Abstract
Background
Access to high-quality cancer care is affected by environmental exposures and structural inequities. This study sought to investigate the association between the environmental quality index (EQI) and achievement of textbook outcomes (TO) among Medicare beneficiaries over the age of 65 who underwent surgical resection for early-stage pancreatic adenocarcinoma (PDAC).
Methods
Patients diagnosed with early-stage PDAC from 2004 to 2015 were identified using the SEER-Medicare database and combined with the US Environmental Protection Agency’s EQI data. High EQI category indicated poor environmental quality, whereas low EQI indicated better environmental conditions.
Results
A total of 5,310 patients were included, of which 45.0% (n = 2,387) patients achieved TO. Median age was 73 years and more than half were female (n = 2,807, 52.9%), married (n = 3,280, 61.8%), and resided in the Western region of the US (n = 2,712, 51.1%). On multivariable analysis, patients residing in moderate and high EQI counties were less likely to achieve a TO (referent: low EQI; moderate EQI: OR 0.66, 95% CI 0.46–0.95; high EQI: OR 0.65, 95% CI 0.45–0.94; p < 0.05). Increasing age (OR 0.98, 95%CI 0.97–0.99), racial minorities (OR 0.73, 95% CI 0.63–0.85), having a Charlson co-morbidity index > 2 (OR 0.54, 95%CI 0.47–0.61) and stage II disease (OR 0.82, 95%CI 0.71–0.96) were also associated with not achieving a TO (all p < 0.001).
Conclusion
Older Medicare patients residing in moderate or high EQI counties were less likely to achieve an “optimal” TO after surgery. These results demonstrate that environmental factors may drive post-operative outcomes among patients with PDAC.
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References
Barlass U, Deshmukh A, Beck T, Bishehsari F. Opioid use as a potential risk factor for pancreatic cancer in the United States: An analysis of state and national level databases. PLoS ONE. 2021 [accessed 2022 Dec 21];16(1). /pmc/articles/PMC7787381/. https://doi.org/10.1371/JOURNAL.PONE.0244285
Khalaf N, El-Serag HB, Abrams HR, Thrift AP. Burden of Pancreatic Cancer: From Epidemiology to Practice. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. 2021 [accessed 2022 Dec 21];19(5):876–884. https://pubmed.ncbi.nlm.nih.gov/32147593/. https://doi.org/10.1016/J.CGH.2020.02.054
Shavers VL, Brown ML. Racial and ethnic disparities in the receipt of cancer treatment. Journal of the National Cancer Institute. 2002 [accessed 2022 Oct 30];94(5):334–357. https://pubmed.ncbi.nlm.nih.gov/11880473/. https://doi.org/10.1093/JNCI/94.5.334
Basu A, Ghosh D, Mandal B, Mukherjee P, Maji A. Barriers and explanatory mechanisms in diagnostic delay in four cancers – A health-care disparity? South Asian Journal of Cancer. 2019 [accessed 2022 Oct 30];8(4):221. /pmc/articles/PMC6852640/. https://doi.org/10.4103/SAJC.SAJC_311_18
Fu SJ, George EL, Maggio PM, Hawn M, Nazerali R. The Consequences of Delaying Elective Surgery: Surgical Perspective. Annals of surgery. 2020 [accessed 2022 Oct 30];272(2):e79–e80. https://pubmed.ncbi.nlm.nih.gov/32675504/. https://doi.org/10.1097/SLA.0000000000003998
