Family-Centered Care in Childhood Disability: Theory, Research, Practice 3031342518, 9783031342516

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Family-Centered Care in Childhood Disability Theory, Research, Practice Livio Provenzi Serena Grumi Renato Borgatti Editors

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Family-Centered Care in Childhood Disability

Livio Provenzi  •  Serena Grumi Renato Borgatti Editors

Family-Centered Care in Childhood Disability Theory, Research, Practice

Editors Livio Provenzi Department of Brain and Behavioral Sciences University of Pavia Pavia, Italy

Serena Grumi Developmental Psychobiology Lab IRCCS Mondino Foundation Pavia, Italy

Renato Borgatti Pediatric Neuroscience Center IRCCS Mondino Foundation Pavia, Italy

ISBN 978-3-031-34251-6    ISBN 978-3-031-34252-3 (eBook) https://doi.org/10.1007/978-3-031-34252-3 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Care for the Most Vulnerable: A Landscape of Opportunities

It is fascinating to see how the philosophy of family-centered care (FCC) and its principles are translated into the everyday practice of health professionals who care for children with developmental risks or disabilities. Health professionals from different disciplines collaborate with each other and with the parents to create a landscape of opportunities where every child can reach their developmental potential, always prioritizing the family unit as a whole. This means that the care and the interventions are provided “with” and “within” the family, not “for” or “instead” of them. Naturally, the successful cooperation between health professionals and families is based on awareness and understanding of the specific roles of each participant, as well as mutual trust and respect. Professional support remains extremely important, as parents need professional knowledge, competencies, and support to aid their efforts in providing developmentally sensitive care, beginning in the postnatal period and continuing throughout early childhood. Nowadays, early interventions have found their way into the family home, the best place for developmentally appropriate experiences—the family home is a child’s natural setting and familiar surroundings make them feel more secure and more open to cooperating. Before they reach the family home, the journey of early interventions for children at risk of developmental disorders begins in the neonatal intensive care unit (NICU). Just a few decades ago, when we were young pediatric residents, entering the NICU was a special event, almost like entering another universe, another landscape. In this landscape, removed from everyone else, health staff cared for the most vulnerable population of infants, aided by technology—infants who were born too early (before completed 37 weeks of pregnancy) were sick or had congenital abnormalities. Care was provided in an open-bay room, in a space often too small for the number of incubators and with limited space between them. It was usual to see bright lights, hear noisy alarms and other equipment, with hurried staff on a strict schedule to get infants fed, diagnosed, treated, and cared for. Parents were largely thought of as visitors and their presence in the unit was short, limited by restrictive visiting rules. Mothers were separated from infants and breastfeeding was rare. Being in a highly technological environment was often a frightening experience for parents, while separation from their infant, worry and uncertainty about the infant’s health and inadequate communication with healthcare staff often led to parents feeling a loss of control, anxiety, stress, and lack of competence for their specific role as parents of NICU infants. Everyday life in the NICU used to look very different for v

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infants, their parents, and staff, even though at the time for us health providers, it seemed “normal.” Medical care of the infant was prioritized, and medical staff was considered the expert who best knew how to take care of the infants. Not enough attention was paid to the unfavorable effects of the NICU environment on infant development outcomes. The implementation of best evidence from the 1970s was very slow to find its way to medical school curricula and clinical practice, including the importance of attachment and bonding, and innovations like kangaroo care (KC). Although the advance of medical science and the availability of high technology in recent decades had reduced the mortality rates for vulnerable infants, the prevalence of major morbidities resulting from very premature birth (less than 32 weeks of pregnancy) or perinatal brain injury, such as intraventricular hemorrhage and periventricular leukomalacia, hypoxic-ischemic encephalopathy, sepsis, bronchopulmonary dysplasia, retinopathy of prematurity, and necrotizing enterocolitis, has not changed significantly. Moreover, the developmental outcomes of survivors have not improved—many of them face serious health problems resulting in long-term disability, like cerebral palsy, intellectual impairment as well as vision and hearing impairment or loss. The NICU is the first extra-uterine environment that premature and sick newborns live in, and many infants spend weeks or even months in the unit environment. Traditionally, it has been an environment in which infants are overwhelmed by sensory stimulation while simultaneously being deprived of interaction with their parents. For vulnerable preterm infants with immature organ systems and a rapidly developing brain, living in an environment with unfavorable influences often leads to adverse neurodevelopmental outcomes. In recent decades, a growing body of scientific evidence has shown that infant-parent interaction and parental involvement in infant care in a supportive environment are critical for an infant to achieve positive developmental outcomes and overall well-being. Furthermore, separation from their infant can have long-term detrimental effects on parents’ mental health. Naturally, questions ensue about how to make the unit environment more supportive for infant development. How could the NICU be made more homelike, a place where parents can always be present, caring for their infant with gentle, developmentally supportive care? It was clear that the future development of neonatal intensive care that aims to ensure vulnerable infants not only survive but thrive must be simultaneously directed toward the utilization of complex technology delivered by highly educated staff and the involvement of parents as active participants in infant care from day one. According to the United Nations Convention on the Rights of the Child (Articles 7 and 9) a child has the right, from birth, to be cared for by his or her parents and shall not be separated from his or her parents against their will. Parents are guardians and co-creators of the child's physical and mental health—their crucial role for child well-being needs to be recognized and supported. Thus, a paradigm shift in the philosophy of neonatal intensive care was necessary, requiring change in the mindset of healthcare professionals and a greater focus on the holistic and salutogenic

