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Site of Oncologic Specialty Care for Older Adolescents in Utah

Karen H. Albritton, Charles H. Wiggins, Harold E. Nelson, Jane C. Weeks

From the Dana-Farber Cancer Institute, Boston, MA; University of Utah, Salt Lake City, Utah; and the University of New Mexico, Albuquerque, NM

Address reprint requests to Karen Albritton, MD, Dana-Farber Cancer Institute, 44 Binney St, Boston, MA 02115; e-mail: karen_albritton{at}dfci.harvard.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Purpose Adolescents with cancer may access oncologic care from pediatric or adult medical centers, given overlapping age eligibility. However, some recent data suggest a benefit to adolescents with certain cancers when treated at pediatric centers or on pediatric protocols. We used a population-based registry to determine the site of care of children, adolescents, and young adults (age 0 to 24 years) with newly diagnosed cancer.

Patients and Methods From the Utah Cancer Registry 1994 to 2000, new malignant cases in patients aged 0 to 24 years were chosen; data including diagnosis, home ZIP code and sites of oncologic care were abstracted. Distance between home ZIP code and Primary Children's Medical Center (PCMC; Salt Lake City, Utah), the state's sole site of pediatric oncology care, was determined.

Results Sixty-six percent of Utah 15- to 19-year-olds with cancer were never seen by a PCMC oncologist. Even among this narrow age range, utilization of the pediatric center dropped with each additional year of age. Not unexpectedly, few of those with epithelial malignancies in this age group were seen at PCMC. But surprisingly, 47% of the older adolescents with leukemia, 66% with brain tumors, and 71% with lymphoma never saw a pediatric oncologist. After consideration of age and diagnosis, distance the patient lived from PCMC had a negligible effect on the likelihood of an adolescent being seen there.

Conclusion The referral of adolescents with cancer to a pediatric oncology center diminishes greatly with age, and is moderately influenced by diagnosis and minimally by distance from center. Further study should investigate reasons for referral patterns, and impact on outcomes.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Approximately 4,100 American adolescents aged 15 to 19 years are diagnosed with cancer each year; malignancy is the leading cause of disease-related death in this age group.¹ Unlike younger or older patients, these patients may access two systems of care: medical oncology or pediatric oncology. Medical oncologists are more numerous and geographically accessible; there are 2.4 board-certified medical oncologists for every 15- to 19-year-old diagnosed in the United States, but only 0.44 pediatric oncologists (calculated from Jamal et al¹ and American Board of Internal Medicine [http://www.abim.org/resources/dnum.shtm] and American Board of Pediatrics [http://www.abp.org/stats/WRKFRC/Hemo.ppt] board certification data).

A definitive association between provider specialty and outcomes of adolescents with cancer has not yet been established. However, recent provocative data suggest that for adolescents with acute lymphoblastic leukemia^2-5 and Ewing sarcoma,⁶ outcomes may be better when care is delivered in a pediatric center or according to a pediatric protocol. There is also concern that the lower utilization of pediatric oncology services and clinical trials is partially responsible for this group's lack of survival improvement in the last 25 years.⁷

Little is known about sites of care for US adolescents with cancer. A convenience sample of participating hospitals in the National Cancer Data Base found that 34% of adolescents aged 15 to 19 years were treated at centers that had National Cancer Institute (NCI) pediatric cooperative group affiliation.⁸ In Canada, 30% of adolescents 15 to 19 years old were treated at pediatric oncology centers.⁹ A study in Ohio found that 51% of adolescents utilized a pediatric center, but methodologic issues may have overestimated utilization.¹⁰

Our objective was to determine, for US cancer patients ages 0 to 24 years, the influence of age, cancer diagnosis, and distance on referral to a pediatric center. The state of Utah provides an advantageous setting for such a population-based study. The Utah Cancer Registry (UCR) was established in 1966 and has been a member of NCI's Surveillance, Epidemiology, and End Results (SEER) program since its inception in 1973.¹¹ Primary Children's Medical Center (PCMC), in Salt Lake City, is the sole pediatric cancer care center in Utah. Only a small geographic area of Utah, in which a very small percent of the population resides, is closer to an out-of-state pediatric center than to PCMC (Fig 1). Therefore, determination of care at PCMC is a simple but accurate way to capture pediatric subspecialist utilization by Utah adolescents.

