Unique Considerations in Caring for Rural Patients with Rectal Cancer: A Scoping Review of the Literature from the USA and Canada
Abstract
1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Study Selection
2.3. Definitions
2.4. Data Extraction
3. Results
3.1. Treatment Modalities
3.2. Oncologic Outcomes/Response to Treatment
3.3. Presentation and Diagnostic Work Up
3.4. Tumor Characteristics
3.5. Preferences, Costs, and Other Outcomes
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Acknowledgments
Conflicts of Interest
Abbreviations
CRS | Colorectal surgery |
cCR | Clinical complete response |
pCR | Pathologic complete response |
HVH | High-volume hospital |
HVS | High-volume surgeon |
RUCC | Rural–urban continuum codes |
RUCA | Rural–urban commuting areas |
DFS | Disease-free survival |
OS | Overall survival |
CSS | Cancer-specific survival |
LAR | Low anterior resection |
APR | Abdominoperineal resection |
LHA | Local health authority |
OR | Odds ratio |
HR | Hazard ratio |
APC | Annual percent change |
CI | Confidence interval |
Appendix A
Study Information | Loc. | Data Source | Inclusion Criteria |
---|---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | USA | Single institution retrospective cohort using EMR chart review | Included: inpatient, >18 yrs, rectal, underwent proctectomy between 1 January 2014 and 1 January 2018, residing within WI or WI-bordering state Excluded: outside institution surgery, trans-anal excision, multi-visceral excision, metastatic at presentation, had histologic diagnosis other than rectal adenocarcinoma |
Tan J.Y. et al. Int. J. Cancer 2024 [29] | USA | US Centers for Disease Control and Prevention’s Wide-Ranging Online Data for Epidemiologic Research (CDC WONDER) from 1999 to 2020 | CRC (ICD-10 codes [ICD-10] C18.0–C18.9 and C19–C20) as the underlying cause of death |
Shulman R.M. et al. JAMA Netw. Open 2024 [30] | USA | National Cancer Database | Patients with locally advanced rectal cancer treated with neoadjuvant therapy and surgery between 1 January 2004 and 31 December 2017 |
Sha S.T. et al. Adv. Radiat. Oncol. 2023 [31] | USA | Medicare Claims Data | Had fee-for service Medicare Claims, 1 April 2016 to 30 September 2018, non-metastatic rectal cancer Excluded: age <65, ESRD, stage IV disease, had pre-existing cancer in look-back period 1 October 2015 to 31 March 2016, nursing home residents, underwent trans-anal excision |
Sutton T.S. et al. PLoS One 2023 [32] | USA | Single institution retrospective cohort at a CoC-accredited tertiary care center, chart review of EMR | Patients >18 yrs, rectal adenocarcinoma, 1 January 2016 to 12 December 2021, tumors of upper/middle/lower rectum as confirmed by endoscopy, as measured 15 cm from anal verge OR receiving therapy consistent with rectal adenocarcinoma (e.g., RT) |
Goffredo P. et al. J. Gastrointest. Surg. 2023 [33] | USA | Iowa Cancer Registry and Patient survey | Inclusion: adults with microscopically confirmed stage II and III rectal cancer between 2013 and 2017 who received cancer-directed surgery with curative intent, alive as of October 2018 |
Hao S. et al. Int. J. Colorectal Dis. 2023 [34] | USA | National Cancer Database (NCDB) | Inclusion: patients with primary rectal adenocarcinoma, between 2004 and 2017, only stage II and III Exclusion: rectal cancer not primary/no rectal cancer, clinical stage missing, stage 0/I/IV, treated at multiple facilities, first treatment unknown |
Emile S.H. et al. Surgery 2023 [35] | USA | Retrospective case-controlled study using NCDB | Inclusion: non-metastatic rectal adenocarcinoma, underwent proctectomy, between 2010 and 2017 Exclusion: metastatic disease, unknown stage, no surgery, local excision only, total proctocolectomy, unknown surgery type, patients who had planned readmission, or where information on 30 d readmission was missing |
Del Vecchio N.J. et al. Dis. Colon Rectum 2022 [36] | USA | Iowa Cancer Registry to identify patients for survey, as well as for demographic and cancer data | Iowa residents, age > 18, microscopically confirmed stage II and III rectal cancer, between 2013 and 2017, who received cancer-directed surgery, alive as of October 2018, cognitively/physically able to participate in survey |
Sho S. et al. Dis. Colon Rectum 2020 [37] | USA | NSABP R-04 Clinical Trial Data, two independent reviewers reviewed pathology reports from study patients between 2004 and 2010 and compared those reports against College of American Pathologist (CAP) 2013 guidelines | Rectal adenocarcinoma, resection July 2004–August 2010 |
Matthews K.A. et al. J. Rural Health 2020 [38] | USA | Iowa Cancer Registry | Iowa residents; diagnosed with rectal cancer, 2010–2014, received surgery, histologies, mucinous adenocarcinoma, signet ring cell carcinoma Exclusion: no surgery, two or more tumors diagnosed within study period, unstaged tumors, select histologies, missing treatment facility information |
Gotfrit J. et al. Public Health Pract. 2020 [39] | Canada | CHORD Consortium outcomes database | Inclusion: patients from BC, Alberta, Ontario, and Newfoundland, 2005–2013, locally advanced rectal cancer (stage II and III), underwent curative intent neoadjuvant chemoradiation followed by surgery Exclusion: prior malignancy (except non-melanoma skin cancer) |
Fields A.C. et al. J. Surg. Oncol. 2020 [40] | USA | NCDB | Inclusion: patients with rectal cancer, stage I–III, age >18, with survival data available, either underwent surgery with curative intent OR refused surgery Exclusion: rectosigmoid cancer, stage IV, local excision, ineligible for surgery |
Ofshteyn A. et al. Am. J. Surg. 2020 [41] | USA | NCDB | Inclusion: age 18+, between 2006 and 2014, clinical stage II and III rectal cancer, received neoadjuvant radiation prior to curative proctectomy Exclusion: patients receiving >5040 cGy radiation, patients who received intentional short-course radiation (2500 cGy or 2000–3000 cGy in 5–10 fractions) |
Springer J.E. et al. Ann. Surg. Oncol. 2020 [42] | Can | Retrospective cohort using Canadian Institute of Health Information Discharge Abstract Database (CIHI), Hospital Morbidity Database | Inclusion: age 18+, underwent elective rectal resection for rectal cancer, April 2008–March 2014, in Canada Exclusions: Quebec |
