Efecto del estrés térmico en el periodo prenatal sobre la salud, la reproducción y la producción láctea en vacuno de leche hasta la tercera lactación

Inmaculada Cuevas-Gómez¹, Javier Lozano², Dimitrios Rizos³, José María Sánchez⁴

(1)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Madrid, Spain. (2)-Explotación Agropecuaria Las Rozuelas del Valle S.L, Torrecampo, Córdoba, Spain. (3)-Departmento de Reproducción Animal, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Madrid, Spain.
(4)-Instituto Andaluz de Investigación y Formación Agraria, Pesquera, Alimentaria y de la Producción Ecológica (IFAPA), Hinojosa del Duque, Córdoba, Spain.

In cattle, maternal factors such as nutrition, milk yield, and diseases during gestation indirectly influence offspring long-term performance through fetal programming. Heat stress (HS), with well-documented direct effects on milk production and reproductive performance, has gained attention as one of these factors. However, its impact during oocyte development/early and late gestation remains less understood. During these stages, HS exposure may cause permanent structural and functional changes in the developing embryo/foetus, with potential long-term consequences for the offspring. We hypothesize that HS during early and late gestation negatively impacts offspring health, reproduction, and milk production. This retrospective cohort study aims to evaluate the association between HS exposure during these critical periods and offspring outcomes up to the third lactation. The dataset included records of 1,227 Holstein females (offspring F1) born between 2016 and 2022 on a single farm, monitored during the first lactation, with 440 and 286 followed through their second and third lactation, respectively. Offspring (F1) were grouped in three HS groups: (i) HS during early gestation (HS_EARLY), mean daily maximum temperature-humidity index (THI) >= 72 over the two months before and 45 days after successful insemination date; (ii) HS during late gestation (HS_LATE), mean daily THI >= 72 over the two months before calving date; and (iii) thermoneutral conditions (NO_HS), mean daily THI < 72 during both early and late gestation. Notably, dams (F0) were housed in bedded pack barns and cooled every 4 hours between 6 a.m. and 10 p.m. during the warm season (June-September) using fans and soakers operating for 45 minutes (45-second soaking, 3-minute fan intervals). Daily THI was calculated using meteorological data from a nearby AEMET station as follow: (1.8×Tºmax+32)-(0.55-0.0055×RHmin)×(1.8×Tºmax-26). Generalized linear mixed models were constructed in SAS to analyse associations between health, reproduction and milk production outcomes and the independent variable (HS group), adjusting for covariates related to the offspring (birth year, dam’s parity, genetic indexes, passive immune transfer failure, diarrhoea, bovine respiratory disease [BRD], weaning average daily gain [ADG], HS at artificial insemination [AI], semen type, calving difficulty, HS during calving season, calf breed, calf sex, and postpartum diseases). Repeated milk yield measures (first 30 weeks in milk) were analysed with ANOVA (MIXED procedure) for each lactation, and mortality risk was assessed using a Cox proportional hazards model. Results are summarised in Table 1. Regarding health, NO_HS and HS_LATE heifers showed the highest incidence of preweaning diarrhoea and BRD (P<0.05), respectively, but no differences were observed in postpartum diseases incidence (retained placenta, metritis, ketosis, or displaced abomasum) or survival probability across groups. Regarding reproduction, no differences were observed in age (∼422 d) or pregnancy per AI at first AI (P/AI) during the heifer period. However, HS_EARLY heifers tended to require more AI per conception (AI/C; P=0.08), leading to a greater age at first calving compared to NO_HS and HS_LATE (P<0.05). During the first lactation, HS_EARLY cows showed reduced P/AI, longer calving-to-pregnancy interval, and required more AI/C compared to NO_HS and HS_LATE cows (P<0.01). No differences in reproductive parameters were observed across the second and third lactations. Regarding milk production, HS_EARLY cows had lower milk yield by 0.7 and 1.0 L/day compared to NO_HS during the first and second lactations (P<0.05), respectively, and by 0.7 L/day compared to HS_LATE during the first lactation (P=0.046). Cows in the HS_EARLY group exhibited impaired reproductive and milk production outcomes, supporting our hypothesis. Conversely, HS_LATE cows showed no substantial impairments compared to NO_HS, likely due to the active cooling strategy implemented in our farm, which has been shown previously to mitigate the negative effects of late-gestation HS. In conclusion, HS exposure during early gestation was associated with reduced offspring milk production during the first two lactations and impaired reproductive performance, particularly until the first lactation. Although causality cannot be established due to the observational nature of this study, these findings highlight the importance of considering conception timing in on-farm breeding and management strategies. Future research should investigate the mechanisms underlying these associations.

Table 1. Health, reproduction, and milk production outcomes variables of offspring (F1) from dams (F0) exposed to early (HS_EARLY) or late gestation heat stress (HS_LATE), and thermoneutral conditions (NO_HS).

Within a row, Lsmeans ± SE or percentages with different superscripts differ (^a,bP<0.05) or tend to differ (^x,yP=0.10-0.05).

¹Two months before and 45 days after successful insemination date.

²Two months before calving date.