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Clinical Changes of Patients with Cystic Fibrosis during Transition from Pediatric to Adult Care
Journal of Adolescent Health 43 (2008) 459 – 465
Original article
Clinical Changes of Patients with Cystic Fibrosis during Transition from Pediatric to Adult Care Ingrid Duguépéroux, Ph.D.a, Aline Tamalet, M.D.a,b, Isabelle Sermet-Gaudelus, M.D., Ph.D.c, Muriel Le Bourgeois, M.D.c, Michèle Gérardin, M.D.d, Nadine Desmazes-Dufeu, M.D.a, and Dominique Hubert, M.D.a,* b
a CRCM—service de Pneumologie, Hôpital Cochin, APHP, Paris, France CRCM—service de Pneumologie pédiatrique, Hôpital Trousseau, APHP, Paris, France c CRCM—service de Pédiatrie, Hôpital Necker, APHP, Paris, France d CRCM—service de Pédiatrie, Hôpital Robert Debré, APHP, Paris, France Manuscript received November 16, 2007; manuscript accepted March 18, 2008
Abstract
Purpose: To evaluate the clinical changes of adults with cystic fibrosis (CF) during transition from a pediatric to adult CF center. Methods: Data were collected at the time of transfer, 1 year earlier and 1 year later, for all patients in our adult CF center arriving from one of the three pediatric CF centers in Paris between January 2001 and June 2004. Results: Sixty-three of the 68 patients (transferred at a median age of 21.0 years) were regularly attending this adult CF center after 1 year and one had died. The mean number of outpatient visits increased in the year after transfer (5.7 vs. 3.8 in the year before, p ⬍ .001). The occurrence of clinical events and the rate of bronchial colonization did not change. Pseudomonas aeruginosa was found in about 60% of patients at any time. Pulmonary function declined regularly with no statistically significant difference in the rate of decline between the 2 years of follow-up (FEV1 was 54.7% predicted at transfer). Nutritional status remained stable (mean body mass index was 19.1 kg/m2). The number and duration of oral and i.v. antibiotic courses did not change, but more patients received them at home (p ⬍ .001) and self-administered physiotherapy after transfer (p ⫽ .001). The proportion of students decreased from 79.3% to 48.1% (p ⫽ .02) and the proportion in the workforce increased from 12.7% to 20.4% after transfer. Conclusions: Patients with CF remained clinically stable during transition and progressively acquired autonomy. © 2008 Society for Adolescent Medicine. All rights reserved.
Keywords:
Cystic fibrosis; Transition; Pediatric center; Adult center; Disease management
Cystic fibrosis (CF) is the most frequent serious genetic disease in Caucasian populations, with 1 in 3500 live births [1]. The prognosis has improved considerably over the past decades. Median survival age is now over 35 years in most European and North American countries, where about 40%
This study was supported by Vaincre la Mucoviscidose. *Address correspondence to: Dominique Hubert, M.D., CRCM— service de Pneumologie, Hôpital Cochin, 27 rue du Faubourg SaintJacques, 75679 Paris cedex 14, France. E-mail address: [email protected]
of patients with CF are adults [2– 4]. Life expectancy exceeding 50 years looks realistic for those born in 2000, despite no proven effective therapy to correct the basic CF defect [2]. Because of increased emphasis on physical fitness and nutrition, attention to infection control, and continuing improvements in treatment, the trend toward an aging CF population should continue. Older patients with CF finish school, join the workforce, pay taxes, marry, start families, and generally take on the problems of everyday life [5]. As increasing numbers of young people with CF are surviving into adulthood, the need for age-appropriate care
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is becoming more obvious and acute [6]. Adult physicians are more experienced in counseling patients about adult issues, including social and emotional maturation, leaving home and learning to live with others or with a partner, managing a home, and joining the workforce [7]. The major challenge of transition from pediatric to adult care has already been described for patients suffering from severe chronic diseases [8 –12], including CF [13–19]. However, no study about transition to adult care has focused on data rather than opinion or policy. This transition is defined [20] as “the purposeful, planned movement of adolescents and young adults with chronic physical and medical conditions from child-centered to adult-orientated health-care systems,” and addresses both physical and psychological factors. All studies agree that the transfer should be lengthily prepared and planned with the adolescent and his relatives, should be as gentle and smooth as possible, and should be carried out efficiently when the patient is ready. Our adult CF clinic in Paris is the oldest in France. The initially small number of CF patients attending the clinic now exceeds 300, and each year 30 to 35 are referred by their pediatricians. This study aimed to examine the clinical and psychosocial changes of young adults with CF during transition from pediatric CF care to our adult CF center, to evaluate the impact of this transfer. Methods Patients Seven CF centers in the Paris, France, area manage more than 1000 patients with CF: four are pediatric centers (Necker, Trousseau, and Robert Debré hospitals inside Paris, and André Mignot hospital in Versailles), one is a mixed pediatric and adult CF center (Créteil), and two are specifically adult CF centers (ours at Cochin hospital, Paris, and another one at Foch hospital, Suresnes). A retrospective survey was performed, including all patients arriving at our center from January 1, 2001 to June 30, 2004, from one of the three pediatric CF centers in Paris. Three dates were chosen to define the transition period from the pediatric center to the adult CF one. The date the new patient was included in our adult CF population was defined as the date of the second consecutive outpatient visit with an adult physician at our CF center (T 0). The date of the outpatient visit at the pediatric CF center occurring 12 months earlier (T ⫺12) marked the beginning of the 2-year transition period and the date of the outpatient visit at our adult CF center 12 months later (T ⫹12) marked the end, thus establishing a 2-year follow-up period. Context of transfer from pediatric to adult care In the three pediatric clinics, the decision of transfer to adult care was up to the pediatrician in charge of the patient,