View larger version (40K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Location of pediatric centers in Utah and surrounding states. Lines and numbers signify shortest driving distance (in miles) between Salt Lake City, Utah, and cities that have a pediatric oncology center that is a National Cancer Institute–funded Children's Oncology Group member.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
UCR registrars in local hospitals identified incident cases of cancer through routine and systematic review of pathology reports, medical records, radiation therapy records, hospital discharge lists, and vital records in accordance with SEER¹² and North American Association of Central Cancer Registries¹³ standards. Cancer histology and primary site were coded according to the International Classification of Disease for Oncology (ICD-O).¹⁴ UCR also routinely documented the facilities where treatment was administered, sex, race/ethnicity, age, and place of residence at diagnosis. Estimates of completeness of case coverage consistently exceeded 98% during the study period.

All incident cases of malignancy among Utah residents under the age of 25 years between 1994 and 2000 were identified from the UCR database; benign and in situ lesions were excluded. Using histology and site codes, cases were assigned to 12 diagnostic categories derived from the International Childhood Cancer Classification system,¹⁵ then further grouped into six broader categories (Table A1, online only).

PCMC was the only medical center in Utah staffed with pediatric oncologists during the study period, and the state's only NCI-funded Children's Oncology Group member. PCMC policy was to accept care of any child younger than 22 years at the time of cancer diagnosis. PCMC physicians maintain academic affiliations with the University of Utah (UU; Salt Lake City), whose adult oncology service was the only academic oncology program and the only NCI-designated cancer center in the state. Seven hospitals in Utah had American College of Surgeons (ACS)-approved cancer programs; UU and PCMC together represented one ACS-accredited program.

For each patient, UCR files were queried to identify up to six facilities that had provided care at any time since cancer diagnosis. Utah residents diagnosed in neighboring states were identified through an exchange agreement with their cancer registries, and appropriately coded in UCR records. For this analysis, cases were placed in one of four exclusive categories: (1) patients ever seen at PCMC; (2) patients ever seen at UU, but not PCMC; (3) patients ever seen in one of the remaining six hospitals with ACS-approved cancer programs (but not PCMC or UU); and (4) patients seen solely at facilities not included in the previous categories.

To estimate the distance between PCMC and the patient's residence, we ascertained the latitude and longitude of PCMC and the post office associated with the ZIP code of residence at diagnosis. The distance in miles between these two sets of coordinates was calculated using the North American Association of Central Cancer Registries Great Circles algorithm.¹⁶ To correct for the leftward skewed distribution, we transformed the data using the square root of distance.

Analyses were conducted with SAS 9.1 (SAS Institute, Cary, NC). ² was used to test for significance in univariate analyses; the Cochrane-Armitage test was used to test for trend. A multivariate logistic regression model predicting adolescents' receipt of care at PCMC included diagnosis and age as categoric variables and distance as a linear variable. We used Wald ² type 3 analysis of effect to test the impact of these three variables on the model. For individual categories within each variable, odds ratios (ORs) of receiving care at PCMC were reported, adjusted for the remaining two variables.

	RESULTS

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There were 1,355 patients younger than 25 years diagnosed with invasive cancer in Utah during these 6 years. Fifty-three percent were male, 88% were white, and 8% were Hispanic, representative of the demographics of the state. Three hundred twenty-one cases were between 15 and 19 years old at diagnosis.

Univariate Analyses
As shown in Figure 2, the proportion of patients ever seen at PCMC declined with age. Nearly all children age 0 to 9 (97%) with cancer received some oncology care at PCMC. Between 10 and 14 years of age, 82% were seen at the pediatric center. The percentage seen at PCMC began a linear decline starting at age 14 years, and only 34% of adolescents 15 to 19 years of age were ever seen at PCMC. As expected, less than 1% of those older than 19 years were seen at the pediatric center. Overall, nonwhites were more likely than whites to be seen at PCMC (57.9% v 45.8%; P = .004). A similar trend was seen in the limited group aged 15 to 19 years (46.7% v 32.3%; P = .11), but it did not reach statistical significance, perhaps because of small sample size (only 30 nonwhites).

View larger version (48K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Site of care for cancer patients in Utah by age. PCMC, ever seen at Primary Children's Medical Center; UU, ever seen at University of Utah Hospitals but not PCMC; ACS, ever seen at a Utah American College of Surgeon's accredited cancer center, but not PCMC or UU; Other, never seen at PCMC, UU, or another ACS site.

Diagnosis
Among adolescents aged 15 to 19 years, the referral pattern differed by diagnostic category (Fig 3). Nearly all patients with bone sarcomas were seen at PCMC, as were 67% of patients with acute lymphoblastic leukemia (ALL) and 52% of patients with soft tissue sarcomas. In contrast, only 34% of older adolescents with brain tumors, 32% with non-Hodgkin's lymphoma, and 28% with Hodgkin's disease were ever seen at PCMC. Patients older than 14 years with melanoma and non–germ cell gynecologic cancers, and thyroid and germ cell cancer patients older than 16 years were never seen at PCMC. The use of an academic medical center, other cancer centers, and community hospitals varied by diagnosis. A majority of Hodgkin's lymphomas, gonadal germ cell tumors, thyroid cancers, gynecologic cancers, melanomas and other cancers were seen outside the university-affiliated programs.

