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Oxytocin effects in mothers and during

Oxytocin integrates the function of several body systems and exerts many effects in mothers and infants during breastfeeding. This article explains the pathways of oxytocin release and reviews how oxytocin can affect behaviour due to its parallel release into the blood circulation and the . Oxytocin levels are higher in the than in the mother and these levels are affected by mode of . The importance of skin-to-skin contact and its association with breastfeeding and mother-infant bonding is discussed.

Kerstin Uvnäs Moberg Oxytocin – a system activator increased function of inhibitory alpha-2 3 MD, PhD xytocin, a small of just nine adrenoceptors . Professor of amino acids, is normally associated The regulation of the release of oxytocin Swedish University of Agriculture O with labour and the milk ejection reflex. is complex and can be affected by different [email protected] However, oxytocin is not only a types of sensory inputs, by such Danielle K. Prime but also a and a as oestrogen and even by the oxytocin 1,2 molecule itself. This article will focus on PhD paracrine substance in the brain . During Breastfeeding Research Associate breastfeeding it is released into the brain of four major sensory input nervous Medela AG, Baar, Switzerland both mother and infant where it induces a pathways (FIGURES 2 and 3) activated by: great variety of functional responses. 1. Sucking of the mother’s , in which Through three different release pathways the sensory nerves originate in the (FIGURE 1), oxytocin functions rather like a . system activator and often influences the 2. Sucking in the infant, in which the release of other signalling substances such sensory nerves originate in the infant as , , and oral mucosa. noradrenaline. Through these activations, 3. The presence of food in the different behavioural and physiological gastrointestinal tract, affecting vagal effects are facilitated and coordinated into sensory nerves. adaptive patterns, which are influenced by 4. Skin-to-skin contact in both mothers the type of stimuli and environmental and infants, in which the sensory nerves 3 Keywords factors . that originate in the skin respond to Through the endogenous release of oxytocin; breastfeeding; skin-to-skin; warmth, touch, stroking and light anti-stress; milk ejection; bonding oxytocin or its administration, for example pressure. by nasal spray in humans, various types of Key points socially interactive behaviours can be The mother stimulated. These include maternal and Uvnäs Moberg K., Prime D.K. Oxytocin Milk ejection effects in mothers and infants during sexual behaviours as well as the develop- 4 Oxytocin is critical for milk removal in, breastfeeding. Infant 2013; 9(6): 201-06. ment of bonding and attachment . 1. Oxytocin is released in the mother and Oxytocin stimulates well-being, it induces perhaps, its most renowned role: the milk infant during breastfeeding and skin-to- anti-stress effects, decreases sensitivity to ejection reflex. Following sucking, the skin contact. pain, decreases and release of oxytocin causes the contraction 2. Milk ejection patterns vary between stimulates processes related to growth and of myoepithelial cells in the breast pushing women. healing. In addition, repeated exposure to milk from the alveoli, through the milk 3. Oxytocin is released into circulating oxytocin may give rise to long-term effects ducts and toward the nipple. blood and brain structures, in parallel. by influencing the production or function In general, it takes around a minute of 4. Oxytocin levels are higher in the infant of other signalling systems. For example, infant sucking or with a breast than in the mother and differ with noradrenergic activity in the brain pump before milk ejection occurs5,6. mode of birth. may decrease as a consequence of the Interestingly, the milk ejection reflex can be infant VOLUME 9 ISSUE 6 2013 201 REVIEW

have continuous milk ejections throughout the milk removal session. Both of these Parvocellular Central oxytocin release: patterns can remove similar volumes of project into brain Magnocellular neurons milk successfully, but the second scenario structures and Central oxytocin release: Dendritic extracellular would require more to reach that 5 Axons of same level of milk removal . Similar parvocellular neurons repeatability has been observed in

