Colorectal Cancer after Kidney Transplantation: A Screening Colonoscopy Case-Control Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Screening Methodology
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
FOBT | faecal occult blood tests |
FIT | faecal immunochemical test |
KDIGO | Kidney Disease Improving Global Outcomes |
CRC | colorectal cancer |
BMI | body mass index |
TAC | tacrolimus |
MMF | mycophenolate mofetil |
STER | steroids |
CyA | cyclosporine |
Ever | everolimus |
IBD | inflammatory bowel disease |
References
- Veroux, M.; Corona, D.; Veroux, P. Kidney transplantation: Future challenges. Minerva Chir. 2009, 64, 75–100. [Google Scholar]
- Coemans, M.; Süsal, C.; Döhler, B.; Anglicheau, D.; Giral, M.; Bestard, O.; Legendre, C.; Emonds, M.-P.; Kuypers, D.; Molenberghs, G.; et al. Analyses of the short- and long-term graft survival after kidney transplantation in Europe between 1986 and 2015. Kidney Int. 2018, 94, 964–973. [Google Scholar] [CrossRef] [PubMed]
- Veroux, M.; Puliatti, C.; Fiamingo, P.; Cappello, D.; Macarone, M.; Puliatti, D.; Vizcarra, D.; Gagliano, M.; Veroux, P. Early de novo malignancies after kidney transplantation. Transplant. Proc. 2004, 36, 718–720. [Google Scholar] [CrossRef]
- Piselli, P.; Serraino, D.; Segoloni, G.P.; Sandrini, S.; Piredda, G.B.; Scolari, M.P.; Rigotti, P.; Busnach, G.; Messa, P.; Donati, D.; et al. Risk of de novo cancers after transplantation: Results from a cohort of 7217 kidney transplant recipients, Italy 1997–2009. Eur. J. Cancer 2013, 49, 336–344. [Google Scholar] [CrossRef]
- Hortlund, M.; Mühr, L.S.A.; Storm, H.; Engholm, G.; Dillner, J.; Bzhalava, D. Cancer risks after solid organ transplantation and after long-term dialysis. Int. J. Cancer 2016, 140, 1091–1101. [Google Scholar] [CrossRef] [PubMed]
- Safaeian, M.; Robbins, H.; Berndt, I.S.; Lynch, C.F.; Fraumeni, J.F., Jr.; Engels, E.A. Risk of Colorectal Cancer After Solid Organ Transplantation in the United States. Arab. Archaeol. Epigr. 2016, 16, 960–967. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hall, E.C.; Pfeiffer, R.M.; Segev, D.L.; Engels, E.A. Cumulative incidence of cancer after solid organ transplantation. Cancer 2013, 119, 2300–2308. [Google Scholar] [CrossRef]
- Engels, E.A.; Pfeiffer, R.M.; Fraumeni, J.F.; Kasiske, B.L.; Israni, A.K.; Snyder, J.J.; Wolfe, R.A.; Goodrich, N.P.; Bayakly, A.R.; Clarke, C.A.; et al. Spectrum of Cancer Risk Among US Solid Organ Transplant Recipients. JAMA 2011, 306, 1891–1901. [Google Scholar] [CrossRef]
- Collins, M.; Teo, E.; Cole, S.R.; Chan, C.-Y.; McDonald, S.P.; Russ, G.R.; Young, G.; Bampton, A.P.; Coates, P.T. Screening for colorectal cancer and advanced colorectal neoplasia in kidney transplant recipients: Cross sectional prevalence and diagnostic accuracy study of faecal immunochemical testing for haemoglobin and colonoscopy. BMJ 2012, 345, e4657. [Google Scholar] [CrossRef] [Green Version]
- Kwon, J.H.; Koh, S.-J.; Kim, J.Y.; Kim, J.W.; Lee, K.L.; Kim, B.G.; Im, J.P.; Kim, J.S. Prevalence of Advanced Colorectal Neoplasm After Kidney Transplantation: Surveillance Based on the Results of Screening Colonoscopy. Dig. Dis. Sci. 2015, 60, 1761–1769. [Google Scholar] [CrossRef]
- Wong, G.; Chapman, J.R.; Craig, J. Cancer Screening in Renal Transplant Recipients: What Is the Evidence? Clin. J. Am. Soc. Nephrol. 2008, 3, S87–S100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, T.; Kakuta, Y.; Abe, T.; Yamanaka, K.; Imamura, R.; Okumi, M.; Ichimaru, N.; Takahara, S.; Nonomura, N. The benefits of cancer screening in kidney transplant recipients: A single-center experience. Cancer Med. 2015, 5, 153–158. [Google Scholar] [CrossRef]
- World Health Organization. Colorectum Fact Sheet. 2018. Available online: https://www.who.int/news-room/fact-sheets/detail/cancer (accessed on 8 July 2021).