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aspects of care. In other words, it required changing the NICU culture by implementing the FCC approach. Family-centered care is a concept that recognizes that the family is a child’s primary source of strength and support and that optimal health outcomes can only be achieved when parents play an active role in providing infants with emotional, social, and developmental support. The concept of FCC is based on a partnership between health professionals and parents, the involvement of parents in care and decision-making, and recognizing parents as experts in the care of their own infant. However, creating a culture of change in the NICU takes time—it is a process that cannot happen overnight. This process has required that staff change their traditional role from that of the infant’s primary caregiver to that of parental educator, mentor, and supporter. Staff training became a priority, as did changes in staff attitudes, behaviors, and communication skills, which were needed for staff to be able to support and empower parents to reach a new level of parental expertise. FCC principles have been present in neonatal intensive care for almost three decades, during which a variety of interventions and models of care have been developed and implemented, including (a) parent support interventions—targeted to NICU parents without direct involvement of the infant (for example, psychoeducational support and techniques to improve communication); (b) parent-delivered interventions—performed by parents targeted to both the parent-infant dyad (for example, basic newborn care, breastfeeding, and talking to the child); and (c) models of parent-partnered neonatal care—involved parents, infant, and staff where parents and healthcare providers are full partners in delivering infant care (for example, in KC and family integrated care). Other interventions under the FCC umbrella include Infant–Family-Centered Developmental Care, Newborn Individualized Developmental Care and Assessment Program, Neonatal Integrative Developmental Care, and Close Collaboration in Care [1]. Worldwide, KC and breastfeeding are the two activities NICU parents most frequently perform. When you enter a contemporary NICU you will see a mother resting in a comfortable chair or bed alongside an incubator, doing KC by holding her premature infant in skin-to-skin contact (STS) where the infant, clad only in a diaper (and sometimes a cap), is held in an upright prone position against the bare chest of the mother and covered with clothing or a blanket. While providing KC, the mother gently hums a lullaby to her infant. A screen is in place to protect their privacy. Alongside another incubator you may see parents who are carefully and gently changing their infant’s diaper, while the mother speaks to the infant quietly. The incubator’s port holes are carefully closed, almost silently. The alarms are quiet and the lights are dimmed. The only thing that can be heard is the mother’s voice, the best melody for an infant. Alongside the next incubator another mother is breastfeeding her premature infant, with support from a nurse who is helping her latch her infant onto the breast. Everyday life in the NICU is very different than it was just a few decades ago. Today, the NICU is a community that welcomes parents, who are present during rounds and medical procedures and are included in the decision-­ making process. We strive to make the NICU a landscape of opportunities where every participant in care can achieve their highest potential—for the infant, this

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means positive neurodevelopmental and health outcomes; for parents this means increased resilience and confidence, strengthened parental self-efficacy through active participation in their infant’s care. For staff, this means personal growth and well-being while providing infant care in partnership with parents, supporting and empowering them in their roles. It is noteworthy that both KC and breastfeeding should not be considered interventions—for human beings they represent the most natural way of human caregiving; they are biological imperatives. It could be said that Mother Nature offers us an optimal solution through KC and human milk, biologically orchestrated as if it was composed by a master musician; it’s up to us to respect and, as far as we can, understand the process. Upon seeing a fragile preterm infant cared for using KC we are aware that at this particular moment they are receiving gentle care in the most supportive environment possible. Here on their mother’s chest all of the infant’s senses are stimulated and the best auditory, olfactory, visual, kinesthetic, and tactile stimulation is achieved. This multisensory stimulation contributes to reinforcing the infant's behavior and regulation and improves neurodevelopment. The neuroprotective effects of kangaroo mother care for preterm infants persist up to young adulthood and may improve their lifetime functionality and quality of life [2]. KC should ideally be practiced continuously (24 h/day, 7 days/week) or (less ideally) intermittently, with each episode of STS contact lasting at least 60–90 min. Naturally, both parents can practice KC, as well as siblings and other family members. For parents, having an infant in STS contact is an intense emotional experience, a time when both participants of the dyad learn about and from each other, a time when stress is alleviated or goes away in its entirety, a time of bonding and first breastfeeding. Human milk is the best food for all infants. It is especially important for the premature infant, providing short- and long-term health benefits, including a reduction of necrotizing enterocolitis, retinopathy of prematurity, and improved neurodevelopment. A growing body of evidence on the unique biological properties of human milk, which contains protective factors, human milk microbiota, microRNA, and stem cells, suggests that human milk is the most specific personalized medicine an infant can receive, from day one. Mothers of preterm and sick infants perceive their milk as a connection between them and the infant—every drop of this “liquid gold” is important. For some mothers, having enough milk becomes an imperative that can prove her achievement of being a “good mother.” However, the initiation and maintenance of lactation is challenging and most NICU mothers need practical help and ongoing support throughout the hospital stay and beyond. Nowadays, the principles of the FCC are recognized as one of the key components to support breastfeeding and human milk feeding in all infants. Since 1991, the Ten Steps to Successful Breastfeeding of the Baby Friendly Hospital Initiative (BFHI), developed by the World Health Organization (WHO) and UNICEF, are considered the “gold standard” for breastfeeding support in maternity wards. Although the BFHI standards had transformed organizational and breastfeeding culture of maternity wards and to some extent breastfeeding culture in neonatal wards, the breastfeeding support criteria for very preterm and sick infants remained outside the scope of the

