Pediatr Blood Cancer 2014;61:697–701
Identification of Risk Factors for an Unsuccessful Transition from Pediatric to Adult Sickle Cell Disease Care Biree Andemariam, MD,1* Jasmine Owarish-Gross, BA,1 James Grady, DrPH,2 Donna Boruchov, Roger S. Thrall, PhD,4 and J. Nathan Hagstrom, MD3 Background. A successful transition from pediatric to adult sickle cell disease (SCD) care is paramount to continued improvements in survival. In order to enhance transition success, our pediatric SCD transition process was modified to include combined adult and pediatric provider clinics that incorporated participation by our local SCD community-based organization. All children ages 16 and over participated in this newly-formed transition program. Procedure. After 5 years of implementation of the modified SCD transition program, we retrospectively studied clinical and non-clinical risk factors for an unsuccessful transition. Risk factor categories studied included patient demographics, transition clinic attendance, and disease severity. Results. Thirty-two percent of patients did not transition successfully. Demographic factors such as gender, race,
3 MD,
and type of insurance did not influence transition outcome, although travel distance to the adult SCD center was an identifiable risk factor for an unsuccessful transition. While transition clinic attendance rate did not affect transition outcomes, older age at first modified combined transition clinic visit was a significant risk factor for lack of transition. Patients with clinical markers of milder disease severity (SC and Sbþ genotypes and no chronic transfusion therapy) were at higher risk for an unsuccessful transition than patients with severe disease. Conclusions. We have identified several risk factors for lack of transition success which will allow us to modify our transition efforts going forward to capture this highest risk subset. Pediatr Blood Cancer 2014;61:697–701. # 2013 Wiley Periodicals, Inc.
Key words: sickle cell disease; transition
INTRODUCTION Until the 1970s, only 50% of children with sickle cell disease (SCD) lived until adulthood [1]. Now, more than 90% of children with SCD live beyond the age of 21 years [2]. This improvement in survival is primarily due to enhanced pediatric care that includes early identification of disease via newborn screening. The diagnosis of SCD at birth has, in turn, allowed for the institution of early penicillin prophylaxis against potentially deadly pneumococcal sepsis and routine screening for stroke risk. With near-universal expectation that a child born with SCD today will live into adulthood, a defined transition program that assists these patients with transitioning from pediatric to adult care is critical [3]. This notion is supported by key findings of a recent study of the Dallas Newborn Cohort (DNC) which showed that SCD patients are at the greatest risk for mortality when they are transition-aged. The DNC study identified that seven of the most recent deaths in the cohort were age 18 years or older, and six of these patients had recently transitioned out of pediatric care [2]. Most of these patients died from SCD-related complications such as acute chest syndrome, stroke, and organ failure. This suggests that it is important for patients who transition out of pediatric SCD care to do so successfully in order to maximize the prospects of continued survival. Recognizing this, a formal combined transition program between our region’s existing pediatric SCD center at Connecticut Children’s Medical Center (CCMC) and the newly-forming adult SCD center at the University of Connecticut Health Center (UCHC) was established in 2007 in connection with a Connecticut Department of Public Health grant. After 5 years of implementation, we sought to evaluate the successes and failures of a new transition program. Existing research on the process of transitioning in SCD has primarily focused on evaluating the transition process and programmatic structure. These studies have included questionnaire-based evaluations in order to gather the opinions of patients and their caregivers about their expectations of, and concerns about, C
2013 Wiley Periodicals, Inc. DOI 10.1002/pbc.24870 Published online 18 December 2013 in Wiley Online Library (wileyonlinelibrary.com).
the transition process [4,5]. Additionally, other studies have evaluated the transition process by surveying pediatric and adult care providers [6–8]. By contrast, our study seeks to identify potential demographic and clinical factors associated with an unsuccessful transition, or one that does not result in the establishment of care at the adult SCD center. As such, determining risk factors for an unsuccessful transition may, in turn, allow us to modify our existing transition program to insure improved success going forward.
METHODS Implementation of Combined SCD Transition Program Prior to implementation of the combined CCMC/UCHC SCD transition program, the pediatric SCD program at CCMC had been guiding adolescent and young adult patients through the transition process beginning during late adolescence around age 15 or 16 and continuing until the mid-twenties, around age 24. The transition 1
Adult Sickle Cell Center, Division of Hematology-Oncology, University of Connecticut Health Center, Farmington, Connecticut; 2 Department of Community Health and Health Care, University of Connecticut Health Center, Farmington, Connecticut; 3Department of Pediatrics, Connecticut Children’s Medical Center, Hartford, Connecticut; 4Department of Research, Hospital for Special Care, New Britain, Connecticut Grant sponsor: Connecticut Institute for Clinical and Translational Science (CICATS); Grant sponsor: The State of Connecticut Department of Public Health Conflict of interest: Nothing to report.
