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Typical Time to Treatment of Patients With Lung Cancer in a Multisite, US-Based Study
Abstract
The importance of high-quality, timely lung cancer care and the need to have indicators to measure timeliness are increasingly discussed in the United States. This study explored when and why delays occur in lung cancer care and compared timeliness between two states with divergent disease incidence.
Patients with small-cell or non–small-cell lung cancer were recruited through cancer centers, outpatient clinics, and community approaches, and interviewed over the phone. Statistical analysis of patient-reported dates included descriptive statistics and comparing time intervals between states and across the sites with Mann-Whitney U tests. Additionally, data from patients with longer timelines were qualitatively analyzed to identify possible reasons for delays.
On the basis of the dates reported by 275 patients, the median time from first presentation to a clinician to treatment was 52 days; 29% of patients experienced a wait of 90 days or more. Median times for key intervals were 36.5 days from abnormal radiograph to treatment, 9.5 days from initial presentation to specialist referral, 15 days from patient informed of diagnosis to first therapy, and 16 days from referral to treatment to first therapy. More than one quarter of patients perceived delays in care. No significant differences in length of time intervals were identified between states. Monitoring of small nodules, missed diagnosis, and other reasons for longer timelines were documented.
Lung cancer is a common and deadly malignancy affecting more than 221,000 Americans each year.1 The 5-year survival rate is only 17%.1 The aggressive growth rate of non–small-cell lung cancer (NSCLC) has been characterized by O’Rourke and Edwards,2 who reported a 19% median increase (range, 0%-373%) in cross-sectional tumor size over a median 54-day interval, and Mohammed et al,3 who described a 35% median increase (range, 7%-300%) over a median 94-day interval between two computed tomography (CT) scans. Small-cell lung cancer (SCLC) is a rapidly progressing cancer with a mean doubling time of 86 days (range, 25-217 days).4 Timely diagnosis and treatment of lung cancer is critical because delays can lead to missed opportunities for both curative and life-prolonging therapies.
Delays in lung cancer care have been documented in many countries.5 To monitor and improve care, some countries developed clinical practice guidelines setting goals for maximum time intervals related to the diagnosis and treatment of lung cancer. For example, the British Thoracic Society recommended that patients with suspected lung cancer be seen by a respiratory specialist within 7 days of referral; a specialist visit should occur within 2 weeks of an abnormal radiograph, and surgery should be within 8 weeks of a visit to a respiratory specialist.6
The importance of high-quality, timely lung cancer care and the need to have indicators to measure timeliness have been increasingly discussed in the United States.7,8 The RAND Corporation suggested that the diagnosis of lung cancer should be established within 2 months of abnormal radiography, and treatment should begin within 6 weeks of diagnosis.9 However, relatively few studies on timeliness of lung cancer care in the United States have been completed, and those that are published indicate substantial variability.8 The majority of these analyses were performed in the Veterans Administration (VA) hospital system and reported on time from the first abnormal radiograph or pathologic diagnosis to cancer treatment.10 To our knowledge, no one has quantified the typical time to treatment in the United States from the first visit to a health care provider with symptoms indicative of cancer until the first treatment. Further, timeliness of the various steps along the continuum of care has been insufficiently researched, and the causes of lung cancer care delays are only partially understood.
One possible reason for delay is that physicians’ knowledge and beliefs about treatments may not be consistent with scientific evidence.11 Hospital type—private or public—may also influence care delays.12 In the VA system, researchers identified a lack of care coordination and follow-up communication with patients, as well as other system factors influencing delays.13 However, Schultz et al14 found that institutional characteristics explained less than 1% of the observed variation in treatment times in VA facilities. Thus, further examination of the causes of delay in lung cancer care is necessary.
This mixed-methods study was designed to deepen current understanding about when and why delays occur in the care of patients ultimately diagnosed with lung cancer by characterizing a series of time intervals from initial presentation to evaluation, referral, diagnosis, and first treatment. Our study was carried out across multiple health systems in two US states, one with a higher and one with a lower incidence of lung cancer. We intend for the results to inform guideline development, help establish metrics for determining timeliness of care, identify avoidable delays in the diagnosis-to-treatment continuum, and characterize a baseline for further interventions to ensure timely access to evidence-based treatments for patients with lung cancer.