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BFHI standards until the revision of the BFHI in 2018. In order to bridge that gap, the Baby-friendly Hospital Initiative for Neonatal Wards (Neo-BFHI) was developed by a Nordic and Canadian (Quebec) working group in 2009–2015 as an expansion of the WHO/UNICEF Ten Steps for maternity wards. The Neo-BFHI recommendations include the Three Guiding Principles as basic tenets, Ten Steps adapted to the needs of preterm and sick infants closely following the original BFHI and adherence to the International Code of Marketing of Breast-Milk Substitutes. The Neo-BFHI also includes a family-centered approach: Guiding Principle 2 of the Neo-BFHI states that “The facility must provide family-centred care, supported by the environment” [3]. Currently, Neo-BFHI recommendations are partially implemented in many countries. A large international study that included 917 neonatal wards from 36 countries from all continents found variable compliance with Neo-­ BFHI recommendations with a median international score of 77 (out of 100). It is important to highlight that FCC compliance (Guiding Principle 2) reached a high median international score of 82 (country range score 51–96) suggesting that the family-centered approach is recognized as a pivotal construct for NICU breastfeeding support [3]. In the last two decades a growing body of research has shown the positive health and well-being outcomes for parents and infants when family-centered interventions or models of care are implemented. For infants, FCC can improve breastfeeding and weight gain, shorten the hospital length of stay, promote cardiovascular stability and reduce pain and stress, improve neurodevelopmental outcomes, and increase parent-infant interaction, closeness, and bonding. For parents, FCC can improve confidence in their parenting role, increase overall satisfaction with care in the NICU, and decrease stress and anxiety. In addition, a recent longitudinal, multicenter cohort study conducted in 23 NICUs across 15 countries showed that parents’ perceptions of FCC (more specifically, parents’ participation in infant care, care-related decisions, and emotional support provided by health staff) were associated with fewer depressive symptoms after a NICU stay, at infants’ 4 months corrected age [4]. These findings suggest that FCC may protect the mental health of parents not only during hospital stay, but also for some time after discharge. This is especially important in light of the fact that the transition to home and beyond is a novel and challenging period for parents. FCC has been recognized as a key component of neonatal intensive care and endorsed by organizations such as the WHO, UNICEF, the American Academy of Pediatrics, and the European Foundation for the Care of Newborn Infants (EFCNI). However, despite the evidence of the positive effects of FCC and professional recommendations, family-centered models of care are still underutilized in many NICU settings. It is important to highlight that the successful implementation of the family-centered approach in neonatal intensive care requires fundamental change in healthcare policies, protocols, facility design, organizational infrastructure, and everyday practices, which may be difficult considering local context and culture. Protocols and standards are needed to guide the consistent implementation of family-centered interventions. Recently, EFCNI, the first pan-European organization and network to represent the interests of preterm and newborn infants and their

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parents, published standards for infant–family-centered care. These standards were developed in cooperation between health professionals and parents, thus adding the “voice” of patients (through parents) to the vision of what this care should look like. As healthcare providers we must ask ourselves if we can know a parent’s expectations, fears, questions, and need for answers. How can we “walk in their shoes”? Only parents who have experienced having their infant in the NICU (veteran parents) know what it’s like. Worldwide, veteran parents selflessly help current NICU parents by supporting them and giving advice on how to deal with the challenges they face. In addition, veteran parents are now in the new role of being the “voice” of and spokesperson for preterm and sick infants and their parents—they are the growing and driving force behind numerous initiatives aimed at raising awareness of optimal care for premature and sick infants. Advocacy by parents’ associations can motivate stakeholders in  local communities and governments at all levels to more quickly adopt changes to improve the quality of care for the most vulnerable infants. We are all aware that change sometimes moves at the pace of the slowest freight train, but with a strong locomotive—propelled by the energy of researchers, clinicians, and parents working towards a common goal—the well-being of infants and families can be more and more prioritized over time. It has been a long and arduous journey in the almost 30 years since the introduction of FCC principles in NICUs. We have moved from highly restricted visits in a medically oriented NICU to a situation where the new norm is being in a parent’s arms while getting highly specialized treatment using sophisticated technology. With more than two decades of experience with family-centered methods of care, we have reached maturity and are still evolving. Sometimes, challenges arise and it becomes an opportunity for innovative solutions and personal growth. The textbook example of this was the shortage of incubators for and high mortality rates of fragile premature infants due to infections in Columbia that led to an innovative solution— the use of KC—which improved infant survival and development. KC has become an investment towards the health of future generations. Another more recent example was during the COVID-19 pandemic, where social distancing and quarantine endangered the implementation of FCC in NICUs. Technology was used to bridge the literal gap between health staff, parents, and infants as much as possible. Health staff could keep the parents informed on their child’s condition through teleconference and video calls and text messages. Parents, largely out of options, could use video cameras to at least see their child. But, as convenient as it may seem, it is not actually real. It lacks humanity and personal connection. No amount of i-, smart- or tele-devices and initiatives could replace the warmth of a mother’s embrace. Currently, FCC is considered the gold standard for neonatal and pediatric health care. While providing family-centered interventions in the NICU is considered a (very) early intervention in infants at a high risk for developmental disorders, one should be aware that this is only the first step in support aimed at improving infant’s developmental outcomes, and that effective early intervention can be achieved only through the provision of continuous care over a longer period of time. Providing quality care means doing the right thing in the right place at the right time [5]. After NICU discharge, the landscape of care opportunities becomes even wider and