Correspondence to: Biree Andemariam, Assistant Professor of Medicine, Director, Adult Sickle Cell Center, Division of HematologyOncology, University of Connecticut Health Center, 263 Farmington Avenue, MC 1628, Farmington, CT 06030. E-mail: [email protected] Received 7 June 2013; Accepted 31 October 2013
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period was defined as having three phases: preparatory, transitional, and completion. The preparatory phase was primarily focused on patient education regarding SCD and patient-specific health issues and management. The transitional phase was focused on empowering the individual patient to navigate the health care system in the context of increasing responsibility. The completion phase was focused on establishing effective patterns of health care in the adult setting. The preparatory phase was conducted over a period of 6–10 visits done every 4–6 months over a 3-year period. The transitional phase included at least four family meetings with pediatric health care staff (including social work, nursing, and medical staff) to review health summaries, problem lists, and treatment plans. Patients were discharged from the pediatric practice by age 21 and given a referral to one of the many adult hematology physicians in the community for continued SCD care. At this point, the patient entered the completion phase which consisted of supporting the patient after transition with extra social and care coordination support on an ad hoc basis primarily as initiated by the individual patient when the need arose. At the time the combined transition program was formalized in 2007, there were 47 SCD patients receiving care at CCMC who were age 16 or older and were therefore identified as appropriate for participation in the modified transition process. These patients were in various stages of the transition period. The three-phase approach already in place was continued. However, the preparatory and transition phases were changed such that both began at age 16. The transitional and completion phases were then jointly carried out by the adult and pediatric teams and involved a monthly combined transition clinic held at the pediatric center (10 miles away from UCHC) and attended by the individual patients, family members, a representative from the local SCD community-based organization (CBO), and both adult and pediatric health care personnel, including social work, nursing, and medical staff. Each patient was expected to attend at least four of the combined transition clinics over several years until finally transferring his/her care to the UCHC adult SCD center at the age of 21. During the combined transition clinics, each patient was further educated about his/her disease and had the opportunity to meet face-to-face with both the pediatric and adult care provider teams. A patient navigator/advocate from the region’s SCD CBO (Citizens for Quality Sickle Cell Care, Inc.) was present for all combined transition clinics. Patients were informed about the resources available to them both at UCHC’s adult SCD center and in the community. Patients were able to ask questions and express any concerns about transitioning. Moreover, patients were invited to make an appointment for a tour of the adult SCD center which was given by the CBO patient navigator/advocate. During the tour, patients were able to ask questions, have their concerns addressed, and express any anxiety surrounding leaving their pediatric care-givers. As a patient approached his/her 21st birthday, he/she attended a final combined transition clinic. At that time, a brochure from the UCHC adult SCD program was given to the patient containing the phone number and address of the center. The patient was advised to make an appointment for transfer of care. If the patient was on chronic transfusion therapy, he/she was given (verbally or in writing) an appointment for his/her next transfusion at the adult center. Patients signed a consent form allowing medical records to be sent to the adult SCD program in advance of their first appointment. Pediatr Blood Cancer DOI 10.1002/pbc
Ideally, patients scheduled their first visit to the adult SCD center prior to reaching their 21st birthday, and prior to their last appointment at the pediatric SCD clinic. Each patient received a call from the adult SCD nurse as a reminder of the appointment and detailed directions to the clinic were provided. Patients who did not show for their appointment were called by the adult SCD nurse. Boundaries to accessing care were explored and then addressed by both the adult and pediatric teams. The patient’s appointment was then rescheduled during that conversation. The status of all patients who were to have transferred care to the adult SCD center were reviewed by the adult and pediatric provider teams at the beginning of each monthly combined transition clinic. Patients who had not yet made or kept an appointment at the adult SCD center were contacted by the pediatric SCD nurse and/or social worker to assess for roadblocks and to encourage timely establishment of care. If, after 1 year, the patient had not transferred care to the adult SCD center, a certified letter was sent from the pediatric SCD program to the patient formally advising them to contact the pediatric SCD program for assistance.
Retrospective Chart Review After obtaining approval from the Institutional Review Boards at CCMC and UCHC, we conducted a retrospective chart review of all patients age 16 and older with SCD from 2007 to 2012. Charts were reviewed for demographic factors (gender, age, race/ethnicity, insurance type, and location of residence), clinical information (genotype, 3-year admission history for vaso-occlusive crisis or acute chest syndrome episodes, and whether or not they were on hydroxyurea or a chronic transfusion therapy program), and transition clinic attendance. Patients were categorized as either having a successful or unsuccessful transition. Successful transition was defined as attendance of at least one outpatient visit at the UCHC adult SCD center after being discharged from the CCMC pediatric SCD program.
Statistical Analysis Statistical methods used for data analysis included chi-square tests for assessing association among categorical variables (e.g., transitioned (Y or N) vs. gender) and two-group t-tests for comparing group means (e.g., distance from home to the adult sickle cell center, by transitioned, Yor N). When the assumptions of the chi-square were not met, we reported Fisher’s Exact Test. All analyses were performed using SAS1 statistical software (SAS Institute, Inc., Cary, NC).
RESULTS Transition Population Characteristics Forty-seven pediatric SCD patients between the ages of 16 and 24 years began the modified transition process between the years 2007 and 2012. Tables I and II outline the patient characteristics including demographics, clinical factors, and transition clinic attendance. Fifty-seven percent of the patients were female. Although 87% of patients were Black, there was representation from other racial groups as well. Fifty-eight percent of the patients had private insurance. The remainder of the patients had insurance coverage through the Connecticut state Medicaid program. There was an expected distribution of hemoglobin
Risk Factors for Unsuccessful Sickle Cell Transition TABLE I. Demographic Data of All Transition-Aged Patients
Gender Male Female Race Black Hispanic White Indian Insurancea Private Medicaid Age at the start of transition (years) 16–18 19–20 21 and older Distance from home to adult center (miles)a 0–5 6–10 11–15 16–20 21–25 26–30 Average transition clinic attendance Attended 50% Clinics Attended >50% Clinics
n
%
20 27
43 57
41 4 1 1
87 9 2 2
25 18
58 42
18 21 8
38 45 17
5 14 4 11 8 1
12 33 9 26 19 2
21 26
45 55
a All data in this table reflect demographic data which were obtained from the charts of all 47 children who underwent the transition process during the study period. However, insurance and distance information was only available for 43 patients, as indicated.
genotypes (62% SS or Sb0, 38% Sbþ or SC). All patients lived within 30 miles of the adult sickle cell center. At the time of their last routine pediatric SCD clinic visit, 62% of patients were on a chronic transfusion therapy program and less than 10% of patients were taking hydroxyurea. When examining hospitalization records over the 3 years prior to their final pediatric SCD clinic visit, 77% of patients had four or less vaso-occlusive crisis admissions and 76% of patients had not experienced an episode of acute chest syndrome. While nearly 40% of patients attended their first modified transition clinic by the age of 18, a majority of patients were already age 19 or older. In fact, 17% of patients were already at least 21 years old at the start of the modified transition program and had to undergo a rapid process of transition to the adult SCD center.
