In the initial evaluation of prostate cancer (the most-commonly diagnosed non-cutaneous malignancy among US men), a patient's chances of receiving guideline-concordant imaging may be more dependent on where he lives than on his disease characteristics. Clinicians use imaging variably across regions where the setting on a thermostat may be dialed up high in some areas, where most patients receive scans, and dialed down low in other areas where few are scanned.
This suggests policies focused solely on reducing inappropriate imaging might simply dial the thermostat down, potentially risking a reduction in appropriate imaging. In order to design and implement policies to optimize prostate cancer imaging, it is important to understand regional variation in prostate cancer imaging and the extent to which the thermostat model contributes to it.
This Career Development Award focused on understanding these principles and informing an implementation effort to decrease inappropriate prostate cancer imaging across VHA.
The goals of this research project were to understand the scope, the causes and the effects of regional variation in prostate cancer imaging.
The goals of this CDA were to provide training to the awardee as he became an independently funded leader in urologic health services research and implementation science.
In Specific Aim #1, the candidate tested the thermostat model in data from the VA Central Cancer Registry and SEER-Medicare, systems with different payment models, system structures, and eligibility criteria. Aim #1 also explored imaging patterns in the country of Sweden, another healthcare system without direct physician financial incentives.
To understand further the potential causes of imaging variation the project explored regional prostate cancer imaging rates across delivery systems (Specific Aim #2) and contributed further depth and detail to these data through semi-structured interviews (Specific Aim #3) to determine physicians' and patients' attitudes regarding imaging.
To determine the effects of regional imaging variation, the candidate is constructing a decision analytic model (Specific Aim #4) assessing the tradeoffs in cost and disease detection of various imaging strategies. These model-based strategies will be compared to current care in order to determine the magnitude of possible benefit which a new strategy might deliver.
Specific Aim #1: A project assessing the outcomes of a Swedish effort to provide data on prostate cancer imaging use and imaging guidelines to clinicians was associated with a reduction in inappropriate imaging over a 10-year period, as well as slightly decreased appropriate imaging in high-risk patients. This finding confirms the presence of the thermostat model in a model without direct financial incentives for medical providers and has important implications for implementation of a program to reduce inappropriate prostate cancer imaging in the VA.
We also assessed imaging utilization among Veterans using VACCR data. We found high rates of inappropriate imaging among men with low risk prostate cancer (41%) as well as lower than optimal rates of appropriate imaging among men with high risk prostate cancer (70%). Veterans who utilized Medicare-reimbursed care outside the VA had higher rates of inappropriate imaging but not necessarily higher rates of appropriate imaging. Despite the VA providing a centralized organizational structure, facilitating the efficient flow of information and policy, and providing a compensation structure which dissociates payment from the volume of services delivered, the imaging rates seen in the VA were not dissimilar from those observed among patients treated in a fee-for-service Medicare setting, though inappropriate imaging was somewhat reduced.
Specific Aim #2: We sought to determine the effect of health care system on the appropriateness of care. To do this, we had to create a novel dataset combining SEER-Medicare and VA data. During this past year, we completed the clean-up and merging of the VACCR and SEER-Medicare data - no small feat! We created a novel facility volume variable to try and adjust for potential differences in quality. Regardless of whether this variable is included, it seems that, for appropriate care, there is no difference between patients treated in the VA, patients treated in Medicare, or VA patients who sought care outside the VA. However, inappropriate care is more like to happen among patients treated in Medicare or VA patients who sought care outside the VA, as compared to patients cared for only in the VA. The project was presented as a podium presentation at the 2015 HSR&D meeting and the manuscript has been submitted for review.
