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Published in: World Journal of Surgery 11/2019

01-11-2019 | Colorectal Cancer | Surgery in Low and Middle Income Countries

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

Authors: Gregory C. Knapp, Avinash Sharma, Bolatito Olopade, Olusegun I. Alatise, Olalekan Olasehinde, Olujide O. Arije, Philip E. Castle, T. Peter Kingham

Published in: World Journal of Surgery | Issue 11/2019

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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.
Literature
1.
go back to reference Karsa LV, Lignini TA, Patnick J, Lambert R, Sauvaget C (2010) The dimensions of the CRC problem. Best Pract Res Clin Gastroenterol 24(4):381–396CrossRef Karsa LV, Lignini TA, Patnick J, Lambert R, Sauvaget C (2010) The dimensions of the CRC problem. Best Pract Res Clin Gastroenterol 24(4):381–396CrossRef
2.
go back to reference Lambert R, Sauvaget C, Sankaranarayanan R (2009) Mass screening for colorectal cancer is not justified in most developing countries. Int J Cancer 125(2):253–256CrossRef Lambert R, Sauvaget C, Sankaranarayanan R (2009) Mass screening for colorectal cancer is not justified in most developing countries. Int J Cancer 125(2):253–256CrossRef
3.
go back to reference Ishola F, Omole O (2016) A vision for improved cancer screening in Nigeria. Lancet Glob Health 4(6):e359–e360CrossRef Ishola F, Omole O (2016) A vision for improved cancer screening in Nigeria. Lancet Glob Health 4(6):e359–e360CrossRef
4.
go back to reference 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–e151CrossRef 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–e151CrossRef
5.
go back to reference Irabor DO (2017) Emergence of colorectal cancer in West Africa: accepting the inevitable. Niger Med J 58(3):87–91CrossRef Irabor DO (2017) Emergence of colorectal cancer in West Africa: accepting the inevitable. Niger Med J 58(3):87–91CrossRef
6.
go back to reference 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):020404CrossRef 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):020404CrossRef
7.
go back to reference 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):305–310CrossRef 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):305–310CrossRef
8.
go back to reference 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.e3CrossRef 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.e3CrossRef
9.
go back to reference 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):297–300CrossRef 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):297–300CrossRef
10.
go back to reference Laiyemo AO, Brawley O, Irabor D, Boutall A, Ramesar RS, Madiba TE (2016) Toward colorectal cancer control in Africa. Int J Cancer 138(4):1033–1034CrossRef Laiyemo AO, Brawley O, Irabor D, Boutall A, Ramesar RS, Madiba TE (2016) Toward colorectal cancer control in Africa. Int J Cancer 138(4):1033–1034CrossRef
11.
go back to reference 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 5:1–22PubMed 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 5:1–22PubMed
12.
go back to reference 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):82–90CrossRef 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):82–90CrossRef
13.
go back to reference 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):805–816CrossRef 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):805–816CrossRef
14.
go back to reference 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):171–1484CrossRef 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):171–1484CrossRef
15.
go back to reference 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):2766–2773CrossRef 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):2766–2773CrossRef
16.
go back to reference 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):1511–1515CrossRef 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):1511–1515CrossRef
17.
go back to reference 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):99–107CrossRef 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):99–107CrossRef
18.
go back to reference 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):2178–2183CrossRef 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):2178–2183CrossRef
19.
go back to reference 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):578–582CrossRef 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):578–582CrossRef
20.
go back to reference 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):2208–2212CrossRef 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):2208–2212CrossRef
21.
go back to reference 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):462–464CrossRef 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):462–464CrossRef
22.
go back to reference 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):146–152PubMedPubMedCentral 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):146–152PubMedPubMedCentral
23.
go back to reference 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):1048–1055CrossRef 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):1048–1055CrossRef
24.
go back to reference 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):285–294CrossRef 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):285–294CrossRef
25.
go back to reference 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):e2542CrossRef 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):e2542CrossRef
27.
go back to reference 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):934–935CrossRef 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):934–935CrossRef
28.
go back to reference 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):115–118CrossRef 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):115–118CrossRef
29.
go back to reference 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):20–28 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):20–28
30.
go back to reference Navarro M, Nicolas A, Ferrandez A, Lanas A (2017) Colorectal cancer population screening programs worldwide in 2016: an update. World J Gastroenterol 23(20):3632–3642CrossRef Navarro M, Nicolas A, Ferrandez A, Lanas A (2017) Colorectal cancer population screening programs worldwide in 2016: an update. World J Gastroenterol 23(20):3632–3642CrossRef
31.
go back to reference 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):756–762CrossRef 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):756–762CrossRef
32.
go back to reference Oluyemi A, Awolola N, Oyedeji O (2016) Clinicopathologic review of polyps biopsied at colonoscopy in Lagos, Nigeria. Pan Afr Med J 24:333CrossRef Oluyemi A, Awolola N, Oyedeji O (2016) Clinicopathologic review of polyps biopsied at colonoscopy in Lagos, Nigeria. Pan Afr Med J 24:333CrossRef
33.
go back to reference Irabor D, Adedeji OA (2009) Colorectal cancer in Nigeria: 40 years on. A review. Eur J Cancer Care 18(2):110–115CrossRef Irabor D, Adedeji OA (2009) Colorectal cancer in Nigeria: 40 years on. A review. Eur J Cancer Care 18(2):110–115CrossRef
34.
go back to reference 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 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.
go back to reference Brenner H, Werner S (2017) Selecting a cut-off for colorectal cancer screening with a fecal immunochemical test. Clin Transl Gastroenterol 8(8):e111CrossRef Brenner H, Werner S (2017) Selecting a cut-off for colorectal cancer screening with a fecal immunochemical test. Clin Transl Gastroenterol 8(8):e111CrossRef
36.
go back to reference 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):e003671CrossRef 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):e003671CrossRef
37.
go back to reference 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):187–193CrossRef 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):187–193CrossRef
38.
go back to reference 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):75–82CrossRef 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):75–82CrossRef
39.
go back to reference 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.e5CrossRef 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.e5CrossRef
Metadata
Title
An Exploratory Analysis of Fecal Immunochemical Test Performance for Colorectal Cancer Screening in Nigeria
Authors
Gregory C. Knapp
Avinash Sharma
Bolatito Olopade
Olusegun I. Alatise
Olalekan Olasehinde
Olujide O. Arije
Philip E. Castle
T. Peter Kingham
Publication date
01-11-2019
Publisher
Springer International Publishing
Published in
World Journal of Surgery / Issue 11/2019
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-019-05100-0

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