Paraventricular individual infants at successive breast- nucleus (PVN) feeds14; these mother-derived patterns may explain why some infants are quick feeders (SON) and others take a bit more time. Axons of magnocellular Oxytocin-induced effects in the brain neurons It is not known why mothers have such varied milk ejection patterns but, since Oxytocin oxytocin is involved in so many functions, these release patterns may not only impact Capillary on milk removal. Systemic oxytocin release and its release into the brain may result in many other outcomes involving Peripheral oxytocin release: breastfeeding and mother-infant Axonal release into blood to target distant organs interactions. For example, breastfeeding in mothers is associated with physiological and psychological adaptations including: ■ Increased social interaction FIGURE 1 The release of oxytocin from the supraoptic (SON) and paraventricular (PVN) nuclei ■ Decreased of the . Magnocellular neurons in the SON and PVN release oxytocin centrally ■ and peripherally from the posterior pituitary, resulting in effects that include milk ejection and Decreased levels ■ . Parvocellular neurons, located in the PVN, project axons directly into brain Decreased blood pressure structures involved in the regulation of social interaction, anxiety, the activity of the ■ Increased gastrointestinal tract 15-17 hypothalamic-pituitary-adrenal axis, well-being and the autonomic (eg the function . , hypothalamus, anterior pituitary, , nucleus tractus solitarius and These effects are exerted in the brain but the dorsal vagal motor nucleus). are associated with circulating oxytocin levels, supporting the concept that oxytocin is released systemically and into easily conditioned and many women can birth, but there is still a strong correlation the brain in parallel, as has previously been experience spontaneous milk ejections between the amount of oxytocin released demonstrated in sheep in response to between feeds7,8 as the sight, thought, on the two occasions within individual suckling18. sound and smell of the infant (or even a women13. breast pump in pump-dependent mothers) One pulse of oxytocin is generally The infant can cause milk ejection and dripping of associated with one milk ejection and there Infants produce oxytocin too and in fact, milk from the . Indeed, it is is a relationship between the amount of the production of oxytocin begins in the common that milk ejection occurs prior to oxytocin released and the number of fetus. An understanding of the infant the physical attachment of the infant or a oxytocin pulses during the first 10 minutes oxytocin system is complicated by breast pump7,9. of breastfeeding12. The number of milk difficulties in collecting repeat blood Milk ejection can be associated with ejections during breastfeeding ranges from samples and measuring circulating different sensations that vary dramatically one to 17 over a period of up to 25 oxytocin levels in the newborn. between women. These may be localised to minutes6,7. Similarly, pulsatile patterns of Nevertheless, some studies exist in which the breast such as a ‘drawing’ pain or two to 14 milk ejections are seen during a oxytocin levels have been measured in the tingling, to more systemic sensations such 15 minute breast expression5. The simil- newborn while other studies have as nausea, thirst, fainting or even mental arity between the milk ejection pattern demonstrated the release of oxytocin anxiety and depression8. resulting from breastfeeding and breast indirectly via expression of oxytocin-linked Sucking- and pumping-induced pumping is demonstrated in FIGURE 4. effect patterns. Information can also be oxytocin release has been described as Tracking an individual mother over drawn from animal experiments, as pulsatile7,10. On average, oxytocin pulses time, it appears that her pattern of milk oxytocin exerts similar effect patterns in all occur with 90-second intervals over the ejection repeats throughout the first nine mammals. first 10 minutes of breastfeeding in the first months of lactation5. If a mother has two few days after birth11,12. The amount of or three milk ejections she will continue Infant oxytocin levels are affected by the oxytocin that is released within a 10 that pattern, removing all her milk in these mode of delivery minute breastfeed is much higher at four brief episodes. Other mothers may follow a In infants born by vaginal delivery, months when compared to four days after more constant pulsing profile in that they oxytocin levels in umbilical arterial blood

202 VOLUME 9 ISSUE 6 2013 infant REVIEW were actually higher than in infants born by : 69pg/mL Skin-to-skin contact (range 20-315pg/mL) vs 33pg/mL (range 9-195pg/mL), respectively. Mothers also had higher oxytocin levels if they delivered vaginally, compared to caesarean Oxytocin release into section. In the first 30 minutes after birth, brain structures infants (born both vaginally and by PVN caesarean) had higher oxytocin levels than Mother’s breast SON those of mothers: approximately 30pg/mL

(range 13-158pg/mL). Over subsequent Systemic NTS hours and days the differences due to oxytocin mode of birth diminish, yet infants will release maintain a higher oxytocin level than their mothers (FIGURE 5). In addition, oxytocin levels recorded postpartum in infants born Sensory nerves enter the vaginally correlate inversely with fetal spinal cord/ and Infant oral mucosa arterial pH and also with the duration of connect to the NTS labour. This suggests that the elevated oxytocin levels recorded postpartum are linked to the stress of being born (Bystrova et al 2013, unpublished results)19.

