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• W2120878548 abstract "After completing this article, readers should be able to: “Compared with newborns of other species, the human neonate is relatively helpless in motor capabilities and relatively precocious in sensory capabilities.”—T. Berry BrazeltonBehavioral CompetenceAvery’s Neonatology. 5th ed. 1999Accumulating evidence suggests a connection between the developing brain and the developing skin. In this view, the skin, broadly considered, functions as a neurodevelopmental boundary in the very low-birthweight (VLBW) preterm infant. The epidermis, for example, plays a role as a specialized ectodermal derivative closely linked to both neuroperception and noninvasive monitoring in intensive care environments. The terminal differentiation product of the epidermis, the stratum corneum, is considered a prototypical smart material. The concept of the skin as a neurodevelopmental interface may be broadened to include its role as an interface with the caregiver and a boundary for primary care delivery in the neonatal intensive care unit.Recent reviews have demonstrated the persistence of a high incidence of severe neurodevelopmental disability in VLBW preterm infants (Fig 1 ). (1) Severe neurodevelopmental disability generally is defined as subnormal cognitive function, cerebral palsy, blindness, deafness, or a combination of these factors. The continuing high incidence of neurodevelopmental handicap raises several questions: 1) Given the complexity and relative inaccessibility of the central nervous system (CNS), is it advantageous to consider alternative viewpoints for the etiology and therapy of neurodevelopmental handicaps? 2) Given the close embryologic connection between brain and skin, should cognition be considered a complex function or outcome not merely of the brain, but also of the interlinked boundary of the developing preterm infant? This article focuses primarily on the skin, but, by extension, it includes specialized sensory epithelia such as the cochlear hair cells of the ear and the retina of the eye.In developing this conceptual approach, it is useful to consider the analogy between the related fields of computer science and cognitive science. Figure 2 shows a simplified schema in which the development of central processing units (computers) depends on the simultaneous development of more adaptive and flexible user interfaces. In this system, feedback is an important component of informational closure. Without it, optimal function of the system as a whole would not be feasible.Analogously, the field of cognitive science is a rapid and flourishing field that increasingly places emphasis on concepts such as “situatedness” and “embodiment.” As with computers, isolated brains are ineffectual; they require sensorimotor feedback and intelligent interfacing with the environment (Fig. 3 ). The development of adaptive physiologic interfaces, therefore, is a logical prerequisite for the development of more complex CNS mechanisms. In cognitive terms, brains must be embodied for normal functioning.In this context, specific disorders of the VLBW preterm infant are associated with developmental immaturity of epithelial/environmental interfaces (Fig. 4 ). Specifically, neurodevelopmental deficits are considered in the context of altered feedback loops between peripheral interfaces and central structures. Neonatal animals, such as the kitten and the rodent, are useful models to study the effect of sensory inputs on CNS development. (2) These models have indicated clearly that sensory signals are required during critical developmental periods for proper CNS maturation. In humans, clinical studies have demonstrated various effects of tactile stimulation during infancy. For example, Field et al (3) have shown that tactile stimulation of hospitalized preterm infants results in greater weight gain and higher Brazelton behavioral scores. Such studies require corroboration and further investigation.The focus on tactile development singles out one subset of possible neurosensory feedback. It is well known, for example, that compared with other primates, the skin and brain of humans exhibit unique evolutionary features (Fig. 5 ). No other primates have such a large and complex brain, and no other primate has the same unique and relatively hairless skin surface marked by a thick interfollicular epidermis. Both epidermis and brain share a common embryologic origin as ectodermal derivatives. Structural and functional interactions between skin and brain are established prenatally. In the VLBW preterm infant, such interactions occur in an abnormal external environment.Figure 6 shows a simple functional schema of the nervous system organized as a feedback loop. Clearly, closure of the feedback loop via the CNS is a requisite for normal functioning. Less obvious, however, is the fact that structural organization in the form of a loop architecture requires closure at the periphery. Peripheral closure of the nervous system