usually between 17 and 20 years of age, at the end of high school. Nevertheless, transfer was avoided at time of rapid deteriorating condition and patients had to agree with the transfer procedure. Common clinical protocols were used within the pediatric and adult services, namely for antibiotic treatments, visit with the dietitian (at least once a year and at arrival at the adult unit), frequency of appointments (every 3 months and additional visits in case of pulmonary exacerbation or for severely ill patients), missed appointments (the pediatrician called the parents and the adult physician called directly the adult). Measures Data were recorded retrospectively from the patients’ files at the three pediatric centers and at our adult center. Demographic data included sex, age at CF diagnosis, age on arrival at the pediatric CF center, and age at transfer. Data were also gathered about the date of the first visit to the adult CF center, the mode of transition (visits to the pediatric center with the adult physician, presence of the pediatrician during the first visit to the adult center, outpatient visits alternated between the pediatric and adult CF centers) and the attendance of at least one parent during visits to the adult center. At T ⫹12, we evaluated the follow-up status of patients in our cohort (under follow-up at our center, dead, transferred to another center, lost to follow-up). Genotypes were classified into three categories according to the probable effect of their mutations on CFTR function [21] regardless of clinical severity. These categories include severe genotype (two severe mutations), mild genotype (at least one mild mutation), or undetermined genotype (at least one unidentified mutation and no mild mutation). Patients were classified as pancreatic sufficient (fecal elastase ⬎200 g/g or fecal fat ⬍6 g/day) or pancreatic insufficient. Sputum culture results and time of first colonization with Pseudomonas aeruginosa were recorded. Pulmonary function test results (forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) were expressed as the percentage of the predicted value [22]. Body mass index (BMI) (weight/height2) was also recorded at each step. Other collected data included common comorbidities (diabetes mellitus, glucose intolerance, liver cirrhosis, allergic bronchopulmonary aspergillosis, and pregnancy/paternity) and reasons for diagnosis. National newborn screening was introduced in France in 2002, after our patients were born. Clinical follow-up data were collected for the year before and the year after transfer. It included the number of outpatient visits and hospitalizations, the number and duration of oral and intravenous (i.v.) antibiotic courses (adminis-
I. Duguépéroux et al. / Journal of Adolescent Health 43 (2008) 459 – 465
tered at the hospital or at home). Other treatments, including physiotherapy (with a physiotherapist, alone, or with parents), inhalation therapy, oxygen treatment, pancreatic enzyme therapy, and nutritional supplementation were noted. Information about social status concerned educational (secondary school/university) or occupational activity, living conditions (single or with a partner, with or without children, living with parents versus having an independent residence), regular participation in sports and social supports. Statistical analysis Quantitative variables for each time point (T ⫺12, T 0, T ⫹12) are expressed as means with standard deviation, range and median indicated as appropriate. Student’s t-test and one-way analysis of variance (ANOVA) were used for data analysis when distribution was normal. In case of nonnormal distribution, a Mann-Whitney test was chosen. Descriptive data were considered according to occurrence of the event (yes/no) and are expressed as percentages of those for whom data were available. The chi-square test was used for comparison of these data. Longitudinal measurement was also carried out. The T ⫺12 to T 0 period was compared to the T 0 to T ⫹12 period. Significance was defined as p ⱕ .05 for all analyses. Epi Info 6.04 software was used for statistical analysis.
Results Demographic data Sixty-eight patients were included in the present study. They came from one of the three pediatric CF centers in Paris (35 from Necker [51.5%], 19 from Trousseau [27.9%], and 14 from Robert Debré [20.6%]). Approximately 100 adults with CF had arrived at our CF center between January 1, 2001 and June 30, 2004. Thirty-six of these 68 patients were women (52.9%) and 32 were men (47.1%). The mean age at diagnosis was 3.8 ⫾ 5.2 years; the mean age at first arrival at the pediatric CF center in Paris was 6.0 ⫾ 5.5 years. The median age of these patients when they arrived at Cochin hospital was 21.0 years (range 18.0 –35.0, mean 21.6 years). The mean age at transfer was similar for men and women, but was significantly different between the patients from the three pediatric centers. Patients from Necker arrived later (22.4 years old) than those from Robert Debré (21.9 years old) and Trousseau (20.2 years old) (p ⫽ .01). One year after arriving at the Cochin adult CF center, 63 patients (92.6%) were regularly attending this center. Two patients were not examined at T ⫹12, but are still under care at our center: one patient with mild disease was seen 6 months and 18 months after T 0; the second was living in Africa and had outpatient visits 6 months and 2 years after
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T0. Two patients had transferred to another adult CF center and one had died because of massive hemoptysis. Transition period The mean time interval between the first and the second consecutive outpatient visits with one adult physician at our center was 3.12 ⫾ 6.12 months (0 –24). Four women and two men (8.8% of the patients) had outpatient visits alternating between the pediatric and adult centers. In most of these cases, a first outpatient visit at the adult center was followed by a visit at the pediatric center before regular follow-up at the adult center. The first visit at the adult CF center for 22.1% of the patients (15 patients) was conducted by a pediatrician. The first visit at the adult CF center for 4.4% of the patients (three patients) was carried out jointly by a pediatrician and an adult physician. None had an outpatient visit at the pediatric center with an adult physician or had the opportunity to become familiar with the adult CF center before transfer. Half of the patients had at least one relative attending the outpatient visits at the pediatric center 12 months before transfer and at the time of transfer to the adult center. Only 19.5% had a relative coming with them 1 year later. Descriptive data Diagnosis had been suggested by positive family history (n ⫽ 2), meconium ileus (n ⫽ 7), malnutrition (n ⫽ 27), chronic diarrhea (n ⫽ 33), respiratory problems (n ⫽ 33), rectal prolapse, or nasal polyps (n ⫽ 3). Ninety percent of the patients were pancreatic insufficient. The CFTR genotype was considered severe in 52 (76.5%), mild in 13 (19.1%), and undetermined in three patients (4.4%). Thirty-six patients (52.9%) were F508del homozygous. The frequencies with which common comorbidities occurred were similar at each of the three time points: diabetes mellitus was present in 27.1% of the patients at T ⫺12, in 27.2% at T 0, and in 29.1% at T ⫹12, glucose intolerance was present in 16.4% at T ⫺12, in 16.1% at T 0, and in 21.2% at T ⫹12, liver cirrhosis in 5.1% at T ⫺12, in 6.2% Table 1 Results of sputum cultures 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12) Percentage of patients with
T ⫺12
T0
T ⫹12
MSSA MRSA H. influenzae P. aeruginosa S. maltophilia B. cepacia
50.9 1.8 11.3 60.4 3.8 0
41.3 1.6 12.7 65.0 3.2 0
48.2 5.3 7.1 58.9 5.3 0
MSSA ⫽ methicillin-sensitive Staphylococcus aureus; MRSA ⫽ methicillin-resistant Staphylococcus aureus; H. influenzae ⫽ Haemophilus influenzae; P. aeruginosa ⫽ Pseudomonas aeruginosa; S. maltophilia ⫽ Stenotrophomonas maltophilia; B. cepacia ⫽ Burkholderia cepacia.