- Park, J.M.; Choi, M.-G.; Kim, S.W.; Chung, I.-S.; Yang, C.W.; Kim, Y.S.; Jung, C.K.; Lee, K.Y.; Kang, J.-H. Increased Incidence of Colorectal Malignancies in Renal Transplant Recipients: A Case Control Study. Arab. Archaeol. Epigr. 2010, 10, 2043–2050. [Google Scholar] [CrossRef]
- Baxter, N.N.; Goldwasser, M.A.; Paszat, L.F.; Saskin, R.; Urbach, D.R.; Rabeneck, L. Association of Colonoscopy and Death From Colorectal Cancer. Ann. Intern. Med. 2009, 150, 1–8. [Google Scholar] [CrossRef]
- Lieberman, D.A. Screening for Colorectal Cancer. N. Engl. J. Med. 2009, 361, 1179–1187. [Google Scholar] [CrossRef] [PubMed]
- Hewitson, P.; Glasziou, P.; Watson, E.; Towler, B.; Irwig, L. Cochrane Systematic Review of Colorectal Cancer Screening Using the Fecal Occult Blood Test (Hemoccult): An Update. Am. J. Gastroenterol. 2008, 103, 1541–1549. [Google Scholar] [CrossRef]
- Canadian Medical Association. Colorectal cancer screening. Recommendation statement from the Canadian Task Force on Preventive Health Care. CMAJ 2001, 165, 206–208. [Google Scholar]
- Sirovich, B.E.; Schwartz, L.M.; Woloshin, S. Screening Men for Prostate and Colorectal Cancer in the United States. JAMA 2003, 289, 1414–1420. [Google Scholar] [CrossRef] [Green Version]
- Acuna, S.; Lam, W.; Daly, C.; Kim, S.J.; Baxter, N.N. Cancer evaluation in the assessment of solid organ transplant candidates: A systematic review of clinical practice guidelines. Transplant. Rev. 2018, 32, 29–35. [Google Scholar] [CrossRef]
- Kasiske, B.L.; Zeier, M.G.; Chapman, J.R.; Craig, J.; Ekberg, H.; Garvey, C.A.; Green, M.D.; Jha, V.; Josephson, M.A.; Kiberd, B.A.; et al. KDIGO clinical practice guideline for the care of kidney transplant recipients: A summary. Kidney Int. 2010, 77, 299–311. [Google Scholar] [CrossRef] [Green Version]
- Wong, G.; Howard, K.; Craig, J.; Chapman, J.R. Cost-Effectiveness of Colorectal Cancer Screening in Renal Transplant Recipients. Transplantation 2008, 85, 532–541. [Google Scholar] [CrossRef] [PubMed]
- Wong, G.; Li, M.W.; Howard, K.; Hua, D.K.; Chapman, J.R.; Bourke, M.; Turner, R.; Tong, A.; Craig, J. Health benefits and costs of screening for colorectal cancer in people on dialysis or who have received a kidney transplant. Nephrol. Dial. Transplant. 2012, 28, 917–926. [Google Scholar] [CrossRef] [Green Version]
- Kiberd, B.A.; Keough-Ryan, T.; Clase, C.M. Screening for Prostate, Breast and Colorectal Cancer in Renal Transplant Recipients. Arab. Archaeol. Epigr. 2003, 3, 619–625. [Google Scholar] [CrossRef] [PubMed]
- Gioco, R.; Corona, D.; Ekser, B.; Puzzo, L.; Inserra, G.; Pinto, F.; Schipa, C.; Privitera, F.; Veroux, P.; Veroux, M. Gastrointestinal complications after kidney transplantation. World J. Gastroenterol. 2020, 26, 5797–5811. [Google Scholar] [CrossRef] [PubMed]