Given that lung cancer incidence varies across the United States,1 we hypothesized that time-to-treatment intervals in a high-incidence state (North Carolina) could be different from a low-incidence state (Wisconsin). We also anticipated identifying differences in timeliness of care by research site.
The study inclusion criteria were patient age ≥ 18 years, having SCLC or NSCLC, and being diagnosed within the prior year. Multiple strategies were used to include diverse patients. Patients were recruited through convenience sampling from June 2012 to June 2014 at three comprehensive cancer centers affiliated with academic institutions, one community cancer center, one multispecialty clinic with multiple locations, and community recruitment approaches (eg, disseminating study information through small rural clinics, relevant Web sites, and newsletters).
Data from patients were collected using telephone interviews. We pilot-tested this method with a small sample of patients with lung cancer in Wisconsin and found that interviewing patients was a reliable method of collecting dates regarding diagnosis and treatment. Although comparisons between patient-reported and chart-reported dates revealed minor discrepancies, patients were able to recall most of the dates, and their recall was sufficiently accurate to justify the use of patient interviews.15
On the basis of data collection protocols shared by researchers from Denmark16 and Canada17 and a VA-based study by Powell et al,13 we developed and piloted a questionnaire.15 This questionnaire was incorporated into computer software and used to conduct semistructured telephone interviews with patients focusing on 12 dates. Nine of them are listed here because they define the key time intervals reported in this article. These dates pertained to the following events: A—first visit to health care provider with symptoms indicative of lung cancer; B—first imaging result with a lung abnormality; C—referral to a specialist; D—first visit to a specialist; E—first diagnostic test; F—last diagnostic test; G—patient informed of the biopsy result; H—first referral to treatment; and I—first treatment. Each interview was audio-recorded, and the interviewer entered dates and notes in the database during and immediately after the interview. We also collected the following information from medical records or health care providers: diagnosis as stated in the pathology report confirming lung cancer, date when the pathology report was signed, and lung cancer stage.
Statistical analysis consisted of comparing subject characteristics by state with t tests and χ2 or Fisher’s exact tests. Time intervals were summarized with medians and ranges, compared between states with Mann-Whitney U tests and compared across the sites with Mann-Whitney U tests. Comparison tests for all time intervals had Holm P value adjustments to maintain a familywise error rate of 0.05. Further, post hoc pairwise Wilcoxon rank sum tests with Holm adjustments were used to determine which sites were different.
Additionally, we identified patients who experienced a 90-day or longer wait between initial presentation and treatment (interval AI). These patients were more closely reviewed to develop insights about possible reasons for delays or missed opportunities to timely diagnose and treat the disease. Study team members reviewed the recorded dates and interviewer notes, listened to the recordings of selected interviews, and discussed the patients and emerging themes. This study was approved by the University of Wisconsin Health Sciences Institutional Review Board and the institutional review boards of all recruitment sites.
We recruited 347 patients. A total of 276 were interviewed, and 275 interviews were suitable for data analysis; 202 patients were from Wisconsin and 73 were from North Carolina (Appendix Table A1, online only). The majority (69%) had NSCLC. Respondents ranged in age from 30 to 92 years, were predominately white, with the vast majority having a history of smoking. Education level varied from high school to postbaccalaureate education. Fifty percent had Medicare for their insurance coverage. Not all individuals were able to provide all dates; thus, the number of patients analyzed for each period was variable.
We measured patient reports of intervals from time of first visit to a health care provider to treatment (Table 1). Median time from first visit to treatment (AI) was 52 days, with a range of 1 to 1,687 days. Individual time intervals are presented in waterfall plots (Fig 1). Twenty-nine percent of patients experienced a wait of 90 days or more for treatment after first presentation to a clinician. Analysis of the stage of disease among these patients indicated that 33% had advanced disease (NSCLC stage IIIB/IV; extensive-stage SCLC), 16% had locally advanced disease (NSCLC stage IIIA; limited-stage SCLC), 33% had localized disease (NSCLC stage I, II), and 17% had lung cancer of unknown stage. Overall, 28% of patients with SCLC experienced above-the-median time to treatment.