Chioreso C. et al. Ann. Surg. 2021 [43] | USA | Retrospective analysis of SEER Medicare Data | Inclusion: stage II and III primary rectal adenocarcinoma, between 2007 and 2011, not diagnosed at time of death/autopsy Exclusion: prior cancer within 6 m of diagnosis, died within 3 m of diagnosis, patients whose zip code did not have a corresponding RUCA classification |
Wolbert T. et al. Am. Surg. 2018 [44] | USA | Retrospective chart review and Cabell Huntington Hospital Cancer Registry vs. North American Association of Central Cancer Registries and SEER data | Rectal cancer patients with lower margin <15 cm from anal verge, between 2003 and 2016, living in the Appalachian Tristate Area |
Arsoniadis E.G. et al. Ann. Surg. Oncol. 2018 [45] | USA | Nationwide Inpatient Sample (NIS) dataset | Inclusion: patients with ICD-9 codes for rectal cancer, 1998–2012, who received proctectomy (LAR ± colostomy or APR) Exclusion: patients with concurrent excluding diagnoses (carcinoids, inflammatory bowel disease, regional enteritis, rectosigmoid cancer), metastatic disease, surgery that involved resection of other pelvic organ, trans-sacral surgery |
Lefresne S. et al. Am. J. Surg. 2018 [46] | Can | BC Cancer Agency’s (BCCA) Gastrointestinal Cancer Outcomes Unit (GICOU) database | Inclusion: patients with stage II and III rectal adenocarcinoma, between 2004 and 2009 |
Loree J.M. et al. J. Rural Health 2017 [47] | Can | BC Cancer Agency’s (BCCA) Gastrointestinal Cancer Outcomes Unit (GICOU) database | Inclusion: patients diagnosed with stage II and III rectal cancer, between 1 January 1999 and 31 December 2009, referred to BCCA center Exclusion: primary colon cancer, synchronous colon cancer, histology other than rectal adenocarcinoma, timing of radiation therapy not assessed in patients diagnosed before 2005 |
Nostedt M.C. et al. Can. J. Surg. 2014 [48] | Can | Manitoba Cancer Registry Database, survey rectal cancer patient recruited by rectal cancer-treating surgeons who were identified by convenience sample | Patients diagnosed with adenocarcinoma of the colon or rectum, 1 January 2004 and 31 December 2006, English speaking patients, stage I–III disease, who had not yet undergone curative-intent surgery, but were scheduled to undergo curative-intent surgery |
Monson J.T. et al. Ann. Surg. 2014 [49] | USA | Retrospective review of NCDB | Inclusion: patients diagnosed with rectal cancer, stage II and III, between 2006 and 2011, who underwent surgical resection, histology: adenocarcinoma, mucinous adenocarcinoma, signet rig cell carcinoma |
Sankaranarayanan J. et al. Expert. Rev. Pharmacoecon. Outcomes Res. 2014 [50] | USA | National Cancer Registry | Inclusion: colorectal cancer patients, age 19+, between January 1998 and December 2003, diagnosed with colon cancer, rectosigmoid cancer, or rectal cancer Exclusions: ICD-O-3 codes C18.1, C21, C26.0, recurrence |
Hines R. et al. Am. J. Public Health 2014 [51] | USA | Georgia Comprehensive Cancer Registry | Patients diagnosed with colon or rectal cancer, diagnosed between 2000 and 2007, age 45–85 years Exclusion: no prior lifetime cancer diagnosis (excluding non-melanoma skin cancer), multiple primary tumors, appendiceal tumors |
Fleming S.T. et al. J. Rural Health 2014 [52] | USA | Cancer Registries of Kentucky, Ohio, Pennsylvania, and North Carolina, Center for Medicare and Medicaid Services Medicare Claims database | Inclusion: between 2005 and 2009, stage I–III colon cancer cases and stage III rectal cancer cases Exclusion: histology not adenocarcinoma, in situ cancers/stage missing, not first primary, multiple tumors, 66 < age > 80, metastases, no surgery |
Helewa R.M. et al. Dis. Colon Rectum 2013 [53] | Can | Manitoba Cancer Registry, local recurrence information from chart review (paper and electronic charts) | Inclusion: diagnosed with stages I–III rectal adenocarcinoma, 2004–2006, treated at CancerCare Manitoba, had APR, pelvic exenteration, LAR, Hartmann’s, proctocolectomy, or trans-anal excisions Exclusions: rectosigmoid cancers treated as colon cancers, anal cancers, metastatic disease, unresectable disease at time of index operation, only polypectomy |
Stewart D.B. et al. Ann. Surg. Oncol. 2013 [54] | USA | Pennsylvania Cancer Registry, linked to medical claims data provided by Highmark Inc. (insurance company) | Inclusion: rectal cancer, treated with surgical resection, 2004–2006 Exclusion: local excision, in situ carcinoma |
Hines R.B. et al. J. Rural Health 2012 [55] | USA | SEER data from participating counties in Georgia (Atlanta Registry and Rural Georgia Registry) | Inclusion: patient diagnosed with colon/rectal cancer, first lifetime cancer diagnosis (excluding non-melanoma skin cancer), 1992–2007 Exclusion: appendix cancer |
Sankaranarayanan J. et al. Am. J. Manag. Care 2010 [56] | USA | Nebraska Cancer Center Registry | Inclusion: patients age > 19, 1998–2003, diagnosed: colon cancer, rectosigmoid cancer, or rectal cancer, initial tumor Exclusion: carcinoid of appendix, anal canal carcinoma, or unspecified digestive organs, subsequent tumors if multiple |
Esnaola N.F. et al. Ann. Surg. 2009 [57] | USA | South Carolina Central Cancer Registry | Inclusion: non-metastatic primary invasive colon and rectal cancer, 1996–2002 Exclusion: diagnosis at autopsy, metastatic disease, select morphology codes |
Appendix B
“((((((((((((“Rectal Neoplasms”[Mesh]) OR (“Rectal Neoplasm”[Title/Abstract])) OR (“Rectum Neoplasm”[Title/Abstract])) OR (“Rectal Tumor”[Title/Abstract])) OR (“Rectal Tumors”[Title/Abstract])) OR (“Cancer of Rectum”[Title/Abstract])) OR (“Rectal Cancer”[Title/Abstract])) OR (“Rectum Cancers”[Title/Abstract])) OR (“Rectal Cancers”[Title/Abstract])) OR (“Rectum Cancer”[Title/Abstract])) OR (“Cancer of the Rectum”[Title/Abstract])) OR (“Rectal Neoplasms”[Title/Abstract])) |
AND |
((((((rural)) OR (“Rural Health”[Mesh])) OR (“Rural Health Services”[Mesh])) OR (“Rural Population”[Mesh])) OR (“Hospitals, Rural”[Mesh])) OR (“non-urban”)” |
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Study Information | Loc. | Data Source | Primary Outcomes | Measure of Rurality |
---|---|---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | USA | Single institution retrospective cohort, using EMR chart review | Overall mortality, disease recurrence, and quality of life | Distance to urban/specialized treatment center |
