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      Uterine and systemic inflammation influences ovarian follicular function in postpartum dairy cows

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          Abstract

          The objective of this study was to determine the effects of uterine and systemic inflammatory responses to uterine bacterial contamination at calving in dairy cows on the growth and ovulatory outcomes of the first dominant follicle postpartum. Ovulatory capability of the first dominant follicle postpartum was predicted in 53 multiparous cows by using a combination of follicle growth characteristics and circulating estradiol concentrations. Endotoxin levels were assayed in follicular fluid samples that were aspirated the day after ovulatory outcome prediction. Plasma levels of haptoglobin, a proinflammatory acute phase protein, and paraoxonase, a negative acute phase protein were determined. Uterine bacteria and inflammation were evaluated in three uterine fluid samples from each cow collected on the day of calving, the day after follicle aspiration, and at 35 days postpartum. Cows that had a strong initial uterine inflammatory response (robust recruitment of polymorphonuclear leukocytes of ≥ 35% and cows with uterine pH < 8.5 on the day of calving) were more likely to have an ovulatory first dominant follicle. Follicular fluid endotoxin levels were higher in non-ovulatory cows compared with ovulatory cows. Endotoxin levels in circulation were not different between ovulatory groups but were higher prepartum than on day 7 and 14 postpartum. Systemic inflammation characterized by elevated haptoglobin concentrations was higher in non-ovulatory cows despite similar bacterial contamination and circulating endotoxin levels. Paraoxonase activity in follicular fluid was significantly associated with the paraoxonase activity in plasma, however, plasma paraoxonase concentrations were not different between non-ovulatory and ovulatory cows. Cows with a higher uterine bacterial load on the day of calving had slower ovarian follicle growth. In summary, a robust uterine inflammatory response on the day of calving was positively associated with ovarian function while elevated systemic inflammation during the early postpartum period was negatively associated with the ovulatory status of the first dominant follicle postpartum.

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          Reproductive loss in high-producing dairy cattle: where will it end?

          M Lucy (2001)
          The dairy industry in the United States has changed dramatically in the last decade. Milk production per cow has increased steadily because of a combination of improved management, better nutrition, and intense genetic selection. Dairy farms are larger, and nearly 30% of the dairy cows in the United States are on farms with 500 or more cows. The shift toward more productive cows and larger herds is associated with a decrease in reproductive efficiency. Cows with the greatest milk production have the highest incidence of infertility, but epidemiological studies suggest that, in addition to milk production, other factors are probably decreasing reproductive efficiency in our dairy herds. The reproductive physiology of dairy cows has changed over the past 50 yr, and physiological adaptations to high milk production may explain part of the reproductive decline. Critical areas for new research include control of the estrous cycle, metabolic effects of lactation on reproduction, mechanisms linking disease to reproduction, and early embryonic mortality. Solving reproductive loss in dairy cows will not be easy because only a small number of research groups study reproduction in postpartum dairy cows. Therefore, the present research base will need to be expanded. For this to occur, research funding must be increased above its current level and a renewed emphasis must be placed on solving the emerging crisis of infertility in dairy cows.
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            Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle.

            First postpartum dominant follicles are preferentially selected in the ovary contralateral to the previously gravid uterine horn. The aim of the present study was to test the hypothesis that uterine bacterial contamination alters the location of ovarian follicle emergence and selection, and inhibits follicle growth and function. Swabs were collected from the uterine body lumen of cattle on days 7, 14, 21 and 28 after parturition. Bacteria were identified by aerobic and anaerobic culture; bacterial growth was scored semiquantitatively and animals were categorized into standard or high bacterial contamination categories on the basis of the number of colonies detected. Follicular growth and function were monitored by daily transrectal ultrasonography, and estimation of plasma FSH, oestradiol and progesterone concentrations. There was no effect of bacterial contamination on plasma FSH concentration profiles or emergence of the ovarian follicle wave. When uterine bacterial growth scores were high on day 7 or day 21 after parturition, fewer first (1/20 versus 15/50; P < 0.05) or second (1/11 versus 13/32; P < 0.05) dominant follicles were selected in the ipsilateral compared with the contralateral ovary, respectively. The diameter of the first dominant follicle was smaller in animals with a high day 7 bacterial score (P < 0.001), dominant follicle growth was slower (P < 0.05) and oestradiol secretion was decreased (P < 0.05). The present study provides evidence for an effect of the uterus on the ovary after parturition, whereby uterine bacteria have a contemporaneous localized effect on ovarian follicle selection and subsequent growth and function, but not on initial emergence.
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              Prevalence of endometritis and its effects on reproductive performance of dairy cows.

