Pediatric to adult transition care in neurogastroenterology and motility: A position paper from the American Neurogastroenterology and Motility Society and European Society of Neurogastroenterology and Motility.

The presence of a coordinator, usually a nurse, nurse practitioner or other allied healthcare professional, has been proposed as the single most important factor to the development of an effective transition service ( 44 ). In addition to improving communication between patients, caregivers, and providers, transition coordinators may have the critical time needed to work with patients on skills related to self-management and self-advocacy. The value of transition coordinators has been demonstrated in the adolescent IBD population ( 45 ). Indeed, patients who had transition overseen by a coordinator demonstrated significantly higher scores in transition readiness and self-management skills versus those without this support ( 45 ). Moreover, compared to patients who did not work with a coordinator, the presence of a coordinator meant it was more likely for IBD patients to maintain clinical remission ( 45 ).

The age at which adolescence commences and the transition point into adulthood can be interpreted through various biological, cultural, religious, and legal lenses and will vary between different patients. The advent of unprecedented social forces, including digital media, delays in the completion of education, marriage, and parenthood were proposed in The Lancet as reasons to support a shift in the definition of adolescence from 10-19 years to 10-24 years ( 65 ). Indeed, self-management skills are thought to be mastered after the age of 18-20 years for AYAs with IBD and other chronic disorders ( 66 , 67 ). Since adult milestones are achieved at a lower rate amongst individuals with pediatric chronic disease ( 68 ), it is possible that skills in self-management and self-advocacy are delayed further for patients with NGM disorders compared to healthy peers. Often, for practical reasons, such as AYAs entering the college system in the USA, age 18 years is typically used to delineate between pediatric and adult care in clinical practice, and individuals aged between 16-19 years are transitioned to adult services for management of ongoing healthcare requirements ( 69 ). An argument could be made that the transition process should begin as early as 11 to 12 years of age, since this may lead to improved knowledge, skills and the confidence required to negotiate adult healthcare ( 70 , 71 ). This supports the recommendation made by the anorectal malformation working group to commence transition at 12 to 13 years of age ( 72 ). However, training programs, at least in the USA, do not require trainees to be familiar with the care of patients below the age of 18 years, so adult gastroenterologists may not always have the appropriate training or resources to manage disorders that are more frequently encountered in the pediatric setting e.g., esophageal atresia and cloacal malformations. As such, it is not unheard of for some patients to remain with their pediatric providers well into adulthood due a lack of adult healthcare providers in their geographical region. A comprehensive assessment of transition readiness, which should be independent of an arbitrary age, ought to begin at the time a pediatric team decides that adult care may be necessary in future. Validated self-administered questionnaires have been developed to assess readiness for transition and can help identify areas for improving patient education and track progress throughout the transition process ( 73 ). One systematic review ( 73 ) identified ten different generic and disease-specific assessment tools with only one tool – the Transition Readiness Assessment Questionnaire (TRAQ) – which demonstrated adequate content validity, construct validity, and internal consistency. The TRAQ, originally published in 2010 ( 74 ) and refined in 2014 ( 75 ), is a disease-neutral patient-report instrument with 29 questions that assess AYAs’ disease self-management and healthcare utilization skills before and during transition. Older age and a primary diagnosis of an activity limiting physical condition were shown to be associated with higher scores in the self-management domain, whilst female gender and a primary diagnosis of an activity limiting physical condition were associated with higher scores in self-advocacy ( 74 ). Interestingly, no association between age and different TRAQ scores was identified on the self-advocacy domain, which suggests that health management skills are independent of age ( 74 ). The ‘Ready, Steady, Go’ program, a generic stepwise framework used widely across the UK National Health Service, helps young people with long-term health conditions transition into adult services ( 70 ). Healthcare providers are permitted to use ‘Ready Steady Go’ material, developed by researchers at University Hospital Southampton NHS Foundation Trust, in their original format purely for non-commercial purposes ( 70 ). Briefly, the ‘ready’ aspect of the program gives young people (from the age of 11 years, if developmentally appropriate) and their caregivers an opportunity to explore knowledge about their health condition and issues related to self-advocacy, daily living, school, leisure activities, and emotions. The ‘steady’ questionnaire, completed around 13-14 years of age, is used to monitor progress on issues identified in the ‘ready’ questionnaire as well as new themes which can be tackled over the next two years. The ‘Go’ questionnaire, completed at approximately 16 years of age, ensures that patients have the correct skills and knowledge to 'Go' into adult services, which is followed by the ‘Hello’ questionnaire when the patient enters adult services. Unfortunately, there do not appear to be any validated transition questionnaires for caregivers of patients who lack capacity to make independent decisions related to their healthcare. In such cases, there is often a conversation between caregivers and healthcare providers to develop a transition timeline.