- Gioco, R.; Puzzo, L.; Patanè, M.; Corona, D.; Trama, G.; Veroux, P.; Veroux, M. Post-transplant colitis after kidney transplantation: Clinical, endoscopic and histological features. Aging 2020, 12, 24709–24720. [Google Scholar] [CrossRef]
- Veroux, M.; Zerbo, D.; Basile, G.; Gozzo, C.; Sinagra, N.; Giaquinta, A.; Sanfiorenzo, A.; Veroux, P. Simultaneous Native Nephrectomy and Kidney Transplantation in Patients With Autosomal Dominant Polycystic Kidney Disease. PLoS ONE 2016, 11, e0155481. [Google Scholar] [CrossRef]
- Schoenfeld, P.; Cash, B.; Flood, A.; Dobhan, R.; Eastone, J.; Coyle, W.; Kikendall, J.W.; Kim, H.M.; Weiss, D.G.; Emory, T.; et al. Colonoscopic Screening of Average-Risk Women for Colorectal Neoplasia. N. Engl. J. Med. 2005, 352, 2061–2068. [Google Scholar] [CrossRef]
- Regula, J.; Rupinski, M.; Kraszewska, E.; Polkowski, M.; Pachlewski, J.; Orlowska, J.; Nowacki, M.P.; Butruk, E. Colonoscopy in Colorectal-Cancer Screening for Detection of Advanced Neoplasia. N. Engl. J. Med. 2006, 355, 1863–1872. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.-E.; Liao, Y.-C.; Hu, J.-M.; Wu, W.-C.; Chou, W.-Y.; Chen, Y.-C.; Chou, Y.-C.; Hung, C.-F.; Tian, Y.-F.; You, S.-L.; et al. Correlation between kidney transplantation and colorectal cancer in haemodialysis patients: A nationwide, retrospective, population-based cohort study. BMC Cancer 2019, 19, 1120–1127. [Google Scholar] [CrossRef]
- Gioco, R.; Corona, D.; Agodi, A.; Privitera, F.; Barchitta, M.; Giaquinta, A.; Alba, I.; D’Erricod, S.; Pintod, F.; Pasquale, C.D.; et al. De Novo Cancer Incidence and Prognosis After Kidney Transplantation: A Single Center Analysis. Transpl. Proc. 2019, 51, 2927–2930. [Google Scholar] [CrossRef]
- Veroux, M.; Giuffrida, G.; Bianco, S.L.; Cannizzaro, M.A.; Corona, D.; Giaquinta, A.; Palermo, C.; Carbone, F.; Carbonaro, A.; Cannizzaro, M.T.; et al. Thyroid disease and cancer in kidney transplantation: A single-center analysis. BMC Surg. 2019, 18, 80. [Google Scholar] [CrossRef]
- Revuelta, I.; Rull, D.M.; García-Herrera, A.; Rovira, J.; de la Peña, F.A.; Misiego, A.; Guzmán, F.; Oppenheimer, F.; Albanell, J.; Campistol, J.M. Role of Oncogenic Pathways and KRAS/BRAF Mutations in the Behavior of Colon Adenocarcinoma in Renal Transplant Patients. Transplantation 2012, 93, 509–517. [Google Scholar] [CrossRef]
- Wong, G.; Hope, R.L.; Howard, K.; Chapman, J.R.; Castells, A.; Roger, S.D.; Bourke, M.J.; Macaskill, P.; Turner, R.; Williams, G.; et al. One-Time Fecal Immunochemical Screening for Advanced Colorectal Neoplasia in Patients with CKD (DETECT Study). J. Am. Soc. Nephrol. 2019, 30, 1061–1072. [Google Scholar] [CrossRef]
- Rosales, B.M.; De La Mata, N.; Vajdic, C.M.; Kelly, P.J.; Wyburn, K.; Webster, A.C. Cancer mortality in kidney transplant recipients: An Australian and New Zealand population-based cohort study, 1980–2013. Int. J. Cancer 2019, 146, 2703–2711. [Google Scholar] [CrossRef]
