Background
Chronic diseases in adolescent patients can be an enormous burden when the time of moving out of their parental home and becoming independent coincide with the first referral to the adult clinic after many years of paediatric health care. Loss of continuity of care at transfer might endanger disease remission. Onset of inflammatory bowel diseases (IBD) appears frequently in young age [
1]. The incidence of Crohn’s disease (CD) amounts up to 6.6 per 100,000 people in Germany, while the prevalence is 100 to 200/100,000 people [
2]. Ulcerative colitis (UC) affects up to 250 of 100,000 people and up to 4/100,000 people are newly diagnosed each year [
3]. About 25% of IBD patients are being diagnosed before the age of 18 years [
4]. Thanks to effective modern therapy options, adolescents with IBD can achieve disease remission and a normal life [
5]. However, young adults need a different clinical setting than adolescents in order to live independently with their disease. A structured transition program has important benefits and can provide a comprehensive, accompanied transition from adolescent to adult care. This is because deficiencies in care during this particularly critical phase can result in treatment interruptions, insufficient treatment compliance, and increased frequency of complications that are probably avoidable [
6]. Research in transition care for IBD patients was long time limited to expert recommendations and experiences. Strengthening the disease management skills of adolescents, while providing information about transition and slowly reducing the parental involvement was described as beneficial by health care providers and patients [
7,
8]. However, the definition of an effective transition process is still a matter of intensive debate. The American Association of Paediatrics (AAP) described six core elements as a guidance for transition programs: transition policy, monitoring, readiness and planning, as well as transfer of care and transfer completion [
9]. While transition care developed relatively slowly in Germany, three out of four specialist paediatric centres for IBD in the United Kingdom (UK) offered social support for transition already in 2007 [
10]. However, structured transition has developed increasingly in the last 10 years in Germany and some initiatives demonstrate promising results. Transition clinics, case managers and a standardised medical summary for the adult gastroenterologist are the main parts of the nationwide Berlin Transition Program (BTP) [
11,
12]. In addition, there are successful patient education programs in place, which inform the patient about the program, risky health behavior, sexuality and the search for a new physician within these services [
13,
14].
A study from the UK could demonstrate several clinical benefits in IBD patients after visiting a multi-disciplinary transition clinic [
15]. A Canadian study, however, failed to find an alteration of acute health care utilisation depending on the post-transfer setting (community based vs. specialised tertiary centre) two years after transfer [
16]. Nonetheless, most of the studies evaluating the disease course of IBD after transition did not include economic parameters and only a few investigated the psychosocial outcome [
17]. We thus aimed to compare the clinical and socioeconomic long-term outcome in young adults with and without utilisation of a structured transition program at a German hospital.
Discussion
Although there is a number of expert recommendations [
7,
29] and some outcome analyses in recent literature, the precise variables of an effective transition process still need to be clarified. One of the first transition outcome analyses for IBD patients found significant clinical improvements 2 years after transition support [
15]. Lower surgery and hospitalisation rates, better clinic attendance rates, improved adherence to medication and reduced cumulative doses of radiation were reported benefits of the transition process. Bennett et al. (2016) published a survey from 46 IBD patients, previously treated in the paediatric clinic and transferred into adult care compared to a cohort of 35 IBD patients with a similar age, which were diagnosed before the age of 18, but were immediately followed up at an adult specialist clinic and thus did not went through a transition process. They also noted psychosocial outcome benefits and a positive perception of the transition process, but found neither an effect on clinical nor on psychosocial development [
17]. After all, a survey by Dabadie et al. (2008) found that IBD patients and parents considered a structured transition in terms of a joint medical visit as highly beneficial for building confidence with the new adult gastroenterologist in almost every case [
30]. Thus, transition care enables IBD patients to maintain the treatment success during paediatric care and on the other hand, empowers the physician-patient relations.
Prevalence of IBD-related intestinal complications was significantly lower in our transition group patients compared to IBD patients without transition support. In general, intestinal complications tend to be more frequent in IBD with paediatric onset [
31,
32]. In addition, other studies showed that surgery and admission rates were significantly higher in IBD patients without transition support or lower in patients, who frequently attended transition clinics, compared to adult controls [
15,
33]. This might result from lower rates of intestinal complications in post-transition patients and is therefore consistent with our findings. Furthermore, intestinal complications like perianal fistulas in CD patients do not only lead to higher health care utilisation rates, but are also associated with higher morbidity rates, impaired quality of life and relevant high expenses for following biological treatment [
34,
35]. The prevention of intestinal complications by structured transition is thus of utmost importance for the clinical outcome of young adults with IBD, both, from a medical and economical point of view.