Benson AB, Abrams TA, Ben-Josef E, Bloomston PM, Botha JF, Clary BM, Covey A, Curley SA, D’Angelica MI, Davila R, et al. Hepatobiliary Cancers: Clinical Practice Guidelines in OncologyTM. Journal of the National Comprehensive Cancer Network : JNCCN. 2009 [accessed 2022 Oct 30];7(4):350. /pmc/articles/PMC4461147/. https://doi.org/10.6004/JNCCN.2009.0027
Thornton RLJ, Glover CM, Cené CW, Glik DC, Henderson JA, Williams DR. Evaluating Strategies For Reducing Health Disparities By Addressing The Social Determinants Of Health. Health affairs (Project Hope). 2016 [accessed 2022 Oct 30];35(8):1416–1423. https://pubmed.ncbi.nlm.nih.gov/27503966/. https://doi.org/10.1377/HLTHAFF.2015.1357
Diaz A, Hyer JM, Barmash E, Azap R, Paredes AZ, Pawlik TM. County-level Social Vulnerability is Associated with Worse Surgical Outcomes Especially among Minority Patients. Annals of Surgery. 2021 [accessed 2022 Oct 30];274(6):881–891. https://journals.lww.com/annalsofsurgery/Fulltext/2021/12000/County_level_Social_Vulnerability_is_Associated.1.aspx. https://doi.org/10.1097/SLA.0000000000004691
Kind AJH, Buckingham WR. Making Neighborhood-Disadvantage Metrics Accessible — The Neighborhood Atlas. The New England journal of medicine. 2018 [accessed 2022 Oct 30];378(26):2456. /pmc/articles/PMC6051533/. https://doi.org/10.1056/NEJMP1802313
Kolak M, Bhatt J, Park YH, Padrón NA, Molefe A. Quantification of Neighborhood-Level Social Determinants of Health in the Continental United States. JAMA network open. 2020 [accessed 2022 Oct 30];3(1). https://pubmed.ncbi.nlm.nih.gov/31995211/. https://doi.org/10.1001/JAMANETWORKOPEN.2019.19928
Arcaya MC, Tucker-Seeley RD, Kim R, Schnake-Mahl A, So M, Subramanian S v. Research on neighborhood effects on health in the United States: A systematic review of study characteristics. Social science & medicine (1982). 2016 [accessed 2022 Oct 30];168:16–29. https://pubmed.ncbi.nlm.nih.gov/27637089/. https://doi.org/10.1016/J.SOCSCIMED.2016.08.047
McGinnis JM. Income, Life Expectancy, and Community Health: Underscoring the Opportunity. JAMA. 2016 [accessed 2022 Oct 30];315(16):1709–1710. https://pubmed.ncbi.nlm.nih.gov/27063840/. https://doi.org/10.1001/JAMA.2016.4729
Chetty R, Hendren N, Katz LF. The Effects of Exposure to Better Neighborhoods on Children: New Evidence from the Moving to Opportunity Experiment. The American economic review. 2016 [accessed 2022 Oct 30];106(4):855–902. https://pubmed.ncbi.nlm.nih.gov/29546974/. https://doi.org/10.1257/AER.20150572
DR W, C C. Racial residential segregation: a fundamental cause of racial disparities in health. Public health reports (Washington, D.C. : 1974). 2001 [accessed 2022 Oct 30];116(5):404–416. https://pubmed.ncbi.nlm.nih.gov/12042604/. https://doi.org/10.1093/PHR/116.5.404
Beyond Health Care: The Role of Social Determinants in Promoting Health and Health Equity | KFF. [accessed 2022 Oct 30]. https://www.kff.org/racial-equity-and-health-policy/issue-brief/beyond-health-care-the-role-of-social-determinants-in-promoting-health-and-health-equity/
Hahn RA, Truman BI, Williams DR. Civil rights as determinants of public health and racial and ethnic health equity: Health care, education, employment, and housing in the United States. SSM - population health. 2018 [accessed 2022 Oct 30];4:17–24. https://pubmed.ncbi.nlm.nih.gov/29250579/. https://doi.org/10.1016/J.SSMPH.2017.10.006