View larger version (23K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 3. Site of care for adolescent Utah cancer patients age 15 to 19 years by diagnosis. CNS, CNS tumors; GYN, gynecologic; PCMC, ever seen at Primary Children's Medical Center; UU, ever seen at University of Utah Hospitals but not PCMC; ACS, ever seen at a Utah American College of Surgeons accredited cancer center, but not PCMC or UU; Other, never seen at PCMC, UU, or another ACS site.

Even among this narrow age range (15- to 19-year-old patients), utilization of the pediatric center dropped with each additional year of age, and age was a highly significant variable in the adjusted model (P < .0001). There were no significant interactions between distance and age or diagnosis. There was an insufficient number of cases to reliably evaluate interaction between diagnosis and age.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
In this population-based study of children, adolescents, and young adults diagnosed with cancer in Utah between 1994 and 2000, we found a steep age-dependent decline in utilization of the state's only site of pediatric oncology care. Two thirds of Utah 15- to 19-year-olds with cancer were never seen by a pediatric oncologist.

The type of cancer had a strong influence on site of care for older adolescents. The cancers most likely to be referred to the pediatric center were sarcomas and ALL, whereas virtually all adolescents with epithelial cancers were treated outside PCMC. This suggests that the adolescents who physicians are referring to the pediatric center are primarily those with cancers rarely seen in adults. Even so, only half of the leukemia and soft tissue sarcoma patients and one third of the brain tumor and lymphoma patients, those with cancers comfortably managed by both medical and pediatric providers, were seen at PCMC. These diagnoses may constitute a particularly important subgroup for future studies examining determinants of referral patterns.

The geographic vastness of Utah might suggest a lower likelihood of access to a sole pediatric center, but we found rates similar to previous estimates. Any use of out-of-state pediatric centers by those living near the state borders would only make our results an overestimate of the impact of distance. Nearly all families with young children with cancer were willing to travel long distances to PCMC when it was perceived as the best medical option. We had hypothesized that distance might have a greater effect on patterns of care for older adolescents, both because the families' dynamics might be different and because they could opt to receive care from a medical oncologist closer to home. However, distance had only a modest, non–statistically significant effect in the 15- to 19-year-olds. The fact that 63% of the adolescents living within 12 miles of PCMC did not utilize its services further underscores the conclusion that reluctance to travel was not a primary determinant of site of care.

Lastly, the decline in utilization of the pediatric center from age 15 to 21 years suggests that several fluid factors are likely influencing health service delivery, rather than a single factor that occurs at a delineated age (such as age eligibility at the pediatric center, insurance coverage, driver's license, legal age, etc).

How generalizable are our results to other geographic locations? Our cohort was geographically defined, population-based, and obtained from an established SEER cancer registry. Any unreported cases are most likely from hospitals with lower cancer volumes, and without established cancer registrars (ie, nonacademic, non–ACS accredited centers). Such cases would drive our estimate of adolescents seen at PCMC even lower. Despite Utah's size, a majority of the population lives in close proximity to Salt Lake City: 78% of our sample lived within 50 miles of PCMC. This does not differ dramatically from the national pattern, where 86% of children live within 50 miles of a pediatric oncologist (M. Mayer, personal communication, January 2006). When we restricted our sample to those living within 50 miles, which may replicate the situation of states with multiple, geographically distributed pediatric centers, the findings were unchanged. Our center's upper age limit of 21 years would not have limited admission of older adolescents; however, in 1999, some pediatric centers in the US had upper age limits as low as 16 years (A. Bleyer, personal communication, October 1999), which would further restrict access. Utah's population is overwhelmingly white, and has moderately higher socioeconomic status indicators than the national average (Table A2, online only). A study in Los Angeles County, CA, found that children in the highest socioeconomic status brackets had lower rates of pediatric cooperative group registration, but did not find any variation by race.¹⁷ Therefore, demographic characteristics may influence patterns of care for pediatric or adolescent cancer, and our findings may not be fully generalizable to regions where demographics are dramatically different from Utah's. Furthermore, there may be other unmeasured confounders such as medical coverage for indigent patients, primary care practice differences, or cultural differences that would influence outcomes in other states. The similarity of our results to those obtained in Canada, where there is universal health care, suggests that issues other than insurance, such as primary provider preference, drive the referral pattern.