Ingestion of oxytocin from maternal milk FIGURE 2 Different kinds of sensory nerves can release oxytocin during mother-infant Human milk contains many different interaction. While various sensory nerves can initiate this pathway, the nucleus tractus hormones and growth factors and it also solitarius (NTS) acts as a common relay station for sensory input to the oxytocin-producing contains small amounts of oxytocin. The paraventricular (PVN) and supraoptic (SON) nuclei. (Image © Medela.) concentration of oxytocin in maternal milk is approximately 8pg/mL in the first few days after birth and then decreases with increased milk production. Even if the ingested oxytocin was able to survive the acid milieu of the and was Milk entering the stomach Oxytocin release into absorbed from the small intestine of the brain structures fetus, the dilution within the circulation PVN would limit any significant rise of oxytocin SON levels. It would also be unlikely that transport to the brain would occur because Systemic NTS of the blood-brain-barrier. oxytocin release Oxytocin release by sucking While the intake of oxytocin from human milk has negligible effects, sucking in newborns is associated with infant oxytocin release. In calves, the act of (CCK) sucking at the udder is associated with a rise in oxytocin levels but not when 20 drinking/lapping milk from a bucket . This Vagal sensory nerve effect is caused by activation of sensory nerves in the oral mucosa during sucking. FIGURE 3 The ingestion of food into the infant’s stomach can trigger oxytocin release. Food Furthermore, oxytocin is released when intake results in the release of the gut hormone cholecystokinin (CCK), which, via activation of milk reaches the gastrointestinal tract sensory vagal nerve fibres, results in central and peripheral oxytocin release. (Image © Medela.) (FIGURE 3). Food intake is linked to release of the gut hormone cholecystokinin (CCK) The mother and infant and urogenital tract. Light pressure, which, via activation of the afferent warmth and stroking contribute to Skin-to-skin contact (sensory) vagal nerve fibres, triggers oxytocin release caused by ‘pleasant’ or oxytocin release21. In support of this, infant Oxytocin can be released by activation of ‘non-noxious’ sensory stimulation of the plasma levels of CCK have been shown to several types of sensory nerves originating skin23. rise during breastfeeding22. from the skin, nipples, gastrointestinal tract When newborn infants are put on their infant VOLUME 9 ISSUE 6 2013 203 REVIEW

