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An Exploratory Analysis of Fecal Immunochemical Test Performance for Colorectal Cancer Screening in Nigeria

  • Gregory C. KnappEmail author
  • Avinash Sharma
  • Bolatito Olopade
  • Olusegun I. Alatise
  • Olalekan Olasehinde
  • Olujide O. Arije
  • Philip E. Castle
  • T. Peter Kingham
Surgery in Low and Middle Income Countries

Abstract

Introduction

The fecal immunochemical test (FIT) for hemoglobin is recommended for colorectal cancer (CRC) screening in resource-limited environments. However, there are several unique variables that may alter FIT performance in this setting, including endemic intestinal parasites and high ambient temperature. This prospective study evaluated the performance of FIT in asymptomatic, average-risk individuals of screening age in rural Nigeria.

Methods

Three hundred and twenty-four community volunteers completed a questionnaire and provided stool specimens for parasitology and microbiome analysis. Specimens were frozen and stored at −80 °C. Of 324 subjects, 139 met criteria for average-risk CRC screening and had a stool sample for analysis. These were thawed and tested with a qualitative FIT. Specimens positive for occult blood were retested every two days to evaluate the impact of time and temperature on test performance.

Results

Of 139 individuals, 69 (49.6%) were positive for intestinal parasites and 10 (7.2%) were positive for occult blood. The most common pathogen was Cryptosporidium (40.6%). Among patients with intestinal parasites, 10.1% (7/69) had a positive FIT. Only 4.3% (3/70) of patients without parasites had a positive FIT (p = 0.208). On bivariate analysis, sociodemographic variables were not associated with a positive FIT result. Thirty percent (3/10) of the FIT-positive specimens became FIT-negative with routine storage.

Conclusion

Although a positive FIT result was more common in those with parasitic infection, the relationship was not significant in this small cohort. The impact of high ambient temperature on test positivity may necessitate shorter processing time guidelines for equatorial countries. Additional prospective studies are needed to validate FIT performance in Nigeria.

Notes

Acknowledgements

The Global Cancer Disparities Initiative is funded by Memorial Sloan Kettering Cancer Center, with support from the Thompson Family Foundation. This research was funded in part through the NIH/NCI Cancer Center Support Grant P30 CA008748. The authors would like to acknowledge the dedicated surgical research team at OAUTHC for their help with data entry and stool specimen processing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Referencess