The cumulative radiation exposure during the study period was significantly lower in our transition group than in patients without transition support, which might be explained by the lower incidence of intestinal complications and subsequent surgery in the transition group. On the other hand, patients in the transition cohort were most commonly followed up by abdominal ultrasound and received only routine low-dose imaging studies such as chest x-rays before anti-Tumor Necrosis Factor alpha (anti-TNF) therapy. Disease course in IBD patients is commonly accompanied with high effective doses of radiation due to follow-up and diagnostic procedures over a lifetime [
24], in particular in IBD patients with disease onset at an early age. A cumulated radiation exposure of more than 75 mSv already increased the risk of cancer related death by 7.3% in a cohort of 409 CD patients with an IBD diagnosis before the age of 17 years [
36,
37].
Despite we observed a trend towards a lower prevalence of surgeries within the study period, the number of hospitalisations did not significantly differ between our transfer and the transition group. This is in contrast with findings from other IBD transition outcome studies. As already discussed by Cole et al. (2015), decreased admission rates in the transition period could result from optimised medication and adherence achieved by frequent alternating assessments by a paediatric and an adult medical team [
15]. However, this approach was not a standardised part of the transition program used in our present study. Another explanation for our findings could be the methodology of the outcome analysis like the length of the reviewed follow-up period. Various studies also recommend the evaluation and optimisation of transition readiness before the final transfer date and its role to prevent early relapse or complications. Although we avoided to transfer patients with unstable disease, we did not utilise validated tools acknowledging clinical as well as socio-ecological factors to access transition readiness before the first visit at the adult clinic [
38‐
40]. Furthermore, the impact of biological treatment on hospital admission and surgery rates should be taken into consideration [
41,
42]. Reduction of surgery and hospitalisation rates is still an important target for transition support.
The overall incidence of psychiatric comorbidities showed no difference between our study groups, except for variance of newly diagnosed eating disorders and disordered eating behaviours. However, eating disorders like anorexia nervosa, but more importantly dysfunctional eating habits including both skipping meals and binge eating are common in IBD patients. Nutritional deficiencies as well as obesity are possible consequences of these psychological comorbidities and are potentially worsening IBD [
43‐
45]. A 41% greater trend towards misuse of medication and excessive exercise to achieve a desired body image was described in patients with diet-related chronic health conditions such as type 1 diabetes, cystic fibrosis and IBD [
46]. Preparation for transition should enlighten the consequences of non-adherence and inadequate diet as long as intervention is possible. Non-adherence to medication might be one of the most important issues in IBD care and is crucial for successful transition to the adult setting. Thirty to 45% of IBD patients are non-adherent, which increases costs and causes negative effects on disease outcome [
47,
48]. Improved medication adherence in adolescents has been described for larger IBD clinics [
33]. Adherence rates to medication (based on patients’ survey data) did not significantly differ between our two study groups and therapeutic drug monitoring was not systematically performed in our patients.
A significant higher number of transfer group patients had a documented history of delayed puberty at the time of transfer into adult health care compared to patients in the transition group. It should be noted, however, that sexual development data by Tanner staging was not systematically assessed in our patients like in other retrospective studies [
49]. Body growth and weight outcome data showed no significant differences between our relatively small study groups during the transition period. However, it is known that about 20% of patients with childhood onset CD have a significantly reduced adult height in larger IBD cohorts [
50,
51]. A higher BMI is also associated with a lower risk for surgery, clinical relapse and loss of response to anti-TNF therapy [
52]. Although anthropometric outcome might not be directly affected by transition care, prevention of underweight and growth retardation is still an important task during the transition process.
Seven out of 24 transition patients (39%) stated active nicotine consumption compared to none in the transfer group. Forty-four percent of our UC patients were active smokers in contrast to 17% of our CD patients, whereas at the same time the number of UC patients was higher in our transition cohort (
n = 11/24; 46%) compared to our transfer cohort (
n = 2/11; 18%). Even though there is published evidence for beneficial effects of smoking in UC patients [
53] we did not believe that this may have affected the clinical outcomes during our study period.
Educational and employment status evaluated after the 4-year observation period did not significantly vary between our transfer and transition group patients. Although young college students with IBD feel less successful and admitted their class attendance rates to be less regular than their healthy controls [
54], IBD patients achieved a diploma or a post-secondary school degree more frequently than their healthy peers and earn more money per annum [
55,
56]. Since time of transfer and graduation from school occur at a similar time, transition support may enable more patients to start into a successful work life as an adult.
