Effect of circadian system disruption on the concentration and daily oscillations of cortisol, progesterone, melatonin, serotonin, growth hormone, and core body temperature in periparturient dairy cattle

Abstract

Metabolic, circadian, sleep, and reproductive systems are integrated and reciprocally regulated, but the understanding of the mechanism is limited. To study this integrated regulation, the circadian timing system was disrupted by exposing late pregnant nonlactating (dry) cows to chronic shifts in the light-dark phase, and rhythms of body temperature and circulating cortisol (CORT), progesterone (P4), serotonin (5HT), melatonin (MEL), and growth hormone (GH) concentrations were measured. Specifically, across 2 identical studies (1 and 2), at 35 d before expected calving (BEC) multiparous cows were assigned to control (CON; n = 24) and exposed to 16 h light and 8 h dark or phase shift (PS; n = 24) treatments and exposed to 6-h light-dark phase shifts every 3 d until parturition. All cows were exposed to control lighting after calving. Blood samples were collected in the first study at 0600 h on d 35 BEC, d 21 BEC, and 2 d before calving, and d 0, 2, 9, 15, and 22 postpartum (PP). A subset of cows (n = 6/group) in study 1 was blood sampled every 4 h over 48 h beginning on d 23 BEC, 9 BEC, and 5 PP. Body temperature was measured every 30 min (n = 8-16/treatment) for 48 h at 23 BEC and 9 BEC in both studies; and at 14 PP and 60 PP only in study 2. Treatment did not affect levels of CORT, GH, or P4 at 0600 h, but overall level of 5HT was lower and MEL higher in PS cows across days sampled. A 2-component versus single-component cosinor model better described [>coefficient of determination (R 2 ); <Akaike information criterion and <Bayesian information criterion] daily oscillations of all hormones and tempera-ture for both treatments. Circadian rhythm fit (R 2 ) of body temperature and MEL increased from 23 BEC to 9 BEC in CON and was marked by loss of feeding time influence on oscillations in both treatments. Both treatments exhibited circadian rhythms of CORT at 9 BEC, CON cows also exhibited circadian rhythms in P4 at 23 BEC, and 5HT at 9 BEC. Daily oscillations in temperature and hormones, except CORT, were affected by PS treatment in the prepartum and were associated with longer gestation. In the PP, circadian rhythmicity was lost or diminished for all hormones and body temperature in both treatments. Stronger rhythms of body temperature and multiple hormones at 1 wk prepartum may indicate a synchronizing cue to time parturition. Therefore, dairy systems may need to consider management factors that affect circadian clocks in late-gestation cows.

Circadian clocks and their integration with metabolic and reproductive systems: our current understanding and its application to the management of dairy cows

“…In primates, the nocturnal onset of labor coincides with increased sensitivity of the pregnant uterus to oxytocin and melatonin, two hormones driving pregnancy associated uterine contractions ( Hirst et al, 1993 ; Olcese et al, 2013 ; Olcese 2014 ). Studies of sheep have shown that circadian disruption during pregnancy increased gestation length ( Gatford et al, 2019 ), and we similarly found longer gestation length in cows exposed to chronic light-dark phase shifts during the dry period ( Suarez-Trujillo et al, 2022 ). In this study we observed that cows exposed to regular 24 h light-dark cycles (control) exhibited more robust circadian rhythms of core body temperature, cortisol, and serotonin as they approached parturition.…”

“…Ruminants also show food anticipatory activity, as circadian rhythms of activity and temperature similarly shifted in response to timed meal feeding in sheep and goats ( Piccione et al, 2003 , 2007 ; Giannetto et al, 2010 ). Our studies of dairy cows found evidence for a food anticipatory rise in core body temperature at three weeks before expected calving in non-lactating (dry) cows ( Suarez-Trujillo et al, 2022 ). In lactating cows, feeding time affects circadian rhythms of feeding and lying behavior, and core body temperature ( Niu et al, 2014 ).…”

“…At the onset of lactation, cow activity becomes significantly diminished with daily patterns of activity influenced by milking and feeding times ( Piccione et al, 2011 ). During the transition from late gestation to early lactation dairy cows ( Suarez-Trujillo et al, 2022 ) and goats ( Kalyesubula et al, 2021 ) exhibited diminished temporal organization of daily rhythms of body temperature and multiple hormones. The major physiological changes that occur in dairy cows at parturition with the initiation of lactation are accompanied by major changes in management that include housing, social interactions, initiation of milking and feed.…”

Melatonin in Health and Disease: A Perspective for Livestock Production

“…There is evidence that cattle exhibit a distinguished circadian rhythm in body temperature which fluctuates by season and reproductive stages [ 51 , 52 ]. In humans, the core body temperature reaches its lowest point at 03:00 to 06:00 a.m., completely opposite of the observed increase in melatonin synthesis [ 53 ].…”

Rodent control of chamber brightness leads to the emergence of unique circadian rhythms

“…The circadian cycles of free-ranging nocturnal rodents are shortened under constant-dark (DD) conditions 9,10 and extended under constant-light (LL) conditions 11,12 relative to those lasting 24 h per day. Under anomalous environmental rhythms such as a 16-h light/8-h dark cycle 13 and delayed 14 or advanced 15,16 phase shifts, rodents respond by altering their circadian cycles within a certain range but may also exhibit some physiological malfunctions 17,18 . Indeed, discrepancies between environmental and internal rhythms cause stress and often lead to social and psychological disorders 6,19,20 .…”