Closing the gap in a generation: health equity through action on the social determinants of health - Final report of the commission on social determinants of health. [accessed 2022 Oct 30]. https://www.who.int/publications/i/item/WHO-IER-CSDH-08.1
Peters A, Hoek G, Katsouyanni K. Understanding the link between environmental exposures and health: does the exposome promise too much? Journal of epidemiology and community health. 2012 [accessed 2022 Oct 30];66(2):103–105. https://pubmed.ncbi.nlm.nih.gov/22080817/. https://doi.org/10.1136/JECH-2011-200643
Messer LC, Jagai JS, Rappazzo KM, Lobdell DT. Construction of an environmental quality index for public health research. Environmental Health: A Global Access Science Source. 2014 [accessed 2022 Oct 30];13(1):1–22. https://ehjournal.biomedcentral.com/articles/https://doi.org/10.1186/1476-069X-13-39. https://doi.org/10.1186/1476-069X-13-39/TABLES/14
Jagai JS, Messer LC, Rappazzo KM, Gray CL, Grabich SC, Lobdell DT. County-level cumulative environmental quality associated with cancer incidence. Cancer. 2017 [accessed 2022 Oct 30];123(15):2901–2908. https://onlinelibrary.wiley.com/doi/full/https://doi.org/10.1002/cncr.30709. https://doi.org/10.1002/CNCR.30709
Environmental Quality Index (EQI) | US EPA. [accessed 2022 Oct 30]. https://www.epa.gov/healthresearch/environmental-quality-index-eqi
Lobdell DT, Jagai JS, Rappazzo K, Messer LC. Data sources for an environmental quality index: Availability, quality, and utility. American Journal of Public Health. 2011 [accessed 2022 Oct 30];101(SUPPL. 1). https://doi.org/10.2105/AJPH.2011.300184
Messer LC, Jagai JS, Rappazzo KM, Lobdell DT. Construction of an environmental quality index for public health research. Environmental Health: A Global Access Science Source. 2014 [accessed 2022 Oct 30];13(1). https://doi.org/10.1186/1476-069X-13-39
Krajewski AK, Rappazzo KM, Langlois PH, Messer LC, Lobdell DT. Associations between cumulative environmental quality and ten selected birth defects in Texas. Birth Defects Research. 2021 [accessed 2022 Oct 30];113(2):161–172. https://doi.org/10.1002/BDR2.1788
Gray CL, Lobdell DT, Rappazzo KM, Jian Y, Jagai JS, Messer LC, Patel AP, DeFlorio-Barker SA, Lyttle C, Solway J, et al. Associations between environmental quality and adult asthma prevalence in medical claims data. Environmental Research. 2018 [accessed 2022 Oct 30];166:529–536. https://doi.org/10.1016/J.ENVRES.2018.06.020
Jagai JS, Krajewski AK, Shaikh S, Lobdell DT, Sargis RM. Association between environmental quality and diabetes in the USA. Journal of Diabetes Investigation. 2020 [accessed 2022 Oct 30];11(2):315–324. https://doi.org/10.1111/JDI.13152
Patel AP, Jagai JS, Messer LC, Gray CL, Rappazzo KM, Deflorio-Barker SA, Lobdell DT. Associations between environmental quality and infant mortality in the United States, 2000–2005. Archives of Public Health. 2018 [accessed 2022 Oct 30];76(1). https://doi.org/10.1186/S13690-018-0306-0
Shapiro M, Chen Q, Huang Q, Boosalis VA, Yoon CH, Saund MS, Whang EE, Gold JS. Associations of socioeconomic variables with resection, stage, and survival in patients with early-stage pancreatic cancer. JAMA Surgery. 2016 [accessed 2022 Dec 17];151(4):338–345. https://doi.org/10.1001/jamasurg.2015.4239