|
| Full Sample (N = 275) | Median by Site | ||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Interval | No. | Mean | SD | Min | Q1 | Median | Q3 | Max | Site 1 (n = 72) | Site 2 (n = 26) | Site 3 (n = 39) | Site 4 (n = 40) | Site 5 (n = 49) | Com. WI (n = 41) | Com. NC (n = 8) | P* | |
| AI | Initial presentation-treatment | 256 | 104.0 | 170.7 | 1 | 28.0 | 52.0 | 104.0 | 1687 | 67.5 | 55.0 | 45.0 | 47.5 | 33.0 | 76.0 | 60.0 | .108 |
| BI | Abnormal radiograph-treatment | 262 | 73.3 | 147.8 | 1 | 22.0 | 36.5 | 69.0 | 1687 | 41.0 | 48.0 | 36.0 | 30.0 | 23.5 | 60.0 | 35.5 | .018 |
| AC | Initial presentation-specialist referral | 238 | 51.6 | 127.0 | 0 | 2.0 | 9.5 | 42.2 | 1183 | 12.5 | 11.5 | 3.0 | 7.0 | 7.0 | 17.0 | 9.0 | .454 |
| CD | Specialist referral-specialist consultation | 228 | 8.9 | 12.6 | 0 | 2.0 | 4.5 | 12.0 | 119 | 6.0 | 3.0 | 3.0 | 4.0 | 4.0 | 7.0 | 5.0 | .416 |
| DI | Specialist consultation-treatment | 259 | 55.6 | 138.2 | 0 | 14.0 | 27.0 | 47.0 | 1430 | 27.0 | 42.5 | 25.0 | 26.0 | 17.0 | 37.5 | 34.5 | .018 |
| EF | First diagnostic test-last test | 259 | 42.4 | 141.9 | 0 | 5.0 | 13.0 | 29.0 | 1680 | 17.5 | 19.0 | 7.0 | 12.0 | 10.0 | 16.0 | 8.5 | .168 |
| AG | Initial presentation-confirmed diagnosis | 239 | 85.2 | 171.5 | 0 | 13.5 | 34.0 | 74.0 | 1656 | 42.0 | 45.0 | 30.5 | 28.0 | 22.0 | 48.0 | 43.0 | .454 |
| GI | Confirmed diagnosis-treatment | 227 | 20.0 | 20.9 | 0 | 7.0 | 15.0 | 27.0 | 180 | 20.5 | 22.0 | 13.0 | 15.0 | 8.5 | 24.0 | 18.0 | < .001 |
| HI | Treatment consultation-treatment | 254 | 25.9 | 91.0 | 0 | 7.0 | 16.0 | 26.0 | 1430 | 17.5 | 24.5 | 14.0 | 16.0 | 10.5 | 20.0 | 15.5 | .199 |
Site 1: a comprehensive cancer center affiliated with academic institution in Wisconsin. Sites 2 and 3: comprehensive cancer centers affiliated with academic institutions in North Carolina. Site 4: a community cancer center in Wisconsin. Site 5: a multispecialty clinic with multiple locations in Wisconsin.
Abbreviations: Com. NC, community recruitment in North Carolina; Com. WI, community recruitment in Wisconsin; min, minimum; max, maximum; Q1, first quartile; Q3, third quartile; SD, standard deviation.
*Holm adjusted P values for nine tests. Intervals GI, BI, and DI showed significant time differences between sites. Median (range) GI length for Site 5 (8.5 [0-48]) was significantly shorter than Com. WI (24 [1-76]; post hoc P = .002); Site 2 (22 [0-145]; post hoc P = .010); and Site 1 (20.5 [0-60]; post hoc P < .001). Median BI length for Site 5 (23.5 [3-570]) was significantly shorter than Com. WI (60 [6-275]; post hoc P = .006) and Site 2 (48 [6-158]; post hoc P = .045). Median DI length for Site 5 (17 [0-1399]) was significantly shorter than Com. WI (37.5 [4-237]; post hoc P = .005) and Site 2 (42.5 [1-207]; post hoc P = .024).
FIG 1. Waterfall plot showing the time to first treatment from initial visit to health care provider with symptoms indicative of lung cancer by stage of diagnosis: AI interval, from initial presentation to first treatment overall, and by stage. Advanced stage: NSCLC stage IIIB/IV; extensive stage SCLC, locally advanced stage: NSCLC stage IIIA; limited stage SCLC, localized stage: NSCLC stage I/II.
