Exposure to chronic light–dark phase shifts during the prepartum nonlactating period attenuates circadian rhythms, decreases blood glucose, and increases milk yield in the subsequent lactation

Abstract

Maintaining metabolic balance is a key factor in the health of dairy cattle during the transition from pregnancy to lactation. Little is known regarding the role of the circadian timing system in the regulation of physiological changes during the transition period. We hypothesized that disruption of the cow's circadian timing system by exposure to chronic light-dark phase shifts during the prepartum period would negatively affect the regulation of homeostasis and cause metabolic disturbances, leading to reduced milk production in the subsequent lactation. The objective was to determine the effect of exposure to chronic light-dark phase shift during the last 5 wk prepartum of the nonlactating dry period on core body temperature, melatonin, blood glucose, β-hydroxybutyric acid (BHB) and nonesterified fatty acid (NEFA) concentrations, and milk production. Multiparous cows were moved to tiestalls at 5 wk before expected calving and assigned to control (CTR; n = 16) or phase-shifted (PS; n = 16) treatments. Control cows were exposed to 16 h of light and 8 h of dark. Phase-shifted cows were exposed to the same photoperiod; however, the light-dark cycle was shifted 6 h every 3 d until parturition. Resting behavior and feed intake were recorded daily. Core body temperature was recorded vaginally for 48 h at 23 and 9 d before expected calving using calibrated data loggers. Blood concentrations of melatonin, glucose, BHB, and NEFA were measured during the pre-and postpartum periods. Milk yield and composition were measured through 60 DIM. Treatment did not affect feed intake or body condition. Cosine fit analysis of 24-h core body temperature and circulating melatonin indicated attenuation of circadian rhythms in the PS treatment compared with the CTR treatment. Phase-shifted cows had lower rest consolidation, as indicated by more total resting time, but shorter resting period durations. Phase-shifted cows had lower blood glucose concentration compared with CTR cows (4 mg/mL decrease), but BHB and NEFA concentrations were similar between PS and CTR cows. Milk yield and milk fat yield were greater in PS compared with CTR cows (2.8 kg/d increase). Thus, exposure to chronic light-dark phase shifts during the prepartum period attenuated circadian rhythms of core body temperature, melatonin, and rest-activity behavior and was associated with increased milk fat and milk yield in the postpartum period despite decreased blood glucose pre-and postpartum. Therefore, less variation in central circadian rhythms may create a more constant milieu that supports the onset of lactogenesis.

Chronic prepartum light-dark phase shifts in cattle disrupt circadian clocks, decrease insulin sensitivity and mammary development, and are associated with lower milk yield through 60 days postpartum

“…Although there was no treatment difference in amplitude at 23 d BEC, at 9 d BEC the PS cows had a lower amplitude at 9 d BEC compared with the CON group. These findings were similar to our previous study (Suarez-Trujillo et al, 2020) and support that the CTS was disrupted in PS cattle.…”

“…Across all cows, temperature MESOR and AUC increased between 23 and 9 d BEC. These results are in agreement with Suarez-Trujillo et al (2020), and likely reflect the increased metabolic output as cows transition to lactation (Gamo et al, 2013). At 14 DIM, there was no difference in R 2 or amplitude between treatments, and across all cattle R 2 was significantly lower than during 23 and 9 d BEC recording periods.…”

“…As detailed by Suarez-Trujillo et al (2020), in the prepartum period, all animals were housed in the same experimental tiestall barn, which was partitioned to separate treatments with floor to ceiling draping of 2 layers of fire-retardant tarps (Tarps Plus, Abadak Inc., Georgetown, TX). Outside sources of light were blocked by covering windows with black plastic and caulking was used around doors to block natural light.…”

“…A crossover study design of dairy cattle found that exposure to chronic light-dark phase shifts during an established lactation decreased milk yield (Casey et al, 2014). On the other hand, late pregnant nonlactating dry cows exposed to chronic light-dark phase shifts over the last 5 wk of gestation had reduced plasma glucose concentrations and yielded a greater amount of milk during the following 2 mo of lactation compared with a group under a consistent timing of light (Suarez-Trujillo et al, 2020). Restricting feeding time to normal times of rests disrupts the CTS.…”

Chronodisruption: effects on reproduction, transgenerational health of offspring and epigenome

“…However, exposure to a light-dark cycle until postnatal day 90 did not restore either the normal metabolic state or the daily rhythm of AVP, VIP and PER1 in the SCN of adult rats indicating a permanent impairment to the SCN during lactation (Madahi et al 2018). In addition, exposure to chronic light-dark phase shifts during the prepartum period was associated with increased milk fat and milk yield in the postpartum period despite decreased blood glucose preand postpartum (Suarez-Trujillo et al 2020). Thus, less variation in central circadian rhythms provides a more constant milieu to support the onset of lactogenesis.…”