Pastrana Del Valle J, Mahvi DA, Fairweather M, Wang J, Clancy TE, Ashley SW, Urman RD, Whang EE, Gold JS. Associations of gender, race, and ethnicity with disparities in short-term adverse outcomes after pancreatic resection for cancer. Journal of surgical oncology. 2022 [accessed 2022 Dec 17];125(4):646–657. https://pubmed.ncbi.nlm.nih.gov/34786728/. https://doi.org/10.1002/JSO.26748
Geographic Levels. [accessed 2022 Dec 11]. https://www.census.gov/programs-surveys/economic-census/guidance-geographies/levels.html
Quan H, Li B, Couris CM, Fushimi K, Graham P, Hider P, Januel JM, Sundararajan V. Updating and validating the Charlson comorbidity index and score for risk adjustment in hospital discharge abstracts using data from 6 countries. American journal of epidemiology. 2011 [accessed 2022 Oct 30];173(6):676–682. https://pubmed.ncbi.nlm.nih.gov/21330339/. https://doi.org/10.1093/AJE/KWQ433
Quan H, Sundararajan V, Halfon P, Fong A, Burnand B, Luthi JC, Saunders LD, Beck CA, Feasby TE, Ghali WA. Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Medical care. 2005 [accessed 2022 Oct 30];43(11):1130–1139. https://pubmed.ncbi.nlm.nih.gov/16224307/. https://doi.org/10.1097/01.MLR.0000182534.19832.83
Huang YQ, Gou R, Diao YS, Yin QH, Fan WX, Liang YP, Chen Y, Wu M, Zang L, Li L, et al. Charlson comorbidity index helps predict the risk of mortality for patients with type 2 diabetic nephropathy. Journal of Zhejiang University. Science. B. 2014 [accessed 2022 Oct 30];15(1):58–66. https://pubmed.ncbi.nlm.nih.gov/24390745/. https://doi.org/10.1631/JZUS.B1300109
U.S. Department of Agriculture Economic Research Service. Rural-Urban Continuum Codes. 2023. Accessed February 13, 2023. https://www.ers.usda.gov/data-products/rural-urban-continuum-codes/
County Health Rankings & Roadmaps. Explore Health Rankings. Rankings Data & Documentation. 2023. Accessed February 13, 2023. https://www.countyhealthrankings.org/explore-health-rankings/rankings-data-documentation
Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th Edition of the AJCC Cancer Staging Manual and the Future of TNM. [accessed 2022 Oct 30]. https://doi.org/10.1245/s10434-010-0985-4
Ramia JM, Soria-Aledo V. Textbook outcome: A new quality tool. Cirugía Española (English Edition). 2022 [accessed 2022 Oct 30];100(3):113–114. https://doi.org/10.1016/J.CIRENG.2021.06.021
Merath K, Chen Q, Bagante F, Beal E, Akgul O, Dillhoff M, Cloyd JM, Pawlik TM. Textbook Outcomes Among Medicare Patients Undergoing Hepatopancreatic Surgery. Annals of surgery. 2020 [accessed 2022 Oct 30];271(6):1116–1123. https://pubmed.ncbi.nlm.nih.gov/30499800/. https://doi.org/10.1097/SLA.0000000000003105
Social determinants of health. [accessed 2022 Dec 20]. https://www.who.int/health-topics/social-determinants-of-health#tab=tab_1
Braveman P, Gottlieb L. The social determinants of health: it’s time to consider the causes of the causes. Public health reports (Washington, D.C. : 1974). 2014 [accessed 2022 Dec 20];129 Suppl 2(Suppl 2):19–31. https://pubmed.ncbi.nlm.nih.gov/24385661/. https://doi.org/10.1177/00333549141291S206
Marmot M, Friel S, Bell R, Houweling TA, Taylor S. Closing the gap in a generation: health equity through action on the social determinants of health. Lancet (London, England). 2008 [accessed 2022 Dec 20];372(9650):1661–1669. https://pubmed.ncbi.nlm.nih.gov/18994664/. https://doi.org/10.1016/S0140-6736(08)61690-6