The median time from abnormal radiograph to treatment (BI) was 36.5 days; 16% experienced a wait of more than 90 days for treatment after the first lung abnormality was identified by imaging. The median time from initial presentation to specialist referral (AC) was 9.5 days; 13% of patients experienced a wait of more than 90 days for this interval. The median time from when the patient was informed that his or her biopsy was conclusive for lung cancer to the start of treatment (GI) was 15 days. Twenty-two percent of patients experienced more than a 30-day lapse between their biopsy results and the start of treatment. Using the RAND Corporation metric of optimum initiation of treatment within 42 days of NSCLC diagnosis and within 14 days of SCLC diagnosis,9 21% of NSCLC patients and 5% of SCLC patients in our study would be defined as having experienced treatment delays.
When patients were asked, “In your opinion, were there any unnecessary delays in diagnosing or treating your disease?” 26% answered affirmatively. Of those who perceived a delay, 39% believed this happened at the level of primary care, 11% at the point of referral, 23% at specialty care, 14% at treatment, and 44% at other points in the care continuum (percentages exceed 100 because some individuals perceived multiple delays). Of the patients who perceived a delay, 44% experienced a wait of more than 90 days from the first visit to treatment.
No significant differences between key time intervals were detected between Wisconsin (a low-incidence state) and North Carolina (a high-incidence state). Intervals BI, DI, and GI showed significant time differences between sites; patients treated in a fully integrated health care system, which supports continuity of care among primary, specialty, and hospital care (Site 5), experienced shorter time to treatment than at other sites (Table 1).
The majority of patients with extended time to treatment fell into two categories: incidental small nodules that were being monitored via serial CT scans and eventually progressed (appropriate delay) and missed diagnoses. Missed diagnoses occurred primarily at the level of primary care and in the emergency department. Avoidable delays in emergency care included lack of communication of positive radiologic findings to the primary care provider and/or patient. Other reasons for treatment delay included patient factors, such as change of insurance or patient choice to vacation between findings and treatment; clinical delays due to other health conditions or the need for respiratory therapy before surgery; and clinician or systems factors, such as delays in scheduling tests or specialist visits and lack of clinician follow-up on findings. When diagnostic work-ups were longer than the median time, it was often due to multiple clinical evaluations required for accurate staging. Notably, patients with deep vein thrombosis, seizures, or chest pain had relatively fast work-ups. Patients with cough, back pain, or other common symptoms took longer to identify as having lung cancer.
Patient examples for short, long, and median time to treatment are depicted in Fig 2. Short time to treatment was exemplified by recognition that a symptom was serious enough to warrant quick follow-up, and biopsy and treatment planning occurred expeditiously. Median time to treatment involved a primary care provider actively referring a patient to a specialist and a reasonable timeline for staging and treatment planning. A long time to treatment was due to a lack of suspicion of lung cancer from the primary care provider and pulmonologist.
FIG 2. Patient examples with time intervals. The presented narratives are paraphrased stories shared by the patients. A, first visit to primary care provider/any clinician with unusual symptoms or symptoms indicative of lung cancer; B, first imaging result with a lung abnormality (ie, a suspicious nodule or mass on an x-ray, computed tomography scan, etc.; if repeated scans, the date of the first scan); C, referral to a specialist (eg, pulmonologist, thoracic surgeon, oncologist, multidisciplinary lung cancer clinic); D, first visit to a specialist; E, first diagnostic test (any lung cancer-related evaluative procedure occurring after the first radiograph and before diagnosis, including any imaging tests after the initial radiograph); F, last diagnostic test that occurred before the beginning of treatment; G, patient was informed of the result of the initial biopsy confirming lung cancer; H, first referral to treatment (ie, the earliest date after initial radiography on which the patient was referred for radiation therapy, chemotherapy, targeted therapy, or a surgical treatment); and I, first treatment received (ie, the earliest date after diagnosis on which the patient received radiation therapy, chemotherapy, targeted therapy, or a surgical treatment). AI, time from initial presentation to treatment; BI, time from abnormal radiograph to treatment; AC, time from initial presentation to specialist referral; CD, time from specialist referral to specialist consultation; DI, time from specialist consultation to treatment; EF, time from first diagnostic test to last test; AG, time from initial presentation to confirmed diagnosis; GI, time from confirmed diagnosis to treatment; and HI, time from treatment consultation to treatment.
