INTRODUCTION

Within moments of a natural vaginal birth, without invasive birthing practices, newborns demonstrate innate feeding behaviors and instinctively seek out and ‘crawl’ toward the mother’s breast to attach themselves [1,2] their hands exploring and massaging the breast [3]. The functional steps that lead mammalian infants to seek out the nipple and attach themselves to it before proper sucking sets in are not fully understood [2], but it is known that early sucking behavior is easily upset by unfavorable conditions [4].

The human female’s areolar region is of special interest in this journey, because numerous features linked to the natural progression of the birth to breastfeeding continuum are concentrated in it [5] Apart from providing the infant with access to colostrum and milk, the nipple region provides chemical signals that appear to be particularly important to the neonate [6]. The attractiveness of maternal breast odors in the biological context of breastfeeding has a similar function to the role of ‘nipple search pheromone’ in guiding newborn mammalians to the nipple. Although maternal odors may not be as critical for nipple localization in the human species, they may nevertheless facilitate early breastfeeding attempts [7]. In addition to helping to guide the infant directly to the nipple, maternal breast odors affect other aspects of neonatal behavior that increase the probability of successful nipple grasping and feeding [8]. At the same time, they may help the infant to recognize its mother and, therefore, play a role in infant-mother bonding [9,10].

The areola region contains a dense accumulation of apocrine and sebaceous skin glands, which could contribute to producing attractive chemical signals or serve as odor fixatives that prolong the effectiveness of the odor [5]. In addition, the diffusion of odorous molecules may be enhanced by the relatively high surface temperature of the areola, due to the rich supply of blood vessels in this region [11,12]. There is some scientific evidence that describes how the infant behaves and responds to the odors that are naturally released by breasts of lactating women [13].

This study aimed to examine in greater detail how the infant locates the mother’s breast and to assess a number of previously overlooked dermatologic features. The primary objective of this study was to measure the temperature of the areola and the corresponding inside superior quadrant early after birth. Breast pH and elasticity were also assessed.

RESULTS

The maternal and neonatal anthropometrical and clinical characteristics are outlined in Table 1.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 1. Maternal and neonatal anthropometrical and clinical characteristics at birth.

https://doi.org/10.1371/journal.pone.0118774.t001

The mothers’ mean age was approximately 33 years and about 20% underwent a caesarean section, with 60% of these being elective. They were breastfeeding exclusively when they were enrolled in the study. At discharge, most of the mothers were still breastfeeding exclusively, with seven (10%) giving their infants some formula milk. The infants’ mean body weight at discharge was 5.7% lower than their birth weight.

Table 2 shows the dermatologic features of the areola and corresponding inside breast quadrant.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 2. Dermatologic features of the areola and corresponding inside breast quadrant.

https://doi.org/10.1371/journal.pone.0118774.t002

The mean temperature values of the areola skin were significantly higher than the adjacent quadrant (34.60 ±1.40°C vs. 34.04 ±2.00°C, p<0.001).

The mean pH levels of the areola skin were also significantly higher then the adjacent quadrant (4.60±0.59 vs. 4.17±0.59, p<0.001).

In contrast, the mean elasticity values of the areola were significantly lower than the adjacent quadrant (23.52±7.83 vs. 29.02±8.44 cu, p<0.003).

DISCUSSION

This study provides new information about some of the dermatologic properties of the areolar region in lactating mothers and some aspects of the ‘breast crawl’ phenomenon. Our findings show, for the first time, that the areolar region has a higher temperature than the surrounding breast skin, together with higher pH values and lower elasticity.

To the best of our knowledge, these dermatological features have never been examined using a scientific method during the period that breastfeeding is being established, nor have they been compared quantitatively with the surrounding quadrant skin. Higher areolar temperature, alone or combined with multiple sources of odorants and lipid fixatives, may serve as a heat-based communicative function and act as a thermal signal to guide the infant directly to the nipple.

Newborns can perceive the difference in temperature between the areola and the rest of the breast skin [16–18], just as they seem to be sensitive to, and exhibit a preference for, their mother’s scent [19]. In a series of studies, neonates were found to consistently prefer, and to move towards, the smell of their mothers’ breasts [20]. This could be due to a double action, both on the mouth sensitivity receptors and on the olfactory receptor neurons. In fact, lips and fingertips are often considered to be the areas with the highest concentrations of receptor cells [18]. Moreover, the areas of the brain that receive messages from touch receptors in the lips and hands are much larger than those receiving messages from less sensitive places and more brain power is spent interpreting touch sensations from the lips and fingers than from other areas [18].

This thermal characteristic may also play a role in regulating the local evaporation rate of odorants, thereby enhancing their effective role in stimulation. This is linked to olfactory learning, which is essential for neonatal behavioral adaptation in many mammals, including humans [19–21]. Birth and the first hours of life are crucial for olfactory learning. During this period the smells emanating from the mother and newborn interact with one other and animal studies have shown that there is an interaction in processing olfactory signals on both sides [21,22]. Thermal and olfactory signals may help the newborn to locate the nipple and attach to it, leading to the first sucking experience.

Although it is only small, the nipple-areolar region is densely supplied with varied exocrine and enlarged sebaceous skin glands, with small prominences that Morgagni called ‘‘tubercles” [2], coalescing sebaceous glands and miniature mammary acini [2,23]. Colostrum and milk are released from the nipple through the main lactiferous ducts and their intrinsic olfactory qualities and odorants reflect the mother’s diet, metabolism and genetic constitution [24]. These varied sources of substrates combine to create a composite, highly complex odor cocktail. The higher pH found in the areolar skin originates from this mixture and may indeed favor, or act as an odor fixative, to improve the stability of the olfactory complex that is formed on the surface of the areolar [25]. In addition, Haller’s sub areolar vascular plexus provides the areolar with a higher surface temperature than the nipple and the rest of the breast [11]. As we hypothesized earlier in this paper, this thermal characteristic may regulate the local evaporation rate of odorants, thereby enhancing their stimulating effectiveness. A vaginal delivery sets off a surge of catecholamine, which facilitates the newborn’s adaptation to extra uterine life and extensive crying [26]. It is interesting to note that the areola’s thermal feature is triggered by the crying infant [27], resulting in optimal conditions for odor release in anticipation of when the infant is offered the mother’s breast.

We presume that the characteristics of the areolar region that we report here have a biological significance. Firstly, the higher pH during early lactation may be linked to local epidermal and ductal protection from pathogens [28]. Secondly, lower areolar elasticity and greasy secretions may help to preserve the skin from the corrosive action of the infant’s saliva and from sucking-related stress [29]. Thirdly, skin gland secretions, infant saliva and lower elasticity may all be needed to create the hermetic seal that makes sucking effective [30].

Using bioengineering methods to assess nipple and breast skin features during the natural progression from birth to breastfeeding has not eliminated several study limitations. In particular, it was impossible to calculate the statistical power as there is no data in the literature regarding areolar pH, temperature or elasticity. More information about the ‘breast crawl’ phenomenon would be necessary to clarify other variables (i.e. maternal age, parity, if labor was induced, if and what type of analgesics were used, and the delivery route) that could influence mothers’ hormonal and neuroendocrinal response [31] and confound the final outcome. We did not observe the mothers’ attitude nor did we monitor their psycho-emotional and hormonal changes during the ‘breast crawl’ and early breastfeeding which could influence breast skin pH, temperature, and elasticity. These and the fact that there was no control group, can be considered other study limits.