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Table 2 Pulmonary data 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12) T ⫺12 FVC Mean Mean FEV1 Mean Mean
(% pred) decrease (% pred)
73.7
(% pred) decrease (% pred)
59.8
T ⫹12
T0 68.7 ⫺5.1
66.6 ⫺2.0
54.7 ⫺5.1
p
NS 53.6
⫺1.1
NS
at T 0, and in 7.3% at T ⫹12, allergic bronchopulmonary aspergillosis in 13.5% at T ⫺12, in 7.5% at T 0, and in 12.7% at T ⫹12. Occurrence of other clinical events (e.g., nasal polyposis, gastroesophageal reflux, sinusitis, hemoptysis, and psychological problems requiring specific followup) were recorded for at least two patients at each time point and remained constant over the study period. One patient at T ⫺12, two patients at T 0, and three patients at T ⫹12 were pregnant. No paternity was recorded. Results of sputum cultures The percentages of patients with various bacterial infections were not significantly different across the three time points (Table 1). Pseudomonas aeruginosa had been identified at least once in 52 of the 68 patients (77.6%), with a mean age at first colonization of 12.9 ⫾ 6.6 years (n ⫽ 46, range 0.0 –26.0) and a mean age at chronic colonization of 15.0 ⫾ 5.5 years (n ⫽ 39, range 2.0 –31.0). Pulmonary and anthropometrical data Fifty-three of the 68 included patients (77.9%) underwent pulmonary function tests at each of the three steps of
the study (Table 2). There was no significant difference in pulmonary function across the three time points. Forty-two of the included patients had anthropometrical measures taken at each step, showing that they had reached adult stature: mean height was 165 ⫾ 8 cm (146 –185). Mean weight varied within 1 kg (51.9 –52.9) during the entire follow-up period. Consequently, the mean BMI was stable (close to 19 kg/m2). Clinical follow-up and treatments There were significantly more outpatient visits during the year after transfer (Table 3). The proportion of patients receiving oral or i.v. antibiotic courses, the mean number of courses and the mean duration of courses during the year after transfer were not significantly different from those the year before transfer. However, more patients received their i.v. antibiotic courses at home the year after transfer. The proportion of patients receiving most other treatments did not change significantly the year after transfer, except the proportion receiving nutritional supplementation which increased. Most of the patients had physiotherapy, but the proportion of those not receiving physiotherapistdelivered care had increased 1 year after transfer. Social status The proportion of patients who were studying (high school, university) significantly decreased during the 2 years of the study (Table 4). The proportion of those working increased nonsignificantly. The proportion of those without any activity significantly increased the year after transfer. More than 80% of our patients were single, whatever the time point. The proportion of couples (with or without a child) increased nonsignificantly.
Table 3 Clinical follow-up and treatments in the year before and the year after transfer T ⫺12 Outpatient visits (No./year) Antibiotic treatments Oral antibiotic courses (% of patients) Oral antibiotic courses (days/year) IV antibiotic courses (% of patients) Number (No./year) Given at the hospital (% of patients) Given at home (% of patients) Given at the hospital and at home (% of patients) Physiotherapy (% of patients) With a physiotherapist (% of patients) Alone or with parents (% of patients) Inhalation therapy (% of patients) Inhaled bronchodilators (% of patients) Inhaled steroids (% of patients) Oxygen therapy (% of patients) Pancreatic enzymes (% of patients) Nutritional supplementation (% of patients)
85.4 69.7 72.4 76.0 30.0 24.0 11.7 92.1 25.5
T ⫹12
T0
p
3.8 [1–12]
5.7 [3–15]
⬍.001
71.4 40 83.3 2.7 ⫾ 1.3 29 42 29
68.5 37 77.6 3.0 ⫾ 2.2 24 71 5
NS NS NS NS NS ⬍.001 ⬍.001 NS NS .001 NS NS NS NS NS 0.05
89.2 67.2 58.7 65.7 45.4 25.7 13.4 89.5 35.8
96.3 66.0 88.7 66.1 49.0 29.0 12.5 91.0 48.1
I. Duguépéroux et al. / Journal of Adolescent Health 43 (2008) 459 – 465 Table 4 Social status 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12)
Activity (% of patients) Studying Having a job Without activity Single (% of patients) With a child (% of patients) Living independently of the parents (% of patients) Participate in sports (% of patients)
T ⫺12
T0
T ⫹12
p
79.3 12.7 7.9 91.8 1.6
59.1 18.2 22.7 83.1 3.1
48.1 20.4 31.5 81.5 9.3
.002 NS .005 NS NS
12.1
22.2
26.9
NS
57.1
50
53.3
NS
More and more patients lived independently of their parents. However, these changes were not significant. Approximately half the patients regularly participated in sports (including dance, football, bodybuilding, skiing, tennis, bicycling, horseback riding) at each time point. Discussion Improvement in care of patients with CF has resulted in longer survival. A larger proportion of patients now reach adulthood. These patients require an age-appropriate care and counseling about adult issues, for example, independence acquisition, career choices, and reproduction. In the last 10 years, pediatric and adolescent health professionals have emphasized the need for developmentally appropriate health care and a smooth transition from pediatric care for young adults with chronic conditions [23,24]. Our adult CF center at Cochin hospital in Paris was established 20 years ago because pediatricians realized the need to transfer young adults into an adult specialist unit. At that time, transition was not a planned process. Cooperation between the three pediatric CF centers in Paris and our adult CF center aimed to standardize transition programs, focusing on continuity of care, by adopting the same diagnostic and treatment protocols. Thus, we evaluated the clinical impact of transition from pediatric centers to our adult CF center. This is important because some families and pediatricians worry that care in adult centers leads to rapid worsening of the disease, greater treatment burden, and more bronchial infections. Moreover, patients are particularly at risk during this period of life as noncompliance with treatment is frequent. The median age of our patients at the time of transfer was 21 years, which is older than the age recommended by European consensus (16 –18 years) [23]. We found that patients from Trousseau were transferred at a younger age. This is possibly because a pediatrician from this CF pediatric center was coordinating transition and patients had the first appointment at the adult center with this physician. However, the time of transfer should be flexible, reflecting
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the adolescent’ social maturity and health status. The large range of ages highlights the need of standardization, establishing a multistep plan for transition. Physicians should introduce the concept of transition early when outlining the long-term care of CF. The mean time interval between the first two visits was 3 months, consistent with the recommended schedule for follow-up in CF centers [23,24]. Transition must include the patient, his relatives, and the caregiving teams (pediatric and adult) [12,13,16,25]. One year after transfer, most of the patients were regularly attending our adult CF center without returning to the initial pediatric center. Occurrence of CF common comorbidities during the first year at the adult center was not significantly different than that during the last year at the pediatric center. Although one severely ill patient died of massive hemoptysis in the year after transfer, there was no difference in its occurrence between the year after and the year before transfer. Bacterial colonization did not change significantly. No patient was colonized at any time with B. cepacia. Approximately half were colonized with MSSA and 60% with P. aeruginosa. These values are consistent with French CF Registry data for the year 2004 [4], and are between those for children