This study provides the first definition of typical time to treatment of patients with lung cancer across a variety of health systems in different US locales. Additionally, it is the first study to use patient reports of timeliness of care starting from the first presentation of symptoms indicative of lung cancer to a health care provider. Our study is also unique in that it includes a large sample of patients across the full spectrum of disease stages and types.
We documented a 52-day median time to treatment from the first visit to a health care provider and a 36.5-day median time to treatment from the first abnormal radiography result. The latter interval is shorter than median times for the same interval in published VA studies, which ranged from 63 to 84 days.13,14,18-20 In our study, the median time a patient waited between hearing the biopsy result and treatment was 15 days, which was, again, better than the median time for a similar interval in the VA studies, which ranged from 22 to 28 days.14,18,20 The same time interval was measured in a study using the National Cancer Data Base; the reported median was 34 days for patients diagnosed and treated in the same hospital and 40 days for patients diagnosed and treated in different hospitals.21 In another study conducted at three hospitals affiliated with an academic medical center, the median time from confirmed diagnosis to first treatment was 33 days.12 Our results may reflect a true difference between the samples, or they may indicate global improvements in time to treatment in the years between earlier studies and ours. Importantly, our analysis revealed no significant differences between Wisconsin and North Carolina, suggesting these results may apply broadly.
British guidelines suggest an interval of no more than 62 days from referral to specialist to treatment of lung cancer.6 The Dutch national practice guideline for NSCLC staging and treatment recommends that the diagnostic trajectory be completed within 21 calendar days from the first visit to a pulmonologist and that therapy be started within 35 days from the first visit to a pulmonologist.22 Our median results are in keeping with these time frames. However, more than one fifth of the NSCLC patients in our sample would be defined as having experienced treatment delays per RAND Corporation guidelines.9 Future guidelines should determine under which scenarios timelines of this length represent avoidable delays in care.
Consistent with other studies,12-14,20,21 we observed extreme variability in time to treatment of patients with lung cancer. Notably, more than one quarter of patients in our study perceived delays in their care, and our analysis of patients with longer timelines identified avoidable delays at all points in the care continuum. One study assessing patient perceptions of care identified delays as causing physical or mental harm, suggesting a role for such patient-reported outcomes in quality metrics.23
Because the US medical system is diverse, each health care organization must examine the pathways by which patients with lung cancer arrive at their doors—and what happens afterward—to determine opportunities for improvements. Multiple approaches have been tested globally and may inform improvement efforts in the United States. A Time to Treat Program was implemented at the University of Toronto and reduced the time from suspicion of lung cancer to diagnosis from 128 to 20 days.24 This improvement was accomplished through creating stronger links between multidepartmental patient care, instituting a navigator for care coordination, diagnostic and treatment algorithms, and changes in scheduling. In one study in the United Kingdom, patients were randomly assigned to usual outpatient care versus admission to a central hospital, where staging CT, bronchoscopy, and biopsy were performed.25 This centralized approach reduced time to treatment by 4 weeks, which resulted in more eligible patients receiving curative treatment and increased patient satisfaction. With recent advances in targeted therapy and immunotherapy,26 there is more opportunity than ever to treat even advanced-stage patients with significant life-prolonging options, but only if their health does not decline substantially before treatment. Nearly one third of patients in our sample who experienced an extreme delay in care (more than 90 days from first presentation to treatment) were advanced-stage patients. These findings indicate existing room for improvement with respect to timeliness of lung cancer care.
Regardless of the process a health system uses, any given care setting cannot improve time to treatment of lung cancer without measuring it. Having established standards and national benchmarks is also instrumental in the improvement process. Because we examined time to treatment in various locations, among diverse groups of patients with diverse stages of cancer, we believe our results are largely indicative of routinely achievable time-to-treatment scenarios in the United States. We therefore suggest that future guideline developers consider that 52 days, the median time we observed from first presentation to treatment, be set as the maximum desirable time to treatment of patients with lung cancer. Exceptions to this desired maximum time may be warranted, such as for the presence of small lesions that may not pose a large risk to the health of the patient. Future research may clarify how differences in disease stage, patient comorbidities, and other patient-specific considerations can inform time-to-treatment guidelines.