  1. 1.
    Karsa LV, Lignini TA, Patnick J, Lambert R, Sauvaget C (2010) The dimensions of the CRC problem. Best Pract Res Clin Gastroenterol 24(4):381–396CrossRefPubMedGoogle Scholar
  2. 2.
    Lambert R, Sauvaget C, Sankaranarayanan R (2009) Mass screening for colorectal cancer is not justified in most developing countries. Int J Cancer 125(2):253–256CrossRefPubMedGoogle Scholar
  3. 3.
    Ishola F, Omole O (2016) A vision for improved cancer screening in Nigeria. Lancet Glob Health 4(6):e359–e360CrossRefPubMedGoogle Scholar
  4. 4.
    Morhason-Bello IO, Odedina F, Rebbeck TR, Harford J, Dangou JM, Denny L et al (2013) Challenges and opportunities in cancer control in Africa: a perspective from the African organisation for research and training in cancer. Lancet Oncol 14(4):e142–e151CrossRefPubMedGoogle Scholar
  5. 5.
    Irabor DO (2017) Emergence of colorectal cancer in West Africa: accepting the inevitable. Niger Med J 58(3):87–91CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Graham A, Adeloye D, Grant L, Theodoratou E, Campbell H (2012) Estimating the incidence of colorectal cancer in sub-Saharan Africa: a systematic analysis. J Glob Health 2(2):020404CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Saluja S, Alatise OI, Adewale A, Misholy J, Chou J, Gonen M et al (2014) A comparison of colorectal cancer in Nigerian and North American patients: is the cancer biology different? Surgery 156(2):305–310CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Robertson DJ, Lee JK, Boland CR, Dominitz JA, Giardiello FM, Johnson DA et al (2017) Recommendations on fecal immunochemical testing to screen for colorectal neoplasia: a consensus statement by the US multi-society task force on colorectal cancer. Gastroenterology 152(5):1217–1237.e3CrossRefPubMedGoogle Scholar
  9. 9.
    Winawer SJ, Krabshuis J, Lambert R, O'Brien M, Fried M, World Gastroenterology Organization Guidelines Committee (2011) Cascade colorectal cancer screening guidelines: a global conceptual model. J Clin Gastroenterol 45(4):297–300CrossRefPubMedGoogle Scholar
  10. 10.
    Laiyemo AO, Brawley O, Irabor D, Boutall A, Ramesar RS, Madiba TE (2016) Toward colorectal cancer control in Africa. Int J Cancer 138(4):1033–1034CrossRefPubMedGoogle Scholar
  11. 11.
    Lopes G, Stern MC, Temin S, Sharara AI, Cervantes A, Costas-Chavarri A et al (2019) Early detection for colorectal cancer: ASCO resource-stratified guideline. J Glob Oncol 5:1–22PubMedGoogle Scholar
  12. 12.
    van Rossum LG, van Rijn AF, Laheij RJ, van Oijen MG, Fockens P, van Krieken HH et al (2008) Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology 135(1):82–90CrossRefPubMedGoogle Scholar
  13. 13.
    Sharp L, Tilson L, Whyte S, O'Ceilleachair A, Walsh C, Usher C et al (2012) Cost-effectiveness of population-based screening for colorectal cancer: a comparison of guaiac-based faecal occult blood testing, faecal immunochemical testing and flexible sigmoidoscopy. Br J Cancer 106(5):805–816CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Lee JK, Liles EG, Bent S, Levin TR, Corley DA (2014) Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta-analysis. Ann Intern Med 160(3):171–1484CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Alatise OI, Ayandipo OO, Adeyeye A, Seier K, Komolafe AO, Bojuwoye MO et al (2018) A symptom-based model to predict colorectal cancer in low-resource countries: results from a prospective study of patients at high risk for colorectal cancer. Cancer 124(13):2766–2773CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Grazzini G, Ventura L, Zappa M, Ciatto S, Confortini M, Rapi S et al (2010) Influence of seasonal variations in ambient temperatures on performance of immunochemical faecal occult blood test for colorectal cancer screening: observational study from the Florence district. Gut 59(11):1511–1515CrossRefPubMedGoogle Scholar
  17. 17.
    van Roon AH, Hol L, van Vuuren AJ, Francke J, Ouwendijk M, Heijens A et al (2012) Are fecal immunochemical test characteristics influenced by sample return time? A population-based colorectal cancer screening trial. Am J Gastroenterol 107(1):99–107CrossRefPubMedGoogle Scholar
  18. 18.
    Cha JM, Lee JI, Joo KR, Shin HP, Park JJ, Jeun JW et al (2012) Performance of the fecal immunochemical test is not decreased by high ambient temperature in the rapid return system. Dig Dis Sci 57(8):2178–2183CrossRefPubMedGoogle Scholar
  19. 19.
    Efunshile AM, Olawale T, Stensvold CR, Kurtzhals JA, Konig B (2015) Epidemiological study of the association between malaria and helminth infections in Nigeria. Am J Trop Med Hyg 92(3):578–582CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Adeoye GO, Osayemi CO, Oteniya O, Onyemekeihia SO (2007) Epidemiological studies of intestinal helminthes and malaria among children in Lagos, Nigeria. Pak J Biol Sci 10(13):2208–2212CrossRefPubMedGoogle Scholar
  21. 21.
    Akinbo FO, Omoregie R, Eromwon R, Igbenimah IO, Airueghiomon UE (2011) Prevalence of intestinal parasites among patients of a tertiary hospital in Benin city, Nigeria. N Am J Med Sci 3(10):462–464CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Tyoalumun K, Abubakar S, Christopher N (2016) Prevalence of intestinal parasitic infections and their association with nutritional status of rural and urban pre-school children in Benue state, Nigeria. Int J MCH AIDS 5(2):146–152PubMedPubMedCentralGoogle Scholar