and adults. These results underline the fact that there is no additional risk to visit an adult CF-center from the point of infection. BMI was stable and similar to that of an adult CF population [26]. As expected, pulmonary function declined regularly with no statistically significant difference in the rate of decline, although there appeared to be a more substantial decrease before transfer. These values are consistent with an annual FEV1 loss of 4.2 ⫾ 2.6% pred/year in CF adults with severe respiratory insufficiency [27]. There were a few changes in disease management after transfer. The increased proportion of patients on nutritional supplementation 1 year following transfer could be explained by more intensive approach to nutritional interventions at the time of transfer, as all patients had a visit with the dietitian at that time. Despite a similar number of i.v. antibiotic courses yearly, patients had more courses at home and fewer courses at the hospital. The management of physiotherapy also changed, with more patients doing physiotherapy alone and fewer with a physiotherapist. As almost all French CF children receive physiotherapist-delivered care, which is completely covered by a national health insurance, self-administered physiotherapy reflected a desire for more autonomy. The decrease in hospital stays with the same burden of i.v. antibiotic courses also showed the patients tried to integrate their treatments in their everyday life. Our good results might be explained by the fact that all patients who arrived at our adult center were in stable condition and had given their consent for this transfer. Moreover, we insisted on more frequent visits in the early period after transfer every time patients felt worse or were
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worried about any question concerning their CF. This was the condition to create a confident relationship between the young adults and their new caregivers. These findings are consistent with the evolution of the social situations of our patients. Many were finishing studies and entering professional life. However, a large proportion had not found jobs 1 year after transfer; thus, more patients had no occupational activity at this time. Most patients with CF find paid employment, but often later than healthy persons [28]. One study has shown that age and FEV1 did not differ between employed and unemployed U.S. patients with CF [29]. The proportion of couples (with or without children) and the number of patients with an independent residence seemed to increase slightly the year after arrival at our adult CF center, but this change was not statistically significant. Approximately half the patients regularly participated in sports at each time point examined. Our study is the first one to assess the detailed clinical status in a large sample of patients on transfer from pediatric to adult care. Many policy papers and position statements have urged careful attention to the notion of transition to adult health care, not only in CF, but also in other chronic disorders such as rheumatic disease [30], renal disease [8,31], diabetes [32], and congenital heart defects (CHD) [10]. However, no paper describes the outcomes of young people who transfer to adult services. In one study of young adults with complex CHD [10], successful transfer from pediatric to adult care was associated with more intensive pediatric care (pediatric cardiovascular surgeries, comorbid conditions, using dental antibiotic prophylaxis). It was also related to documented recommendations and beliefs that adult CHD care should be at an adult CHD center. Patients transferred to our adult CF center appeared to gain autonomy while entering adult life, without rupture in the management of their disease. Acquisition of independence in everyday life was accompanied by greater autonomy in managing illness. Most of our patients were not severely ill. Caregivers in pediatric and adult centers must also deal with other situations, for example, patients with severe respiratory insufficiency and/or awaiting lung transplantation. An organized, smooth transition system aims to minimize stress in young adults and their families in such circumstances [33]. Conclusion Clinical status and care of young adults with CF did not change after transfer from a pediatric center to our adult CF center. There was no noticeable change in bacterial pulmonary colonization and in the main treatments. Nevertheless, they acquired autonomy in everyday life and in their disease management after transfer. These findings are likely the result of good transition policies and implementation within the various CF centers referred to. In addition to trying to improve survival, pediatricians and adult physicians need to
understand better how social and emotional outcomes of their patients can improve and to support their emerging capacity for self-management from adolescence to young adult life [34]. Similar data should be obtained at the time of transfer for other chronic illnesses to evaluate its impact. Acknowledgments We thank the physicians from the pediatric CF centers in Paris, A. Clément, B. Fauroux, J. Just (Hôpital Trousseau), A. Munck (Hôpital Robert Debré), G. Lenoir, J. de Blic, M. Sorin (Hôpital Necker), and from the Cochin adult CF center (D. Dusser, R. Kanaan, P.R. Burgel, and D. Manach) for their care of the patients. References [1] Southern KW, Munck A, Pollitt RJ, et al. A survey of newborn screening for cystic fibrosis in Europe. J Cyst Fibros 2007;6:57– 65. [2] Dodge JA, Lewis PA, Stanton M, Wilsher J. Cystic fibrosis mortality and survival in the United Kingdom, 1947 to 2003. Eur Respir J 2007;29:522– 6. [3] Cystic Fibrosis Foundation. Patient Registry annual data report 2004. Bethesda, MD: Cystic Fibrosis Foundation, 2005. [4] INED, Vaincre la Mucoviscidose. Observatoire National de la Mucoviscidose. Bilan des données 2004. Paris, France: INED, 2006. [5] Davis PB. Cystic fibrosis since 1938. Am J Respir Crit Care Med 2006;173:475– 82. [6] McDonagh JE, Viner RM. Lost in transition? Between pediatric and adult Services. It’s time to improve the transition of adolescents from pediatric to adult services. Br Med J 2006;332:435– 6. [7] Madge S, Bryon M. A model for transition from pediatric to adult care in cystic fibrosis. J Pediatr Nurs 2002;17:283–5. [8] Cameron JS. The continued care of children with renal disease into adult life. Paediatr Nephrol 2001;16:680 –5. [9] Dommergues JP, Alvin P. Transition from pediatric to adult care in severe chronic diseases in children. Arch Pediatr 2003;10:295–99. [10] Reid GJ, Irvine MJ, McCrindle BW, et al. Prevalence and correlates of successful transfer from pediatric to adult health care among a cohort of young adults with complex congenital heart defects. Pediatrics 2004;113:197–205. [11] Rettig P, Athreya BH. Adolescents with chronic disease: transiton to adult health care. Arthritis Care Res 1991;4:174 – 80. [12] Sawyer SM, Blair S, Bowes G. Chronic illness in adolescents: transfer or transition to adult services? J Paediatr Child Health 1997;33: 88 –90. [13] Anderson DL, Flume PA, Hardy KK, Gray S. Transition programs in cystic fibrosis centers: perceptions of patients. Pediatr Pulmonol 2002;33:327–31. [14] Conway SP. Transition from paediatric to adult-orientated care for adolescents with cystic fibrosis. Disabil Rehabil 1998;20:209 –16. [15] Flume PA, Anderson DL, Hardy KK, Gray S. Transition programs in cystic fibrosis centers: perceptions of pediatric and adult program directors. Pediatr Pulmonol 2001;31:443–50. [16] Hubert D, Dusser D. Passage de la prise en charge pédiatrique à la prise en charge en médecine adulte. Rev Mal Respir 1999;16(S3): 130 –1. [17] Nasr SZ, Campbell C, Howatt W. Transition program from pediatric to adult care for cystic fibrosis patients. J Adolesc Health 1992;13: 682–5. [18] Wallaert B, Turck D. La mucoviscidose: transition de l’enfant à l’adulte. Rev Mal Respir 2002;19:401–3.