              Hostein cows (n=141) in five commercial dairy herds in central New York were examined for endometritis by examination of endometrial aspirates for presence of inflammatory cells, principally neutrophils, by endometrial cytology at 40-60 days postpartum. The prevalence of cytologically-diagnosed endometritis was 53%; within herds the prevalence varied from 37 to 74% (P=0.02). There was excellent agreement between two examiners (Kappa=0.864; P<0.0001). Parity did not influence prevalence of endometritis (P=0.53). Cytologically diagnosed endometritis was associated with profoundly impaired reproductive performance; Kaplan-Meier survival analysis revealed lower overall pregnancy rate (P<0.0001). Median days open was 206 for cows with endometritis and 118 for cows free of the condition. Overall, 76% of cows in this study became pregnant by 300 days postpartum; 63% of cows with endometritis and 89% of cows without endometritis were confirmed pregnant by 300 days postpartum (P<0.003). (For these two groups, 69, and 90% respectively, became pregnant during the duration of the study). Pregnancy to first service percentage was lower (11 versus 36%; P=0.001) for cows with than without endometritis, and these cows required more services before 50% became pregnant (3 versus 2; P=0.006). In a second study using 22 cows in a university-owned herd, the prevalence of cytological evidence of inflammation was 100% at 2 weeks postpartum, and dropped to 89, 58, and 41% at 4, 6, and 8 weeks, respectively. Endometritis diagnosed by endometrial cytology late in the voluntary waiting period was highly prevalent and exerted a profoundly detrimental effect on subsequent reproductive performance, making this condition potentially extremely costly to the North American dairy industry.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 May 2017
                2017
                : 12
                : 5
                : e0177356
                Affiliations
                [1 ]Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America
                [2 ]Department of Animal Science, Cornell University, Ithaca, New York, United States of America
                University of Florida, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: ROG WRB SHC.

                • Formal analysis: SHC AS WRB ROG.

                • Funding acquisition: ROG WRB.

                • Investigation: SHC OGS VAA AS.

                • Methodology: ROG WRB SHC.

                • Project administration: ROG WRB SHC.

                • Resources: ROG WRB.

                • Software: SHC.

                • Supervision: SHC WRB ROG.

                • Visualization: SHC AS.

                • Writing – original draft: SHC WRB ROG.

                • Writing – review & editing: OGS VAA AS.

                [¤a]

                Current address: Department of Clinical Studies, New Bolton Center, University of Pennsylvania School of Veterinary Medicine, Kennett Square, Pennsylvania, United States of America

                [¤b]

                Current address: Department of Nutrition, Universidade Federal de Pelotas, Pelotas, Brazil

                [¤c]

                Current address: Department of Clinical Sciences, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts, West Indies

                Author information
                http://orcid.org/0000-0001-9002-7589
                Article
                PONE-D-16-45401
                10.1371/journal.pone.0177356
                5438135
                28542500
                f1df29d7-0434-4939-b922-3f55ec40835e
                © 2017 Cheong et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 November 2016
                : 26 April 2017
                Page count
                Figures: 3, Tables: 3, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;
                Award ID: 2007-35203-18420
                Award Recipient :
                This project was supported by National Research Initiative Competitive Grant no. 2007-35203-18420 from the USDA National Institute of Food and Agriculture to ROG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Toxicology
                Toxic Agents
                Toxins
                Bacterial Toxins
                Endotoxins
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Toxicology
                Toxic Agents
                Toxins
                Bacterial Toxins
                Endotoxins
                Biology and Life Sciences
                Immunology
                Immune Response
                Inflammation
                Medicine and Health Sciences
                Immunology
                Immune Response
                Inflammation
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Inflammation
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Inflammation
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Follicular Fluid
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Follicular Fluid
                Biology and Life Sciences
                Physiology
                Body Fluids
                Follicular Fluid
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Follicular Fluid
                Biology and Life Sciences
                Anatomy
                Reproductive System
                Ovaries
                Follicular Fluid
                Medicine and Health Sciences
                Anatomy
                Reproductive System
                Ovaries
                Follicular Fluid
                Biology and Life Sciences
                Biochemistry
                Proteins
                Plasma Proteins
                Haptoglobins
                Biology and Life Sciences
                Organisms
                Bacteria
                Anaerobic Bacteria
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Biology and Life Sciences
                Anatomy
                Reproductive System
                Uterus
                Medicine and Health Sciences
                Anatomy
                Reproductive System
                Uterus
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Estradiol
                Custom metadata
                All relevant data are presented within the paper and supplemental material.

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