is unlikely to be a function of isolated nerve endings. Nerve endings, in fact, never touch the environment. Interfacing with the environment in mammalian systems is mediated directly by specialized epithelial structures derived from the embryonic ectoderm.Central to the organization of the nervous system as a sensorimotor feedback loop is the idea of the skin as a neurodevelopment boundary that interfaces the organism and the environment. This organizational schema places the skin in a strategic location to affect subsequent development. As an interface with the environment, the skin links directly to the developing brain as well as to external factors, including both physical stimuli (light, sound, heat) and interactions with caregivers.The concept of the skin functioning as a “smart material” interface derives from the engineering sciences. (5)(6) It is useful for interpreting the functional role of the skin surface, particularly with respect to the outermost terminally differentiated layer of the epidermis, the stratum corneum. This layer constitutes the primary barrier to water loss in normal skin and has many of the properties of a smart material (Fig. 7 ). The stratum corneum is the continually produced boundary of an autopoietic (self-organizing/self-producing) system that provides the physical means by which the organism is structurally coupled to its environment. In its role as the limiting surface of the body, the stratum corneum simultaneously forms both the perceived surface of the observer and the biologic boundary of the organism. In other words, the stratum corneum and by extension the skin in general, corresponds, in a simple but nontrivial manner, to the logical distinction between subject and object.Most textbooks of neurophysiology generally consider sensory signal processing to begin with the nerve ending. As mentioned previously, nerve endings never touch the environment except by means of intermediary structures located at the boundary of the organism. This view of the boundary as a sensorimotor interface is important for understanding innovative approaches to skin-CNS interactions as put forth by Ansel and associates. (7) In investigating the complex coupling mechanism between the biologic system and the observer, superficial interfacial structures, such as the stratum corneum, emerge as logical candidates to distinguish and explore.Biophysical properties of this interface, therefore, must be considered as important mediators of sensory signal processing. For example, Figure 8 notes a number of measureable physical properties of the skin that influence tactile perception both by the patient (preterm infant) and the caregiver (nurse or parent). Similarly, a number of biophysical properties of the skin mediate visual signal processing (Fig. 9 ). These properties change rapidly during the first few days of life following adaptation to air and accelerated formation of the epidermal barrier. A careful, in-depth cataloging of the changing physical properties of the skin surface as a function of gestation, postnatal age, and anatomic region has yet to be performed in the preterm infant. A number of sophisticated noninvasive bioinstruments may aid in physical testing. (8) In particular, study of the electrical properties of the skin may be relevant in the VLBW preterm infant. The electrical resistance of the epidermal barrier in the preterm infant is likely to be very low due to relative deficiencies of both vernix and stratum corneum.One of the most intriguing aspects of the skin is its utility in noninvasive monitoring. It is often forgotten that Einthoven, who won the 1924 Nobel Prize in Medicine for the discovery of the mechanism of the electrocardiogram (ECG), was intensely interested in measuring the electrical properties of the skin. Direct measurements of the skin carry valuable information about internal organ functioning. Such noninvasive approaches are important for the future of neonatology. The field of evoked potential (EP) testing of the brain, for example, holds promise for the assessment of multiple clinical conditions, such as birth asphyxia (Fig. 10 ). In contrast to ECG measurements, EP testing of the electrical activity of the brain produces low-amplitude voltages that are greatly affected by optimization of the skin-electrode contact surface (Fig. 11 ).The high electrical resistance of the skin, in particular, makes EP testing difficult. For that reason, electrical signals often are obtained after abrading or wounding the skin surface to reduce the electrical resistance. This practice potentially confounds the measurement of low-voltage signals. Recently, Wakai and associates (9), while evaluating the new technique of magnetic fetal cardiac imaging, demonstrated the development of a high electrical impedance barrier in utero (Fig. 12 ). Prior to birth, the amplitude of the fetal ECG can be measured from the maternal abdomen during the first half of gestation. After 26 to 27 weeks’ gestation, the amplitude gradually