Risk Factors for an Unsuccessful Transition Out of the 47 patients planned for transition from the pediatric to the adult SCD center from 2007 to 2012, 68% successfully transitioned. Of note, all patients who met this definition also established continual, ongoing, comprehensive care. The remaining 32% of patients who did not successfully transition have not, to our knowledge, established longitudinal hematology care elsewhere. As indicated in Table III, transition success was not influenced by gender as 63% of female patients and 75% of male patients transitioned successfully (P ¼ 0.38). Race was also not associated with transition outcome (P ¼ 0.67). There was no statistically significant difference in type of insurance amongst those that Pediatr Blood Cancer DOI 10.1002/pbc
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TABLE II. Clinical Data of All Transition-Aged Patients n Genotype SS 26 SC 9 S bþ 9 3 S b0 Chronic transfusion therapy Yes 14 No 33 Hydroxyurea utilization Yes 4 No 43 ACS episodesa,b 0 35 1 5 2þ 6 VOC episodes requiring hospitalizationb,c 0 20 1–4 15 5–7 6 15þ 4
% 55 19 19 6 30 70 9 91 76 11 13 44 33 13 8
a
All data in this table reflect demographic data obtained from the medical charts of all 47 children who underwent the transition process during the study period. However, information regarding Acute Chest Syndrome (ACS) episodes was only available for 46 patients. bACS episodes and vaso-occlusive crisis (VOC) episodes were totaled over a 3-year period prior to last pediatric hematology visit. cInformation regarding VOC episodes requiring hospitalization was only available for 45 patients.
transitioned (53% private vs. 47% Medicaid) compared to those that did not successfully transition (69% private versus 31% Medicaid) (P ¼ 0.33). Mean combined transition clinic attendance rate and mean number of scheduled transition clinic visits was not associated with transition success (both P > 0.25). Those that transitioned had higher mean combined transition clinic visits attended, but the difference was not statistically significant (2.1 vs. 1.5, P ¼ 0.07). Both clinical and non-clinical factors significantly influenced transition success outcomes. SC or Sbþ genotype and a lack of a need for chronic transfusions were significantly higher in the unsuccessfully transitioned group of patients. Specifically, 21% of SC/Sbþ patients did not transition successfully compared to only 21% of SS/Sb0 patients (P ¼ 0.04). Of those patients who did not successfully transition, 93% were not on a chronic transfusion therapy program, a significantly higher rate than the 59% who did transition (P ¼ 0.02). There was no significant difference in utilization of hydroxyurea among the successfully and unsuccessfully transitioned patients (12.5% vs. 0%, P ¼ 0.29). The frequency of acute chest syndrome episodes was also not different between the two groups of patients with approximately 90% in each group having at most one episode (P ¼ 0.99). Vaso-occlusive crisis episode hospitalization frequency was similar between the two groups with 73% of transitioned and 87% of non-transitioned patients experiencing four or fewer admission for VOC over a 3-year period (P ¼ 0.13). Later age at the start of the modified transition process also negatively influenced transition success. Only 25% of patients who
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TABLE III. Transition Outcomes Transitioned Yes n (%)
No n (%)
Demograhics Gender Female 17 (63) 10 Male 15 (75) 5 Race Black 28 (68) 13 Hispanic 3 (75) 1 White 1 (100) 0 Indian 0 (0) 1 Insurancea Private 16 (64) 9 Medicaid 14 (78) 4 Age at the start of transition 20 3 (33) 6 Clinical factors Genotype 9 (50) 9 SC or Sbþ SS or Sb0 23 (79) 6 Chronic transfusion therapy Yes 13 (93) 1 No 19 (58) 14 Hydroxyurea utilization Yes 4 (13) 0 No 28 (87) 15 ACS episodes 0 23 (74) 12 1 4 (13) 1 2þ 4 (13) 2 VOC episodes requiring hospitalization 0 10 (34) 10 1–4 12 (40) 3 5–7 4 (13) 2 15þ 4 (13) 0 Transition clinic attendance Average transition clinic attendance 50% Clinics 14 (67) 7 >50% Clinics 18 (69) 8 Total transition clinic attendanceb Attended 2.2 (1.22) 1.5 Scheduled 3.5 (2.21) 2.7
P value
(37) (25)
0.38
(32) (25) (0) (100)
0.67
(36) (22)
0.33
(23) (65)
0.008
(21) (67)
0.01
(50) (21)
0.04
(7) (42)
0.02
(0) (100)
0.29
(80) (7) (13)
0.99
(67) (20) (13) (0)
0.13
(33) (31)
0.851
(1.13) (2.02)
0.07 0.24
a
Insurance information was only available for 43 patients. bTotal transition clinic attendance is expressed as a mean (SD).
began the modified combined transition process at the age of 21 or older successfully transitioned, whereas 77% of patients who began before age 21 did so successfully (P ¼ 0.008). Distance from home to the adult SCD center also influenced transition outcomes as those patients who lived more than 20 miles away were less likely to transition than those who lived closer (33% vs. 79%, P ¼ 0.01).