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different interventions can be implemented in different healthcare settings and at home, for different age groups and provided by different health professionals. Continuity of care for high-risk infants should ideally be carried out in their home and family environment with strict follow-up care and support from health professionals. “There is no place like home” were the words of Dorothy, the protagonist from the film the Wizard of Oz. Truly, at home, in their natural environment, family-­ centered interventions with active parental involvement may result in more positive health outcomes. All the experiences that parents gained during their infant’s NICU stay can help build their skills to continue caring for their infant after discharge. Moreover, with the support of home visits, outpatient services and ongoing education parental confidence and skills can continue to grow after hospital discharge [5]. For example, performing KC at home can empower parents to become more attuned to sensitive caring, preparing them for their infant’s further needs [2]. Every child with developmental risks or disabilities and their families are a unique microcosm, different from all others in the same situation. Different risks and developmental disabilities also bring different challenges. As a rule, their problems are complex and require a multidisciplinary approach where health professionals are collaborating to provide individualized care, optimized for each child and family and tailored to their needs, creating and supporting opportunities for achieving the developmental potential of the child and well-being of the family. A multidisciplinary team of health professionals includes primary care pediatricians, health visitors, neuropediatricians, psychologists, physiotherapists, occupational therapists, speech-language therapists, and social workers, and each has an important role in planning and implementing care. However, active parental participation in child care is still a determining factor for the successful implementation of all early childhood interventions and therapies. Bearing all this in mind, it is time that the family becomes an integral part of child care in every NICU around the world, in every hospital, pediatric ward, pediatric clinic, and any place where children receive medical care, creating a landscape of opportunities where children can achieve their highest potential. This is especially important for children at a high risk for developmental disorders or those who have a disability, for whom the family unit provides the best support on their life journey. In each chapter of this book, experts in different fields will present knowledge on how this can be achieved in high-risk children or those with developmental disabilities using the most effective evidence-based interventions based on a family-­ centered approach.

References 1. Franck LS, O’Brien K. The evolution of family-centered care: from supporting parent-delivered interventions to a model of family integrated care. Birth Defects Research 2019;111(15):1044–59. https://doi.org/10.1002/bdr2.1521. 2. Charpak N, Tessier R, Ruiz JG, Uriza F, Hernandez JT, Cortes D, Montealegre-­ Pomar A. Kangaroo mother care had a protective effect on the volume of brain

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structures in young adults born preterm. Acta Paediatrica 2022;111(5):1004–14. https://doi.org/10.1111/apa.16265. 3. Maastrup R, Haiek LN; Neo-BFHI Survey Group. Compliance with the “baby-­ friendly hospital initiative for neonatal wards” in 36 countries. Maternal Child Nutrition 2019;15(2):e12690. https://doi.org/10.1111/mcn.12690. 4. Axelin A, Feeley N, Campbell-Yeo M, Silnes Tandberg B, Szczapa T, Wielenga J, Weis J, Pavicic Bosnjak A, Jonsdottir RB, George K, Blomqvist YT, Bohlin K, Lehtonen L, Separation, Closeness Experiences in Neonatal Environment (SCENE) Research Group. Symptoms of depression in parents after discharge from NICU associated with family-centred care. Journal of Advanced Nursing 2022;78(6):1676–87. https://doi.org/10.1111/jan.15128. 5. World Health Organization. Survive and thrive: transforming care for every small and sick newborn. Key findings. Geneva: World Health Organization; 2018. Division on Breastfeeding Support, Anita Pavicic Bosnjak Human Milk Bank, Croatian Tissue and Cell Bank, Department for Transfusion Medicine and Transplantation Biology University Hospital Centre Zagreb Zagreb, Croatia

Contents

Part I Theory 1

 Sensory Processing and Meaning-­Making in Early Development��������   3 Isabelle Mueller and Ed Tronick

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Collaborative Consultation with Families in the Context of Developmental Disability����������������������������������������������������������������������  13 Anna Lengyel

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A Meta-Theoretical and Multidimensional Guidance to Understand and Support Parenting in the Context of Child Disability: The Porridge-Like Framework ������������������������������  31 Eleonora Fullone, Lorenzo Giusti, and Livio Provenzi

Part II Research 4

When Eye-Contact Is Challenged: Understanding Early Interactions Between Low-Vision Infants and Their Parents����������������  53 Serena Grumi, Giorgia Aprile, Federica Morelli, Antonella Luparia, Elena Capelli, Luisa Vercellino, Livio Provenzi, and Sabrina Signorini

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From the Early Detection to Early Intervention at Home: The Role of Technology in Infancy ����������������������������������������������������������  71 Elena Beani, Silvia Filogna, Giovanni Cioni, and Giuseppina Sgandurra