disappears, concomitant with the intrauterine development of an epidermal barrier consisting of vernix caseosa and the developing stratum corneum. This disappearance is secondary to a high electrical impedance barrier between the fetus and the amniotic fluid and putatively reflects progressive electrical isolation of the fetus from the mother and growing fetal autonomy.The presence of high electrical resistance is typical of human skin. Figure 13 provides data on the electrical resistance of a number of comparative skin samples measured under in vitro conditions. As shown, excised human skin has a high resistance, which is confined almost entirely to the stratum corneum, the outermost layer of the skin. For this reason, EP testing often employs contact pastes that are gritty and abrade the skin surface. Also shown in Figure 13 are relative electrical resistances of the skin of common rodent laboratory models. The newborn rat has an electrical resistance that is remarkably comparable to human skin.The Sprague-Dawley rat at birth is hairless, pink, and semitransparent (milk in the stomach is readily visible) (Fig. 14 ). Over the first 2 weeks of life, it greatly increases in size and develops hair follicles and a coat of fur. Additionally, the eyelids unfuse and the ear canals open. Only at birth does the animal exhibit an epidermal appearance comparable to humans, which is manifested by a thick epidermis and a well-developed stratum corneum coupled with high electrical resistance. Human skin development is marked by an apparent prolongation of the skin state normally found at birth in the rat. This skin state consists of a thick interfollicular epidermis, a well-developed stratum corneum, and suppression of fur development.There is ample evidence that development of the immature CNS is critically dependent on sensory input during the immediate postnatal period. Experimental interference with several sensory modalities, such as vision, touch, and hearing, results in profound anatomical, functional, and biochemical impairment of the CNS structures that regulate such modalities. In newborn rats, for example, tactile stimulation is an important regulator of somatic growth. Studies by Schanberg et al (10) have clearly linked tactile stimulation with the regulation of ornithine decarboxylase (ODC). ODC is a sensitive index of the maturation and growth of internal organs such as the heart, liver, and brain. Brain, liver, and heart ODC levels are decreased by 35%, 81%, and 53%, respectively, when rat pups are removed from their mothers for periods as short as 1 hour. ODC activity normalizes quickly after pups are returned to their mothers or are provided with nonspecific tactile stimulation. Touch, not nutrition, is the specific regulator of this biochemical response.Figures 15 and 16 summarize a corollary experiment in which tactile stimulation influenced circulating levels of lactate, an important energy substrate for cerebral metabolism. (11) Lactate levels are very high immediately following birth and fall rapidly over the first few hours of age, subsequently plateauing. In this experiment, timed-gestation Sprague-Dawley rat pups were removed from the nest and received tactile stimulation by means of rostral-caudal stroking with a camel hair brush similar to the methodology established by Schanberg. During the first 24 to 48 hours, tactile stimulation elicited a marked increase in serum lactate that persisted for up to 30 minutes following cessation of the stimulus. The same stimulus failed to elicit an increase in serum lactate at 1 week of age. Results are noteworthy insofar as the brain of the early suckling rat uses lactate in preference to other metabolic fuels such as glucose and 3-hydroxybutyrate. This experiment demonstrates in a specific neonatal animal model that sensory interaction between the organism and the environment is a regulator of the availability of cerebral energy substrates in the newborn mammal. Such studies have yet to be performed in humans and may be relevant for distinguishing appropriate from inappropriate touch. In this animal experiment, lactate levels increased without development of hypoxic metabolic acidosis.One of the major advantages of focusing on the skin surface in the newborn relates to the multiple roles served by the skin as a primary care interface (TableT1 ) . These roles run the gamut from infection control and adhesive application to noninvasive monitoring and clinical evaluation. On the one hand, the multiplicity of practical care applications for the skin and its sheer obviousness often preclude recognition of the importance of this care interface. On the other hand, linking the skin in a relevant manner to neurodevelopment emphasizes the importance of each of these primary care functions.The preterm infant, in particular, requires close and meticulous attention to skin care (Fig. 17 ). Compared with older infants and adults, the skin surface of the preterm infant manifests extraordinarily rapid changes in its