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Original article
Clinical Changes of Patients with Cystic Fibrosis during Transition from Pediatric to Adult Care Ingrid Duguépéroux, Ph.D.a, Aline Tamalet, M.D.a,b, Isabelle Sermet-Gaudelus, M.D., Ph.D.c, Muriel Le Bourgeois, M.D.c, Michèle Gérardin, M.D.d, Nadine Desmazes-Dufeu, M.D.a, and Dominique Hubert, M.D.a,* b
a CRCM—service de Pneumologie, Hôpital Cochin, APHP, Paris, France CRCM—service de Pneumologie pédiatrique, Hôpital Trousseau, APHP, Paris, France c CRCM—service de Pédiatrie, Hôpital Necker, APHP, Paris, France d CRCM—service de Pédiatrie, Hôpital Robert Debré, APHP, Paris, France Manuscript received November 16, 2007; manuscript accepted March 18, 2008
Abstract
Purpose: To evaluate the clinical changes of adults with cystic fibrosis (CF) during transition from a pediatric to adult CF center. Methods: Data were collected at the time of transfer, 1 year earlier and 1 year later, for all patients in our adult CF center arriving from one of the three pediatric CF centers in Paris between January 2001 and June 2004. Results: Sixty-three of the 68 patients (transferred at a median age of 21.0 years) were regularly attending this adult CF center after 1 year and one had died. The mean number of outpatient visits increased in the year after transfer (5.7 vs. 3.8 in the year before, p ⬍ .001). The occurrence of clinical events and the rate of bronchial colonization did not change. Pseudomonas aeruginosa was found in about 60% of patients at any time. Pulmonary function declined regularly with no statistically significant difference in the rate of decline between the 2 years of follow-up (FEV1 was 54.7% predicted at transfer). Nutritional status remained stable (mean body mass index was 19.1 kg/m2). The number and duration of oral and i.v. antibiotic courses did not change, but more patients received them at home (p ⬍ .001) and self-administered physiotherapy after transfer (p ⫽ .001). The proportion of students decreased from 79.3% to 48.1% (p ⫽ .02) and the proportion in the workforce increased from 12.7% to 20.4% after transfer. Conclusions: Patients with CF remained clinically stable during transition and progressively acquired autonomy. © 2008 Society for Adolescent Medicine. All rights reserved.
Keywords:
Cystic fibrosis; Transition; Pediatric center; Adult center; Disease management
Cystic fibrosis (CF) is the most frequent serious genetic disease in Caucasian populations, with 1 in 3500 live births [1]. The prognosis has improved considerably over the past decades. Median survival age is now over 35 years in most European and North American countries, where about 40%
This study was supported by Vaincre la Mucoviscidose. *Address correspondence to: Dominique Hubert, M.D., CRCM— service de Pneumologie, Hôpital Cochin, 27 rue du Faubourg SaintJacques, 75679 Paris cedex 14, France. E-mail address: [email protected]
of patients with CF are adults [2– 4]. Life expectancy exceeding 50 years looks realistic for those born in 2000, despite no proven effective therapy to correct the basic CF defect [2]. Because of increased emphasis on physical fitness and nutrition, attention to infection control, and continuing improvements in treatment, the trend toward an aging CF population should continue. Older patients with CF finish school, join the workforce, pay taxes, marry, start families, and generally take on the problems of everyday life [5]. As increasing numbers of young people with CF are surviving into adulthood, the need for age-appropriate care
1054-139X/08/$ – see front matter © 2008 Society for Adolescent Medicine. All rights reserved. doi:10.1016/j.jadohealth.2008.03.005
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is becoming more obvious and acute [6]. Adult physicians are more experienced in counseling patients about adult issues, including social and emotional maturation, leaving home and learning to live with others or with a partner, managing a home, and joining the workforce [7]. The major challenge of transition from pediatric to adult care has already been described for patients suffering from severe chronic diseases [8 –12], including CF [13–19]. However, no study about transition to adult care has focused on data rather than opinion or policy. This transition is defined [20] as “the purposeful, planned movement of adolescents and young adults with chronic physical and medical conditions from child-centered to adult-orientated health-care systems,” and addresses both physical and psychological factors. All studies agree that the transfer should be lengthily prepared and planned with the adolescent and his relatives, should be as gentle and smooth as possible, and should be carried out efficiently when the patient is ready. Our adult CF clinic in Paris is the oldest in France. The initially small number of CF patients attending the clinic now exceeds 300, and each year 30 to 35 are referred by their pediatricians. This study aimed to examine the clinical and psychosocial changes of young adults with CF during transition from pediatric CF care to our adult CF center, to evaluate the impact of this transfer. Methods Patients Seven CF centers in the Paris, France, area manage more than 1000 patients with CF: four are pediatric centers (Necker, Trousseau, and Robert Debré hospitals inside Paris, and André Mignot hospital in Versailles), one is a mixed pediatric and adult CF center (Créteil), and two are specifically adult CF centers (ours at Cochin hospital, Paris, and another one at Foch hospital, Suresnes). A retrospective survey was performed, including all patients arriving at our center from January 1, 2001 to June 30, 2004, from one of the three pediatric CF centers in Paris. Three dates were chosen to define the transition period from the pediatric center to the adult CF one. The date the new patient was included in our adult CF population was defined as the date of the second consecutive outpatient visit with an adult physician at our CF center (T 0). The date of the outpatient visit at the pediatric CF center occurring 12 months earlier (T ⫺12) marked the beginning of the 2-year transition period and the date of the outpatient visit at our adult CF center 12 months later (T ⫹12) marked the end, thus establishing a 2-year follow-up period. Context of transfer from pediatric to adult care In the three pediatric clinics, the decision of transfer to adult care was up to the pediatrician in charge of the patient,