Tan J.Y. et al. Int. J. Cancer 2024 [29] | USA | US Centers for Disease Control and Prevention’s Wide-Ranging Online Data for Epidemiologic Research | Age-adjusted mortality rate, average annual percent change in colon, rectosigmoid, and rectal cancer | 2013 US census classification: urban (large central metro, large fringe metro, medium metro, and small metro counties) and rural (micropolitan non-metro and non-core non-metro counties) |
Shulman R.M. et al. JAMA Netw. Open 2024 [30] | USA | National Cancer Database | Rate of pCR following neoadjuvant therapy | Assessing urban vs. rural facility, does not specify metrics |
Sha S.T. et al. Adv. Radiat. Oncol 2023 [31] | USA | Medicare Claims Data | Composite of both proctectomy and RT therapy within 180 d. Subset with proctectomy: pre-op RT, pre-op chemo, and MIS | US census definitions of metropolitan (≥50,000 people), micropolitan (10,000–49,999), or small town/rural (<10,000 people), using patient location not treatment facility location |
Sutton T.S. et al. PLoS One 2023 [32] | USA | Single institution retrospective cohort at a CoC-accredited tertiary care center, chart review of EMR | Acuity of presentation, stage at diagnosis before and after COVID-19 | Rural vs. urban/metropolitan defined as per the Federal Office of Rural Health Policy, assessing patient residence |
Goffredo P. et al. J. Gastrointest. Surg. 2023 [33] | USA | Iowa Cancer Registry and patient survey | Association of demographics, tumor location, neoadjuvant CRT, sphincter-sparing rates, and hospital volume | Rural–urban commuting area (RUCA): small rural, large rural, urban |
Hao S. et al. Int. J. Colorectal Dis. 2023 [34] | USA | National Cancer Database | Correlation between distance traveled and receipt of surgery | NCDB uses USDA economic research services definition of rurality: rural (<2500), urban (2500–20,000+ and adjacent to a metro area), and metro (<250,000–1,000,000+ in defined metropolitan areas). Distance traveled to treating hospital measured in quartiles (1st 0–4.6; 2nd 4.6–10.5; 3rd 10.5–25.6; 4th 25.6–4191, all in miles) |
Emile S.H. et al. Surgery 2023 [35] | USA | Retrospective case-controlled study using NCDB | Rate and predictors of 30-day unplanned readmission and the impact of readmission on short-term mortality and overall survival | Per NCDB user file: metropolitan, namely counties in metro areas with <250,000 to ≥1 million population; urban, namely urban population of 2500 to ≥20,000, adjacent or not adjacent to a metro area; and rural, namely completely rural or <2500 urban population, adjacent or not adjacent to a metro area, itself based on USDA economic research service |
Del Vecchio N.J. et al. Dis. Colon. Rectum 2022 [36] | USA | Iowa Cancer Registry used to identify patients for survey, as well as for demographic and cancer data | Characteristics of the hospitals where patients choose to receive surgery | Patient zip codes were classified based on 3-tiered rural–urban commuting area scheme (urban, large rural, and small rural) |
Sho S. et al. Dis. Colon. Rectum 2020 [37] | USA | NSABP R-04 Clinical Trial Data, two reviewers analyzing pathology reports and compared them against College of American Pathologist (CAP) 2013 guidelines | Adherence to the College of American Pathologists guidelines, impact of synoptic reporting, academic status, rural/urban, and hospital size on report quality | American Hospital Association Data Viewer—hospital location data urban/rural |
Matthews K.A. et al. J. Rural Health 2020 [38] | USA | Iowa Cancer Registry | Travel time for CRC patients measured by time to nearest cancer surgery facility, time to actual cancer surgery facility, and number of bypassed facilities | Rural–urban commuting area (RUCA), categorization B: isolated rural, small rural, large rural, urban |
Gotfrit J. et al. Public Health Pract. 2020 [39] | Can | CHORD Consortium outcomes database | Impact of distance, drive time, socioeconomic factors on OS and DFS | Distance in hours and km from patient zip code to closest cancer center; 2016 Canadian census database for rural status and population center size |
Fields A.C. et al. J. Surg. Oncol. 2020 [40] | USA | NCDB | Predictors of surgical refusal | Does not specify what metric they used for classifying a county as urban/rural. Also uses distance tertiles to treatment facility, but they do not specify what distance ranges each of the tertiles represents |
Ofshteyn A. et al. Am. J. Surg. 2020 [41] | USA | NCDB | Predictors of inadequate radiation dosing | Does not specify what metric they used for “rural” status or how they calculated the distance from the hospital |
Springer J.E. et al. Ann. Surg. Oncol. 2020 [42] | Can | Retrospective cohort using Canadian Institute of Health Information Discharge Abstract Database (CIHI), Hospital Morbidity Database | Regional rates for laparoscopy use in rectal cancer surgery | Does not specify how they define urban/rural divide. Uses distance from CRS training program |
Chioreso C. et al. Ann. Surg. 2021 [43] | USA | Retrospective analysis of SEER Medicare Data | Receipt of rectal cancer resection at a HVH and by a HVS/CRS | Rural–urban commuting area classification using zip code from SEER, distance between patient’s zip code and treating hospital |
Wolbert T. et al. Am. Surg. 2018 [44] | USA | Retrospective study via chart review and Cabell Huntington Hospital Cancer Registry compared to North American Association of Central Cancer Registries and Surveillance, Epidemiology, and End Results Program database | Prevalence of CRC in rural Appalachia | All patients classified as rural based on being from/treated in “Appalachian Tristate Area” of western West Virginia, eastern Kentucky, and southeastern Ohio |
Arsoniadis E.G. et al. Ann. Surg. Oncol. 2018 [45] | USA | Nationwide Inpatient Sample (NIS) dataset | Compare rate of APR vs. LAR in African American vs. non-African American rectal cancer patients | Assessing location of hospital based on NIS data. Unclear metric/threshold for designation of hospital as urban vs. rural |
Lefresne S. et al. Am. J. Surg. 2018 [46] | Can | BC Cancer Agency’s (BCCA) Gastrointestinal Cancer Outcomes Unit (GICOU) database | Rates of neoadjuvant RT, chemotherapy, and sphincter-preserving surgery, DFS, OS | Local health authority (LHA) was identified by patient postal code and then determined to be rural (<50% live in community >10,000 people), small (>50% living in community >10,000 people), and large (>95% people living in community >100,000) |