Specific Aim #3: This qualitative aim sought to determine the reasons patients and physicians order prostate cancer imaging. We used a qualitative approach explore patient and provider knowledge and behaviors relating to the use of imaging. We conducted 39 semi-structured interviews total including 22 interviews with patients newly diagnosed with prostate cancer and 17 interviews with physicians caring for them at three VAMCs representing a broad spectrum of inappropriate imaging rates. After core theoretical concepts were identified, the Theoretical Domains Framework (TDF) was selected to explore linkages between themes within the dataset and existing domains within the framework. Themes from patient interviews were categorized within four TDF domains. Patients reported little interest in staging as compared to disease treatment (goals) and many could not remember if they had imaging at all (knowledge). Participants tended to "trust their doctor" to make decisions about appropriate tests (beliefs about capabilities). Some patients expressed a minor concern for radiation exposure, but concern about cancer outcomes outweighed these fears (emotion). Themes from physician interviews were categorized within five TDF domains. Most physicians self-reported that they know and trust imaging guidelines (knowledge) yet some are still likely to follow their own intuition, whether due to clinical suspicion and/or years of experience (beliefs about capabilities). Additionally, physicians reported that medico-legal concerns, fear of missing associated diagnoses (beliefs about consequences), influence from colleagues who image frequently (social influences) and the facility where they practice influences rates of imaging (environmental context). Interviews with patients and physicians suggest that physicians are the primary (and in some cases only) decision-makers regarding staging imaging for prostate cancer. This finding suggests a physician-targeted intervention may be the most effective strategy to improve guideline-concordant prostate cancer imaging. We have completed the project and published our findings in Implementation Science.
For Specific Aim #4 the decision analytic aim, we have amassed background data to determine the consequences associated with false positives and incidental findings from diagnostic imaging procedures performed in low-risk patients. We retrospectively reviewed positive prostate cancer biopsies from the Manhattan VA Health care system. Imaging (CT, MRI, bone scan) use was assessed among patients with low-risk disease, for whom the 2015 NCCN Prostate Cancer imaging guidelines recommend against advanced imaging and among high risk patient for whom imaging is recommended. The rate of inappropriate imaging was calculated based on the cohort of low risk men; 75% were classified as low risk prostate cancer and 25% as high risk prostate cancer. Of the men with low risk Pca, 17% underwent inappropriate staging imaging. Of these, 63% had follow up imaging for incidental findings: this is the false positive rate, which is alarming high. Highlighting the negative effects of inappropriate imaging will likely aid to decrease overuse of health care resources and improve quality of care. We are currently finalizing this manuscript. We have also completed the literature review and are building the decision tree for a decision analytic model.
Understanding the scope, causes and effects of unwanted regional imaging variation has begun to suggest important strategies to control this problem. The findings from this project, especially the qualitative data on barriers to utilization of imaging guidelines, have informed a VA Investigator Initiated Research grant 1 I01 HX002038-01A2, "A multi-modal, physician-centered intervention to improve guideline-concordant prostate cancer imaging," which has been recommended for funding by HSRD. This is a 10 site implementation trial of a physician focused behavioral intervention to improve guideline-concordant imaging to stage men with incident prostate cancer. The trial should start in February 2018.
- Becker DJ, Levy BP, Gold HT, Sherman SE, Makarov DV, Schreiber D, Wisnivesky JP, Pass HI. Influence of Extent of Lymph Node Evaluation on Survival for Pathologically Lymph Node Negative Non-Small Cell Lung Cancer. American journal of clinical oncology. 2018 Aug 1; 41(8):820-825.
- Ciprut S, Sedlander E, Watts KL, Matulewicz RS, Stange KC, Sherman SE, Makarov DV. Designing a theory-based intervention to improve the guideline-concordant use of imaging to stage incident prostate cancer. Urologic oncology. 2018 May 1; 36(5):246-251.
- Sanda MG, Cadeddu JA, Kirkby E, Chen RC, Crispino T, Fontanarosa J, Freedland SJ, Greene K, Klotz LH, Makarov DV, Nelson JB, Rodrigues G, Sandler HM, Taplin ME, Treadwell JR. Clinically Localized Prostate Cancer: AUA/ASTRO/SUO Guideline. Part I: Risk Stratification, Shared Decision Making, and Care Options. The Journal of urology. 2018 Mar 1; 199(3):683-690.