DISCUSSION A successful transition from pediatric to adult specialty care in SCD is critical to prolonged survival. Others have identified Pediatr Blood Cancer DOI 10.1002/pbc
that a lack of adult hematology providers with expertise or interest in SCD has been a major roadblock in successful transition [9]. In our region, we are fortunate that this leading cause of unsuccessful transition nationally is no longer a factor. Fortunately, the elimination of this most prevalent barrier to continued care has allowed us to examine other risk factors for an unsuccessful transition. It is our intention that the findings from this study will guide modification of our existing transition program to insure enhanced attention to the subset of pediatric SCD patients at highest risk for not transitioning and therefore at potentially higher risk for increased morbidity and mortality. The findings of our study demonstrate that both clinical and nonclinical factors are associated with transition success. Non-clinical factors that were identified as risk factors for unsuccessful transitioning were greater travel distance from the patient’s home to the adult SCD center and older age at the time of initiation of the transition process. The significance of geography factors was not surprising and suggests that the SCD centers and patients’ insurers need to address ways to enhance access to care from a transportation standpoint. As a result of our study, our adult SCD center’s social worker now specifically discusses transportation with each patient during the combined transition clinic. If distance is identified as a potential roadblock to getting to the adult SCD center, eligibility for transport assistance will be evaluated and family/community resources for transportation will be explored. The finding that older age at the time of initiation of the modified transition process was associated with poor transition success was also not surprising. We do not anticipate this to be able to influence transition success. Combined transition will be initiated in a timely fashion at the age of 16. Given the sustained and permanent nature of our newly-established program, we should no longer have pediatric patients over age 16 waiting to initiate the transitional phase or over age 21 searching for an adult SCD provider to whom they can transition their care. What was indeed surprising was the lack of an adverse relationship between insurance type and transition success. We had hypothesized that patients with private insurance would be more likely to complete the transition process, however, transition success was not influenced by insurance type. We speculate that this can be explained, in part, by the fact that Medicaid in the state of Connecticut provides medical cab transportation to scheduled provider visits for its insured. This may have allowed for the negative influence of travel distance to have been overcome in this subset of patients. We evaluated clinical factors that are known markers of disease severity: hemoglobin genotype, the need for hydroxyurea or chronic transfusion therapy (CTT), the frequency of acute chest syndrome (ACS) episodes, and hospitalization rates for vasoocclusive crisis (VOC). Hydroxyurea utilization was not predictive of transition success. However, there were very few total patients on hydroxyurea making the lack of an association in this study difficult to generalize. Hospitalization rates for VOC or ACS were not associated with transition success. This is concerning, particularly if the frequency in VOC or ACS episodes has continued in the unsuccessfully transitioned group. Without an identified adult SCD provider, it is likely that these patients are receiving care primarily in emergency departments rather than coordinated multi-disciplinary care by a team of experts.
Risk Factors for Unsuccessful Sickle Cell Transition We had indeed hypothesized that children on CTT would be more likely to transition to the adult SCD center successfully due to the need to continue regular transfusions in a timely manner. The question is why. We now recognize that perhaps the enhanced effort at scheduling initial appointments at the adult SCD center for patients on CTT may be a contributing factor. This includes a more concerted effort and communication amongst the pediatric and adult SCD nurses to insure timely scheduling of the next transfusion. Additionally, calls to remind patients of these transfusion appointments are made over and above the reminder calls for the outpatient clinic visit. Whether the increased effort on the part of the adult SCD staff to insure patients on CTT are scheduled for transfusion is the sole reason for improved transition success in this group is not entirely clear. It is possible that patients who are on CTT perceive themselves as more sick or that the rationale for maintaining a SCD provider relationship is more implicit than for patients who do not get regular transfusions as part of their disease management. Supporting this notion is our finding that patients with genotypes SC and Sbþ were at highest risk for not transitioning. SCD patients with these genotypes are generally perceived by healthcare providers to have less severe disease. It is plausible that these patients receive less reinforcement or education about the potential severity of their disease. This suggests that we need to engage our patients in the comprehensive well visit process more so they perceive and experience tangible benefit from coming to visits even when feeling well. We also must pay special emphasis on educating our patients with SC and Sbþ disease about the risks of SCD even in the face of what may have been a relatively smooth pediatric clinical course. Although not directly studied, we believe that the development of combined adult/pediatric transition clinics enhanced our transition process and contributed to its successes. Additionally, the incorporation of the SCD CBO as an active participant in the role of patient navigator likely improved the comfort and trust levels of the patients and their families as they moved into a new care environment. We did not develop specific measures to evaluate the impact of the presence of adult SCD providers or the CBO, therefore data on their involvement is not available. However, we do plan to specifically measure the potential impact going forward. For example, was transition success influenced by direct patient interaction with our adult SCD providers and CBO, by patients touring the adult facility with the CBO navigator, or by the presence of the CBO navigator in the adult SCD clinic? These are important questions and, if studied with appropriate measures, could be the basis for further research that may give insights to other transition programs about unique ways to incorporate CBOs and adult SCD providers in the transitioning process. It is important to note that there are potential limitations to our study, including ones that may affect its generalizability. The retrospective nature of this review of our clinical program’s
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effectiveness without a comparison group may allow for confounding variables making us falsely conclude that having a program such as ours makes a difference when in fact it does not. Additionally, the study results are based on analysis of a relatively small cohort of patients attending a uniquely designed combined specialty clinic that incorporates a CBO in the role of patient navigator/advocate. However, the general methods and practices are portable to other practices and areas of the country where potential partnerships between adult and pediatric hematology providers could be fostered, many of which share the same campus or hospital (unlike our programs). We have no reason to believe that our population of patients differs significantly from other populations. However, our patients may be more spread out geographically than populations from more concentrated metropolitan areas. Additionally, our adult program is situated in a suburban location, which is not typical for sickle cell centers. In conclusion, we have elucidated easily identifiable risk factors for failure to transition successfully. Enhanced and early education of all pediatric SCD patients regarding the need to continue comprehensive care in the adult setting is imperative, particularly among those patients who may perceive their SCD to not be as serious as it is for others. Additionally, similar diligence in assisting transitioned patients on CTT with scheduling the first adult SCD provider appointment should be employed uniformly with all patients regardless of their CTT status. Our study has provided important insights into how we can further modify of our transition efforts to insure that no young adults with SCD get lost in the process.
ACKNOWLEDGMENTS This work was supported by grants from the Connecticut Institute for Clinical and Translational Science (CICATS) Clinical and Translational Scholars K12 Award (B.A.), and the State of Connecticut Department of Public Health (B.A., J.O-G, D.B., J.N.H., R.S.T).