Loree J.M. et al. J. Rural Health 2017 [47] | Can | BC Cancer Agency’s (BCCA) Gastrointestinal Cancer Outcomes Unit (GICOU) database | Impact of rural/urban and distance on CSS | Canadian Census Analyzer + postal codes: The Canadian census divides “population centers” into small (1000–29,999), medium (30,000–99,999), and large (100,000+). Population centers are areas with at least 1000 people and a population density of at least 400/km2. Rural areas are any places outside an indicated population center. They were also evaluated according to whether they traveled >100 km or <100 km to the center at which they received the majority of their care |
Nostedt M.C. et al. Can. J. Surg. 2014 [48] | Can | Manitoba Cancer Registry Database, survey rectal cancer patient recruited by rectal cancer-treating surgeons, who were identified using a convenience sample | Preferences and factors considered in determining treatment location | Hospitals not in Winnipeg were classified as rural. Surgeons at designated urban and rural hospitals in Manitoba were contacted to refer patients for convenience sample telephone interview |
Monson J.T. et al. Ann. Surg. 2014 [49] | USA | Retrospective review of NCDB | Adherence to neoadjuvant CRT guidelines in rectal cancer patients by geographic regions, institution volume, and time | Population density of patient residence not otherwise specified |
Sankaranarayanan J. et al. Expert Rev. Pharmacoecon. Outcomes Res. 2014 [50] | USA | National Cancer Registry | Colon and rectal cancer survival by age, race, rurality, and other socioeconomic factors | OMB metropolitan classification: urban metro (large >1 M or small 50 k–1 M), micropolitan (10 k–50 k), or non-core/non-metro/rural (0–10 k) |
Hines R. et al. Am. J. Public Health 2014 [51] | USA | Georgia Comprehensive Cancer Registry | Overall survival based on geographic residence/census tract | Rural–urban commuting area (RUCA) primary codes from the US Department of Agriculture: rural (RUCA codes 7–10), suburban (RUCA codes 2–6), and urban (RUCA code 1) |
Fleming S.T. et al. J. Rural Health 2014 [52] | USA | Cancer Registries of Kentucky, Ohio, Pennsylvania, and North Carolina, Center for Medicare and Medicaid Services Claims database | Guideline concordance in treating rectal cancer measured by adjuvant chemotherapy, ≥12 lymph, and RT | 2003 USDA rural–urban continuum codes |
Helewa R.M., et al. Dis. Colon Rectum 2013 [53] | Can | Manitoba Cancer Registry, local recurrence information from chart review (paper and electronic charts) | Population-based rates and risk factors for recurrence in Manitoba | Patient and hospital performing the surgery were classified as either urban/Winnipeg or rural/Manitoba. Classified by distance traveled from place of residence to CancerCare Manitoba (site of only radiation therapy): <21 km, 21–100 km, 101–500 km, and >500 km |
Stewart D.B. et al. Ann. Surg. Oncol. 2013 [54] | USA | Pennsylvania Cancer Registry, linked to medical claims data provided by Highmark Inc. (insurance company) | Use of neoadjuvant RT and CSS by hospital type (urban/rural, large/small, academic/community) | Assessing hospital rurality. Rural–urban commuting area codes were mapped to the zip code of the treating hospital |
Hines R.B. et al. J. Rural Health 2012 [55] | USA | SEER data from participating counties in Georgia (Atlanta Registry and Rural Georgia Registry) | Rate of late stage (III and IV) at diagnosis, treatment received, cancer-specific mortality by geographic area and race | Used the rural–urban continuum code (RUCA) classification: urban counties were those with RUCA codes ≤3, and rural counties were defined as those with RUCA codes ≥6 |
Sankaranarayanan J. et al. Am. J. Manag Care 2010 [56] | USA | Nebraska Cancer Center Registry | Receipt of surgery, radiation, and/or chemotherapy for CRC by anatomic site, residence county (rural/urban), and age | Office of Management and Budget (OMB) classifications into three categories: “urban metro” counties with large (>1 million) or small-metro (50,000 to <1 million residents) central counties; micropolitan counties (centered on urban clusters with 10,000–49,999 residents, plus surrounding counties); and “rural” counties containing a town of 1 to 9999 residents |
Esnaola N.F. et al. Ann. Surg. 2009 [57] | USA | South Carolina Central Cancer Registry | Odds of surgical resection for rectal cancer by race | Urban/rural classification based on metropolitan statistical area of the county in which the patient resided, as per HHS Office of Rural Health Policy |
Study | Rurality Measure | Surgical Treatment |
---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | Distance to treatment center | No statistically significant difference according to long vs. short distance traveled to treatment center in the percentage of patients who underwent LAR, APR, vs. total proctocolectomy (p = 0.325). |
Sha S.T. et al. Adv. Radiat. Oncol. 2023 [31] | US census classifications | Rural patients had a statistically significant greater likelihood of proctectomy within 180 d of diagnosis (small/rural 33.2%, micropolitan 28.4%, metropolitan 28.6%; p < 0.01). Metropolitan patients had statistically significant fewer days until surgery (80.7 d vs. 87.0 d, p = 0.05), a higher percent of patients receiving MIS surgery (61.6% vs. 53.8%, p < 0.01), and were more likely to be treated by a colorectal surgeon or surgical oncologist as opposed to a general surgeon (56.1% vs. 44.1%, p < 0.01). |
Hao S. et al. Int. J. Colorectal Dis. 2023 [34] | USDA economic research service classification Distance from treating facility (in quartiles) | There was no statistically significant difference in the receipt of surgery by rural/urban/metro status: metro (ref), urban (0.92, p = 0.08), rural (1.02, p = 0.89). There was a statistically significant difference in the receipt of surgery between 1st and 4th quartile of the distance traveled to the care provider (with more people in the 4th quartile receiving surgery), but not the 2nd and 3rd: 1st (ref), 4th (1.37, p < 0.001). |