tractus solitarius (NTS) in the brainstem, Milk ejections during breastfeeding exert a powerful influence on the activity 3 of the HPA axis by stimulating production of CRF in the hypothalamus and activity in 2 the sympathetic nervous system. Oxytocin may decrease stress levels by counteracting 1 the activity in these noradrenergic pathways: administration of oxytocin or 0 the release of oxytocin from oxytocinergic 0246810nerves that terminate in the LC and the Minutes A Milk duct (mm) diameter increase NTS, increases the number or function of inhibitory alpha-2 adrenoceptors located FIGURE 4 Examples on the noradrenergic neurons30,31. Milk ejections during breast expression of the pulsatile 0.6 This type of oxytocin-linked, anti-stress patterns of milk pattern is facilitated in certain situations, ejection during for example, when the skin is exposed to breastfeeding and touch, warmth and light pressure, which breast expression. 0.4 Graph A explains why mothers and newborn infants demonstrates four experiencing skin-to-skin contact exhibit a marked anti-stress pattern. The high levels pulses measured 0.2 during a breastfeed (g/s) Milk flow rate of oxytocin seen in both mothers and by monitoring the infants after vaginal birth (FIGURE 5) may size of the milk duct play an important role. with ultrasound; as 0 24 6 810Bonding and attachment milk is ejected B Minutes through the ductal The act of sucking may also enhance system the milk duct diameter expands (image courtesy of Dr Donna Geddes, Australia). Graph bonding between mothers and newborn B demonstrates four pulses measured during breast expression by monitoring the rate of flow infants and the infant’s attachment to their of milk; as milk is ejected through the ductal system the milk flow rate increases. mother. In support of this, newborn lambs that are allowed to suck at the udder soon mother’s chest immediately after birth, birth, the infant expresses an inborn after birth recognise and follow their oxytocin is released into the maternal breast-seeking behaviour – a ‘social mothers more quickly than those that are circulation (FIGURE 2). The effect is, in part, approach behaviour’25. Both mother and separated from their mothers in the early 32 linked to massage of the by the infant become more socially interactive days after birth . It seems that neural infant24. However, the oxytocin release that and synchronise their interactions26. reflexes induced from the oral mucosa by is induced by skin-to-skin contact does not Mother and infant become calmer, the the touching of the nipple (FIGURE 2) and occur in short pulses in the same way as infant cries less, the pain threshold also the presence of colostrum in the gastrointestinal tract are involved in the oxytocin induced by sucking, but rather in increases, cortisol levels decrease and skin creation of this primitive ‘attachment’ a few protracted pulses. It is not associated temperature of the mother’s breast and of behaviour (FIGURE 3). with milk ejection, but may instead ‘prime’ the infant increases27,28. As discussed below, the ensuing breastfeeding interaction. these effects are likely to involve oxytocin Long-term effects It has not yet been demonstrated that release in the brain. peripheral oxytocin levels rise in response Research has shown that mothers who to skin-to-skin contact in human Oxytocin and inhibition of stress have breastfed for several weeks have lower basal, systolic and diastolic blood pressure newborns. Even if circulating oxytocin It is well known that cortisol release is levels do not rise, it may be assumed that and also lower stress reactivity. This controlled by the hypothalamic-pituitary- oxytocin levels increase in the infant brain supports the existence of a long-term, anti- adrenal (HPA) axis. In this mechanism of in response to these types of stimuli. In the stress influence of oxytocin in humans. interactions, corticotrophin releasing factor following sections a number of effect The finding of a reduced risk for certain (CRF) released from the hypothalamus, patterns, both short- and long-term will be kinds of cardiovascular disease and type 2 stimulates the release of adrenocortico- described. These can be attributed to diabetes in mothers who have breastfed, is trophic hormone (ACTH) from the oxytocin release and/or function in the further support of the connection between brain and are triggered in both the mother anterior pituitary, which in turn releases repeated exposure to endogenous oxytocin and the infant during breastfeeding and cortisol into the circulation from the and long-term, anti-stress effects33. skin-to-skin contact. adrenal cortex. Oxytocin can inhibit the The act of skin-to-skin contact between function of the HPA axis at each of these mother and infant during the first two Social interaction, well-being and levels29. hours after birth has been associated with stress levels What is not well-known is that long-term outcomes. These include When the mother and the newborn infant noradrenergic neurons originating in the enhanced interaction between mother and are placed in skin-to-skin contact after coeruleus (LC) and the nucleus infant and a better ability to handle stress