The list of healthcare professionals that should form an NGM transition service is extensive and must be tailored to local resources and patients’ needs. For instance, the healthcare professionals required to manage the three patients described in table 2 will differ largely because the AYAs have different underlying diagnoses and corresponding sequelae. The nuances of specific cases aside, the authors reached a consensus that the following healthcare professionals should ideally form the foundation of a secondary care NGM transition service ( figure 2 ): a transition coordinator, an adolescent psychologist/psychiatrist (ideally both as they have different clinical skills), a dietitian, a pediatric neurogastroenterologist, an adult neurogastroenterologist, an adult gastrointestinal surgeon (with a subspecialty interest in NGM), a pediatric gastrointestinal surgeon (with a subspecialty interest in NGM), and nurse specialist (whose role will depend on the condition being addressed e.g., a stoma nurse or nutrition nurse). A primary care physician is critical for providing continuity of care in the community but has not been referred to the above list, since they are not present in the secondary care setting.

Based on non-peer reviewed data from a tertiary care UK NGM transition service (University College London and Great Ormond Street Hospitals), 56.5% of AYAs had a psychiatric diagnosis and psychological interventions were found to be necessary in 69% of AYAs ( 15 ). Similarly, in the USA, co-morbid psychiatric conditions were present in 90% of patients who were in a tertiary care transition service ( 14 ). The high prevalence of comorbid psychiatric diagnoses in the NGM transition setting, as well as the importance of brain-gut behavior therapies in the management of NGM disorders more broadly ( 46 , 47 ), underscores the importance of integrating of psychologists and psychiatrists in the transition team. Mental health professionals not only help AYAs conceptualize their symptoms through the biopsychosocial model, but also help patients navigate the psychosocial factors associated with adolescence, including the strive for greater autonomy, educational/employment goals, psychosocial health, sexuality, and reproduction. Moreover, mental health professionals who specialize in psychogastroenterology – a field dedicated to applying effective psychological techniques to gastrointestinal problems – help address the cognitive, emotional, and behavioral factors associated with NGM disorders ( 46 ). Unfortunately, there is ever increasing pressure on adolescent mental health services ( 48 ), so identifying suitably qualified mental health professionals, let alone those who are adept in psychogastroenterology focused treatment, may be challenging. Reassuringly, based on non-peer reviewed data from a tertiary care NGM transition service, a psychiatric diagnosis has not been shown to result in a suboptimal transition outcome ( 49 ), defined as a return to pediatric care or an emergency room visit for a gastrointestinal-related complaint during the transition period.

Poor communication between pediatric and adult care services may lead to incomplete transfer of healthcare information. Across numerous healthcare settings across the world, there is arguably greater scope and flexibility for caregivers to choose a suitable pediatrician for their family’s needs than it is for adults to select a clinician. When transition care is necessary, families often expect pediatricians to take the lead and identify a suitable adult practitioner with whom a pediatrician has an established relationship. Transfer of information may be facilitated by direct communication between healthcare providers, but this may become challenging when patients have complex healthcare needs and/or where multiple, often geographically scattered, providers are involved. Where a transition service is not fully formed and a transition coordinator is not present to orchestrate communication, we would encourage the pediatric team to work with the patient and their caregivers to develop a ‘health passport’. Aside from containing a patient’s medical history, a well-constructed ‘health passport’ should contain a compendium of personal, social, and medicolegal data, including but not limited to a patient’s living environment, education/employment goals, consent/mental capacity, and best interest decision-making. Colver et al. ( 89 ) attempted to study the efficacy of health passports in the transition phase in a National Institute of Health Research study, however, their analysis was limited by a small sample size (n=13). Although insufficient quantitative data were generated from which to formulate robust conclusions, strikingly, none of the 13 participants said that they completed the health passport alone and although the majority said that they thought passports were ‘useful’, only half of them took them to health care appointments. In other settings, participants used this document occasionally and its perceived utility was limited ( 90 ). Priority areas for developing a health passport in the NGM setting include a more thorough understanding of the essential components of this document, the individuals who would benefit most from their use, as well as strategies to improve patient engagement with the tool.