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 Listening to Bodily Sensations: Subjective Experience of Embodied Sensitivity and Body-to-Body Interaction in Mothers of Children with Neurodevelopmental Disability��������������������������������������������������������  97 Rosario Montirosso, Eleonora Visintin, Elisa Rosa, Nicole Galli, Simone Frassoni, Annalisa Castagna, and Eleonora Mascheroni

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Part III Practice  7 PICCOLO:  Observing and Coaching Caregiver-Child Interaction to Support Early Development in Children With and Without Disabilities�������������������������������������������������������������������������������������������������� 115 Mark S. Innocenti, Rosa Vilaseca, and Lori Roggman  8 Early  Intervention in Cerebral Palsy: From Theory to Current Practice������������������������������������������������������������������������������������ 149 Fabrizia Festante, Camilla Antonelli, Sara Mazzotti, and Andrea Guzzetta  9 Video-Feedback  Interventions to Support Parents of Children with Neurodevelopmental Disabilities������������������������������������������������������ 193 Serena Grumi, Elisa Roberti, Shaghayegh Parsanejad, Renato Borgatti, and Livio Provenzi 10 Assessment  and Intervention Potentials of the Face-to-Face Still-Face (FFSF) Paradigm in Developmental Clinical Settings���������� 213 Giorgia Anceresi and Livio Provenzi

Part I Theory

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Sensory Processing and Meaning-­Making in Early Development Isabelle Mueller and Ed Tronick

1.1 Introduction To successfully engage with our environment, we are processing a vast amount of sensory information from the world around us and integrating it into meaningful states of consciousness. Bruner [1] described humans as makers of meaning, a concept easily linked to the first principles of dynamic systems principles [2]. Humans, when conceived of as meaning-making open systems, utilize energy to garner information to create complexly organized, coherent, integrated, and flexible states of consciousness that contain the private meanings an individual creates about their place in the world. When they fail to appropriate information their states of consciousness dissipate. They become less complex, less coherent, more rigid, and increasingly constricted in making sense of the world. However, though meaningmaking is a typical species characteristic it is not automatic but an effortful developmental process and one that is more fraught for at-risk children. To be effective or adaptive the information must be fitted to environmental demands. The demands are at least two-fold: one demand is “natural” in the sense that it emerges from our biological makeup. The other demand is acculturated, that is the “arbitrary” historical demands embedded in culture and social exchanges. For example, a biological demand might be to gaze at other individuals’ eyes, but a cultural demand might be to not look directly at your elders. For a young child, there may be a mismatch

I. Mueller Department of Psychiatry, Columbia University Medical Center, New York, NY, USA e-mail: [email protected] E. Tronick (*) Departments of Psychiatry and Pediatrics, Chan Medical School, University of Massachusetts, Worcester, MA, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 L. Provenzi et al. (eds.), Family-Centered Care in Childhood Disability, https://doi.org/10.1007/978-3-031-34252-3_1

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between the biological and acculturated demands, and resolution of this conflict may be difficult and take time to resolve. The sensory system receives input from different senses and integrates them for optimal functioning and appropriate adaption to environmental demands and perceives information from visual, auditory, gustatory, and tactile stimulation. In addition, the proprioceptive sense provides constant information about our body’s position in space, while the vestibular sense is associated with our perception of balance and movement. The information a human receives from these complex sensory sources can be corresponding and redundant, or disjunctive. For example, when the vestibular system conveys stability, but the visual system perceives quick whirling movements, a person needs additional information about the current situation to make meaning of this experience. A resolution may come easily in the form of an individual’s action, testing and verifying the information received. This could be as simple as taking a step forward and remaining upright, confirming the world is stable. Overall, the sensory-related information we receive from the environment not only shapes the perception of our environment but simultaneously our sense of safety or threat. This is especially true for at-risk individuals with atypical sensory processing. Well-adapted processing and integration of sensory information enables perception of a colorful and chaotic world. On the contrary, atypical processing of the same environmental stimuli can be overwhelming and challenge an individual’s sense of security. How we perceive and integrate information around us has major consequences on our participation in the world and how we make meaning of events and experiences. Sensory integration can be observed in early infancy but matures slowly during childhood [3]. Throughout the first months of life children already pay increased attention to multisensory stimuli [4], but more complex sensory processing, such as integration of visual with tactile information only develops around the 8th year of life [5, 6]. The eventual integration of redundant systems facilitates the detection of meaningful information, but the different maturational timelines can result in a mismatching and disorganization of information. One can imagine a kind of shearing force between the more mature auditory system and the more slowly developing visual system. What meaning is made when a sound locates an object, but it is not located visually? Adding to the complexity we know little about how sensory information is integrated with the feedback from action systems which serve as the validator of sensory information, especially disparate information. Furthermore, the characteristics of different sensory systems and the quality of their integration show great individual variation. Deficits or what more generally could be better thought of as extreme variations in sensory processing and multisensory integration have been found to be comorbid with several clinical conditions, such as autism spectrum disorder (ASD), social anxiety, preterm birth, and schizophrenia. Even when the variation is small, the deviation from the non-at-risk value is small and the extent to which perception is disturbed, the alteration nonetheless may generate difficulties in social interactions. An at-risk child may see a smile as others see it, but recoils from a “normal” vocal volume resulting in a disruption of

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the interaction. If recoiling becomes chronic the child is deprived of social experience which may shape the child’s entire interpersonal understanding and how the child makes meaning of the world in social and inanimate environments.