REFERENCES 1. Scott RB. Health care priority sickle cell anemia. JAMA 1970;214:731–734. 2. Quinn CT, Rogers ZR, McCavit TL, et al. Improved survival of children and adolescents with sickle cell disease. Blood 2010;115:3447–3452. 3. Wojciechowski EA, Hurtig A, Dorn L. A natural history and study of adolescents and young adults with sickle cell disease as they transfer to adult care: A need for case management services. J Pediatr Nurs 2002;17:18–27. 4. McPherson M, Thaniel L, Minniti CP. Transition of patients with sickle cell disease from pediatric to adult care: Assessing patient readiness. Pediatr Blood Cancer 2009;52:838–841. 5. Telfair J, Myers J, Drezner S. Transfer as a component of the transition of adolescents with sickle cell disease to adult care: Adolescent, adult, and parent perspectives. J Adolesc Health 1994;15:558–565. 6. Por J, Goldberg B, Lennox V, et al. Transition of care: Health care professionals view. J Nurs Manag 2004;12:354–361. 7. Scal P. Transition for youth with chronic conditions: Primary care physicians’ approaches. Pediatrics 2002;110:1315–1321. 8. Telfair J, Alexander L, Loosier P, et al. Providers’ perspective and beliefs regarding transition to adult care for adolescent with sickle cell disease. J Health Care Poor Underserved 2004;15:443–461. 9. Sobota A, Neufeld EJ, Sprinz P, et al. Transition from pediatric to adult care for sickle cell disease: Results of a survey of pediatric providers. Am J Hematol 2011;86:512–515.
Identification of Risk Factors for an Unsuccessful Transition from Pediatric to Adult Sickle Cell Disease Care Biree Andemariam, MD,1* Jasmine Owarish-Gross, BA,1 James Grady, DrPH,2 Donna Boruchov, Roger S. Thrall, PhD,4 and J. Nathan Hagstrom, MD3 Background. A successful transition from pediatric to adult sickle cell disease (SCD) care is paramount to continued improvements in survival. In order to enhance transition success, our pediatric SCD transition process was modified to include combined adult and pediatric provider clinics that incorporated participation by our local SCD community-based organization. All children ages 16 and over participated in this newly-formed transition program. Procedure. After 5 years of implementation of the modified SCD transition program, we retrospectively studied clinical and non-clinical risk factors for an unsuccessful transition. Risk factor categories studied included patient demographics, transition clinic attendance, and disease severity. Results. Thirty-two percent of patients did not transition successfully. Demographic factors such as gender, race,
3 MD,
and type of insurance did not influence transition outcome, although travel distance to the adult SCD center was an identifiable risk factor for an unsuccessful transition. While transition clinic attendance rate did not affect transition outcomes, older age at first modified combined transition clinic visit was a significant risk factor for lack of transition. Patients with clinical markers of milder disease severity (SC and Sbþ genotypes and no chronic transfusion therapy) were at higher risk for an unsuccessful transition than patients with severe disease. Conclusions. We have identified several risk factors for lack of transition success which will allow us to modify our transition efforts going forward to capture this highest risk subset. Pediatr Blood Cancer 2014;61:697–701. # 2013 Wiley Periodicals, Inc.
Key words: sickle cell disease; transition
INTRODUCTION Until the 1970s, only 50% of children with sickle cell disease (SCD) lived until adulthood [1]. Now, more than 90% of children with SCD live beyond the age of 21 years [2]. This improvement in survival is primarily due to enhanced pediatric care that includes early identification of disease via newborn screening. The diagnosis of SCD at birth has, in turn, allowed for the institution of early penicillin prophylaxis against potentially deadly pneumococcal sepsis and routine screening for stroke risk. With near-universal expectation that a child born with SCD today will live into adulthood, a defined transition program that assists these patients with transitioning from pediatric to adult care is critical [3]. This notion is supported by key findings of a recent study of the Dallas Newborn Cohort (DNC) which showed that SCD patients are at the greatest risk for mortality when they are transition-aged. The DNC study identified that seven of the most recent deaths in the cohort were age 18 years or older, and six of these patients had recently transitioned out of pediatric care [2]. Most of these patients died from SCD-related complications such as acute chest syndrome, stroke, and organ failure. This suggests that it is important for patients who transition out of pediatric SCD care to do so successfully in order to maximize the prospects of continued survival. Recognizing this, a formal combined transition program between our region’s existing pediatric SCD center at Connecticut Children’s Medical Center (CCMC) and the newly-forming adult SCD center at the University of Connecticut Health Center (UCHC) was established in 2007 in connection with a Connecticut Department of Public Health grant. After 5 years of implementation, we sought to evaluate the successes and failures of a new transition program. Existing research on the process of transitioning in SCD has primarily focused on evaluating the transition process and programmatic structure. These studies have included questionnaire-based evaluations in order to gather the opinions of patients and their caregivers about their expectations of, and concerns about, C
2013 Wiley Periodicals, Inc. DOI 10.1002/pbc.24870 Published online 18 December 2013 in Wiley Online Library (wileyonlinelibrary.com).
the transition process [4,5]. Additionally, other studies have evaluated the transition process by surveying pediatric and adult care providers [6–8]. By contrast, our study seeks to identify potential demographic and clinical factors associated with an unsuccessful transition, or one that does not result in the establishment of care at the adult SCD center. As such, determining risk factors for an unsuccessful transition may, in turn, allow us to modify our existing transition program to insure improved success going forward.
METHODS Implementation of Combined SCD Transition Program Prior to implementation of the combined CCMC/UCHC SCD transition program, the pediatric SCD program at CCMC had been guiding adolescent and young adult patients through the transition process beginning during late adolescence around age 15 or 16 and continuing until the mid-twenties, around age 24. The transition 1
Adult Sickle Cell Center, Division of Hematology-Oncology, University of Connecticut Health Center, Farmington, Connecticut; 2 Department of Community Health and Health Care, University of Connecticut Health Center, Farmington, Connecticut; 3Department of Pediatrics, Connecticut Children’s Medical Center, Hartford, Connecticut; 4Department of Research, Hospital for Special Care, New Britain, Connecticut Grant sponsor: Connecticut Institute for Clinical and Translational Science (CICATS); Grant sponsor: The State of Connecticut Department of Public Health Conflict of interest: Nothing to report.