Fields A.C. et al. J. Surg. Oncol. 2020 [40] | Unclear metric for urban/rural Distance to treatment facility (in tertiles) | There was a statistically significant difference in regard to whether patients with stage I rectal adenocarcinoma chose to refuse surgery based on the distance from the facility in the bivariate analysis (1st OR ref; 2nd OR 0.6, p < 0.001; 3rd OR 0.3, p < 0.001) and multivariate analysis (1st OR ref; 2nd OR 0.6, p < 0.001; 3rd OR 0.2, p < 0.001). Analysis was not provided for urban–rural designation. There was no statistically significant difference in regard to whether the patients with stage II and III rectal adenocarcinoma chose to refuse surgery based on urban–rural designation in the bivariate analysis (metro OR ref; rural OR 1.0, p = 1), but there was in the multivariate analysis (metro OR ref; rural OR 1.5, p = 0.02). There was a statistically significant difference in regard to whether the patients with stage II and III rectal adenocarcinoma chose to refuse surgery based on the distance from the facility in the bivariate analysis (1st OR ref; 2nd OR 0.6, p < 0.001; 3rd OR 0.5, p < 0.001) and multivariate analysis (1st OR ref; 2nd OR 0.7, p < 0.001; 3rd OR 0.6, p < 0.001). |
Springer J.E. Ann. Surg. Oncol. 2020 [42] | Unclear metric for urban/rural Distance from CRS training program | Patients living >100 km from the colorectal training program were less likely to receive laparoscopic surgery for their rectal cancer than those <25 km (OR 2.38, p < 0.001) or those living 26–100 km (OR 1.79, p < 0.001) from the program. Rural patients had no statistically significant difference in regard to the receipt of laparoscopic surgery than those living >100 km from the CR fellowship program (OR 0.95, p = 0.26). Rural patients were not directly compared to urban patients. A total of 94.2% of patients who received laparoscopic surgery for rectal cancer lived within 100 km of the CR fellowship training facility. A total of 89.9% of patients in low-laparoscopy clusters lived >100 km from a CR fellowship training facility. |
Wolbert T. et al. Am. Surg. 2018 [44] | All patients designated rural based on being from “Appalachian Tristate Area” | Age <50 years: 13% received APR, 38% received LAR, 13% received polypectomy, and 4% received polypectomy with curative intent. It was not stated what, if any, surgical treatment the remaining patients received. Age >50 years: 13% received APR and 13% received polypectomy. It was not stated what, if any, surgical treatment the remaining patients received. |
Arsoniadis E.G. et al. Ann. Surg. Oncol. 2018 [45] | Unclear metrics, designated by location of treating hospital | There was no statistically significant difference in the odds of sphincter-preserving surgery for patients treated in rural vs. urban hospitals as a result of multivariate modeling (urban OR ref; rural OR 0.91, 95%CI 0.81–1.02) |
Lefresne S. et al. Am. J. Surg. 2018 [46] | Local health authority (LHA) size: rural, small, and large | Patients in large urban areas had a slightly higher rate of palliative surgery than small or rural community patients (large LHA 8.7%, small LHA 6.6%, rural LHA 4.4%; p = 0.04), but there was no statistically significant difference in regard to the choice of surgical procedures |
Loree J.M. et al. J. Rural Health 2017 [47] | Canadian population centers according to census: rural, small, medium, and large | No statistically significant difference in the percentage of patients receiving surgery (p = 0.73) when evaluated by distance (>100 km vs. <100 km) from the treatment center, which persisted in the multivariate analysis (>100 km OR 0.69, <100 km ref; p = 0.34). By population center, a statistically significant difference in the percentage of patients receiving surgery occurred (rural 95.1%, small 92.2%, medium 91.5%, large 92.5%; p = 0.02) that did not hold up in the multivariate analysis (rural OR 2.16, p = 0.051; large ref). No statistically significant difference in the TME occurred according to distance or population center (p = 0.78, p = 0.33). The number of days from diagnosis until surgery was longer for those living >100 km from the primary treatment center (61 days vs. 56 days, p = 0.013); however, there was no statistically significant difference in the number of days waited until surgery when analyzed according to the population center (p = 0.12) |
Hines R. et al. Am. J. Public Health 2014 [51] | RUCA | No statistically significant differences in regard to the odds of receiving surgery for rectal cancer between urban, suburban, and rural patients |
Helewa R.M. et al. Dis. Colon Rectum 2013 [53] | Winnipeg vs. non-Winnipeg Manitoba Distance from treating hospital | There were no statistically significant differences in the percentage of patients who achieved R0 resection (Winnipeg–Winnipeg 86.2%, Rural–Winnipeg 88.1%, Rural–Rural 84.1%, p = 0.77). There were no statistically significant differences in regard to the type of surgical resection between the residence–hospital location interaction (p = 0.26) |
Hines R.B. et al. J. Rural Health 2012 [55] | RUCA codes | There was no statistically significant difference in regard to the receipt of surgery (OR 0.92, 95%CI 0.51–1.66) comparing rural and urban patients |
Sankaranarayanan J. et al. Am. J. Manag. Care 2010 [56] | OMB’s classifications of urban metro, micropolitan, and rural | A total of 79.7% of rural patients underwent surgery as opposed to 78% of urban and 77.1% micropolitan patients, which was not statistically significant. The multivariate analysis showed the odds of rural (ref) patients receiving surgery were not statistically significant (p = 0.08) from that of urban patients (OR 0.73) and micropolitan patients (OR 0.58) |
Esnaola N.F. et al. Ann. Surg. 2009 [57] | HHS office of Rural Health Policy’s classification of Metropolitan Statistical Area | There was statistically significant decreased odds of rural patients receiving surgery for rectal cancer (OR 0.59, p < 0.001) when compared to urban patients (ref) |
Study | Rurality Measure | Chemotherapy |
---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | Distance to treatment center | No statistically significant difference was observed in regard to the percentage of patients who received neoadjuvant chemotherapy (short distance 39%, long distance 51%; p = 0.233) |
Sha S.T. et al. Adv. Radiat. Oncol. 2023 [31] | US census classifications | There was no statistically significant difference in the percentage of patients who received chemotherapy within 180 days of diagnosis (rural 38.7%, metro 35.9%, p = 0.07), but there was a statistically significant increased neoadjuvant chemotherapy percentage usage in regard to rural patients (44.4% vs. 37.7%, p = 0.01) |