QoL is known to be significantly reduced in CD [
57] and UC patients [
58] and improving QoL is a major task in the management of IBD patients. Sexual activity was significantly reduced in our transfer group patients compared to transition group patients. This is a common finding in IBD with a rate of up to 58% of patients stating impaired sexual function and libido [
59]. Dissatisfaction with the body image is also present in approximately two-thirds of IBD patients and in up to half of cases, disease already had a negative influence on relationships [
60]. Therefore, our IBD transition program addresses information about sexuality and fertility in preparation for transfer. Evaluation of a German Modular Patient Education Program (
‘ModuS’) indicated a positive effect on patients’ self-efficacy and satisfaction [
61]. Transition patients also tended to subjectively perceive their bowel movements to be less frequently loose than in the transfer group. Better control of intestinal symptoms, also considering the clinical outcomes, might explain this finding. Other domains of the IBDQ did not significantly differ between our study groups.
Total disease management costs during the transition process were another main outcome parameter of our study, but showed no significant differences between our groups. To our knowledge, there are little or no other published studies available, which evaluate the cost-effectiveness of structured transition programs. Importantly, one of the main cost-drivers in both our study groups was the use of biologicals. The implementation of transition programs might also have indirect long-term financial benefits since active disease in IBD patients is associated with high costs by sick leaves, occupational disability and early retirement [
62,
63]. Long-term cost savings might result from prevention of disease relapses during the time of transition when young adults with IBD start their professional training / life. Overall, surgery and admission expenditures tended to be lower in the transition group. This may reflect the significant lower incidence of IBD-related complications and need of surgery in our transition group. One of the main ideas behind transition care is that imparting of disease-related knowledge and self-management skills in patients with chronic conditions prevents disease relapse or exacerbation. A patient education program with an estimated price of 200 US dollar per patient described in a study from the USA showed possible reimbursements in chronically ill patients by lower health care utilisation rates [
64]. The randomised controlled trial by Kennedy et al. (2004) also demonstrated potential cost savings through better adherence, lower admission rates and improved quality of life in IBD patients one year after self-management education [
65]. A validated 24-item questionnaire called CCKNOW (Crohn’s and Colitis Knowledge) examines disease-related knowledge about IBD, medication, diet and complications. Colombara et al. (2014) demonstrated possible reimbursements of about 1,100 € per an increase of 5 points on the CCKNOW scale [
66]. Thus, we attribute the tendentially lower health care utilisation costs to educational core elements of our setting, which includes the improvement of disease-related knowledge, self-management skills and the evaluation of these education parameters at the joint consultation. Our finding that biologicals are not only the main cost drivers in both our study groups, but also have a significant impact on mean total disease management costs per year, is consistent with other cost analyses: 64% of total health care costs in CD and 31% in UC patients were distributed to anti-TNF therapy in a Dutch study, while surgery and hospitalisation expenditures, which were the main cost drivers before introduction of biological therapy in clinical practice, were much lower [
67]. These findings might be explained by the lower health care utilisation rates caused by biological treatment in IBD [
68]. For example, anti-TNF therapy alone leads to average savings of 2,750 pounds per IBD patient after one year in a study from the UK [
69]. Further transition cost analyses should take the influence of anti-TNF therapy on total disease management costs into consideration. Finally, costs for the implementation of structured transition programs need to be considered but are most likely justified by the medical and economic (long-term) benefits of transition support.
The design of our present study might have some potential limitations. Since our retrospective single-centre study included a relatively small number of patients and the study objects were not randomised, most results have to be interpreted as trends and should be further evaluated in larger studies. We decided to use a retrospective study design and a historic patient cohort in this pilot study since our local ethics committee had serious ethical concerns regarding randomization between a simple transfer and structured transition into adult health care. In addition, participation in a structured transition program for adolescents with IBD in Germany is to a certain degree still dependent on a declaration from the health insurer on assumption of the costs. In addition, the outline of the transition process in our present study differs from other larger transition programs. New transition programs in Germany like the BTP, for example, include case managers, information about treatment procedures, attendance surveillance and specialised allied-health IBD professionals. On the other hand, some transition initiatives provide an even closer and more regular support of affected young adults with IBD. For example, a biweekly transition clinic including a paediatric and adult gastroenterologist, as well as an IBD nurse is held for IBD patients by the Barts and the London National Health Service (NHS) trust [
33]. Other transition programs for IBD patients mainly aim to increase adherence to medication by utilisation of smartphone apps as a reminder for daily medication intake [
70]. Future developments in transition medicine and larger studies may confirm and clarify the specific beneficial effects of standardised structured transition support and programs.
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