Singh SK, Singh R. Liver cancer incidence and mortality: Disparities based on age, ethnicity, health and nutrition, molecular factors, and geography. Cancer health disparities. 2020 [accessed 2022 Oct 30];4:e1. /pmc/articles/PMC8218735/
del Valle JP, Fillmore NR, Molina G, Fairweather M, Wang J, Clancy TE, Ashley SW, Urman RD, Whang EE, Gold JS. Socioeconomic disparities in pancreas cancer resection and survival in the Veterans Health Administration. Ann Surg Oncol. 2021 [accessed 2022 Oct 30];29(5):3194–3202. https://link.springer.com/article/https://doi.org/10.1245/s10434-021-11315-0. https://doi.org/10.1245/s10434-021-11250-0
Vick AD, Hery DN, Markowiak SF, Brunicardi FC. Closing the Disparity in Pancreatic Cancer Outcomes: A Closer Look at Nonmodifiable Factors and Their Potential Use in Treatment. Pancreas. 2019 [accessed 2022 Oct 30];48(2):242–249. https://pubmed.ncbi.nlm.nih.gov/30629027/. https://doi.org/10.1097/MPA.0000000000001238
Heller DR, Nicolson NG, Ahuja N, Khan S, Kunstman JW. Association of Treatment Inequity and Ancestry With Pancreatic Ductal Adenocarcinoma Survival. JAMA surgery. 2020 [accessed 2022 Oct 30];155(2). https://pubmed.ncbi.nlm.nih.gov/31800002/. https://doi.org/10.1001/JAMASURG.2019.5047
Social Determinants of Health - Healthy People 2030 | health.gov. [accessed 2022 Oct 30]. https://health.gov/healthypeople/priority-areas/social-determinants-health
Mehta R, Tsilimigras DI, Paredes AZ, Sahara K, Dillhoff M, Cloyd JM, Ejaz A, White S, Pawlik TM. Dedicated Cancer Centers are More Likely to Achieve a Textbook Outcome Following Hepatopancreatic Surgery. Annals of surgical oncology. 2020 [accessed 2022 Dec 20];27(6):1889–1897. https://pubmed.ncbi.nlm.nih.gov/32108924/. https://doi.org/10.1245/S10434-020-08279-Y
Kolfschoten NE, Kievit J, Gooiker GA, van Leersum NJ, Snijders HS, Eddes EH, Tollenaar RAEM, Wouters MWJM, Marang-Van De Mheen PJ. Focusing on desired outcomes of care after colon cancer resections; hospital variations in “textbook outcome.” European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology. 2013 [accessed 2022 Oct 30];39(2):156–163. https://pubmed.ncbi.nlm.nih.gov/23102705/. https://doi.org/10.1016/J.EJSO.2012.10.007
Shwartz M, Restuccia JD, Rosen AK. Composite Measures of Health Care Provider Performance: A Description of Approaches. The Milbank quarterly. 2015 [accessed 2022 Oct 30];93(4):788–825. https://pubmed.ncbi.nlm.nih.gov/26626986/. https://doi.org/10.1111/1468-0009.12165
Nolan T, Berwick DM. All-or-none measurement raises the bar on performance. JAMA. 2006 [accessed 2022 Oct 30];295(10):1168–1170. https://pubmed.ncbi.nlm.nih.gov/16522838/. https://doi.org/10.1001/JAMA.295.10.1168
Reeves D, Campbell SM, Adams J, Shekelle PG, Kontopantelis E, Roland MO. Combining multiple indicators of clinical quality: an evaluation of different analytic approaches. Medical care. 2007 [accessed 2022 Oct 30];45(6):489–496. https://pubmed.ncbi.nlm.nih.gov/17515775/. https://doi.org/10.1097/MLR.0B013E31803BB479
Agarwal V, Thomas MJ, Joshi R, Chaudhari V, Bhandare M, Mitra A, deSouza A, Ambulkar R, Shrikhande S v. Improved Outcomes in 394 Pancreatic Cancer Resections: the Impact of Enhanced Recovery Pathway. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract. 2018 [accessed 2022 Dec 21];22(10):1732–1742. https://pubmed.ncbi.nlm.nih.gov/29777454/. https://doi.org/10.1007/S11605-018-3809-7