- Benoni, H.; Eloranta, S.; Ekbom, A.; Wilczek, H.; Smedby, K.E.; Wilzcek, H. Survival among solid organ transplant recipients diagnosed with cancer compared to nontransplanted cancer patients—A nationwide study. Int. J. Cancer 2019, 146, 682–691. [Google Scholar] [CrossRef]
- Merchea, A.; Shahjehan, F.; Croome, K.P.; Cochuyt, J.J.; Li, Z.; Colibaseanu, D.T.; Kasi, P.M. Colorectal Cancer Characteristics and Outcomes after Solid Organ Transplantation. J. Oncol. 2019, 2019, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Juul, J.S.; Hornung, N.; Andersen, B.; Laurberg, S.; Olesen, F.; Vedsted, P. The value of using the faecal immunochemical test in general practice on patients presenting with non-alarm symptoms of colorectal cancer. Br. J. Cancer 2018, 119, 471–479. [Google Scholar] [CrossRef] [Green Version]
- Westwood, M.; Lang, S.; Armstrong, N.; Van Turenhout, S.; Cubiella, J.; Stirk, L.; Ramos, I.C.; Luyendijk, M.; Zaim, R.; Kleijnen, J.; et al. Faecal immunochemical tests (FIT) can help to rule out colorectal cancer in patients presenting in primary care with lower abdominal symptoms: A systematic review conducted to inform new NICE DG30 diagnostic guidance. BMC Med. 2017, 15, 1–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Characteristics | Entire Study Group | Advanced Colorectal Adenoma | Negative Findings | p Value |
---|---|---|---|---|
N | 160 | 22 | 138 | |
Deceased/living donor | 145/15 | 18/4 | 127/11 | 0.825 |
Age (years) | 49.2 ± 8.15 | 57.3 ± 8.77 | 52.6 ± 10.21 | <0.05 |
Sex (M/F) | 95/65 | 13/9 | 82/56 | 0.228 |
BMI (Kg/m2) | 25.9 ± 12.2 | 26.4 ± 3.8 | 25.7 ± 4 | 0.473 |
Cause of End-stage Renal disease (n, %) | ||||
Polycystic kidney disease | 40 (25) | 6 (27.3) | 34 (24.7) | 0.895 |
Glomerulonephritis | 62 (38.7) | 11 (50) | 51 (36.9) | 0.334 |
Diabetes mellitus | 5 (3.1) | 1 (4.5) | 4 (2.9) | 0.324 |
Others * | 30 (18.9) | 2 (9.1) | 28 (20.3) | 0.222 |
Unknown | 23 (14.3) | 2 (9.1) | 21 (15.2) | 0.332 |
Waiting List (months) | 20.2 ± 10.5 | 18.5 ± 15.6 | 19.4 ± 21.6 | 0.775 |
Pre-transplant dialysis (months) | 41.3 ± 39.5 | 34.7 ± 21.7 | 35.3 ± 40.2 | 0.545 |
Haemodialysis/peritoneal dialysis | 129/16 | 15/5 | 114/11 | 0.645 |
No dialysis (n, %) | 15 (5) | 2 (9) | 13 (9.2) | 0.876 |
Dual kidney transplantation (n, %) | 8 (5) | 2 (9) | 6 (4.2) | 0.777 |
Second transplantation (n, %) | 15 (9.3) | 3 (15) | 12 (8.5) | 0.634 |
Kidney-pancreas transplant (n, %) | 7 (4.3) | 0 (0) | 7 (5) | 0.231 |
Donor age (years) | 47.7 ± 15.8 | 50.8 ± 13.8 | 52.5 ± 11.1 | 0.325 |
Donor terminal serum creatinine (mg/dL) | 1.24 ± 0.6 | 1.22 ± 0.7 | 1.28 ± 0.7 | 0.654 |
Cold ischemia time (min) | 918 ± 335.5 | 921 ± 321.8 | 932 ± 355.5 | 0.644 |
Immunosuppression (n, %) | ||||
Tac/MMF/Ster | 120 (75) | 14 (63.7) | 105 (76) | 0.735 |