Correspondence to: Biree Andemariam, Assistant Professor of Medicine, Director, Adult Sickle Cell Center, Division of HematologyOncology, University of Connecticut Health Center, 263 Farmington Avenue, MC 1628, Farmington, CT 06030. E-mail: [email protected] Received 7 June 2013; Accepted 31 October 2013
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period was defined as having three phases: preparatory, transitional, and completion. The preparatory phase was primarily focused on patient education regarding SCD and patient-specific health issues and management. The transitional phase was focused on empowering the individual patient to navigate the health care system in the context of increasing responsibility. The completion phase was focused on establishing effective patterns of health care in the adult setting. The preparatory phase was conducted over a period of 6–10 visits done every 4–6 months over a 3-year period. The transitional phase included at least four family meetings with pediatric health care staff (including social work, nursing, and medical staff) to review health summaries, problem lists, and treatment plans. Patients were discharged from the pediatric practice by age 21 and given a referral to one of the many adult hematology physicians in the community for continued SCD care. At this point, the patient entered the completion phase which consisted of supporting the patient after transition with extra social and care coordination support on an ad hoc basis primarily as initiated by the individual patient when the need arose. At the time the combined transition program was formalized in 2007, there were 47 SCD patients receiving care at CCMC who were age 16 or older and were therefore identified as appropriate for participation in the modified transition process. These patients were in various stages of the transition period. The three-phase approach already in place was continued. However, the preparatory and transition phases were changed such that both began at age 16. The transitional and completion phases were then jointly carried out by the adult and pediatric teams and involved a monthly combined transition clinic held at the pediatric center (10 miles away from UCHC) and attended by the individual patients, family members, a representative from the local SCD community-based organization (CBO), and both adult and pediatric health care personnel, including social work, nursing, and medical staff. Each patient was expected to attend at least four of the combined transition clinics over several years until finally transferring his/her care to the UCHC adult SCD center at the age of 21. During the combined transition clinics, each patient was further educated about his/her disease and had the opportunity to meet face-to-face with both the pediatric and adult care provider teams. A patient navigator/advocate from the region’s SCD CBO (Citizens for Quality Sickle Cell Care, Inc.) was present for all combined transition clinics. Patients were informed about the resources available to them both at UCHC’s adult SCD center and in the community. Patients were able to ask questions and express any concerns about transitioning. Moreover, patients were invited to make an appointment for a tour of the adult SCD center which was given by the CBO patient navigator/advocate. During the tour, patients were able to ask questions, have their concerns addressed, and express any anxiety surrounding leaving their pediatric care-givers. As a patient approached his/her 21st birthday, he/she attended a final combined transition clinic. At that time, a brochure from the UCHC adult SCD program was given to the patient containing the phone number and address of the center. The patient was advised to make an appointment for transfer of care. If the patient was on chronic transfusion therapy, he/she was given (verbally or in writing) an appointment for his/her next transfusion at the adult center. Patients signed a consent form allowing medical records to be sent to the adult SCD program in advance of their first appointment. Pediatr Blood Cancer DOI 10.1002/pbc
Ideally, patients scheduled their first visit to the adult SCD center prior to reaching their 21st birthday, and prior to their last appointment at the pediatric SCD clinic. Each patient received a call from the adult SCD nurse as a reminder of the appointment and detailed directions to the clinic were provided. Patients who did not show for their appointment were called by the adult SCD nurse. Boundaries to accessing care were explored and then addressed by both the adult and pediatric teams. The patient’s appointment was then rescheduled during that conversation. The status of all patients who were to have transferred care to the adult SCD center were reviewed by the adult and pediatric provider teams at the beginning of each monthly combined transition clinic. Patients who had not yet made or kept an appointment at the adult SCD center were contacted by the pediatric SCD nurse and/or social worker to assess for roadblocks and to encourage timely establishment of care. If, after 1 year, the patient had not transferred care to the adult SCD center, a certified letter was sent from the pediatric SCD program to the patient formally advising them to contact the pediatric SCD program for assistance.
Retrospective Chart Review After obtaining approval from the Institutional Review Boards at CCMC and UCHC, we conducted a retrospective chart review of all patients age 16 and older with SCD from 2007 to 2012. Charts were reviewed for demographic factors (gender, age, race/ethnicity, insurance type, and location of residence), clinical information (genotype, 3-year admission history for vaso-occlusive crisis or acute chest syndrome episodes, and whether or not they were on hydroxyurea or a chronic transfusion therapy program), and transition clinic attendance. Patients were categorized as either having a successful or unsuccessful transition. Successful transition was defined as attendance of at least one outpatient visit at the UCHC adult SCD center after being discharged from the CCMC pediatric SCD program.
Statistical Analysis Statistical methods used for data analysis included chi-square tests for assessing association among categorical variables (e.g., transitioned (Y or N) vs. gender) and two-group t-tests for comparing group means (e.g., distance from home to the adult sickle cell center, by transitioned, Yor N). When the assumptions of the chi-square were not met, we reported Fisher’s Exact Test. All analyses were performed using SAS1 statistical software (SAS Institute, Inc., Cary, NC).
RESULTS Transition Population Characteristics Forty-seven pediatric SCD patients between the ages of 16 and 24 years began the modified transition process between the years 2007 and 2012. Tables I and II outline the patient characteristics including demographics, clinical factors, and transition clinic attendance. Fifty-seven percent of the patients were female. Although 87% of patients were Black, there was representation from other racial groups as well. Fifty-eight percent of the patients had private insurance. The remainder of the patients had insurance coverage through the Connecticut state Medicaid program. There was an expected distribution of hemoglobin
Risk Factors for Unsuccessful Sickle Cell Transition TABLE I. Demographic Data of All Transition-Aged Patients
Gender Male Female Race Black Hispanic White Indian Insurancea Private Medicaid Age at the start of transition (years) 16–18 19–20 21 and older Distance from home to adult center (miles)a 0–5 6–10 11–15 16–20 21–25 26–30 Average transition clinic attendance Attended 50% Clinics Attended >50% Clinics
n
%
20 27
43 57
41 4 1 1
87 9 2 2
25 18
58 42
18 21 8
38 45 17
5 14 4 11 8 1
12 33 9 26 19 2
21 26
45 55
a All data in this table reflect demographic data which were obtained from the charts of all 47 children who underwent the transition process during the study period. However, insurance and distance information was only available for 43 patients, as indicated.
genotypes (62% SS or Sb0, 38% Sbþ or SC). All patients lived within 30 miles of the adult sickle cell center. At the time of their last routine pediatric SCD clinic visit, 62% of patients were on a chronic transfusion therapy program and less than 10% of patients were taking hydroxyurea. When examining hospitalization records over the 3 years prior to their final pediatric SCD clinic visit, 77% of patients had four or less vaso-occlusive crisis admissions and 76% of patients had not experienced an episode of acute chest syndrome. While nearly 40% of patients attended their first modified transition clinic by the age of 18, a majority of patients were already age 19 or older. In fact, 17% of patients were already at least 21 years old at the start of the modified transition program and had to undergo a rapid process of transition to the adult SCD center.