  23. 23.
    Betson M, Sousa-Figueiredo JC, Rowell C, Kabatereine NB, Stothard JR (2010) Intestinal schistosomiasis in mothers and young children in Uganda: investigation of field-applicable markers of bowel morbidity. Am J Trop Med Hyg 83(5):1048–1055CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lehman JS Jr, Mott KE, Morrow RH Jr, Muniz TM, Boyer MH (1976) The intensity and effects of infection with Schistosoma mansoni in a rural community in Northeast Brazil. Am J Trop Med Hyg 25(2):285–294CrossRefPubMedGoogle Scholar
  25. 25.
    Bustinduy AL, Sousa-Figueiredo JC, Adriko M, Betson M, Fenwick A, Kabatereine N et al (2013) Fecal occult blood and fecal calprotectin as point-of-care markers of intestinal morbidity in Ugandan children with Schistosoma mansoni infection. PLoS Negl Trop Dis 7(11):e2542CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Wakid MH (2010) Fecal occult blood test and gastrointestinal parasitic infection. J Parasitol Res.  https://doi.org/10.1155/2010/434801 (Epub 2010 Jul 26)CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Okamoto M, Kawabe T, Ohata K, Togo G, Hada T, Katamoto T et al (2005) Amebic colitis in asymptomatic subjects with positive fecal occult blood test results: clinical features different from symptomatic cases. Am J Trop Med Hyg 73(5):934–935CrossRefPubMedGoogle Scholar
  28. 28.
    Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Olveda RM, McGarvey ST et al (2005) Schistosoma japonicum and occult blood loss in endemic villages in Leyte, the Philippines. Am J Trop Med Hyg 72(2):115–118CrossRefPubMedGoogle Scholar
  29. 29.
    Ugwuoke HJ, Okonkwo BC, Oshilonyah HU (2013) Faecel occult blood and intestinal parasites among patients attending out patient clinic in Agbor, Delta State Nigeria. Arch Biomed Sci Health 1(1):20–28Google Scholar
  30. 30.
    Navarro M, Nicolas A, Ferrandez A, Lanas A (2017) Colorectal cancer population screening programs worldwide in 2016: an update. World J Gastroenterol 23(20):3632–3642CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Alatise OI, Arigbabu AO, Agbakwuru AE, Lawal OO, Sowande OA, Odujoko OO et al (2014) Polyp prevalence at colonoscopy among Nigerians: a prospective observational study. Niger J Clin Pract 17(6):756–762CrossRefPubMedGoogle Scholar
  32. 32.
    Oluyemi A, Awolola N, Oyedeji O (2016) Clinicopathologic review of polyps biopsied at colonoscopy in Lagos, Nigeria. Pan Afr Med J 24:333CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Irabor D, Adedeji OA (2009) Colorectal cancer in Nigeria: 40 years on. A review. Eur J Cancer Care 18(2):110–115CrossRefGoogle Scholar
  34. 34.
    Parkin DM, Ferlay J, Jemal A, Borok M, Manraj SS, N'da GG, Ogunbiyi FJ, Liu B, Bray F (eds) (2018) Cancer in sub-Sahara Africa, International Agency for Research on Cancer, Scientific Publication No. 167. https://publications.iarc.fr. Accessed 3 Feb 2019
  35. 35.
    Brenner H, Werner S (2017) Selecting a cut-off for colorectal cancer screening with a fecal immunochemical test. Clin Transl Gastroenterol 8(8):e111CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Khuhaprema T, Sangrajrang S, Lalitwongsa S, Chokvanitphong V, Raunroadroong T, Ratanachu-Ek T et al (2014) Organised colorectal cancer screening in Lampang province, Thailand: preliminary results from a pilot implementation programme. BMJ Open 4(1):e003671CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Symonds EL, Osborne JM, Cole SR, Bampton PA, Fraser RJ, Young GP (2015) Factors affecting faecal immunochemical test positive rates: demographic, pathological, behavioural and environmental variables. J Med Screen 22(4):187–193CrossRefPubMedGoogle Scholar
  38. 38.
    Catomeris P, Baxter NN, Boss SC, Paszat LF, Rabeneck L, Randell E et al (2018) Effect of temperature and time on fecal hemoglobin stability in 5 fecal immunochemical test methods and one guaiac method. Arch Pathol Lab Med 142(1):75–82CrossRefPubMedGoogle Scholar
  39. 39.
    Chen H, Werner S, Brenner H (2017) Fresh vs frozen samples and ambient temperature have little effect on detection of colorectal cancer or adenomas by a fecal immunochemical test in a colorectal cancer screening cohort in Germany. Clin Gastroenterol Hepatol 15(10):1547–1556.e5CrossRefPubMedGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2019

Authors and Affiliations

  • Gregory C. Knapp
    • 1
    Email author
  • Avinash Sharma
    • 1
  • Bolatito Olopade
    • 2
  • Olusegun I. Alatise
    • 3
  • Olalekan Olasehinde
    • 3
  • Olujide O. Arije
    • 4
  • Philip E. Castle
    • 5
  • T. Peter Kingham
    • 1
  1. 1.Memorial Sloan Kettering Cancer CenterNew YorkUSA
  2. 2.Department of Medical Microbiology and Parasitology, College of Health SciencesObafemi Awolowo UniversityIle-IfeNigeria
  3. 3.Department of Surgery College of Health SciencesObafemi Awolowo UniversityIle-IfeNigeria
  4. 4.Institute of Public HealthObafemi Awolowo UniversityIle-IfeNigeria
  5. 5.Department of Epidemiology and Public HealthAlbert Einstein College of MedicineNew YorkUSA

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