Pediatric and adult gastrointestinal surgeons (with subspecialty interests in NGM) should be involved in the care of patients who have congenital gastrointestinal anomalies, those who have previously undergone a surgical procedure, and/or in cases where surgery is likely to be required in future. The extent of involvement of gastrointestinal surgeons is institution and situation dependent, since many issues may potentially be managed by a gastroenterologist with crucial oversight provided by a surgeon team. Where a stoma has been created, it is not unusual for much of the care to be coordinated by a stoma nurse who liaises directly with gastrointestinal surgeons if complications arise that require correction. During the transition phase, gastrointestinal surgeons may directly or indirectly manage ongoing or new surgical problems, including but not limited to the parastomal hernias (although unusual in AYAs), poorly sited stomas, complications related to anterograde colonic enemas (e.g., new fecal incontinence), blocked/infected enteral feeding tubes, or fundoplication reversal. Diverting enterostomies may be necessary to manage upper and/or lower gastrointestinal motility disorders, including congenital conditions (e.g., anorectal malformation or Hirschsprung’s disease), intractable functional constipation, and pediatric intestinal pseudo-obstruction ( 31 , 61 ). In one study comparing post-operative healthcare outcomes following enterostomy in pediatric patients with (n=62) and without (n=128) a motility disorder, significantly more patients with motility disorders experienced troublesome passage of stools, abdominal pain, and ileus ( 32 ). In addition to the higher post-operative complication rate, children with motility diagnoses had a significantly higher proportion of high-grade complications vs those who had not (61.8% vs. 31.0% p =0.002). Indeed, many motility disorders are pan-enteric in nature so localized surgery to one region may not necessarily eliminate symptoms due to global dysmotility ( 62 , 63 ). Moreover, patients in whom an enterostomy is created to manage symptoms related to a DGBI may have ongoing visceral hypersensitivity, owing to a dysregulated brain-gut axis ( 64 ), which may contribute to the greater frequency or severity of post-operative abdominal pain reported amongst those with NGM disorders versus those without ( 32 ). The remarkably high enterostomy-related complication rate reported in this study, particularly amongst those with an underlying motility disorder, underscores the need for this group of patients to be closely monitored during transition.

There is an argument that the home environment is where transition readiness begins, so caregivers can play an important role in preparing AYAs for transition ( 76 ). Caregivers can face numerous stressors during the transition period which may relate to termination of their relationship with pediatric healthcare providers, the uncertainty associated with forthcoming adult care, and delays in transition initiation ( 77 ). Additional research is required to understand caregivers’ needs in greater detail and develop evidence-based services to support them during the transition phase. It is important for AYAs to eventually become comfortable seeing providers without caregivers and for caregivers to feel comfortable allowing AYAs to consult providers independently, granted this will not always be attainable in patients who have an intellectual disability. Consultations in the absence of caregivers may give patients the opportunity to explore issues which may otherwise be left undisclosed out of embarrassment, including matters related to alcohol, drugs, and sexuality ( 78 ). Consulting a patient independently has been shown to provide a clearer perspective on transition readiness, as evidence suggests that caregivers tend to over-estimate their child’s skills and knowledge related to transition readiness compared to a patient’s self-assessment ( 79 ). In some cases, a caregiver’s behavior may perpetuate the disease process. According to social learning theory, the way in which caregivers respond to children’s abdominal symptoms (reinforcement) and the techniques in which they cope with their own abdominal symptoms (modelling) has been shown to influence abdominal symptom perception in childhood ( 80 - 83 ), which can also impact the frequency of symptoms, disability days, and healthcare visits made by children when they enter adulthood ( 84 ). Psychosocial interventions that aim to reduce protective responses from caregivers and increase a child’s coping skills have been shown to reduce children’s gastrointestinal symptom burden compared with controls in randomized controlled settings ( 85 , 86 ). Given the importance of the patient-caregiver relationship in the evolution of DGBI, experienced psychologists may find it helpful to explore the patient-caregiver relationship to help patients identify thoughts, beliefs and attitudes that may influence future outcomes. In certain cases, it may be appropriate to invite caregivers into consultations, particularly when patients are not seen to demonstrate adequate self-management and healthcare utilization skills. It should be noted that triadic communication ( 87 ) requires a degree of caregiver introspection, and it may be challenging to engage with caregivers who have high expectations and are insensitive to a child’s cues ( 88 ). The plight for independence features prominently during adolescence, so healthcare professionals should sensitively explain to patients the rationale for ongoing caregiver input in the management plan.

