Short-term consumption of the mycotoxin zearalenone by pubertal gilts causes persistent changes in the histoarchitecture of reproductive tissues

Abstract

Abstract Consumption of zearalenone (ZEN) detrimentally affects tissues and systems throughout the body, and these deleterious effects are especially pronounced in swine. The objectives of this project were to determine the effects of short-term consumption of ZEN (at concentrations that could be found on-farm) on growth, carcass weight, liver weight, and reproductive tissues of pubertal gilts, and to determine if the effects are transient or persistent. Cross-bred gilts (107.25 ± 2.69 kg) were randomly assigned to one of three feed treatments: 1) solvent only for 21 d (CON; n = 10), 2) ZEN for 7 d followed by 14 d of solvent (ZEN-7; 6 mg/d; n = 10), and 3) ZEN for 21 d (ZEN-21; 6 mg/d; n = 10). Body weights were collected at the beginning and end of the experiment (189.1 ± 0.8 and 211.1 ± 0.8 d of age, respectively). Carcass weights and tissues were collected at harvest. There were no treatment-based differences in growth, carcass, liver, or reproductive tissue weights. Histological analyses revealed differences based on treatment and the interaction between treatment and luteal status. The thickness of the ampullary muscularis declined with ZEN exposure (P < 0.05), while the isthmic epithelial cell height (P < 0.01) and uterine endometrial thickness (P < 0.02) increased. Interestingly, the thickness of the isthmic muscularis, uterine myometrium, and epithelial cell height only differed in the presence of a corpus luteum. Uterine epithelial cell height in the luteal phase was lowest in ZEN-7 pigs (P < 0.01). The isthmic muscularis in the luteal phase was thinner in pigs from both ZEN treatments (P < 0.01). Conversely, the luteal-stage myometrium was thicker in pigs from both ZEN treatments (P < 0.01). The discovery of these tissue-based differences during the luteal phase is particularly concerning since this corresponds with the time when embryos would be affected by the functional competency of the oviduct and uterus. The results of this work demonstrate that short-term consumption of ZEN produces microscopic, but not macroscopic alterations in reproductive organs which are likely to have negative effects on their subsequent function and that these differences persist even after ZEN consumption ceases. Taken together, these results indicate that it is insufficient to rely solely on outwardly visible symptoms as indicators of zearalenone exposure, as detrimental effects on reproductive tissues were found in the absence of phenotypic and morphologic changes.