Gotfrit J. et al. Public Health Pract. 2020 [39] | Canadian population centers by census: rural, small, medium, and large Distance in kilometers and hours to closest cancer center | There was no statistically significant difference in regard to the receipt of neoadjuvant chemotherapy for those living >100 km from the treatment center (p = 0.44) or for those living >1 h from the treatment center (p = 0.36) |
Chioreso C. et al. Ann. Surg. 2021 [43] | RUCA codes | No statistically significant differences were observed in regard to the medical oncology visits between rural and urban patients. The study does not report directly on the use of chemotherapy |
Lefresne S. et al. Am. J. Surg. 2018 [46] | Local health authority (LHA) size: rural, small, and large | Median waiting time from diagnosis to cancer center visit was longer for rural LHA than for small LHA and large LHA communities (rural LHA 39 d, small LHA 35 d, large LHA 32 d days; p < 0.01). The receipt of chemotherapy was not associated with the patients’ urban/rural status (rural LHA 57%, small LHA 56%, and large LHA 57%; p = 0.89) |
Loree J.M., et al. J. Rural Health 2017 [47] | Canadian population centers according to census: rural, small, medium, and large | No statistically significant differences were observed in regard to the percentage of patients who received adjuvant chemotherapy when analyzed according to the distance from the primary treatment center (p = 0.129), with similar odds between the two groups (<100 km OR ref; >100 km OR 0.90, p = 0.52), in the multivariate analysis. A statistically significant difference was observed in regard to the percentage of patients who received adjuvant chemotherapy when analyzed according to the population center (rural 51.6%, small 44.8%, medium 45.8%, large 54.9%; p = 0.0005); however, in the multivariate analysis, the odds of receiving chemotherapy were not statistically significantly different between the groups (rural OR 0.8, p = 0.15; small OR 0.7, p = 0.15; medium OR 0.74, p = 0.15; large ref) |
Hines R. et al. Am. J. Public Health 2014 [51] | RUCA codes | No statistically significant differences were observed in regard to the odds of receiving chemotherapy between urban, suburban, and rural patients |
Study | Rurality Measure | Radiation |
---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | Distance to treatment center | The data were just shy of statistical significance in regard to the percentage of patients receiving neoadjuvant radiation according to the distance from the treating facility (long 77%, short 59%, p = 0.057) |
Sha S.T. et al. Adv. Radiat. Oncol. 2023 [31] | US census classifications | There were no statistically significant differences in regard to the receipt of radiation within 180 d of diagnosis according to region. In the univariate analysis, a greater percentage of rural patients received neoadjuvant radiation (49.9% vs. 44.4%, p = 0.04) compared to metropolitan patients; however, when analyzed further, the adjusted odds ratio was not statistically significant (rural neoadjuvant OR 1.21, metropolitan ref; p = 0.1). IMRT was favored in metropolitan areas compared to rural areas (metro 50.6%, rural 38.9%, p < 0.01) |
Gotfrit J. et al. Public Health Pract. 2020 [39] | Canadian population centers according to census: rural, small, medium, and large Distance in hours and kilometers to the closest cancer center | There were also no statistically significant differences in regard to the receipt of neoadjuvant radiation therapy for those living >100 km from the treatment center (p = 0.91) or for those living >1 h from the treatment center (p = 0.23) |
Ofshteyn A. et al. Am. J. Surg. 2020 [41] | Unclear metric for urban/rural Distance from hospital | Rural patients were more likely than urban or metropolitan patients to receive inadequate radiation dosing (rural 7.5%, urban 6.5%, metro 5.1%; p < 0.001), as were patients who had to travel a longer distance to the hospital (<50 mi 5–5.6%, >50 mi 6.2–6.8%; p = 0.034), as shown by the univariate analysis. The increased odds of inadequate radiation dosing for rural patients compared to metropolitan patients remained statistically significant in the multivariate analysis (metro OR ref; rural OR 1.42, p = 0.035) |
Chioreso C. et al. Ann. Surg. 2021 [43] | RUCA codes | No statistically significant differences in regard to the radiation oncology visits between rural and urban patients. The study does not report directly on the use of radiation therapy |
Lefresne S., et al. Am. J. Surg. 2018 [46] | Local health authority (LHA) size: rural, small, and large | The median waiting time for RT was 54 days and did not vary according to the urban/rural LHA (p = 0.41). There were no differences according to the urban/rural LHA in regard to whether a patient received any RT (p = 0.8), short vs. long course fractionation RT regimen (p = 0.42), or pre-op vs. post-op RT timing (p = 0.74) |
Loree J.M. et al. J. Rural Health 2017 [47] | Canadian population centers according to census: rural, small, medium, and large | There were no statistically significant differences in regard to the percentage of patients receiving radiation therapy when compared according to the distance from the primary treatment center (p = 0.097), with a similarly non-statistically significant difference in odds (<100 km ref; >100 km OR 1.28, p = 0.3), in the multivariate analysis. A statistically significant difference in regard to the percentage of patients receiving radiation therapy was observed when analyzed according to the population center (rural 83.5%, small 88.1%, medium 87.8%, large 88.0%, p = 0.0057); however, the decreased odds of receiving radiation therapy if the patient was in a rural setting as compared to a large population center was not statistically significant (large OR ref; rural OR 0.68, p = 0.08) in the multivariate analysis |
Hines R. et al. Am. J. Public Health 2014 [51] | RUCA | No statistically significant differences were observed in regard to the odds of receiving radiation therapy between urban, suburban, and rural patients |
Fleming S.T. et al. J. Rural Health 2014 [52] | RUCC | No statistically significant differences were observed in regard to the receipt of radiation therapy for metropolitan (58.3%) vs. non-metropolitan (53.4%) stage III rectal cancer patients living in Appalachia |