AYAs with DGBI, those with primary/secondary motility disorders, and those with artificial feeding requirements have unique healthcare needs that require tailor-made transition services to improve short- and long-term healthcare outcomes. The high prevalence of DGBI within the AYA general population and the dearth of data exploring transition clinics within the NGM field suggests that there are significant gaps and unmet needs within current healthcare structures that must be addressed to optimally care for these patients. Key milestones, from ‘screening’ to ‘post-transfer assessment’, are summarized in figure 3 . The multidisciplinary team of healthcare professionals invested in an AYA’s journey should be patient-specific, however, the authors propose that an NGM transition service in secondary care should ideally include a transition coordinator, an adolescent psychologist/psychiatrist (ideally both as they have different clinical skills), a dietitian, a pediatric neurogastroenterologist, an adult neurogastroenterologist, an adult gastrointestinal surgeon (with a subspecialty interest in NGM), a pediatric gastrointestinal surgeon (with a subspecialty interest in NGM), and nurse specialist (whose role will depend on the condition being addressed e.g., a stoma nurse or nutrition nurse). In addition to the patient, it is vitally important to respect the needs of caregivers and develop family support mechanisms where resources permit. Key areas for future research relate to the development of NGM-specific transition readiness questionnaires, robust tools to assess post-transfer healthcare outcomes for patients with NGM disorders, and educational programs to train healthcare professionals about transition care in NGM.

Diet plays an important role in the development and progression of NGM disorders ( 50 ), so it is perhaps not surprising that dietetic interventions were necessary in 76% of AYAs in a UK tertiary care NGM transition service ( 51 ). Amongst other roles, dietitians help patients achieve adequate nutrient intake, identify ‘fear foods’, and provide guidance on safe refeeding after a period of dietary restriction. The work of dietitians is often closely intertwined with those of other healthcare professionals. For instance, given the association between neurodiversity (e.g., attention deficit hyperactivity disorder / autism spectrum disorder) and DGBI, as well as feeding problems related to food selectivity, food refusal, and poor oral intake ( 52 ), dietitians may collaborate with psychologists to offer a dual psychological-dietetic management approach. Additionally, patients with DGBI have been shown to experience a variety of DSM-5 ® eating disorders, including avoidant-restrictive food intake disorder ( 53 ), which may also benefit from a dual treatment approach ( 50 ). Ideally, dietitians within the multidisciplinary team should be trained in NGM disorders, since the management of these conditions requires expertise that is not always addressed within the broad-based, general training curriculum. However, in many cases a suitably qualified allied healthcare professional cannot be identified, so a transition team should ensure that professionals receive the training they need to deliver optimal outcomes for this patient population.

For this narrative review, a medical librarian (EA, see acknowledgements) in the Mayo Clinic Libraries (Rochester, MN, USA) performed a comprehensive search of the MEDLINE, EMBASE, and Scopus databases. Full details of this search are provided in the supplementary data file . For the first phase, the MEDLINE database was searched for pediatric-adult transition services in the context of general gastroenterology (that is, not specific to NGM). For the second phase, MEDLINE, EMBASE, and Scopus databases were searched specifically for pediatric-adult transition services in the context of NGM. In this search, records with “transition* AND neurogastroenterol*” in the title, abstract, keyword, and keyword heading were identified. Following title and abstract screening, six potentially relevant articles were identified and two were retained in the MEDLINE database, and 16 potentially relevant articles were found in the EMBASE database, with seven retained. The Scopus database had no unique references. In total five unique (non-duplicate) articles or conference abstracts were retrieved which referred specifically to NGM transition care ( 14 - 18 ).