usually between 17 and 20 years of age, at the end of high school. Nevertheless, transfer was avoided at time of rapid deteriorating condition and patients had to agree with the transfer procedure. Common clinical protocols were used within the pediatric and adult services, namely for antibiotic treatments, visit with the dietitian (at least once a year and at arrival at the adult unit), frequency of appointments (every 3 months and additional visits in case of pulmonary exacerbation or for severely ill patients), missed appointments (the pediatrician called the parents and the adult physician called directly the adult). Measures Data were recorded retrospectively from the patients’ files at the three pediatric centers and at our adult center. Demographic data included sex, age at CF diagnosis, age on arrival at the pediatric CF center, and age at transfer. Data were also gathered about the date of the first visit to the adult CF center, the mode of transition (visits to the pediatric center with the adult physician, presence of the pediatrician during the first visit to the adult center, outpatient visits alternated between the pediatric and adult CF centers) and the attendance of at least one parent during visits to the adult center. At T ⫹12, we evaluated the follow-up status of patients in our cohort (under follow-up at our center, dead, transferred to another center, lost to follow-up). Genotypes were classified into three categories according to the probable effect of their mutations on CFTR function [21] regardless of clinical severity. These categories include severe genotype (two severe mutations), mild genotype (at least one mild mutation), or undetermined genotype (at least one unidentified mutation and no mild mutation). Patients were classified as pancreatic sufficient (fecal elastase ⬎200 g/g or fecal fat ⬍6 g/day) or pancreatic insufficient. Sputum culture results and time of first colonization with Pseudomonas aeruginosa were recorded. Pulmonary function test results (forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) were expressed as the percentage of the predicted value [22]. Body mass index (BMI) (weight/height2) was also recorded at each step. Other collected data included common comorbidities (diabetes mellitus, glucose intolerance, liver cirrhosis, allergic bronchopulmonary aspergillosis, and pregnancy/paternity) and reasons for diagnosis. National newborn screening was introduced in France in 2002, after our patients were born. Clinical follow-up data were collected for the year before and the year after transfer. It included the number of outpatient visits and hospitalizations, the number and duration of oral and intravenous (i.v.) antibiotic courses (adminis-
I. Duguépéroux et al. / Journal of Adolescent Health 43 (2008) 459 – 465
tered at the hospital or at home). Other treatments, including physiotherapy (with a physiotherapist, alone, or with parents), inhalation therapy, oxygen treatment, pancreatic enzyme therapy, and nutritional supplementation were noted. Information about social status concerned educational (secondary school/university) or occupational activity, living conditions (single or with a partner, with or without children, living with parents versus having an independent residence), regular participation in sports and social supports. Statistical analysis Quantitative variables for each time point (T ⫺12, T 0, T ⫹12) are expressed as means with standard deviation, range and median indicated as appropriate. Student’s t-test and one-way analysis of variance (ANOVA) were used for data analysis when distribution was normal. In case of nonnormal distribution, a Mann-Whitney test was chosen. Descriptive data were considered according to occurrence of the event (yes/no) and are expressed as percentages of those for whom data were available. The chi-square test was used for comparison of these data. Longitudinal measurement was also carried out. The T ⫺12 to T 0 period was compared to the T 0 to T ⫹12 period. Significance was defined as p ⱕ .05 for all analyses. Epi Info 6.04 software was used for statistical analysis.
Results Demographic data Sixty-eight patients were included in the present study. They came from one of the three pediatric CF centers in Paris (35 from Necker [51.5%], 19 from Trousseau [27.9%], and 14 from Robert Debré [20.6%]). Approximately 100 adults with CF had arrived at our CF center between January 1, 2001 and June 30, 2004. Thirty-six of these 68 patients were women (52.9%) and 32 were men (47.1%). The mean age at diagnosis was 3.8 ⫾ 5.2 years; the mean age at first arrival at the pediatric CF center in Paris was 6.0 ⫾ 5.5 years. The median age of these patients when they arrived at Cochin hospital was 21.0 years (range 18.0 –35.0, mean 21.6 years). The mean age at transfer was similar for men and women, but was significantly different between the patients from the three pediatric centers. Patients from Necker arrived later (22.4 years old) than those from Robert Debré (21.9 years old) and Trousseau (20.2 years old) (p ⫽ .01). One year after arriving at the Cochin adult CF center, 63 patients (92.6%) were regularly attending this center. Two patients were not examined at T ⫹12, but are still under care at our center: one patient with mild disease was seen 6 months and 18 months after T 0; the second was living in Africa and had outpatient visits 6 months and 2 years after
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T0. Two patients had transferred to another adult CF center and one had died because of massive hemoptysis. Transition period The mean time interval between the first and the second consecutive outpatient visits with one adult physician at our center was 3.12 ⫾ 6.12 months (0 –24). Four women and two men (8.8% of the patients) had outpatient visits alternating between the pediatric and adult centers. In most of these cases, a first outpatient visit at the adult center was followed by a visit at the pediatric center before regular follow-up at the adult center. The first visit at the adult CF center for 22.1% of the patients (15 patients) was conducted by a pediatrician. The first visit at the adult CF center for 4.4% of the patients (three patients) was carried out jointly by a pediatrician and an adult physician. None had an outpatient visit at the pediatric center with an adult physician or had the opportunity to become familiar with the adult CF center before transfer. Half of the patients had at least one relative attending the outpatient visits at the pediatric center 12 months before transfer and at the time of transfer to the adult center. Only 19.5% had a relative coming with them 1 year later. Descriptive data Diagnosis had been suggested by positive family history (n ⫽ 2), meconium ileus (n ⫽ 7), malnutrition (n ⫽ 27), chronic diarrhea (n ⫽ 33), respiratory problems (n ⫽ 33), rectal prolapse, or nasal polyps (n ⫽ 3). Ninety percent of the patients were pancreatic insufficient. The CFTR genotype was considered severe in 52 (76.5%), mild in 13 (19.1%), and undetermined in three patients (4.4%). Thirty-six patients (52.9%) were F508del homozygous. The frequencies with which common comorbidities occurred were similar at each of the three time points: diabetes mellitus was present in 27.1% of the patients at T ⫺12, in 27.2% at T 0, and in 29.1% at T ⫹12, glucose intolerance was present in 16.4% at T ⫺12, in 16.1% at T 0, and in 21.2% at T ⫹12, liver cirrhosis in 5.1% at T ⫺12, in 6.2% Table 1 Results of sputum cultures 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12) Percentage of patients with
T ⫺12
T0
T ⫹12
MSSA MRSA H. influenzae P. aeruginosa S. maltophilia B. cepacia
50.9 1.8 11.3 60.4 3.8 0
41.3 1.6 12.7 65.0 3.2 0
48.2 5.3 7.1 58.9 5.3 0
MSSA ⫽ methicillin-sensitive Staphylococcus aureus; MRSA ⫽ methicillin-resistant Staphylococcus aureus; H. influenzae ⫽ Haemophilus influenzae; P. aeruginosa ⫽ Pseudomonas aeruginosa; S. maltophilia ⫽ Stenotrophomonas maltophilia; B. cepacia ⫽ Burkholderia cepacia.