Helewa R.M. et al. Dis. Colon Rectum 2013 [53] | Winnipeg vs. non-Winnipeg Manitoba Distance from treating hospitals | There was a statistically significant difference in regard to the receipt of radiation therapy when assessed according to the distance traveled to the radiation center, driven by the significantly decreased odds of receiving radiation therapy if living 101–500 km away from CancerCare Manitoba (<21 km OR ref; 21–100 km OR 0.76, 95%CI 0.34–1.72; 101–500 km OR 0.23, 0.08–0.63; >500 km OR 0.8, 0.10–6.36; p = 0.032) |
Stewart D.B. et al. Ann. Surg. Oncol. 2013 [54] | RUCA (by hospital location) | In the univariate analysis, there was no statistically significant difference in the use of radiation therapy in urban vs. rural hospitals treating patients with stage II and III rectal cancer (rural 57.7%, urban 62.2%; p = 0.66); however, there was a statistically significant increase in use of neoadjuvant radiation in urban vs. rural hospitals (rural 19.2%, urban 39.2%; p = 0.046) |
Hines R.B. et al. J. Rural Health 2012 [55] | RUCA codes | There was no statistically significant difference in regard to the receipt of radiation (OR 0.70, 95%CI 0.43–1.15) when comparing rural and urban patients |
Sankaranarayanan J. et al. Am. J. Manag. Care 2010 [56] | OMB’s classification of urban metro, micropolitan, and rural | A total of 37.7% of rural patients received radiation therapy as opposed to 43.5% urban and 42.4% micropolitan patients, which was not statistically significant. The multivariate analysis showed odds of rural rectal cancer patients (ref) receiving radiation to be not statistically significantly different (p = 0.32) from urban patients (OR 1.27) and micropolitan patients (OR 1.31) |
Study | Rurality Measure | Combined Therapy |
---|---|---|
Sha S.T. et al. Adv. Radiat. Oncol. 2023 [31] | US census classifications | The combined outcome of both surgery and radiation within 180 d of diagnosis showed that there was a statistically significant higher percentage of rural patients falling into this category (rural 17.8%, metro 13.7%, p < 0.01); likewise, on further analysis, the adjusted sub-hazard ratio in regard to the receipt of both radiation and surgery in <180 days favored rural patients (rural ASHR 1.15, metropolitan ref; p = 0.05) |
Goffredo P. et al. J. Gastrointest. Surg. 2023 [33] | RUCA codes | There were statistically significantly decreased odds of receiving chemoradiation when comparing small rural (OR 0.49, p = 0.01) to urban (ref) patient population. There was no statistically significant difference in regard to the likelihood of treatment with chemoradiation between large rural and urban populations |
Loree J.M. et al. J. Rural Health 2017 [47] | Canadian population centers according to census: rural, small, medium, and large | The odds of receiving surgery and radiation were not statistically significantly different according to the distance from the primary treatment center (<100 km ref; >100 km OR 1.1, p = 0.67) or according to the population center (rural OR 0.9, p = 0.56; small OR 0.88, p = 0.7; medium OR 1.1, p = 0.73; large OR ref) in the multivariate analysis. The odds of receiving surgery, chemotherapy, and radiation were not statistically significantly different according to the distance from the primary treatment center (<100 km OR ref; >100 km OR 0.84, p = 0.31) or according to the population center (rural OR 0.83, p = 0.22; small OR 0.65, p = 0.09; medium OR 0.75, p = 0.16; large ref) in the multivariate analysis |
Monson, J.T. et al. Ann. Surg. 2014 [49] | Population density and patient’s residence not otherwise specified | Patients in rural counties were more likely to receive neoadjuvant chemoradiation than those in metropolitan counties (OR 1.36, p < 0.001) in the multivariate analysis |
Hines R.B. et al. J. Rural Health 2012 [55] | RUCA codes | There was no statistically significant difference in regard to the receipt of combined surgery and radiation (OR 0.78, 95%CI 0.46–1.33) when comparing rural and urban patients |
Study | Rurality Measure | Outcomes/Response to Treatment |
---|---|---|
Peterson K.J. et al. J. Surg. Res. 2024 [28] | Distance to urban/specialized treatment center | According to the distance traveled, no statistically significant differences were observed in regard to the 2-year mortality, 5-year mortality, overall mortality, or recurrence |
Gotfrit J. et al. Public Health Pract. 2020 [39] | Distance in hours and km to closest cancer center; 2016 Canadian census database urban/rural classification | A distance >100 km (HR 1.59 p = 0.006) and a driving time >1 h (HR 1.57, p = 0.003) both decreased the OS in the univariate analysis. Only a driving time >1 h was significant in the multivariate analysis (HR 1.6, p = 0.002). The same pattern was seen in regard to the DFS, with a distance >100 km (HR 1.16 p = 0.01) and drive time >1 h (HR 1.5, p = 0.002), in the univariate analysis, but only the drive time >1 h (HR 1.47 p = 0.0003) in the multivariate analysis. Designated rural vs. urban areas did not affect the OS or DFS. Recurrence (both local and distant) was higher in patients living >100 km (p = 0.02) and >1 h (p = 0.007) from the cancer center (31%) compared to those living closer (22%, p = 0.02) |
Lefresne S. et al. Am. J. Surg. 2018 [46] | Patients’ local health authority (LHA) was identified and classified as rural/small/large, based on population size | No difference was observed in the median time to follow up according to the urban/rural LHA (33 months). No statistically significant difference between urban/rural LHA disease recurrence (p = 0.99), locoregional recurrence (p = 0.88), or development of distance metastasis (p = 0.87). At 5 years, in regard to the Kaplan–Meier analysis, the DFS (rural LHA 84%, small LHA 85%, large LHA 86%; p = 0.98) and OS (rural LHA 58%, small LHA 59%, large LHA 57%; p = 0.99) were not different. This held true in the multivariate analysis of the DFS (rural LHA HR 0.95, small LHA HR 0.97, large LHA HR ref) and OS (rural LHA HR 1.01, small LHA HR 1.02, large LHA HR ref) |