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References IV 1. Ludwig M., Leng G. Dendritic peptide release and Vaginal (IV) peptide-dependent behaviours. Nat Rev Neurosci Infant C-Section (IC) 2006;7:126-36. Vaginal (MV) Mother C-Section (MC) 2. Sofroniew M.W. and oxytocin in the mammalian brain and spinal cord. Trends Neurosci. IC Oxytocin level in 1983;6:467-72. human milk (OM) 3. Uvnäs-Moberg K., Petersson M. Oxytocin, a MV mediator of anti-stress, well-being, social interaction, growth and healing. Z Psychosom Med Oxytocin levels MC Psychother 2005;51:57-80. [Article in German]. 4. Heinrichs M., Domes G. and social behaviour: effects of oxytocin and vasopressin in OM humans. Prog Brain Res 2008;170:337-50. 5. Prime D.K., Geddes D.T., Hepworth A.R. et al. 1 minute 2 hours 4 days Comparison of the patterns of milk ejection during repeated breast expression session in women. Time after birth Breastfeed Med 2011;6:183-90. 6. Ramsay D.T., Kent J.C., Owens R.A., Hartmann P.E. FIGURE 5 The relative levels of blood oxytocin in the mother and infant in relation to the mode Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics 2004;113:361-67. of birth. The graph shows that infants have much higher oxytocin levels than mothers. In both 7. Cobo E. Characteristics of the spontaneous milk mother and infant it is shown that one minute after birth oxytocin levels are much higher in ejecting activity occurring during human . mothers and infants that have delivered/been born vaginally compared to those who were J Perinatal Med 1993;21:77-85. delivered/born via caesarean section. The magnitude of this difference decreases with time 8. Isbister C. A clinical study of the draught reflex in such that the levels of oxytocin are similar between birth modes from approximately two human lactation. Arch Dis Child 1954;29:66-72. hours after birth. Also indicated is the very low level of oxytocin in the mother’s milk, which 9. Prime D.K., Geddes D.T., Spatz D.L. et al. Using milk further decreases as milk production increases. flow rate to investigate milk ejection in the left and right breasts during simultaneous breast expression in the infant – effects which may be after a while, its release and the consequent in women. Int Breastfeed J 2009;4:10. 10. Ueda T., Yokoyama Y., Irahara M., Aono T. Influence 34,35 measured as long as one year after birth . oxytocin-related effects will be triggered in of psychological stress on suckling-induced pulsatile As an example of a mechanism behind the infant by just the sight, voice or smell oxytocin release. Obstet Gynecol 1994;84:259-62. these long-term effects, decreased levels of of the mother. With time, the infant may 11. Jonas K., Johansson L.M., Nissen E. et al. Effects of anxiety and increased social interaction learn to hold the ‘image’ of its mother even intrapartum oxytocin administration and epidural seen in rats exposed to extra sensory stim- when she is not present and in this way the analgesia on the concentration of plasma oxytocin and , in response to suckling during the ulation after birth has been attributed to an infant may remain calm and happy even second day postpartum. Breastfeed Med 2009;4: increased production/function of oxytocin when alone. Only when the infant becomes 71-82. receptors in the amygdala. The anti-stress fearful does it need to return to the secure 12. Nissen E., Uvnäs-Moberg K., Svensson K. et al. effects have been attributed to a decreased base, or in physiological terms, receive Different patterns of oxytocin, prolactin but not function of the HPA axis36. activation of sensory nerves from the skin, cortisol release during breastfeeding in women delivered by caesarean section or by the vaginal when being held close by the mother (or route. Early Hum Dev 1996;45:103-18. Medical interventions during birth another caregiver) to become happy and 13. Uvnäs-Moberg K., Widstrom A.M., Werner S. et al. It can be concluded that oxytocin calm again. In the long-term, the function Oxytocin and prolactin levels in breast-feeding stimulates socially interactive behaviour of the oxytocin system may become well women. Correlation with milk yield and duration of and induces anti-stress effects and that established in those infants receiving breast-feeding. Acta Obstet Gynecol Scand 1990; 69:301-06. these effects may become long lasting if closeness and friendly encounters by 14. Wooldridge M.W., Baum J.D., Drewett R.F. Individual induced early in life. Many medical primary caregivers: a chronic state of patterns of milk intake during breast-feeding. Early interventions during birth interfere with satisfaction and calm develops – secure Hum Dev 1982;7:265-72. spontaneous oxytocin release. For example: attachment. 15. Uvnäs-Moberg K. of the ■ Caesarean section may be linked to a mother-child interaction. Trends Endocrinol Metab 1996;7:126-31. reduced oxytocin release during labour Conclusion 16. Handlin L., Jonas W., Petersson M. et al. Effects of (or none at all if there is no labour) Oxytocin is an integral component of sucking and skin-to-skin contact on maternal ACTH ■ Epidural analgesia may be linked to many body systems with long-term and cortisol levels during the second day reduced oxytocin release as the Ferguson implications for both mother and baby. It postpartum-influence of epidural analgesia and reflex is partly blocked is not only involved in milk ejection from oxytocin in the perinatal period. Breastfeed Med 2009;4:207-20. ■ Infusions of oxytocin may influence the mother, but is also a key hormone for 17. Jonas W., Nissen E., Ransjo-Arvidson A.B. et al. spontaneous oxytocin release via a feed- the infant and can be influenced by skin- Short- and long-term decrease of blood pressure in back inhibitory mechanism. to-skin contact and birthing practices. women during breastfeeding. Breastfeed Med Recent data suggest that such effects can be Consolidation of current understanding 2008;3:103-09. documented at two days after birth11,37. of oxytocin should encourage consider- 18. Kendrick K.M., Keverne E.B., Hinton M.R., Goode J.A. and plasma concentrations of ation of the value of the natural Development of secure attachment oxytocin and vasopressin during parturition and interaction between mother and infant, vaginocervical stimulation in the sheep. Brain Res Oxytocin release is easily conditioned and, at and after birth. Bull 1991;26:803-07.

