Naturally occurring mastitis disrupts developmental competence of bovine oocytes

Abstract

We examined the effects of naturally occurring mastitis on bovine oocyte developmental competence in vitro. Specifically, we investigated the effects of intramammary infection on the ovarian pool of oocytes (i.e., follicle-enclosed oocytes) and their ability to undergo in vitro maturation, fertilization, and further development to the blastocyst stage. Culled Holstein cows (n=50) from 9 commercial dairy farms in Israel were allotted to 3 groups according to somatic cell count (SCC) records of the last 3 monthly milk tests as well as of quarter samples collected before slaughter: (1) low SCC (n=7), (2) medium SCC (n=16), or (3) high SCC (n=27). Means of SCC values differed among low-, medium-, and high-SCC groups: 148,000, 311,000 and 1,813,000 cell/mL milk, respectively. Milk yield and days in milk did not differ among the 3 groups. Bacterial isolates included coagulase-negative staphylococci, Escherichia coli, Streptococcus dysgalactiae, or no bacteria found. Ovaries were collected at the abattoir and brought to the laboratory. Cumulus oocyte complexes were recovered separately from each cow and subjected individually to in vitro maturation and fertilization, followed by 8d in culture. The number of aspirated oocytes did not differ among groups, with a range of 17 to 21 oocytes per cow. The proportion of oocytes that cleaved into 2- to 4-cell-stage embryos (86.1 ± 3.4%) did not differ among groups. In contrast, mean percentages of embryos developed to the blastocyst stage on d 7 and 8 after fertilization were less in both medium- and-high SCC groups than in the low-SCC group (5.6 ± 2.3 and 4.1 ± 1.8 vs. 18.1 ± 4.6%, respectively). Additional analysis indicated that cleavage and blastocyst-formation rates did not differ among the bacterial types in the low-, medium-, and high-SCC groups. These are the first results to demonstrate that naturally occurring mastitis disrupts the developmental competence of the ovarian pool of oocytes, (i.e., oocytes at the germinal vesicle stage). The disruption was associated with elevation of SCC rather than bacterial type. The results may provide a partial explanation for the low fertility of cows that have contracted mastitic pathogens before insemination.

Effects of Escherichia coli- and Staphylococcus aureus-induced mastitis in lactating cows on oocyte developmental competence

“…In particular, a past clinical event occurring up to 10 days prior to AI significantly reduced the probability of conception. Furthermore, we have recently shown that E. coli mastitis occurring during a 90-day period prior to performing IVM/IVF disrupts the ovarian pool of GV stage oocytes, resulting in a decrease in blastocyst formation rate (Roth et al 2013). Taken together, the findings support the view that not only the developing embryo but also the oocyte is highly susceptible to pathogenic (mastitis) stress.…”

Human granulosa–luteal cells initiate an innate immune response to pathogen-associated molecules

“…The same study revealed a negative correlation between systemic LBP and serum progesterone, similar to what was observed in this study (Tremellen et al 2015). In dairy cows, bacterial infections of the mammary gland result in altered steroidogenesis, ovarian function, and oocyte quality following natural or induced disease (Lavon et al 2008, Roth et al 2013, Asaf et al 2014.…”

Comparing the effects of heat stress and mastitis on ovarian function in lactating cows: basic and applied aspects

“…The proportion of oocytes that developed to blastocysts was lower in those obtained from the high SCC versus controls cows. The study showed for the first time that mastitis (diagnosed as clinical or subclinical) impairs oocyte developmental competence and that the ovarian pool of oocytes at the GV stage is vulnerable to this disease [89]. However, the reason for this susceptibility is unclear.…”

“…Cows were defined as clean or mastitic based on SCC records and bacteriology diagnosis within 3 mo before oocyte collection [89]. The proportion of oocytes that developed to blastocysts was lower in those obtained from the high SCC versus controls cows.…”