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Impact of chronodisruption during primate pregnancy on the maternal and newborn temperature rhythms.

Serón-Ferré M, Forcelledo ML, Torres-Farfan C, Valenzuela FJ, Rojas A, Vergara M, Rojas-Garcia PP, Recabarren MP, Valenzuela GJ - PLoS ONE (2013)

Bottom Line: In addition, mean temperature was decreased (34.0±0.6 vs 36.1±0.2°C, in LL and control, respectively P<0.05).Our findings demonstrate that prenatal melatonin is a Zeitgeber for the newborn temperature rhythm and supports normal body temperature maintenance.Altogether these prenatal melatonin effects highlight the physiological importance of the maternal melatonin rhythm during pregnancy for the newborn primate.

View Article: PubMed Central - PubMed

Affiliation: Programa de Fisiopatología, Facultad de Medicina, Universidad de Chile, Santiago, Chile. mseron@med.uchile.cl

ABSTRACT
Disruption of the maternal environment during pregnancy is a key contributor to offspring diseases that develop in adult life. To explore the impact of chronodisruption during pregnancy in primates, we exposed pregnant capuchin monkeys to constant light (eliminating the maternal melatonin rhythm) from the last third of gestation to term. Maternal temperature and activity circadian rhythms were assessed as well as the newborn temperature rhythm. Additionally we studied the effect of daily maternal melatonin replacement during pregnancy on these rhythms. Ten pregnant capuchin monkeys were exposed to constant light from 60% of gestation to term. Five received a daily oral dose of melatonin (250 µg kg/body weight) at 1800 h (LL+Mel) and the other five a placebo (LL). Six additional pregnant females were maintained in a 14∶10 light:dark cycles and their newborns were used as controls (LD). Rhythms were recorded 96 h before delivery in the mother and at 4-6 days of age in the newborn. Exposure to constant light had no effect on the maternal body temperature rhythm however it delayed the acrophase of the activity rhythm. Neither rhythm was affected by melatonin replacement. In contrast, maternal exposure to constant light affected the newborn body temperature rhythm. This rhythm was entrained in control newborns whereas LL newborns showed a random distribution of the acrophases over 24-h. In addition, mean temperature was decreased (34.0±0.6 vs 36.1±0.2°C, in LL and control, respectively P<0.05). Maternal melatonin replacement during pregnancy re-synchronized the acrophases and restored mean temperature to the values in control newborns. Our findings demonstrate that prenatal melatonin is a Zeitgeber for the newborn temperature rhythm and supports normal body temperature maintenance. Altogether these prenatal melatonin effects highlight the physiological importance of the maternal melatonin rhythm during pregnancy for the newborn primate.

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Mean ± SE circadian temperature rhythm in capuchin monkey newborns at 4–6 days of age.Temperature was measured at 15 min intervals by telemetry. Integrated one h values were used to depict the rhythm. LD: newborns from mothers kept in light:dark 14∶10 during pregnancy and reared in LD (n = 6); LL: newborn from mothers maintained in constant light during pregnancy and reared in LL (n = 5); LL+M: newborn from LL mother receiving a daily melatonin replacement at 1800 hours during pregnancy and reared in LL (n = 5). Shaded bars represent light off. Φ indicates the acrophase. The continuous line represents the theoretical 24-h cosinor function fitting the data. The mean data fits a 24-h cosine function (R2 0.83 and 0.82, LD and LL +Mel newborns, respectively).The clocks at the right of the figure show the distribution of acrophases of the individual temperature rhythms in each group of newborns. An arrow denotes the timing of the mean acrophase.
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pone-0057710-g003: Mean ± SE circadian temperature rhythm in capuchin monkey newborns at 4–6 days of age.Temperature was measured at 15 min intervals by telemetry. Integrated one h values were used to depict the rhythm. LD: newborns from mothers kept in light:dark 14∶10 during pregnancy and reared in LD (n = 6); LL: newborn from mothers maintained in constant light during pregnancy and reared in LL (n = 5); LL+M: newborn from LL mother receiving a daily melatonin replacement at 1800 hours during pregnancy and reared in LL (n = 5). Shaded bars represent light off. Φ indicates the acrophase. The continuous line represents the theoretical 24-h cosinor function fitting the data. The mean data fits a 24-h cosine function (R2 0.83 and 0.82, LD and LL +Mel newborns, respectively).The clocks at the right of the figure show the distribution of acrophases of the individual temperature rhythms in each group of newborns. An arrow denotes the timing of the mean acrophase.

Mentions: Maternal chronodisruption by exposure to LL brought changes in the newborn temperature rhythm; these changes were reverted by daily maternal melatonin administration (Table 2). Twenty-four hour body temperature rhythms were detected in all individual LD, LL and LL+ Mel newborns by cosinor analysis (Table 2). However, in the LL newborns, the acrophases of the rhythms were randomly distributed over the 24 h. Acrophases in three of the LL newborns clustered around 2400 h whereas in one newborn the acrophase was almost opposite occurring at 1100 h and in the other at 1700 h. In contrast, acrophases of the body temperature rhythm in newborns of mothers kept in LD during pregnancy and reared in LD after birth concentrated in the late afternoon, between 15.8 and 19.1 h, mean 17.0±0.5 h (P<0.05, Rayleigh’s test, Table 2, Figure 3). A second effect of chronic maternal exposure to constant light during gestation was a decrease in mean body temperature (Table 2). Daily maternal melatonin replacement during pregnancy had a synchronizing effect, restoring the acrophase of the newborn temperature rhythm to the late afternoon (range 17.2 and 18.4 h; mean 17.9±0.2, P<0.05, Rayleigh’s test), clock time similar to that found in the newborns from LD mothers and also restored the mesor (Table 2).