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Table 2 Pulmonary data 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12) T ⫺12 FVC Mean Mean FEV1 Mean Mean
(% pred) decrease (% pred)
73.7
(% pred) decrease (% pred)
59.8
T ⫹12
T0 68.7 ⫺5.1
66.6 ⫺2.0
54.7 ⫺5.1
p
NS 53.6
⫺1.1
NS
at T 0, and in 7.3% at T ⫹12, allergic bronchopulmonary aspergillosis in 13.5% at T ⫺12, in 7.5% at T 0, and in 12.7% at T ⫹12. Occurrence of other clinical events (e.g., nasal polyposis, gastroesophageal reflux, sinusitis, hemoptysis, and psychological problems requiring specific followup) were recorded for at least two patients at each time point and remained constant over the study period. One patient at T ⫺12, two patients at T 0, and three patients at T ⫹12 were pregnant. No paternity was recorded. Results of sputum cultures The percentages of patients with various bacterial infections were not significantly different across the three time points (Table 1). Pseudomonas aeruginosa had been identified at least once in 52 of the 68 patients (77.6%), with a mean age at first colonization of 12.9 ⫾ 6.6 years (n ⫽ 46, range 0.0 –26.0) and a mean age at chronic colonization of 15.0 ⫾ 5.5 years (n ⫽ 39, range 2.0 –31.0). Pulmonary and anthropometrical data Fifty-three of the 68 included patients (77.9%) underwent pulmonary function tests at each of the three steps of
the study (Table 2). There was no significant difference in pulmonary function across the three time points. Forty-two of the included patients had anthropometrical measures taken at each step, showing that they had reached adult stature: mean height was 165 ⫾ 8 cm (146 –185). Mean weight varied within 1 kg (51.9 –52.9) during the entire follow-up period. Consequently, the mean BMI was stable (close to 19 kg/m2). Clinical follow-up and treatments There were significantly more outpatient visits during the year after transfer (Table 3). The proportion of patients receiving oral or i.v. antibiotic courses, the mean number of courses and the mean duration of courses during the year after transfer were not significantly different from those the year before transfer. However, more patients received their i.v. antibiotic courses at home the year after transfer. The proportion of patients receiving most other treatments did not change significantly the year after transfer, except the proportion receiving nutritional supplementation which increased. Most of the patients had physiotherapy, but the proportion of those not receiving physiotherapistdelivered care had increased 1 year after transfer. Social status The proportion of patients who were studying (high school, university) significantly decreased during the 2 years of the study (Table 4). The proportion of those working increased nonsignificantly. The proportion of those without any activity significantly increased the year after transfer. More than 80% of our patients were single, whatever the time point. The proportion of couples (with or without a child) increased nonsignificantly.
Table 3 Clinical follow-up and treatments in the year before and the year after transfer T ⫺12 Outpatient visits (No./year) Antibiotic treatments Oral antibiotic courses (% of patients) Oral antibiotic courses (days/year) IV antibiotic courses (% of patients) Number (No./year) Given at the hospital (% of patients) Given at home (% of patients) Given at the hospital and at home (% of patients) Physiotherapy (% of patients) With a physiotherapist (% of patients) Alone or with parents (% of patients) Inhalation therapy (% of patients) Inhaled bronchodilators (% of patients) Inhaled steroids (% of patients) Oxygen therapy (% of patients) Pancreatic enzymes (% of patients) Nutritional supplementation (% of patients)
85.4 69.7 72.4 76.0 30.0 24.0 11.7 92.1 25.5
T ⫹12
T0
p
3.8 [1–12]
5.7 [3–15]
⬍.001
71.4 40 83.3 2.7 ⫾ 1.3 29 42 29
68.5 37 77.6 3.0 ⫾ 2.2 24 71 5
NS NS NS NS NS ⬍.001 ⬍.001 NS NS .001 NS NS NS NS NS 0.05
89.2 67.2 58.7 65.7 45.4 25.7 13.4 89.5 35.8
96.3 66.0 88.7 66.1 49.0 29.0 12.5 91.0 48.1
I. Duguépéroux et al. / Journal of Adolescent Health 43 (2008) 459 – 465 Table 4 Social status 1 year before (T ⫺12), at (T 0) and 1 year after transfer (T ⫹12)
Activity (% of patients) Studying Having a job Without activity Single (% of patients) With a child (% of patients) Living independently of the parents (% of patients) Participate in sports (% of patients)
T ⫺12
T0
T ⫹12
p
79.3 12.7 7.9 91.8 1.6
59.1 18.2 22.7 83.1 3.1
48.1 20.4 31.5 81.5 9.3
.002 NS .005 NS NS
12.1
22.2
26.9
NS
57.1
50
53.3
NS
More and more patients lived independently of their parents. However, these changes were not significant. Approximately half the patients regularly participated in sports (including dance, football, bodybuilding, skiing, tennis, bicycling, horseback riding) at each time point. Discussion Improvement in care of patients with CF has resulted in longer survival. A larger proportion of patients now reach adulthood. These patients require an age-appropriate care and counseling about adult issues, for example, independence acquisition, career choices, and reproduction. In the last 10 years, pediatric and adolescent health professionals have emphasized the need for developmentally appropriate health care and a smooth transition from pediatric care for young adults with chronic conditions [23,24]. Our adult CF center at Cochin hospital in Paris was established 20 years ago because pediatricians realized the need to transfer young adults into an adult specialist unit. At that time, transition was not a planned process. Cooperation between the three pediatric CF centers in Paris and our adult CF center aimed to standardize transition programs, focusing on continuity of care, by adopting the same diagnostic and treatment protocols. Thus, we evaluated the clinical impact of transition from pediatric centers to our adult CF center. This is important because some families and pediatricians worry that care in adult centers leads to rapid worsening of the disease, greater treatment burden, and more bronchial infections. Moreover, patients are particularly at risk during this period of life as noncompliance with treatment is frequent. The median age of our patients at the time of transfer was 21 years, which is older than the age recommended by European consensus (16 –18 years) [23]. We found that patients from Trousseau were transferred at a younger age. This is possibly because a pediatrician from this CF pediatric center was coordinating transition and patients had the first appointment at the adult center with this physician. However, the time of transfer should be flexible, reflecting
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the adolescent’ social maturity and health status. The large range of ages highlights the need of standardization, establishing a multistep plan for transition. Physicians should introduce the concept of transition early when outlining the long-term care of CF. The mean time interval between the first two visits was 3 months, consistent with the recommended schedule for follow-up in CF centers [23,24]. Transition must include the patient, his relatives, and the caregiving teams (pediatric and adult) [12,13,16,25]. One year after transfer, most of the patients were regularly attending our adult CF center without returning to the initial pediatric center. Occurrence of CF common comorbidities during the first year at the adult center was not significantly different than that during the last year at the pediatric center. Although one severely ill patient died of massive hemoptysis in the year after transfer, there was no difference in its occurrence between the year after and the year before transfer. Bacterial colonization did not change significantly. No patient was colonized at any time with B. cepacia. Approximately half were colonized with MSSA and 60% with P. aeruginosa. These values are consistent with French CF Registry data for the year 2004 [4], and are between those for children and adults. These results