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19. Marchini G., Lagercrantz H., Winberg J., Uvnäs- 25. Widstrom A.M., Ransjo-Arvidson A.B., Christensson 1998;255:115-18. Moberg K. Fetal and maternal plasma levels of K. et al. Gastric suction in healthy newborn infants. 31. Caldji C., Diorio J., Meaney M.J. Variations in , and oxytocin after vaginal Effects on circulation and developing feeding maternal care in infancy regulate the development delivery and elective cesarean section. Early Hum behaviour. Acta Paediatr Scand 1987;76:566-72. of stress reactivity. Biol 2000;48:1164-74. Dev 1988;18:73-79. 26. Velandia M., Matthisen A.S., Uvnäs-Moberg K., 32. Nowak R., Murphy T.M., Lindsay D.R. et al. 20. Lupoli B., Johansson B., Uvnäs-Moberg K., Nissen E. Onset of vocal interaction between Development of a preferential relationship with the Svennersten-Sjaunja K. Effect of suckling on the parents and newborns in skin-to-skin contact mother by the newborn lamb: Importance of release of oxytocin, prolactin, cortisol, gastrin, immediately after elective cesarean section. Birth sucking activity. Physiol Behav 1997;62:681-88. cholecystokinin, somatostatin and in dairy 2010;37:192-201. 33. Lee S.Y., Kim M.T., Jee S.H., Yang H.P. Does long-term cows and their calves. J Dairy Res 2001;68:175-87. 27. Bergman N.J., Linley L.L., Fawcus S.R. Randomized lactation protect premenopausal women against 21. Uvnäs-Moberg K. Role of efferent and afferent vagal controlled trial of skin-to-skin contact from birth hypertension risk? A Korean women’s cohort study. nerve activity during : Integrating versus conventional incubator for physiological Prev Med 2005;41:433-38. function of oxytocin on and behaviour. stabilization in 1200- to 2199-gram newborns. Acta 34. Klaus M.H., Jerauld R., Kreger N.C. et al. Maternal Psychoneuroendocrinology 1994;19:687-95. Paediatr 2004;93:779-85. attachment. Importance of the first post-partum 22. Uvnäs-Moberg K., Marchini G., Winberg J. Plasma 28. Bystrova K., Widstrom A.M., Matthiesen A.S. et al. days. N Engl J Med 1972;286:460-63. cholecystokinin concentrations after breast feeding Skin-to-skin contact may reduce negative 35. Bystrova K., Ivanova V., Edhborg M. et al. Early in healthy 4 day old infants. Arch Dis Child 1993;68 consequences of ‘the stress of being born’: a study contact versus separation: effects on mother-infant (1 Spec No):46-48. on temperature in newborn infants, subjected to interaction one year later. Birth 2009;36:97-109. 23. Uvnäs-Moberg K., Petersson M. Role of oxytocin different ward routines in St. Petersburg. Acta 36. Francis D.D., Champagne F.C., Meaney M.J. related effects in manual therapies. In: King H., Janig Paediatr 2003;92:320-26. Variations in maternal behaviour are associated W., Pattersson M.M. (eds). The Science and 29. Neumann I.D. Involvement of the brain oxytocin with differences in oxytocin levels in the Application of Manual Therapy. Amsterdam: system in stress coping: interactions with the rat. J Neuroendocrinol 2000;12:1145-48. Elsevier; 2011. hypothalamo-pituitary-adrenal axis. Prog Brain Res 37. Nissen E., Gustavsson P., Widstrom A.M., Uvnäs- 24. Matthiesen A.S., Ransjo-Arvidson A.B., Nissen E., 2002;139:147-62. Moberg K. Oxytocin, prolactin, milk production and Uvnäs-Moberg K. Postpartum maternal oxytocin 30. Petersson M., Uvnäs-Moberg K., Erhardt S., Engberg their relationship with traits in women release by newborns: effects of infant hand G. Oxytocin increases alpha 2- after vaginal delivery or Cesarean section. massage and sucking. Birth 2001;28:13-19. adrenoreceptor responsiveness in rats. Neurosci Lett J Psychosom Obstet Gynaecol 1998;19:49-58.

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