- Kirk PS, Borza T, Shahinian VB, Caram MEV, Makarov DV, Shelton JB, Leppert JT, Blake RM, Davis JA, Hollenbeck BK, Sales A, Skolarus TA. The implications of baseline bone-health assessment at initiation of androgen-deprivation therapy for prostate cancer. BJU international. 2018 Apr 1; 121(4):558-564.
- Gyftopoulos S, Smith SW, Simon E, Kuznetsova M, Horwitz LI, Makarov DV. Qualitative Study to Understand Ordering of CT Angiography to Diagnose Pulmonary Embolism in the Emergency Room Setting. Journal of the American College of Radiology : JACR. 2018 Sep 1; 15(9):1276-1284.
- Stone BV, Cohn MR, Donin NM, Schulster M, Wysock JS, Makarov DV, Bjurlin MA. Evaluation of Unplanned Hospital Readmissions After Major Urologic Inpatient Surgery in the Era of Accountable Care. Urology. 2017 Nov 1; 109:94-100.
- Becker DJ, Lin D, Lee S, Levy BP, Makarov DV, Gold HT, Sherman S. Exploration of the ASCO and ESMO Value Frameworks for Antineoplastic Drugs. Journal of oncology practice / American Society of Clinical Oncology. 2017 Jul 1; 13(7):e653-e665.
- Mittakanti HR, Thomas IC, Shelton JB, Makarov DV, Skolarus TA, Cooperberg MR, Chung BI, Sonn GA, Brooks JD, Leppert JT. Accuracy of Prostate-Specific Antigen Values in Prostate Cancer Registries. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2016 Oct 10; 34(29):3586-3587.
- Makarov DV, Sedlander E, Braithwaite RS, Sherman SE, Zeliadt S, Gross CP, Curnyn C, Shedlin M. A qualitative study to understand guideline-discordant use of imaging to stage incident prostate cancer. Implementation science : IS. 2016 Sep 2; 11(1):118.
- Makarov DV, Chrouser K, Gore JL, Marachie J, Nielsen ME, Tessier C, Fagerlin A. AUA White Paper on Implementation of Shared Decision Making into Urological Practice. The Journal of urology. 2016 Sep 1; 3(5):355-363.
- Loeb S, Folkvaljon Y, Robinson D, Makarov DV, Bratt O, Garmo H, Stattin P. Immediate versus delayed prostatectomy: Nationwide population-based study (.). Scandinavian journal of urology. 2016 Aug 1; 50(4):246-54.
- Makarov DV, Li H, Lepor H, Gross CP, Blustein J. Teaching Hospitals and the Disconnect Between Technology Adoption and Comparative Effectiveness Research: The Case of the Surgical Robot. Medical care research and review : MCRR. 2017 Jun 1; 74(3):369-376.
- Loeb S, Walter D, Curnyn C, Gold HT, Lepor H, Makarov DV. How Active is Active Surveillance? Intensity of Followup during Active Surveillance for Prostate Cancer in the United States. The Journal of urology. 2016 Sep 1; 196(3):721-6.
- Guma S, Maglantay R, Lau R, Wieczorek R, Melamed J, Deng FM, Zhou M, Makarov D, Lee P, Pincus MR, Pei ZH. Papillary urothelial carcinoma with squamous differentiation in association with human papilloma virus: case report and literature review. American journal of clinical and experimental urology. 2016 Jan 28; 4(1):12-6.
- Wollin DA, Makarov DV. Guideline of Guidelines: Imaging of Localized Prostate Cancer. BJU international. 2015 Oct 1; 116(4):526-30.
- Makarov DV, Hu EY, Walter D, Braithwaite RS, Sherman S, Gold HT, Zhou XH, Gross CP, Zeliadt SB. Appropriateness of Prostate Cancer Imaging among Veterans in a Delivery System without Incentives for Overutilization. Health services research. 2016 Jun 1; 51(3):1021-51.