underline the fact that there is no additional risk to visit an adult CF-center from the point of infection. BMI was stable and similar to that of an adult CF population [26]. As expected, pulmonary function declined regularly with no statistically significant difference in the rate of decline, although there appeared to be a more substantial decrease before transfer. These values are consistent with an annual FEV1 loss of 4.2 ⫾ 2.6% pred/year in CF adults with severe respiratory insufficiency [27]. There were a few changes in disease management after transfer. The increased proportion of patients on nutritional supplementation 1 year following transfer could be explained by more intensive approach to nutritional interventions at the time of transfer, as all patients had a visit with the dietitian at that time. Despite a similar number of i.v. antibiotic courses yearly, patients had more courses at home and fewer courses at the hospital. The management of physiotherapy also changed, with more patients doing physiotherapy alone and fewer with a physiotherapist. As almost all French CF children receive physiotherapist-delivered care, which is completely covered by a national health insurance, self-administered physiotherapy reflected a desire for more autonomy. The decrease in hospital stays with the same burden of i.v. antibiotic courses also showed the patients tried to integrate their treatments in their everyday life. Our good results might be explained by the fact that all patients who arrived at our adult center were in stable condition and had given their consent for this transfer. Moreover, we insisted on more frequent visits in the early period after transfer every time patients felt worse or were
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worried about any question concerning their CF. This was the condition to create a confident relationship between the young adults and their new caregivers. These findings are consistent with the evolution of the social situations of our patients. Many were finishing studies and entering professional life. However, a large proportion had not found jobs 1 year after transfer; thus, more patients had no occupational activity at this time. Most patients with CF find paid employment, but often later than healthy persons [28]. One study has shown that age and FEV1 did not differ between employed and unemployed U.S. patients with CF [29]. The proportion of couples (with or without children) and the number of patients with an independent residence seemed to increase slightly the year after arrival at our adult CF center, but this change was not statistically significant. Approximately half the patients regularly participated in sports at each time point examined. Our study is the first one to assess the detailed clinical status in a large sample of patients on transfer from pediatric to adult care. Many policy papers and position statements have urged careful attention to the notion of transition to adult health care, not only in CF, but also in other chronic disorders such as rheumatic disease [30], renal disease [8,31], diabetes [32], and congenital heart defects (CHD) [10]. However, no paper describes the outcomes of young people who transfer to adult services. In one study of young adults with complex CHD [10], successful transfer from pediatric to adult care was associated with more intensive pediatric care (pediatric cardiovascular surgeries, comorbid conditions, using dental antibiotic prophylaxis). It was also related to documented recommendations and beliefs that adult CHD care should be at an adult CHD center. Patients transferred to our adult CF center appeared to gain autonomy while entering adult life, without rupture in the management of their disease. Acquisition of independence in everyday life was accompanied by greater autonomy in managing illness. Most of our patients were not severely ill. Caregivers in pediatric and adult centers must also deal with other situations, for example, patients with severe respiratory insufficiency and/or awaiting lung transplantation. An organized, smooth transition system aims to minimize stress in young adults and their families in such circumstances [33]. Conclusion Clinical status and care of young adults with CF did not change after transfer from a pediatric center to our adult CF center. There was no noticeable change in bacterial pulmonary colonization and in the main treatments. Nevertheless, they acquired autonomy in everyday life and in their disease management after transfer. These findings are likely the result of good transition policies and implementation within the various CF centers referred to. In addition to trying to improve survival, pediatricians and adult physicians need to
understand better how social and emotional outcomes of their patients can improve and to support their emerging capacity for self-management from adolescence to young adult life [34]. Similar data should be obtained at the time of transfer for other chronic illnesses to evaluate its impact. Acknowledgments We thank the physicians from the pediatric CF centers in Paris, A. Clément, B. Fauroux, J. Just (Hôpital Trousseau), A. Munck (Hôpital Robert Debré), G. Lenoir, J. de Blic, M. Sorin (Hôpital Necker), and from the Cochin adult CF center (D. Dusser, R. Kanaan, P.R. Burgel, and D. Manach) for their care of the patients. References [1] Southern KW, Munck A, Pollitt RJ, et al. A survey of newborn screening for cystic fibrosis in Europe. J Cyst Fibros 2007;6:57– 65. [2] Dodge JA, Lewis PA, Stanton M, Wilsher J. Cystic fibrosis mortality and survival in the United Kingdom, 1947 to 2003. Eur Respir J 2007;29:522– 6. [3] Cystic Fibrosis Foundation. Patient Registry annual data report 2004. Bethesda, MD: Cystic Fibrosis Foundation, 2005. [4] INED, Vaincre la Mucoviscidose. Observatoire National de la Mucoviscidose. Bilan des données 2004. Paris, France: INED, 2006. [5] Davis PB. Cystic fibrosis since 1938. Am J Respir Crit Care Med 2006;173:475– 82. [6] McDonagh JE, Viner RM. Lost in transition? Between pediatric and adult Services. It’s time to improve the transition of adolescents from pediatric to adult services. Br Med J 2006;332:435– 6. [7] Madge S, Bryon M. A model for transition from pediatric to adult care in cystic fibrosis. J Pediatr Nurs 2002;17:283–5. [8] Cameron JS. The continued care of children with renal disease into adult life. Paediatr Nephrol 2001;16:680 –5. [9] Dommergues JP, Alvin P. Transition from pediatric to adult care in severe chronic diseases in children. Arch Pediatr 2003;10:295–99. [10] Reid GJ, Irvine MJ, McCrindle BW, et al. Prevalence and correlates of successful transfer from pediatric to adult health care among a cohort of young adults with complex congenital heart defects. Pediatrics 2004;113:197–205. [11] Rettig P, Athreya BH. Adolescents with chronic disease: transiton to adult health care. Arthritis Care Res 1991;4:174 – 80. [12] Sawyer SM, Blair S, Bowes G. Chronic illness in adolescents: transfer or transition to adult services? J Paediatr Child Health 1997;33: 88 –90. [13] Anderson DL, Flume PA, Hardy KK, Gray S. Transition programs in cystic fibrosis centers: perceptions of patients. Pediatr Pulmonol 2002;33:327–31. [14] Conway SP. Transition from paediatric to adult-orientated care for adolescents with cystic fibrosis. Disabil Rehabil 1998;20:209 –16. [15] Flume PA, Anderson DL, Hardy KK, Gray S. Transition programs in cystic fibrosis centers: perceptions of pediatric and adult program directors. Pediatr Pulmonol 2001;31:443–50. [16] Hubert D, Dusser D. Passage de la prise en charge pédiatrique à la prise en charge en médecine adulte. Rev Mal Respir 1999;16(S3): 130 –1. [17] Nasr SZ, Campbell C, Howatt W. Transition program from pediatric to adult care for cystic fibrosis patients. J Adolesc Health 1992;13: 682–5. [18] Wallaert B, Turck D. La mucoviscidose: transition de l’enfant à l’adulte. Rev Mal Respir 2002;19:401–3.
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