1.2 The Importance of Sensitive Periods Sensory issues show a developmental course. Their formation is affected by maturational and environmental processes during specific sensitive periods. The importance of sensitive periods for the maturation of sensory pathways has been shown by the distinguished work of Hubel and Wiesel [7]. In their landmark studies with cats, they demonstrated that monocular and binocular closure during an early developmental sensitive period leads to a significant decrease in neuronal connections of the deprived eye or both eyes with limited to no recovery. Hence, if an infant cat doesn’t have any visual input during this critical period, it will be blind for the rest of its life, as the neuronal connections to the eye are irreversible. But the effect was only observed over a specific developmental timeframe. After maturation of the visual system, experimental eye closure caused no detectable long-term effects. This indicates that the maturing brain is vulnerable to environmental effects, but once typical development is completed the sensory systems gain a certain resilience toward adversity even over a prolonged time. In other words, the organization of their states of consciousness is coherent and robust such that it can resist perturbations. But not just early deprivation of sensory experiences impacts developmental trajectories. Stimulation of a sensory system too early in development, or earlier than developmentally expected, can cause harm and influence the maturation and organization of other structures and networks. For example, surgical eye-opening in rat pups on postnatal day (PN) 7, eight days before this occurs naturally, compromises the development of the developing olfactory system that usually matures during this time [8]. Moreover, artificial early visual stimulation starting on PN7 alters behavior, especially social interactions with siblings and conspecifics that rat pups usually start to show about the same time as the eye-opening occurs naturally [9]. These findings indicate stimulation as well as deprivation can have a significant impact on sensory processing. Premature stimulation of one system can impair the neurodevelopment of another. Thus, not just deprivation and stimulation, but their timing and the possible hierarchical order of sensory development seem to impact species-­ typical organization and maturation of sensory processing and successful integration. Obviously, both typical and atypical sensory maturation can affect cognitive development, social perception, and interaction with conspecifics, making a connection between the often-observed sensory issues in ASD, premature infants, and other at-risk children. Studies investigating brain structure and connectivity in atypical sensory processing confirm the maturational aspect, finding differences in white matter structure in children with reported sensory integration problems. It is even assumed that high-risk abnormalities can be detected in MRI scans at birth and linked to later impairments in sensory processing based on factors such as low registration and

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sensation seeking [10–12]. Those results are consistent with studies using DTI technology, identifying microstructural differences in white matter tracts in the posterior cerebral regions in school-aged children that are directly liked to alterations in sensory processing [13–15]. Accordingly, abnormal white matter structure was associated with the etiology of atypical sensory processing, and future studies should investigate the possible predictive value for development and severity of diagnosis. Studies also indicate that the development of sensory gating significantly differs in children with sensory processing problems. Sensory gating refers to the brain’s ability to integrate complementary stimuli. Hence, it is a mechanism to attenuate sensitivity to sensory stimuli and can be detected using electroencephalogram (EEG). Davies and Gavin [16] reported that school-aged children with atypical sensory profiles showed significantly less sensory gating than typically developing children. Further, age and sensory gating were significantly associated but only in typically developing children, while in children with atypical sensory integration, no such relationship between age and sensory gating was evident. Based on EEG data the researchers were able to predict psychopathology with an accuracy of 86%. Further investigation of sensory gating showed that compared with adults and to typically developing children, children with sensory processing disorders followed a different maturational pattern and repeatedly failed to selectively filter sensory stimuli [17]. Overall, behavioral and developmental abnormalities in school-aged children with atypical sensory processing appear to remain stable over development and show high association with underlying neural markers, such as EEG patterns and white matter connectivity. The finding that children with sensory processing disorders don’t show age-associated developmental trajectories indicates again a delay of or failure in maturation of sensory systems. How we perceive our environment shapes our thoughts and experiences, differences in sensory maturation during sensitive periods may irreversibly alter perception and multisensory integration. Moreover, all future learning is then based on a less optimal neuronal network shifting perception from our “normal” to abnormal.

1.3 Sensory Disorders in Preterm Infants and Children with ASD Atypical sensory processing is more common in children born preterm [18–20]. The increased prevalence suggests that maturation of the underdeveloped nervous system in preterm infants may play a critical role. For example, typically developing infants have until birth only limited, muted visual or auditory input, such as the rhythmic heartbeat of the mother, muffled voices, and soft differences in light and dark, protected by the prenatal environment. On the other hand, preterm infants are forced to accelerate or at least adjust their sensory development as they are placed into a brightly lit, noise-filled setting, such as a neonatal intensive care unit (NICU), surrounded by beeping medical instruments, artificial lightning, and no protective membrane between vocal exposure and tactile stimulation from medical personal.

