Gardner D S, Jamall E, Fletcher A J W, Fowden A L, Giussani D A
The Physiological Laboratory, University of Cambridge, UK.
J Physiol. 2004 Jun 15;557(Pt 3):1021-32. doi: 10.1113/jphysiol.2004.061796. Epub 2004 Apr 8.
Twin fetuses experience much higher rates of perinatal mortality/morbidity than age- and weight-matched singletons. Across species, the prepartum increase in fetal plasma cortisol is responsible for maturing a number of systems in preparation for birth and the immediate postnatal period. In sheep, it is known that basal adrenocortical function is delayed in twins relative to singletons. Thus, it could be argued that relative immaturity in twins may explain their increased susceptibility to stress in the perinatal period and their relatively poor perinatal outcome. However, whether adrenocortical responsiveness to stress is also diminished in the twin fetus and whether the fetal cardiovascular, metabolic and endocrine defences to acute stress are comparatively weak in the twin fetus is unknown. This study investigated the effect of twinning on adrenocortical responsiveness to either the physiological stress of acute hypoxaemia or to an exogenous ACTH test, and on the fetal cardiovascular, metabolic and endocrine responses to acute hypoxaemic stress. Twenty Welsh Mountain sheep fetuses were chronically instrumented (1-2% halothane) at 121 +/- 3 days of gestation (term is ca 145 days) with amniotic and vascular catheters and with a transit-time flow probe around a femoral artery. The animals were divided into two groups based upon fetal number (singletons, n= 10; twins, n= 10), as determined at surgery. At 130 +/- 2 days, a 1 h episode of acute, isocapnic hypoxaemia (to reduce carotid P(O(2)) to 12 +/- 1 mmHg) was induced in all fetuses by reducing the maternal inspired O(2) fraction (F(IO(2)); 9% O(2) in N(2)). Fetal cardiovascular variables were recorded at 1 s intervals throughout the experimental protocol and arterial blood samples taken at appropriate intervals for biophysical (blood gases, glucose, lactate) and endocrine (catecholamines, vasopressin, cortisol, ACTH) measures. At 133 +/- 2 days a 2.5 microg bolus dose of synthetic ACTH (Synacthen; Ciba Pharmaceuticals, UK) was injected i.v. into eight of the singleton and six of the twin fetuses to determine adrenocortical steroidogenic sensitivity to exogenous ACTH. Under basal conditions, twins had lower plasma cortisol concentration, arterial blood pressure and femoral blood flow relative to singleton fetuses. Twins responded to acute hypoxaemia with similar pressor and vasopressor responses compared to singleton fetuses. However, the rate pressure product, an index of myocardial work, tended to decrease during hypoxaemia in twins, in contrast to the increase observed in singletons. Similar increases in the fetal plasma concentrations of ACTH, AVP, noradrenaline and adrenaline were observed during hypoxaemia in both groups; however, both the increments in fetal plasma concentration of cortisol in response to acute hypoxaemia and to exogenous ACTH were blunted in twins relative to singletons. This study shows that basal adrenocortical function as well as adrenocortical responsiveness is blunted in the twin relative to the singleton fetus. Further, the mechanism for adrenocortical blunting resides at the level of the adrenal cortex rather than higher up the axis. Relative adrenocortical immaturity in the twin fetus may reflect a specific endocrine adaptation to prolong gestation in multiple ovine pregnancies; however, such an adaptation does not affect the cardiovascular, metabolic or endocrine defence responses to acute hypoxaemia in the twin fetus.
双胎胎儿的围产期死亡率/发病率比年龄和体重匹配的单胎胎儿高得多。在所有物种中,胎儿血浆皮质醇在产前的增加负责使许多系统成熟,为出生及出生后即刻阶段做准备。在绵羊中,已知双胎胎儿的基础肾上腺皮质功能相对于单胎胎儿有所延迟。因此,可以认为双胎胎儿相对不成熟可能解释了它们在围产期对压力的易感性增加以及相对较差的围产期结局。然而,双胎胎儿的肾上腺皮质对应激的反应性是否也降低,以及双胎胎儿对急性应激的胎儿心血管、代谢和内分泌防御是否相对较弱尚不清楚。本研究调查了双胎妊娠对肾上腺皮质对急性低氧血症的生理应激或外源性促肾上腺皮质激素(ACTH)试验的反应性的影响,以及对急性低氧应激的胎儿心血管、代谢和内分泌反应的影响。在妊娠121±3天(足月约为145天)时,对20只威尔士山地绵羊胎儿进行慢性插管(1 - 2%氟烷),插入羊膜和血管导管,并在股动脉周围放置一个渡越时间血流探头。根据手术时确定的胎儿数量将动物分为两组(单胎,n = 10;双胎,n = 10)。在130±2天时,通过降低母体吸入氧分数(F(IO₂);氮气中9%氧气),对所有胎儿诱导1小时的急性等碳酸血症性低氧血症(将颈动脉P(O₂)降至12±1 mmHg)。在整个实验过程中,以1秒的间隔记录胎儿心血管变量,并在适当间隔采集动脉血样本进行生物物理(血气、葡萄糖、乳酸)和内分泌(儿茶酚胺、血管加压素、皮质醇、ACTH)测量。在133±2天时,将2.5微克合成ACTH(赛诺同;英国汽巴制药公司)静脉注射到8只单胎胎儿和6只双胎胎儿中,以确定肾上腺皮质对外源性ACTH的类固醇生成敏感性。在基础条件下,与单胎胎儿相比,双胎胎儿的血浆皮质醇浓度、动脉血压和股血流量较低。与单胎胎儿相比,双胎胎儿对急性低氧血症的升压和血管加压反应相似。然而,与单胎胎儿中观察到的增加相反,双胎胎儿在低氧血症期间心肌作功指标心率血压乘积倾向于降低。两组在低氧血症期间胎儿血浆ACTH、抗利尿激素、去甲肾上腺素和肾上腺素浓度均有类似增加;然而,与单胎胎儿相比,双胎胎儿对急性低氧血症和外源性ACTH反应时血浆皮质醇浓度的增加均减弱。本研究表明,相对于单胎胎儿,双胎胎儿的基础肾上腺皮质功能以及肾上腺皮质反应性均减弱。此外,肾上腺皮质反应减弱的机制存在于肾上腺皮质水平而非轴的更高部位。双胎胎儿相对肾上腺皮质不成熟可能反映了多胎绵羊妊娠中延长妊娠期的一种特定内分泌适应;然而,这种适应并不影响双胎胎儿对急性低氧血症的心血管、代谢或内分泌防御反应。