Lam MB, Raphael K, Mehtsun WT, Phelan J, John Orav E, Jha AK, Figueroa JF. Changes in Racial Disparities in Mortality After Cancer Surgery in the US, 2007–2016. JAMA Network Open. 2020 [accessed 2022 Dec 21];3(12):e2027415–e2027415. https://jamanetwork.com/journals/jamanetworkopen/fullarticle/2773493. https://doi.org/10.1001/JAMANETWORKOPEN.2020.27415
National Academies of Sciences E and M, Division H and M, Practice B on PH and PH, States C on C-BS to PHE in the U, Baciu A, Negussie Y, Geller A, Weinstein JN. The State of Health Disparities in the United States. Communities in Action: Pathways to Health Equity. 2017 Jan 11 [accessed 2022 Oct 30]:1–558. https://www.ncbi.nlm.nih.gov/books/NBK425844/. https://doi.org/10.17226/24624
Azap RA, Paredes AZ, Diaz A, Hyer JM, Pawlik TM. The association of neighborhood social vulnerability with surgical textbook outcomes among patients undergoing hepatopancreatic surgery. Surgery. 2020 [accessed 2022 Oct 30];168(5):868–875. https://doi.org/10.1016/J.SURG.2020.06.032
Munir MM, Alaimo L, Moazzam Z, Endo Y, Lima HA, Shaikh C, Ejaz A, Beane J, Dillhoff M, Cloyd J, et al. Textbook oncologic outcomes and regionalization among patients undergoing hepatic resection for intrahepatic cholangiocarcinoma. Journal of surgical oncology. 2022 [accessed 2022 Oct 30]. https://pubmed.ncbi.nlm.nih.gov/36136327/. https://doi.org/10.1002/JSO.27102
Munir MM, Woldesenbet S, Endo Y, Moazzam Z, Lima HA, Azap L, Katayama E, Alaimo L, Shaikh C, Dillhoff M, Cloyd J, Ejaz A, Pawlik TM. Disparities in Socioeconomic Factors Mediate the Impact of Racial Segregation Among Patients With Hepatopancreaticobiliary Cancer. Ann Surg Oncol. 2023 Apr 25. https://doi.org/10.1245/s10434-023-13449-9.
Gehlke CE, Biehl K. Certain Effects of Grouping upon the Size of the Correlation Coefficient in Census Tract Material. J Am Stat Assoc. 1934 Mar;29(185A):169–70.
Acknowledgements
The collection of cancer incidence data used in this study was supported by the California Department of Public Health pursuant to California Health and Safety Code Section 103885; Centers for Disease Control and Prevention’s (CDC) National Program of Cancer Registries, under cooperative agreement 1NU58DP007156; the National Cancer Institute’s Surveillance, Epidemiology and End Results Program under contract HHSN261201800032I awarded to the University of California, San Francisco, contract HHSN261201800015I awarded to the University of Southern California, and contract HHSN261201800009I awarded to the Public Health Institute. The ideas and opinions expressed herein are those of the author(s) and do not necessarily reflect the opinions of the State of California, Department of Public Health, the National Cancer Institute, and the Centers for Disease Control and Prevention or their Contractors and Subcontractors.
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Shaikh, C.F., Woldesenbet, S., Munir, M.M. et al. Association between the Environmental Quality Index and Textbook Outcomes Among Medicare Beneficiaries Undergoing Surgery for Early-Stage Pancreatic Adenocarcinoma. J Gastrointest Surg 27, 1883–1892 (2023). https://doi.org/10.1007/s11605-023-05757-y
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DOI: https://doi.org/10.1007/s11605-023-05757-y