Loree J.M. et al. J. Rural Health 2017 [47] | Canadian census population center classification of small, medium, large, and rural | The Kaplan–Meier curves for CSS and OS were not different when assessed according to the population center (CSS p = 0.18, OS p = 0.36) or according to the distance (CSS p = 0.88, OS p = 0.47). In the multivariate analysis, CSS was statistically significantly decreased in those living >100 km from their primary treatment center (HR 1.39, p = 0.031) and increased in those living in small population centers (HR 0.42, p = 0.001). No differences in the CSS were observed between large, medium, and rural communities in the multivariate analysis. No differences in the OS in the multivariate analysis were observed when analyzed according to the distance traveled (p = 0.16). A statistically significant increase in the OS for those living in small population centers (HR 0.58, p = 0.011) was observed in the multivariate analysis, but not in regard to large, medium, and rural communities |
Helewa R.M. et al. Dis. Colon Rectum 2013 [53] | Winnipeg vs. non-Winnipeg Manitoba Distance from treating hospitals | The unadjusted rectal cancer local recurrence rates were higher for rural patients (2 yr 12.6%, 3 yr 16.2%, 5 yr 27.5%) when compared with Winnipeg patients (2 yr 5.3%, 3 yr 8.3%, 5 yr 10.3%; p = 0.0003). All the rural patients had higher recurrence rates than their urban counterparts: Winnipeg–Winnipeg treated (2 yr 5.3%, 3 yr 8.4%, 5 yr 10.3%), rural–Winnipeg treated (2 yr 14.3%, 3 yr 14.3%, 5 yr 28.7%), and rural–rural treated (2 yr 11.5%, 3 yr 17.7%, 5 yr 27.2%; p = 0.0013). In the regression analysis, rural residents had a higher local recurrence rate (rural–Winnipeg surgery HR 3.47, rural–rural surgery HR 2.98, Winnipeg–Winnipeg surgery ref; p = 0.0003). Lastly, the OS was decreased in the rural patients (HR 1.90, p = 0.003) compared to Winnipeg patients (ref) |
Hao S. et al. Int. J. Colorectal Dis. 2023 [34] | NCDB uses USDA economic research classification: rural, urban and metro Distance traveled to treating facility in quartiles | Statistically significant differences were observed in the 30 d mortality according to the quartile of the distance traveled (1st 1.6%, 2nd 1.3%, 3rd 1%, 4th 0.8%; p < 0.001) and the odds of 30 d mortality (1st OR ref; 2nd OR 0.8, p = 0.05; 3rd OR 0.59, p < 0.01; 4th OR 0.47, p < 0.01) |
Emile S.H. et al. Surgery 2023 [35] | USDA economic research service classification: metropolitan, urban, and rural | The multivariate regression showed that rural patients had a higher rate of 30 d readmission than metropolitan patients (OR 1.65, p = 0.0004) |
Wolbert T. et al. Am. Surg. 2018 [44] | All patients designated as rural based on being from “Appalachian Tristate Area” | No difference was observed in the OS between rural patients with early vs. average onset rectal cancer (younger 75%, older 60.2%; p = 0.128) |
Sankaranarayanan J. et al. Expert Rev. Pharmacoecon. Outcomes Res. 2014 [50] | OMB metropolitan classification: urban metro, micropolitan, or non-core/non-metro/rural | No differences were observed in the survival time in months (p = 0.29) for rural, urban, and micropolitan patients. In the multivariate regression analysis, urban patients had statistically significantly decreased survival compared with rural patients (rural ref; HR 1.25, p = 0.049) when controlling only for demographic factors. However, when controlling for other factors, including the stage, treatment, and other interaction variables, there was no difference in urban/rural survival. When further broken down into the patients who did not undergo surgery, there was a statistically significantly lower survival rate for micropolitan (HR 2.01, p = 0.0005) and urban (HR 1.49, p = 0.03) patients when compared with rural (ref) patients. No difference in survival according to the urban/rural status was observed when patients underwent surgery |
Stewart D.B. et al. Ann. Surg. Oncol. 2013 [54] | RUCA codes (treating hospital) | No difference in the CSS curve was observed for rectal cancer patients treated in rural vs. urban hospitals (p = 0.83). In the multivariate analysis, there was no difference in the rate of death from rectal cancer in regard to urban vs. rural hospitals (rural HR ref; urban HR 0.954, p = 0.9) |
Hines R.B. et al. J. Rural Health 2012 [55] | Unclear metric, mentions both RUCC and RUCA | No difference in rectal cancer-related death was observed between urban (ref) and rural rectal cancer patients, both overall and when broken down by stage: overall (HR 1.13, 95%CI 0.91–1.41), in situ and stage I (HR 1.29, 95%CI 0.92–1.81), stage II and III (HR 1.17, 95%CI 0.92–1.50), stage IV (HR 1.09, 95%CI 0.73–1.61) |
Tan J.Y. et al. Int. J. Cancer 2024 [29] | US census classification: urban and rural | The age-adjusted mortality rate (per 100,000) increased from 1999 to 2020 (from 2.95 to 3.01) for rural rectal cancer patients, while decreasing for urban patients (from 3.03 to 2.38); APC for urban patients −1.21 (95%CI −1.48 to −0.95) compared with rural patients, APC +0.10 (95%CI −0.24 to 0.44) |
Shulman R.M. et al. JAMA Netw. Open 2024 [30] | Assessing urban vs. rural facility, metrics unspecified | According to the urban/rural treatment facility, a statistically significant difference in the odds of a complete pathologic response in rural facilities (0.8) was observed compared to large metro (ref) facilities. No difference was observed in regard to tumor down-staging |
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Rafferty, L.M.; Hilty Chu, B.K.; Fleming, F. Unique Considerations in Caring for Rural Patients with Rectal Cancer: A Scoping Review of the Literature from the USA and Canada. J. Clin. Med. 2025, 14, 4106. https://doi.org/10.3390/jcm14124106
Rafferty LM, Hilty Chu BK, Fleming F. Unique Considerations in Caring for Rural Patients with Rectal Cancer: A Scoping Review of the Literature from the USA and Canada. Journal of Clinical Medicine. 2025; 14(12):4106. https://doi.org/10.3390/jcm14124106
Chicago/Turabian StyleRafferty, Lydia Manela, Bailey K. Hilty Chu, and Fergal Fleming. 2025. "Unique Considerations in Caring for Rural Patients with Rectal Cancer: A Scoping Review of the Literature from the USA and Canada" Journal of Clinical Medicine 14, no. 12: 4106. https://doi.org/10.3390/jcm14124106
APA StyleRafferty, L. M., Hilty Chu, B. K., & Fleming, F. (2025). Unique Considerations in Caring for Rural Patients with Rectal Cancer: A Scoping Review of the Literature from the USA and Canada. Journal of Clinical Medicine, 14(12), 4106. https://doi.org/10.3390/jcm14124106