Impact of chronodisruption during primate pregnancy on the maternal and newborn temperature rhythms.

Serón-Ferré M, Forcelledo ML, Torres-Farfan C, Valenzuela FJ, Rojas A, Vergara M, Rojas-Garcia PP, Recabarren MP, Valenzuela GJ - PLoS ONE (2013)

Mean ± SE circadian temperature rhythm in capuchin monkey newborns at 4–6 days of age.Temperature was measured at 15 min intervals by telemetry. Integrated one h values were used to depict the rhythm. LD: newborns from mothers kept in light:dark 14∶10 during pregnancy and reared in LD (n = 6); LL: newborn from mothers maintained in constant light during pregnancy and reared in LL (n = 5); LL+M: newborn from LL mother receiving a daily melatonin replacement at 1800 hours during pregnancy and reared in LL (n = 5). Shaded bars represent light off. Φ indicates the acrophase. The continuous line represents the theoretical 24-h cosinor function fitting the data. The mean data fits a 24-h cosine function (R2 0.83 and 0.82, LD and LL +Mel newborns, respectively).The clocks at the right of the figure show the distribution of acrophases of the individual temperature rhythms in each group of newborns. An arrow denotes the timing of the mean acrophase.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585206&req=5

pone-0057710-g003: Mean ± SE circadian temperature rhythm in capuchin monkey newborns at 4–6 days of age.Temperature was measured at 15 min intervals by telemetry. Integrated one h values were used to depict the rhythm. LD: newborns from mothers kept in light:dark 14∶10 during pregnancy and reared in LD (n = 6); LL: newborn from mothers maintained in constant light during pregnancy and reared in LL (n = 5); LL+M: newborn from LL mother receiving a daily melatonin replacement at 1800 hours during pregnancy and reared in LL (n = 5). Shaded bars represent light off. Φ indicates the acrophase. The continuous line represents the theoretical 24-h cosinor function fitting the data. The mean data fits a 24-h cosine function (R2 0.83 and 0.82, LD and LL +Mel newborns, respectively).The clocks at the right of the figure show the distribution of acrophases of the individual temperature rhythms in each group of newborns. An arrow denotes the timing of the mean acrophase.
Mentions: Maternal chronodisruption by exposure to LL brought changes in the newborn temperature rhythm; these changes were reverted by daily maternal melatonin administration (Table 2). Twenty-four hour body temperature rhythms were detected in all individual LD, LL and LL+ Mel newborns by cosinor analysis (Table 2). However, in the LL newborns, the acrophases of the rhythms were randomly distributed over the 24 h. Acrophases in three of the LL newborns clustered around 2400 h whereas in one newborn the acrophase was almost opposite occurring at 1100 h and in the other at 1700 h. In contrast, acrophases of the body temperature rhythm in newborns of mothers kept in LD during pregnancy and reared in LD after birth concentrated in the late afternoon, between 15.8 and 19.1 h, mean 17.0±0.5 h (P<0.05, Rayleigh’s test, Table 2, Figure 3). A second effect of chronic maternal exposure to constant light during gestation was a decrease in mean body temperature (Table 2). Daily maternal melatonin replacement during pregnancy had a synchronizing effect, restoring the acrophase of the newborn temperature rhythm to the late afternoon (range 17.2 and 18.4 h; mean 17.9±0.2, P<0.05, Rayleigh’s test), clock time similar to that found in the newborns from LD mothers and also restored the mesor (Table 2).

Bottom Line: In addition, mean temperature was decreased (34.0±0.6 vs 36.1±0.2°C, in LL and control, respectively P<0.05).Our findings demonstrate that prenatal melatonin is a Zeitgeber for the newborn temperature rhythm and supports normal body temperature maintenance.Altogether these prenatal melatonin effects highlight the physiological importance of the maternal melatonin rhythm during pregnancy for the newborn primate.

View Article: PubMed Central - PubMed

Affiliation: Programa de Fisiopatología, Facultad de Medicina, Universidad de Chile, Santiago, Chile. mseron@med.uchile.cl

ABSTRACT
Disruption of the maternal environment during pregnancy is a key contributor to offspring diseases that develop in adult life. To explore the impact of chronodisruption during pregnancy in primates, we exposed pregnant capuchin monkeys to constant light (eliminating the maternal melatonin rhythm) from the last third of gestation to term. Maternal temperature and activity circadian rhythms were assessed as well as the newborn temperature rhythm. Additionally we studied the effect of daily maternal melatonin replacement during pregnancy on these rhythms. Ten pregnant capuchin monkeys were exposed to constant light from 60% of gestation to term. Five received a daily oral dose of melatonin (250 µg kg/body weight) at 1800 h (LL+Mel) and the other five a placebo (LL). Six additional pregnant females were maintained in a 14∶10 light:dark cycles and their newborns were used as controls (LD). Rhythms were recorded 96 h before delivery in the mother and at 4-6 days of age in the newborn. Exposure to constant light had no effect on the maternal body temperature rhythm however it delayed the acrophase of the activity rhythm. Neither rhythm was affected by melatonin replacement. In contrast, maternal exposure to constant light affected the newborn body temperature rhythm. This rhythm was entrained in control newborns whereas LL newborns showed a random distribution of the acrophases over 24-h. In addition, mean temperature was decreased (34.0±0.6 vs 36.1±0.2°C, in LL and control, respectively P<0.05). Maternal melatonin replacement during pregnancy re-synchronized the acrophases and restored mean temperature to the values in control newborns. Our findings demonstrate that prenatal melatonin is a Zeitgeber for the newborn temperature rhythm and supports normal body temperature maintenance. Altogether these prenatal melatonin effects highlight the physiological importance of the maternal melatonin rhythm during pregnancy for the newborn primate.

Show MeSH
Related in: MedlinePlus