CyA/Ever/Ster | 12 (7.5) | 2 (9) | 10 (7.3) | 0.865 |
Tac/Ever/Ster | 12 (7.5) | 4 (18.3) | 9 (6.5) | 0.745 |
Ever/MMF/Ster | 6 (3.8) | 0 (0%) | 6 (4.4) | 0.553 |
CyA/MMF/Ster | 10 (6.2) | 2 (9) | 8 (5.8) | 0.622 |
Time to transplant (years) | 6.5 ± 8.4 | 8.1 ± 7.7 | 6.8 ± 4.1 | <0.01 |
Mean serum creatinine | 1.90 ± 1.11 | 1.89 ± 1.13 | 1.77 ± 1.31 | 0.432 |
Significant Comorbidities (n, %) | ||||
Diabetes | 13 (8.1) | 3 (13.6) | 10 (7.2) | 0.0308 |
Cardiovascular disease | 22 (13.7%) | 4 (18.1%) | 18 (13) | 0.515 |
Chronic lung disease | 6 (3.7) | 1 (4.5) | 5 (3.6) | 0.832 |
Transplant Recipients (N = 160) (%) | Healthy Controls (N = 594) | p | |
---|---|---|---|
Colonoscopic Findings | |||
Colorectal cancer | 4 (2.5) | 21 (3.5) | 0.535 |
High-grade adenoma | 4 (2.5) | 8 (1.3) | 0.093 |
Tubulovillous, villous adenoma | 10 (6.2) | 22 (3.7) | p < 0.05 |
High-grade tubular adenoma > 10 mm | 4 (2.5) | 12 (2) | 0.735 |
Low-grade tubular adenoma | 5 (3.1) | 42 (7) | 0.723 |
Hyperplastic polyp | 8 (5) | 50 (8.4) | 0.735 |
Ulcerative colitis | 4 (2.5) | 5 (0.8) | p < 0.05 |
Crohn disease | 5 (3.1) | 4 (0.6) | p < 0.05 |
Mycophenolate mofetil- colitis | 9 (5.6) | 0 (0) | p < 0.01 |
Other (Sarcoma di Kaposi, Pseudomembranous colitis) | 3 (1.8) | 0 (0) | p < 0.01 |
Diverticulosis | 20 (12.7) | 87 (14.6) | 0.732 |
Haemorrhoids/Normal Findings | 84 (52.5) | 343 (57.7) | 0.331 |
Advanced Colorectal Neoplasia | Positive | Negative | Total |
---|---|---|---|
Present | 20 | 2 | 22 |
Absent | 96 | 42 | 140 |
Total | 116 | 44 | 160 |
Kidney Transplant Recipients (n = 160) | Control Group (n = 594) | Odds Ratio (95% CI) | p Value | |
---|---|---|---|---|
Advanced Adenoma (%) | 18 (11.2) | 42 (7) | OR 1.65 (0.930–2.981) | 0.04 |
Colorectal cancer (%) | 4 (2.5) | 21 (3.5) | OR 0.69 (0.236–2.063) | 0.688 |
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Privitera, F.; Gioco, R.; Civit, A.I.; Corona, D.; Cremona, S.; Puzzo, L.; Costa, S.; Trama, G.; Mauceri, F.; Cardella, A.; et al. Colorectal Cancer after Kidney Transplantation: A Screening Colonoscopy Case-Control Study. Biomedicines 2021, 9, 937. https://doi.org/10.3390/biomedicines9080937
Privitera F, Gioco R, Civit AI, Corona D, Cremona S, Puzzo L, Costa S, Trama G, Mauceri F, Cardella A, et al. Colorectal Cancer after Kidney Transplantation: A Screening Colonoscopy Case-Control Study. Biomedicines. 2021; 9(8):937. https://doi.org/10.3390/biomedicines9080937
Chicago/Turabian StylePrivitera, Francesca, Rossella Gioco, Alba Ilari Civit, Daniela Corona, Simone Cremona, Lidia Puzzo, Salvatore Costa, Giuseppe Trama, Flavia Mauceri, Aurelio Cardella, and et al. 2021. "Colorectal Cancer after Kidney Transplantation: A Screening Colonoscopy Case-Control Study" Biomedicines 9, no. 8: 937. https://doi.org/10.3390/biomedicines9080937