Although patients were encouraged to use appointment/discharge summaries, medical bills, calendars, and family members as sources of information when responding to questions, this study relied on recall. In addition to recruiting from academic and community practices, we also performed community recruitment, but this method resulted in low recruitment and challenges in obtaining pathology information through medical records release authorizations. A convenience sample was used, which is inherently limited; however, all stages of NSCLC and SCLC were represented. Data collection through patient interviews may have led to oversampling of patients with delays. Because we recruited a smaller sample than planned, the study had low (13%) statistical power to detect differences between states.
Further, this study was undertaken soon after the results of the National Lung Screening Trial were released.27 With lung cancer screening becoming more integrated into clinical practice, clinicians today may be more apt to find and follow small lesions according to established guidelines,8,28 which may lead to faster time to treatment.
We also did not discern appropriate clinical delay to treatment, such as awaiting results of molecular tumor testing to define targeted therapy opportunities, which can take up to 2 weeks after biopsy. As more targets and effective therapies are found, this delay could become more commonplace and therefore should be accommodated in time-to-treatment guidelines. Other emerging diagnostic procedures may appropriately delay the start of therapy.
In conclusion, this study documented a 52-day median time to treatment of lung cancer from first presentation to a health care provider with symptoms indicative of this disease. We recommend using this median time as a benchmark for optimum time to lung cancer treatment, except for small lesions that can be conservatively observed. Many delays in lung cancer care are avoidable through optimized clinical management, which may require individualized clinical pathways, depending on the health care system.
Acknowledgment
This study was supported by an independent medical educational grant from Pfizer. T.C.C. is also supported by the Cambia Foundation’s Sojourns Scholar Leadership Program, which had no role in the design, analysis, or writing of the manuscript. We thank the principal investigators and research teams at the research sites for recruitment of the study participants, and Kurt Oettel, MD, Jessica Donington, MD, and Chris Slatore, MD, for their critical comments on the manuscript. R.M.V. began this work while employed by Free to Breathe (formerly National Lung Cancer Partnership).
Conception and design: Regina M. Vidaver, Marianna B. Shershneva
Administrative support: Marianna B. Shershneva, Toby C. Campbell
Provision of study materials: Toby C. Campbell
Collection and assembly of data: Marianna B. Shershneva
Data analysis and interpretation: All authors
Manuscript writing: All authors
Final approval of manuscript: All authors
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or jop.ascopubs.org/site/misc/ifc.xhtml.
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|
| Characteristic | NC (n = 73) No. (%) | WI (n = 202) No. (%) |
|---|---|---|
| Age, years* | 63.4 (10.9) | 65.5 (9.5) |
| Race | ||
| White | 51 (69.9) | 187 (92.6) |
| African American | 17 (23.3) | 3 (1.5) |
| Other | 5 (6.8) | 12 (5.9) |
| Education | ||
| No HS diploma | 8 (11.0) | 18 (8.9) |
| HS graduate/GED | 18 (24.7) | 80 (39.6) |
| Some college | 24 (32.9) | 59 (29.2) |
| College graduate | 12 (16.4) | 22 (10.9) |
| Postgraduate study | 11 (15.1) | 23 (11.4) |
| Employer insurance - yes | 31 (42.5) | 74 (36.6) |
| Individual insurance - yes | 6 (8.2) | 32 (15.8) |
| Medicare insurance - yes | 30 (41.1) | 108 (53.5) |
| Medicare supplement insurance - yes | 11 (15.1) | 45 (22.3) |
| Medicaid/equivalent insurance - yes | 11 (15.1) | 27 (13.4) |
| Veteran's insurance - yes | 6 (8.2) | 3 (1.5) |
| Other insurance - yes | 12 (16.4) | 39 (19.3) |
Abbreviations: HS, high school; NC, North Carolina; WI, Wisconsin.
*Data are reported as mean (SD) for age and No. (%) for all other characteristics.