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The role of early experiences for sensory integration in human development has been shown in experiments on multisensory integration. One example is called the “McGurk effect” [21]. The effect occurs when conflicting sensory input is given. In the experiment, subjects are listening to a spoken phoneme, while another phoneme is visually pronounced by a speaker. The majority of participants report hearing a third phoneme, a mix between the auditory-processed and the visually processed one. This illusion, caused by multisensory fusion, can be observed in typically developing children as well as in deaf-born children who received cochlear implants during early infancy. However, children with congenital deafness whose hearing was restored after 30 months of age showed a significant visual dominance in the paradigm, indicating that the sensory integration as observed in the McGurk effect is not innate but develops based on experience during early childhood [22]. Hence, atypical sensory processing may indicate neuro-maturational complications during sensitive periods, such as but not limited to the perinatal phase. Deprivation and stimulation, both, may interfere with optimal development depending on the developmental timeframe. Children with ASD, like preterm infants have sensory integration problems. More than 60% of children diagnosed with autism show significant symptoms of sensory processing dysfunction, but this dysfunction was only recently added as part of the diagnostic criteria for ASD [23]. Moreover, while the variation of sensory integrative processes in individuals with ASD increases the complexity and coherence of their states of consciousness, individuals with ASD most often also distort the meaning they make of themselves and the world. The occurrence of “sensory issues” in ASDs is common and has been extensively described in the literature [24]. Interestingly the difference in sensory processing seems to reach both extreme ends of a continuum, spanning from aversion to attraction. For instance, sensory stimulation such as noise, touch, or social situations can cause severe anxiety and distress in individuals with autism, but sensory input can also be linked to extreme fascination and source of interest, as often seen in, and linked to stereotypic behaviors. Tomchek and Dunn [25] reported in a study including 562 children between the age of 3–6 years that children with ASD show a significantly different sensory pattern compared with matched typically developing children. The groups differed most significantly in subcategories of hypo-­ responsiveness, indicating a low level of responsiveness to sensory stimuli, and sensation-seeking, a search for intense levels of sensory input. Such sensation-­ seeking can be seen as actively engaging the world to detect and appropriate information that increases the complexity and coherence of the children’s state of consciousness. Similarly, another study found a unique pattern of hypo-responsiveness to sensory stimuli in children later diagnosed with autism, as early as when they are 5 months of age compared with neurotypical controls or children with other developmental disorders (DDs) [26]. On the other hand, hyper-responsiveness manifested similarly in children with ASD or DDs and was distinguishable to the neurotypical controls. In addition, an observed pattern of over-responsiveness could be connected to estimated development in these two groups (ASD and DD), indicating that

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maturation of sensory systems may be related to overall development. Put another way, as sensory systems mature and become more integrated and coordinated the information can be assimilated in a more coherent fashion. This is interesting, as it indicates that cognitive development may be associated with the maturation of those systems that make meaning out of the sensory input we receive from the world around us. More importantly, if maturation of the sensory integration system deviates early on, all further development is based on a maladaptive foundation, affecting all further perception of the world and associated meaning-making. Insidiously the process may be self-amplifying. Since 2013, sensory impairments are included in the Repetitive and Restricted Behaviors category to diagnose ASD in the DSM-5 [27]. But related sensory disabilities are not just comorbid with DDs, atypical processing is as well reported in individuals with schizophrenia, especially in the auditory and visual domains [28]. Further, high sensitivity to sensory processing was found to be correlated to avoidance behaviors in social anxiety disorder [29]. While those disorders clearly differ in the appearance of their specific psychopathology, characteristics of all of them are different levels of distortion in social perception and difficulty in interpersonal interactions. It is remarkable how we can connect biological evidence to this characteristic distortion in social perception, indicating that each of the observed psychopathologic symptoms of those disorders may be mere attempts to expand coherence and complexity or at least to not dissipate and lose complexity in the light of aberrant perception. Meaning-making in individuals with atypical sensory processing may be related to diverging experiences of threat and safety due to differences in the integration of environmental stimuli.

1.4 Atypical Sensory Integration Throughout Different Developmental Stages A compliment to thinking about sensitive periods is to think of how sensory processes manifest themselves during developmental periods from infancy to school age. During these periods there are typical changes in how children make meaning about the world and the mechanisms they use to make meaning which include increasing mature sensory processes. Sensory disorders thus may have differing effects during these different periods. Infancy  Abnormal sensory processing is usually diagnosed in early childhood through behavioral or developmental impairments. Several prospective studies aimed to identify early markers for the later development of abnormal sensory integration. Rahkonen et al. [12] followed 42 preterm infants over the course of 2 years. White and gray matter anomalies of magnetic resonance imaging (MRI) scan data were obtained at full-term equivalent age and compared with the level of neuromaturation and the Infant Toddler Sensory Profile (ITSP) at 2 years of term-­corrected age. As reported in older children before [30], patterns of low registration were of high prevalence for abnormal sensory behavior. Low registration on the ITSP scale