Transition services are well-recognized in the 21 st century healthcare model and represent a bridge between pediatric and adult healthcare settings. The overall aim of a transition service is to support adolescents and young adults (AYAs) with chronic health conditions, as well as their caregivers, as they gradually move from a child-centered to a more autonomous, adult-orientated medical system ( 1 ). Unlike ‘transfer of care’ which is an event that occurs at a single point in time, transition is a multistep process which caters for the medical, psychological, developmental, and vocational needs of AYAs to ensure that patients are better able to independently manage their healthcare needs ( figure 1 ). Appropriately executed transition services in gastroenterology can increase medication adherence, reduce inpatient admissions, and allow AYAs to achieve their estimated maximum growth potential ( 2 ). Policy documents from professional bodies highlight the importance of transition care, yet it is undertaken poorly in many instances ( 1 , 3 ). Until a publication from the British Society of Gastroenterology Adult and Young People’s Committee in 2017 ( 4 ), no national or international professional body had published consensus guidelines for healthcare professionals coordinating transition care for AYAs with chronic digestive disease, although attempts were made to a promote a discussion in the field. For instance, in 2003, the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition published non-consensus-based recommendations for transition care for AYAs with inflammatory bowel disease (IBD) ( 5 ). In Europe, in 2015, a similar non-consensus-based approach was undertaken by four Italian Societies of Gastroenterology who published recommendations for transition care for AYAs with IBD, celiac disease, and chronic liver disease ( 6 ). At the time of publication, the British Society of Gastroenterology Adult and Young People’s Committee acknowledged the relative dearth of data addressing transition care in neurogastroenterology and motility (NGM) compared to IBD and hepatology ( 4 , 7 - 10 ), which to our knowledge has remained largely unchanged. This is particularly concerning since data suggest that health related quality of life amongst patients with NGM disorders, such as irritable bowel syndrome, fecal incontinence, and/or functional constipation, is at least as impaired as those who have IBD ( 11 , 12 ). Although stakeholders interested in developing NGM transition services may leverage data from IBD or hepatology subspecialties, there are highly specific considerations when managing patients with NGM disorders. Indeed, many NGM disorders, particularly those characterized by visceral hypersensitivity, are multifactorial and do not have an apparent structural or biochemical cause of symptoms that can be identified using routine medical testing, which may de-legitimize the patient experience. Therefore, healthcare professionals managing NGM disorders, particularly DGBI, should be more willing to readily engage with the biopsychosocial model of care ( 13 ). The biopsychosocial framework dictates close collaboration between patients, caregivers, and healthcare professionals to thoroughly understand the reciprocal interaction between biological, psychological, and social factors, rather than focus exclusively on monocausal etiopathogenic processes. The overall aim of this article, endorsed by the American Neurogastroenterology and Motility Society and European Society of Neurogastroenterology and Motility, is to promote a discussion about the role of transition services for patients with NGM disorders. The manuscript’s co-authorship draws on the experience of a variety of healthcare professionals: pediatric neurogastroenterologists, adult neurogastroenterologists, pediatric- and adult gastrointestinal surgeons, psychiatrists, psychologists, and dietitians. In our commitment to patient and public involvement, a person with experience of transition care (SJ) was consulted and contributed to the content of this review.

The importance of performing a post-transfer assessment was recognized as early as 1993 by Blum et al. ( 1 ) who reported that “outcome measures should include rate of completion of referrals, functional outcomes, sense of well-being, and patient satisfaction”. Later, in 2015 ( 91 ), a consensus paper reported eight key indicators to assess successful transition, which was developed by 30 experts in adolescent health using the Delphi process ( table 3 ). Differences in healthcare outcomes between different patient groups with different NGM diagnoses are inevitable, so one key consideration for future research is the development of standardized methods to collect disease- and non-disease specific outcomes based on the ‘normal’ evolution of a specific NGM diagnosis ( 92 ). Aside from identifying what specific measures should be measured and how groups can go about doing this, research should also evaluate the time points at which outcomes are best evaluated. Consistency in data collection would help to ensure that different NGM transition models can be more effectively compared with one another. In addition to the suggestions outlined in table 3 , a non-exhaustive list of non-disease specific outcomes which healthcare professionals may consider collecting in routine NGM practice could include educational success, employment status, insurance coverage, quality of life, and mental health status.