Risk Factors for an Unsuccessful Transition Out of the 47 patients planned for transition from the pediatric to the adult SCD center from 2007 to 2012, 68% successfully transitioned. Of note, all patients who met this definition also established continual, ongoing, comprehensive care. The remaining 32% of patients who did not successfully transition have not, to our knowledge, established longitudinal hematology care elsewhere. As indicated in Table III, transition success was not influenced by gender as 63% of female patients and 75% of male patients transitioned successfully (P ¼ 0.38). Race was also not associated with transition outcome (P ¼ 0.67). There was no statistically significant difference in type of insurance amongst those that Pediatr Blood Cancer DOI 10.1002/pbc
699
TABLE II. Clinical Data of All Transition-Aged Patients n Genotype SS 26 SC 9 S bþ 9 3 S b0 Chronic transfusion therapy Yes 14 No 33 Hydroxyurea utilization Yes 4 No 43 ACS episodesa,b 0 35 1 5 2þ 6 VOC episodes requiring hospitalizationb,c 0 20 1–4 15 5–7 6 15þ 4
% 55 19 19 6 30 70 9 91 76 11 13 44 33 13 8
a
All data in this table reflect demographic data obtained from the medical charts of all 47 children who underwent the transition process during the study period. However, information regarding Acute Chest Syndrome (ACS) episodes was only available for 46 patients. bACS episodes and vaso-occlusive crisis (VOC) episodes were totaled over a 3-year period prior to last pediatric hematology visit. cInformation regarding VOC episodes requiring hospitalization was only available for 45 patients.
transitioned (53% private vs. 47% Medicaid) compared to those that did not successfully transition (69% private versus 31% Medicaid) (P ¼ 0.33). Mean combined transition clinic attendance rate and mean number of scheduled transition clinic visits was not associated with transition success (both P > 0.25). Those that transitioned had higher mean combined transition clinic visits attended, but the difference was not statistically significant (2.1 vs. 1.5, P ¼ 0.07). Both clinical and non-clinical factors significantly influenced transition success outcomes. SC or Sbþ genotype and a lack of a need for chronic transfusions were significantly higher in the unsuccessfully transitioned group of patients. Specifically, 21% of SC/Sbþ patients did not transition successfully compared to only 21% of SS/Sb0 patients (P ¼ 0.04). Of those patients who did not successfully transition, 93% were not on a chronic transfusion therapy program, a significantly higher rate than the 59% who did transition (P ¼ 0.02). There was no significant difference in utilization of hydroxyurea among the successfully and unsuccessfully transitioned patients (12.5% vs. 0%, P ¼ 0.29). The frequency of acute chest syndrome episodes was also not different between the two groups of patients with approximately 90% in each group having at most one episode (P ¼ 0.99). Vaso-occlusive crisis episode hospitalization frequency was similar between the two groups with 73% of transitioned and 87% of non-transitioned patients experiencing four or fewer admission for VOC over a 3-year period (P ¼ 0.13). Later age at the start of the modified transition process also negatively influenced transition success. Only 25% of patients who
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TABLE III. Transition Outcomes Transitioned Yes n (%)
No n (%)
Demograhics Gender Female 17 (63) 10 Male 15 (75) 5 Race Black 28 (68) 13 Hispanic 3 (75) 1 White 1 (100) 0 Indian 0 (0) 1 Insurancea Private 16 (64) 9 Medicaid 14 (78) 4 Age at the start of transition 20 3 (33) 6 Clinical factors Genotype 9 (50) 9 SC or Sbþ SS or Sb0 23 (79) 6 Chronic transfusion therapy Yes 13 (93) 1 No 19 (58) 14 Hydroxyurea utilization Yes 4 (13) 0 No 28 (87) 15 ACS episodes 0 23 (74) 12 1 4 (13) 1 2þ 4 (13) 2 VOC episodes requiring hospitalization 0 10 (34) 10 1–4 12 (40) 3 5–7 4 (13) 2 15þ 4 (13) 0 Transition clinic attendance Average transition clinic attendance 50% Clinics 14 (67) 7 >50% Clinics 18 (69) 8 Total transition clinic attendanceb Attended 2.2 (1.22) 1.5 Scheduled 3.5 (2.21) 2.7
P value
(37) (25)
0.38
(32) (25) (0) (100)
0.67
(36) (22)
0.33
(23) (65)
0.008
(21) (67)
0.01
(50) (21)
0.04
(7) (42)
0.02
(0) (100)
0.29
(80) (7) (13)
0.99
(67) (20) (13) (0)
0.13
(33) (31)
0.851
(1.13) (2.02)
0.07 0.24
a
Insurance information was only available for 43 patients. bTotal transition clinic attendance is expressed as a mean (SD).
began the modified combined transition process at the age of 21 or older successfully transitioned, whereas 77% of patients who began before age 21 did so successfully (P ¼ 0.008). Distance from home to the adult SCD center also influenced transition outcomes as those patients who lived more than 20 miles away were less likely to transition than those who lived closer (33% vs. 79%, P ¼ 0.01).