- Bratt O, Folkvaljon Y, Hjälm Eriksson M, Akre O, Carlsson S, Drevin L, Franck Lissbrant I, Makarov D, Loeb S, Stattin P. Undertreatment of Men in Their Seventies with High-risk Nonmetastatic Prostate Cancer. European Urology. 2015 Jul 1; 68(1):53-8.
- Prabhu V, Lee T, Loeb S, Holmes JH, Gold HT, Lepor H, Penson DF, Makarov DV. Twitter response to the United States Preventive Services Task Force recommendations against screening with prostate-specific antigen. BJU international. 2015 Jul 1; 116(1):65-71.
- Makarov DV, Soulos PR, Gold HT, Yu JB, Sen S, Ross JS, Gross CP. Regional-Level Correlations in Inappropriate Imaging Rates for Prostate and Breast Cancers: Potential Implications for the Choosing Wisely Campaign. JAMA oncology. 2015 May 1; 1(2):185-94.
- Borofsky MS, Walter D, Li H, Shah O, Goldfarb DS, Sosa RE, Makarov DV. Institutional characteristics associated with receipt of emergency care for obstructive pyelonephritis at community hospitals. The Journal of urology. 2015 Mar 1; 193(3):851-6.
- Loeb S, Folkvaljon Y, Makarov DV, Bratt O, Bill-Axelson A, Stattin P. Five-year nationwide follow-up study of active surveillance for prostate cancer. European Urology. 2015 Feb 1; 67(2):233-8.
- Sivarajan G, Taksler GB, Walter D, Gross CP, Sosa RE, Makarov DV. The Effect of the Diffusion of the Surgical Robot on the Hospital-level Utilization of Partial Nephrectomy. Medical care. 2015 Jan 1; 53(1):71-8.
- Acosta-Gonzalez G, Qin J, Wieczorek R, Melamed J, Deng FM, Zhou M, Makarov D, Ye F, Pei Z, Pincus MR, Lee P. De novo large cell neuroendocrine carcinoma of the prostate, case report and literature review. American journal of clinical and experimental urology. 2014 Dec 25; 2(4):337-42.
- Li H, Gail MH, Braithwaite RS, Gold HT, Walter D, Liu M, Gross CP, Makarov DV. Are hospitals “keeping up with the Joneses”?: Assessing the spatial and temporal diffusion of the surgical robot. Healthcare (Amsterdam, Netherlands). 2014 Jul 1; 2(2):152-157.
- Wollin DA, Makarov D. Extended pelvic lymph node dissection for prostate cancer: do more nodes mean better survival? Oncology (Williston Park, N.Y.). 2014 Jul 1; 28(7):601-2.
- Batouli A, Jahanshahi P, Gross CP, Makarov DV, Yu JB. The global cancer divide: relationships between national healthcare resources and cancer outcomes in high-income vs. middle- and low-income countries. Journal of epidemiology and global health. 2014 Jun 1; 4(2):115-24.
- McClintock TR, Chen Y, Parvez F, Makarov DV, Ge W, Islam T, Ahmed A, Rakibuz-Zaman M, Hasan R, Sarwar G, Slavkovich V, Bjurlin MA, Graziano JH, Ahsan H. Association between arsenic exposure from drinking water and hematuria: results from the Health Effects of Arsenic Longitudinal Study. Toxicology and applied pharmacology. 2014 Apr 1; 276(1):21-7.
- Prabhu V, Taksler GB, Sivarajan G, Laze J, Makarov DV, Lepor H. Radical prostatectomy improves and prevents age dependent progression of lower urinary tract symptoms. The Journal of urology. 2014 Feb 1; 191(2):412-7.
- Ma X, Wang R, Long JB, Ross JS, Soulos PR, Yu JB, Makarov DV, Gold HT, Gross CP. The cost implications of prostate cancer screening in the Medicare population. Cancer. 2014 Jan 1; 120(1):96-102.