Reasons adolescents with cancer might not be seen at a pediatric center include issues related to provider practice, logistical or extramedical factors, and patient preference. Adolescents with symptoms heralding their cancer may be more likely than younger children to be seen initially by an "adult" physician,¹⁸ who is more likely to have established referral relationships with medical than with pediatric oncologists. Adolescents with some localized tumors, including sarcomas, brain tumors, melanoma, thyroid cancer, and testicular cancer, may initially see a surgeon. If these adolescents are never seen at a pediatric center, it may be because they are not referred to an oncologist at all (pediatric or medical). The appropriateness of such a lack of referral, to determine the role of adjuvant therapy, is unknown, especially in adolescents. In a study of referral patterns for adults with breast cancer, also a cancer that can start with nonmedical management, "extramedical factors" such as surgeon and patient preferences, employment status, and age were as influential as medical ones in determining whether a patient was referred to a medical oncologist.¹⁹ Finally, adolescents may avoid a pediatric center, feeling that it is geared towards younger children.

How much concern our findings should raise depends on whether outcomes of adolescents with cancer are affected by the specialty of the physicians caring for them. We do not have sufficient sample size or clinical detail to be able to address this question in our cohort. However, other studies provide direct or indirect evidence that site of care may matter. There is strong evidence that older adolescents with ALL treated on pediatric cooperative group trials fare better than those treated on adult trials.^2-5 Likewise, treating selected young adult sarcoma and lymphoma patients with pediatric protocols has resulted in higher survivals compared with historical controls.^20-24 We can surmise that adolescents are more likely to receive such pediatric-type therapy at pediatric centers. Furthermore, pediatric centers enroll more adolescents onto clinical trials (34.8% v 12.1% at nonpediatric centers).^25,26 Although trial enrollment may not benefit the individual patient, children who are treated on clinical trials have a better outcome than those who are not,^27-29and trial data would increase our understanding of cancer in this population and improve outcomes.

Although there are not yet definitive studies, data are beginning to emerge that, beyond treatment or trial, site of care or provider specialty may matter. When pediatric and medical oncologists followed a single protocol for Ewing sarcoma in Germany, care at a pediatric center was associated with improved survival.⁶ Preliminary National Cancer Data Base data found that adolescents with non-Hodgkin's lymphoma, leukemia, liver cancer and bone tumors had a survival advantage when treated at pediatric centers.⁸ Unfortunately, these provocative data have been published only in abstract form. Until more definitive reports are available, we cannot be sure these results are not caused, at least in part, by selection bias, with patients with a better underlying prognosis preferentially being referred to pediatric centers. Also unstudied is the possibility that adolescent patients with "adult" tumors might have better outcomes if they are treated at adult institutions.

In summary, we found that two thirds of 15- to 19-year-olds with cancer were not seen at pediatric institutions, with patterns of care determined largely by age, and to a lesser extent by diagnosis. Clearly, every cancer patient should be treated by an oncologist experienced in the care of similar patients, with the therapy known to produce the best survival outcome for a given diagnosis. The patient should have access to clinical trials and support services appropriate to his or her developmental age. Further outcomes research should seek to determine whether access to these services, and survival, are affected by site of care for adolescents. If outcomes are better overall or for certain subgroups of adolescents when they are treated at pediatric centers, our data suggest that many adolescents with cancer may not be getting optimal care.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Conception and design: Karen H. Albritton, Charles L. Wiggins

Provision of study materials or patients: Charles L. Wiggins

Collection and assembly of data: Charles L. Wiggins

Data analysis and interpretation: Karen H. Albritton, Charles L. Wiggins, Harold E. Nelson, Jane C. Weeks

Manuscript writing: Karen H. Albritton, Charles L. Wiggins, Jane C. Weeks

Final approval of manuscript: Karen H. Albritton, Charles L. Wiggins, Jane C. Weeks

	Appendix

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 

	NOTES

 
Supported by Contract Nos. N01-PC-35141 N01-PC-35138 from the National Cancer Institute.

Presented in part at the 36th Annual Meeting of the American Society of Clinical Oncology, May 20-23, 2000, New Orleans, LA (abstr 990).

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
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4. Boissel N, Auclerc MF, Lheritier V, et al: Should adolescents with acute lymphoblastic leukemia be treated as old children or young adults? Comparison of the French FRALLE-93 and LALA-94 trials. J Clin Oncol 21:774-780, 2003[Abstract/Free Full Text]

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Submitted July 28, 2006; accepted April 24, 2007.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Albritton, K. H. Articles by Weeks, J. C. Search for Related Content PubMed PubMed Citation Articles by Albritton, K. H. Articles by Weeks, J. C. Related Articles Related Editorial Related Correspondence Social Bookmarking                            What's this?