DISCUSSION A successful transition from pediatric to adult specialty care in SCD is critical to prolonged survival. Others have identified Pediatr Blood Cancer DOI 10.1002/pbc
that a lack of adult hematology providers with expertise or interest in SCD has been a major roadblock in successful transition [9]. In our region, we are fortunate that this leading cause of unsuccessful transition nationally is no longer a factor. Fortunately, the elimination of this most prevalent barrier to continued care has allowed us to examine other risk factors for an unsuccessful transition. It is our intention that the findings from this study will guide modification of our existing transition program to insure enhanced attention to the subset of pediatric SCD patients at highest risk for not transitioning and therefore at potentially higher risk for increased morbidity and mortality. The findings of our study demonstrate that both clinical and nonclinical factors are associated with transition success. Non-clinical factors that were identified as risk factors for unsuccessful transitioning were greater travel distance from the patient’s home to the adult SCD center and older age at the time of initiation of the transition process. The significance of geography factors was not surprising and suggests that the SCD centers and patients’ insurers need to address ways to enhance access to care from a transportation standpoint. As a result of our study, our adult SCD center’s social worker now specifically discusses transportation with each patient during the combined transition clinic. If distance is identified as a potential roadblock to getting to the adult SCD center, eligibility for transport assistance will be evaluated and family/community resources for transportation will be explored. The finding that older age at the time of initiation of the modified transition process was associated with poor transition success was also not surprising. We do not anticipate this to be able to influence transition success. Combined transition will be initiated in a timely fashion at the age of 16. Given the sustained and permanent nature of our newly-established program, we should no longer have pediatric patients over age 16 waiting to initiate the transitional phase or over age 21 searching for an adult SCD provider to whom they can transition their care. What was indeed surprising was the lack of an adverse relationship between insurance type and transition success. We had hypothesized that patients with private insurance would be more likely to complete the transition process, however, transition success was not influenced by insurance type. We speculate that this can be explained, in part, by the fact that Medicaid in the state of Connecticut provides medical cab transportation to scheduled provider visits for its insured. This may have allowed for the negative influence of travel distance to have been overcome in this subset of patients. We evaluated clinical factors that are known markers of disease severity: hemoglobin genotype, the need for hydroxyurea or chronic transfusion therapy (CTT), the frequency of acute chest syndrome (ACS) episodes, and hospitalization rates for vasoocclusive crisis (VOC). Hydroxyurea utilization was not predictive of transition success. However, there were very few total patients on hydroxyurea making the lack of an association in this study difficult to generalize. Hospitalization rates for VOC or ACS were not associated with transition success. This is concerning, particularly if the frequency in VOC or ACS episodes has continued in the unsuccessfully transitioned group. Without an identified adult SCD provider, it is likely that these patients are receiving care primarily in emergency departments rather than coordinated multi-disciplinary care by a team of experts.
Risk Factors for Unsuccessful Sickle Cell Transition We had indeed hypothesized that children on CTT would be more likely to transition to the adult SCD center successfully due to the need to continue regular transfusions in a timely manner. The question is why. We now recognize that perhaps the enhanced effort at scheduling initial appointments at the adult SCD center for patients on CTT may be a contributing factor. This includes a more concerted effort and communication amongst the pediatric and adult SCD nurses to insure timely scheduling of the next transfusion. Additionally, calls to remind patients of these transfusion appointments are made over and above the reminder calls for the outpatient clinic visit. Whether the increased effort on the part of the adult SCD staff to insure patients on CTT are scheduled for transfusion is the sole reason for improved transition success in this group is not entirely clear. It is possible that patients who are on CTT perceive themselves as more sick or that the rationale for maintaining a SCD provider relationship is more implicit than for patients who do not get regular transfusions as part of their disease management. Supporting this notion is our finding that patients with genotypes SC and Sbþ were at highest risk for not transitioning. SCD patients with these genotypes are generally perceived by healthcare providers to have less severe disease. It is plausible that these patients receive less reinforcement or education about the potential severity of their disease. This suggests that we need to engage our patients in the comprehensive well visit process more so they perceive and experience tangible benefit from coming to visits even when feeling well. We also must pay special emphasis on educating our patients with SC and Sbþ disease about the risks of SCD even in the face of what may have been a relatively smooth pediatric clinical course. Although not directly studied, we believe that the development of combined adult/pediatric transition clinics enhanced our transition process and contributed to its successes. Additionally, the incorporation of the SCD CBO as an active participant in the role of patient navigator likely improved the comfort and trust levels of the patients and their families as they moved into a new care environment. We did not develop specific measures to evaluate the impact of the presence of adult SCD providers or the CBO, therefore data on their involvement is not available. However, we do plan to specifically measure the potential impact going forward. For example, was transition success influenced by direct patient interaction with our adult SCD providers and CBO, by patients touring the adult facility with the CBO navigator, or by the presence of the CBO navigator in the adult SCD clinic? These are important questions and, if studied with appropriate measures, could be the basis for further research that may give insights to other transition programs about unique ways to incorporate CBOs and adult SCD providers in the transitioning process. It is important to note that there are potential limitations to our study, including ones that may affect its generalizability. The retrospective nature of this review of our clinical program’s
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effectiveness without a comparison group may allow for confounding variables making us falsely conclude that having a program such as ours makes a difference when in fact it does not. Additionally, the study results are based on analysis of a relatively small cohort of patients attending a uniquely designed combined specialty clinic that incorporates a CBO in the role of patient navigator/advocate. However, the general methods and practices are portable to other practices and areas of the country where potential partnerships between adult and pediatric hematology providers could be fostered, many of which share the same campus or hospital (unlike our programs). We have no reason to believe that our population of patients differs significantly from other populations. However, our patients may be more spread out geographically than populations from more concentrated metropolitan areas. Additionally, our adult program is situated in a suburban location, which is not typical for sickle cell centers. In conclusion, we have elucidated easily identifiable risk factors for failure to transition successfully. Enhanced and early education of all pediatric SCD patients regarding the need to continue comprehensive care in the adult setting is imperative, particularly among those patients who may perceive their SCD to not be as serious as it is for others. Additionally, similar diligence in assisting transitioned patients on CTT with scheduling the first adult SCD provider appointment should be employed uniformly with all patients regardless of their CTT status. Our study has provided important insights into how we can further modify of our transition efforts to insure that no young adults with SCD get lost in the process.
ACKNOWLEDGMENTS This work was supported by grants from the Connecticut Institute for Clinical and Translational Science (CICATS) Clinical and Translational Scholars K12 Award (B.A.), and the State of Connecticut Department of Public Health (B.A., J.O-G, D.B., J.N.H., R.S.T).
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