- Wei J, Wang Z, Makarov D, Li X. Current treatments and novel therapeutic targets for castration resistant prostate cancer with bone metastasis. American journal of clinical and experimental urology. 2013 Dec 25; 1(1):30-8.
- Bjurlin MA, Makarov DV. Reply: To PMID 24295245. Urology. 2013 Dec 1; 82(6):1289-90.
- Bjurlin MA, Walter D, Taksler GB, Huang WC, Wysock JS, Sivarajan G, Loeb S, Taneja SS, Makarov DV. National trends in the utilization of partial nephrectomy before and after the establishment of AUA guidelines for the management of renal masses. Urology. 2013 Dec 1; 82(6):1283-9.
- Makarov DV, Loeb S, Ulmert D, Drevin L, Lambe M, Stattin P. Prostate cancer imaging trends after a nationwide effort to discourage inappropriate prostate cancer imaging. Journal of the National Cancer Institute. 2013 Sep 4; 105(17):1306-13.
- Lloyd S, Buscariollo DL, Gross CP, Makarov DV, Yu JB. Determinants of enrollment in cancer clinical trials: the relationship between the current state of knowledge, societal disease burden, and randomized clinical trial enrollment. Journal of the National Comprehensive Cancer Network : JNCCN. 2013 Aug 1; 11(8):928-36.
- Borofsky MS, Makarov DV. Take home messages: outcomes analysis. American Urology Association AUA News. 2013 Jul 1; 18(7):7.
- Borofsky MS, Walter D, Shah O, Goldfarb DS, Mues AC, Makarov DV. Surgical decompression is associated with decreased mortality in patients with sepsis and ureteral calculi. The Journal of urology. 2013 Mar 1; 189(3):946-51.
- Anderson CB, Penson DF, Ni S, Makarov DV, Barocas DA. Centralization of radical prostatectomy in the United States. The Journal of urology. 2013 Feb 1; 189(2):500-6.
- Borofsky MS, Ohmann E, Makarov DV. The transition to value-based care in urology. AUA update series. 2013 Jan 1; 32(31):309-320.
- Prabhu V, Alukal JP, Laze J, Makarov DV, Lepor H. Long-term satisfaction and predictors of use of intracorporeal injections for post-prostatectomy erectile dysfunction. The Journal of urology. 2013 Jan 1; 189(1):238-42.
- Presley CJ, Raldow AC, Cramer LD, Soulos PR, Long JB, Yu JB, Makarov DV, Gross CP. A new approach to understanding racial disparities in prostate cancer treatment. Journal of geriatric oncology. 2013 Jan 1; 4(1):1-8.
- Makarov DV, Yu JB, Desai RA, Penson DF, Gross CP. The association between diffusion of the surgical robot and radical prostatectomy rates. Medical care. 2011 Apr 1; 49(4):333-9.
- Loeb S, Stork B, Gold HT, Stout NK, Makarov DV, Weight CJ, Borgmann H. Tweet this: how advocacy for breast and prostate cancers stacks up on social media. BJU international. 2017 Jun 7; 120(4):461-463.
- Makarov DV, Holmes-Rovner M, Rovner DR, Averch T, Barry MJ, Chrouser K, Gee WF, Goodrich K, Haynes M, Krahn M, Saigal C, Sox HC, Stacey D, Tessier C, Waterhouse RL, Fagerlin A. Shared Decision Making and Prostate Cancer Screening [White paper] American Urological Association and Society for Medical Decision Making Quality Improvement Summit Proceedings. [Abstract]. Urology Practice. 2016 Apr 2; https://doi.org/10.1016/j.urpr.2017.11.005.
Online News Media Articles
- Makarov DV, Fagerlin A, Chrouser K, Gore JL, Maranchie J, Nielsen ME, Saigal C, Tessier C. AUA White Paper on Implementation of Shared Decision Making into Urological Practice. American Urological Association Guidelines [Internet]. 2015 Jan 1. Available from: http://www.auanet.org/guidelines/shared-decision-making.
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Diagnosis, Technology Development and Assessment