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means that individuals have a higher threshold to detect and react to sensory stimuli compared with normative developing children. Children who score high on this dimension need more time and more intense sensory input to perceive changes in sensory information. Moreover, 52% of all participants showed an atypical sensory profile in the ITSP, deviating at least one standard deviation from the normative sample. Abnormal sensation seeking at 2 years was significantly related to observed atypical structures in white and gray matter in the MRI taken at term-equivalent age. And while there likely were some experiential effects such as a lack of curiosity or excitement in novelty, these experiential effects were not considered. A large-scale study with 243 preterm infants also showed that the low registration factor from the ITSP has a high prevalence at 2 years of age [31]. The factor includes items such as “Doesn’t notice when arm is touched,” “Doesn’t perceive facial expressions,” and “Decreased awareness of pain and temperature” [32]. Abnormal scores on the low registration factor were related to mental and psychomotor developmental indexes and predicted poorer language outcomes. Preterm children showed more abnormal patterns on the ITSP compared with term-born infants. Additionally, male sex and abnormal white matter structures in MRI indicated higher risk for impairments in sensory processing at 2 years of age [11]. Again, experiential and motivational consequences were not considered, though it is easy to conceptualize how low registration would affect meaning-making processes and the child’s experience. Only one study used the Test of Sensory Function in Infants (TSFI), which allows for increased accuracy as it does not rely on parental report as the ITSP. Using the TSFI, Chorna, Solomon, Slaughter, Stark, and Maitre [10] report that 82% of the 72 infants included showed abnormal sensory processing in at least one test score. Ocular-motor control was linked to white matter injuries, and overall, male gender, white matter anomalies, and gestational age were related to poorer outcomes in sensory processing. Overall, abnormal white matter structures and high scores on the ITSP, especially on the low registration factor, seem to indicate and predict developmental difficulties in sensory process already during early infancy. Such difficulties may be amplified by experiential effects that emerge from the disorganization of making meaning of distorted sensory input. Preschool Age  A meta-analysis suggests that the reported symptoms of sensory dysfunction increase until the preschool age in individuals later diagnosed with ASD [33]. In a cross-sectional study, Adams, Feldman, Huffman, and Loe [34] found that abnormal sensory integration is more prevalent in preschool children that were born preterm (37%) compared with term-born children (12%). Further, poor sensory processing was associated with executive function evaluated based on performance in a six tasks battery. The increased appearance in preterm children again corroborates the maturational aspect of sensory dysfunction and divergent experiences of the shared world around us. But preterm birth is not just a risk factor for sensory processing abnormalities, there is also an association of preterm birth and risk of developing autism.

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School Age  In a cross-sectional study following 107 children from infancy (1–4 years) to childhood (4–8 years) the prevalence of sensory processing impairments was stable [30]. While the occurrence of abnormal scores in tactile, auditory, and vestibular sensory systems were increased for children that were born premature, no other neurodevelopmental risk factors could be identified. In a sample of males aged 8–12 years, Chang et al. [14] used diffusion tensor imaging (DTI) to investigate the role of white matter. Children with a diagnosis of sensory processing disorders showed lower connectivity between white matter tracts in parietal-occipital regions compared with healthy controls. The region is associated with perception and sensory integration. Further, the connectivity of white matter tracts, the networks between neurons, was significantly related to auditory and attention scores, as well as working memory performance. Those findings were replicated in a mixed-gender cohort, relating white matter microstructure in the parietal region with direct measures of sensory processing in auditory and tactile systems [13].

1.5 Summary Several risk factors for the development of atypical sensory processing, such as preterm birth and previous institutionalized care, indicate that complications in maturational processes of the sensory system may be involved. For instance, suboptimal levels of deprivation or stimulation of sensory systems during critical developmental periods could cause lasting alterations in perception and experience. Earlier detection of sensory difficulties may help to develop new diagnostic measures and therapies for children. Moreover, recognizing that the sensory deficit, an objective marker of dysfunction (e.g., low threshold to respond), has experiential consequences (e.g., anxiety) additionally requires consideration of the experiential effect as part of the diagnosis. Psychopathology in essence is the disturbance of making meaning about one’s self in the world. Over the last few years, increasing evidence indicates a significant neural basis for the atypical sensory processing. Abnormal neuromaturational processes during sensitive periods seem to be involved in deviations in sensory processing. Initial studies in at-risk populations indicate that MRI analysis of white matter abnormalities may be a promising early biomarker for later deviations in sensory integration. EEG studies looking at sensory gating, on the other hand, may inform about developmental trajectories and abnormal patterns in sensory processing. Further, it would be interesting for future studies to investigate whether successful occupational therapy also changes sensory gating as observed in EEG or white matter connectivity. How we integrate and interpret environmental sensory information shapes our perception of the world around us. Deviations in maturational patterns or hierarchies may have severe impact on how we experience the outer world and make meaning out of the impressions provided by our surroundings. This is not limited to raw sensory information but transfers to nonverbal communications, social perception and interpersonal interactions, and how we perceive those from others.

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Moreover, a neuromaturational approach recognizes that the development of sensory perception and integration is highly complex, and disturbance of the maturation may lead to diverse issues on a broad spectrum depending on timing and severity, just as autism cannot be described in a singular set of symptoms but is expressed on a continuum, indicating deep developmental roots of origin. Moreover, and dramatically increasing the complexity is that even a small or limited sensory problem affects many other systems which over time may become causal factors leading to an even greater configuration of effects which could in turn become causal of other effects. However, without attention to experiential effects and the meaning individuals make of themselves and their engagement with the people and things essential information will be left out. Children with atypical sensory processing like all living systems are trying to maximize their growth and development, their coherence, and complexity. The underlying mechanisms are “cold”, and objective, but we also need to recognize that they are experiencing the world, trying to make sense of it, and the experience they have and the meaning they make will have a profound effect on how they live in the world.

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