biophysical, biochemical, and bioelectrical properties during adaptation to postnatal life. The glistening, moist, highly evaporative surface of the VLBW preterm infant immediately following birth contrasts sharply with the dry, desquamating surface of the same infant several weeks later. A plethora of commercial products impinge, impact, and often impair endogenous physiologic mechanisms of epidermal barrier function (Fig. 18 ). These products rarely have been tested in infants in general, much less evaluated specifically for the preterm baby. Fruitful collaboration between commercial developers of skin care products and neonatal caregivers interested in providing evidence-based skin care practices requires recognition by clinicians of the continuing dynamic interfacial roles of the skin as the boundary of a complex system.Recognition of the skin as an important component in primary care delivery attaches value to those disciplines that interact with and care for this boundary. The enhanced value and appreciation of such disciplines promotes organizational efficiency within a health-care system. Among these disciplines are such integral services as nursing, phlebotomy, laundry, anesthesia, physical therapy, and environmental management. Figure 19 illustrates a simple schema in which the skin acts as an interface linking the primary care disciplines of nursing and medicine in a collaborative practice model. Anyone working in a neonatal intensive care unit recognizes the necessity of collaborative practice. Concepts that promote and extend such interactions are valuable to a health-care organization.The concept that the boundary of the organism constitutes a neurodevelopmental interface has unusual conceptual features (Fig. 20 ). The functions of the skin (TableT1 ) lie outside the traditional realm of medical school curricula. The very name internal medicine presupposes an external boundary marking the extent of its domain of practice. The functions served by the skin and the aspects of primary care delivery listed in the Table are generally disease-independent. Hence, this field does not fall within the purview of dermatology, which, like internal medicine, has a primary disease focus. These functions, nevertheless, are absolutely essential for the delivery of high-quality care in both the hospital and home. Seamless and professional execution of these functions has a disproportionate impact on consumer satisfaction. The current diseaseand procedure-based reimbursement systems, however, do not recognize these roles, with most health-care systems capturing reimbursement for these functions under the “room” or “bed” charge. The fiscal invisibility of the skin and the tendency to habituate to what is before our eyes lead to transparency and the common failure to recognize the importance of this interface in care delivery.In engineering terms, recognition of this interface is the first step toward defining the boundary conditions of the body as a complex system. Such a system remains undefined until the boundary conditions are determined. Recognition of this surface, moreover, links to several novel concepts in evolutionary biology that have yet to be firmly established in medical practice. Among these concepts is Richard Dawkins’ idea of the “extended phenotype” in which genetically determined phenotypic structures are viewed as extending beyond the traditional boundary of the organism. (12) This concept receives a practical application in J.S. Turner’s book The Extended Organism, with its focus on external energy fluxes and environmental interactions. (13) The idea that neonatal intensive care environments are structurally determined as a type of extended phenotype is difficult to comprehend without appreciation of the role of the skin as the complex boundary of a dynamic system.Finally, the concept of the skin as a neurodevelopmental interface opens the door for extension to care practices that have yet to be firmly established on an evidentiary basis. Given the limited resources for care delivery and ever-increasing constraints on health-care reimbursement, alternative medical approaches are politically sensitive. It is a reasonable caveat to note that the skin surface is so complex that it cannot be understood without a reductionistic approach. This implies close attention to quantitative, objective, evidence-based studies focused, in the current example, on the VLBW preterm infant. On the other hand, the comfortable familiarity of the skin surface leads to psychological habituation and invisibility such that it cannot be “seen” without a holistic viewpoint. This dynamic tension between reductionistic and holistic viewpoints is part and parcel of a true boundary. Synthesis of these complementary viewpoints in the care of the preterm infant is a challenging opportunity for the future." @default.
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• W2120878548 title "The Skin as a Neurodevelopmental Interface" @default.
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