conceive than cows with a PVD score 0 [score 2 hazard ratio (HR) = 0.74; 95% confidence interval (CI): 0.59–0.94; score 3 HR = 0.65; 95% CI: 0.51–0.84]. Cows with a UE score of 1, 2, 3, or 4 were less likely to conceive than cows with a UE score of 0 (score 1 HR = 0.82; 95% CI: 0.73–0.93; score 2 HR = 0.79; 95% CI: 0.62–1.00; score 3 HR = 0.43; 95% CI: 0.43–0.90; score 4 HR = 0.39; 95% CI: 0.26–0.58). To determine the Se and Sp of PVD or UE score for diagnosis of RTD at the time of PBE, a Bayesian latent class model was fitted on 2,460 individual cow PBE. Flat priors were used for the Se and Sp of UE, whereas informative priors were used for PVD Se (mode = 65%, 5th percentile = 45%) and Sp (mode = 90%, 5th percentile = 80%) and RTD prevalence (mode = 20%, 5th percentile = 10%). Posterior estimates (median and 95% Bayesian probability intervals; BPI) were obtained using ‘rjags' (R Studio). The optimal test thresholds (PVD and UE score ≥1) were selected by assessing the effect of different thresholds on test estimates and using a misclassification cost analysis. Based on these, median (95% BPI) Se for PVD and UE score ≥1 were 44% (29–60%) and 67% (33–100%), respectively. Median Sp for PVD and UE score ≥1 were 90% (86–93%) and 91% (86–93%), respectively. Higher scores in both tests were associated with impaired fertility, and UE scoring with a threshold of ≥1 had the highest test Se and Sp estimates although test Se was conditional on days in milk when the PBE occurred.
Clinical endometritis (CLE) and subclinical endometritis (SCLE) manifesting at the cow- and herd-levels has been associated with multiple risk factors (RFs), but hardly are RFs with direct influences separated from those with mediated indirect influences. This study identified and quantified the direct and indirect associations of cow- and herd-levels RFs with CLE and SCLE cases observed among 466 zero-grazed dairy cows that were in their 21 to 60 days postpartum (dpp). The cases were observed in a cross-sectional survey of smallholder farms (n = 370) in Rwanda. The direct and indirect associations were constructed with odds ratio (OR) derived from multiple logistic regression modelling. The cow-level RFs that had direct positive association with CLE and SCLE were the season of calving (OR: 5.0, 2.1), dystocia (OR: 1.9, 2.2), poor body condition score (OR: 4.1, 2.2), stillbirth (OR: 3.5, 3.3), and retained placenta (OR: 1.4, 1.8) while mastitis (OR: 2.5) and parity (OR: 1.5) had a direct positive association with SCLE. Breed and parity of cow, sex of calf, and twin births had indirect positive association with both CLE and SCLE cases. At the herd-level, unhygienic cowshed (OR: 25.1, 8.9) had direct positive association with both CLE and SCLE cases. In contrast, earthen floor cowshed (OR: 6.6) and large herd size (OR: 3.1) had direct positive association with CLE and not using bedding materials (OR: 1.5) had direct positive association with SCLE. Herd-level RFs that showed indirect positive association with both CLE and SCLE cases were farm size (OR: 2.9) and farmer’s experience in dairying (OR: 1.7) while housing cows within the first 30 dpp (OR: 0.1) showed indirect negative association. These results show which RFs have strong direct and indirect influences on CLE and SCLE cases at the cow- and herd-levels. Effective management of those RFs should be a priority in extension education and services to enable smallholder farmers effectively manage them to prevent and control endometritis among their zero-grazed dairy cows.