Nigerian Medical Journal

REVIEW ARTICLE
Year
: 2017  |  Volume : 58  |  Issue : 3  |  Page : 87--91

Emergence of colorectal cancer in West Africa: Accepting the inevitable


David O Irabor 
 Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria

Correspondence Address:
Dr. David O Irabor
Department of Surgery, University College Hospital, PMB 5116, Ibadan, Oyo State
Nigeria

Abstract

It seems not too long ago that colon and rectal cancer is a “rare” disease in rural Africa; however, over the last 30 years in West Africa, published evidence has shown decade by decade increases in the incidence of colorectal cancer (CRC). Therefore, CRC should now be accepted as a recognized disease in native Africans; nevertheless, we must acknowledge that the incidence is a fraction of what obtains in the developed countries of Europe and America. This presentation will attempt to examine the emergence of CRC within the West African axis over the last four decades.



How to cite this article:
Irabor DO. Emergence of colorectal cancer in West Africa: Accepting the inevitable.Niger Med J 2017;58:87-91


How to cite this URL:
Irabor DO. Emergence of colorectal cancer in West Africa: Accepting the inevitable. Niger Med J [serial online] 2017 [cited 2018 Dec 10 ];58:87-91
Available from: http://www.nigeriamedj.com/text.asp?2017/58/3/87/234076


Full Text

 Introduction



It seems not too long ago that colon and rectal cancer is a “rare” disease in rural Africa; however, over the last 30 years in West Africa, published evidence has shown decade by decade increases in the incidence of colorectal cancer (CRC).[1],[2] Therefore, CRC should now be accepted as a recognized disease in native Africans; nevertheless, we must acknowledge that the incidence is a fraction of what obtains in the developed countries of Europe and America. This presentation will attempt to examine the emergence of CRC within the West African axis over the last four decades.

The crude incidence of CRC in Sub-Saharan Africa (SSA) is estimated at 4.04/100,000 population (4.38 men and 3.69 women).[3]

Most of the studies available showed an average age of between 43 and 46 years (peak age 50–60 years), except Ghana where the average age is 58 years (peak age 70–80 years).[4],[5],[6],[7],[8],[9],[10]

 How Was it Before?



West African populations are of similar genetic origin; thus, much of the subtle or overt differences in cancer incidence are presumably due to different environmental circumstances. The diverse ethnicity of the West African peoples translated into different dietary patterns which more or less reflected the geographical peculiarities of the regions. Diet, as has been extensively researched, is known to be a major determining factor in the development of CRC, which is why the changing dietary patterns along the West African subregion should be subjected to closer scrutiny.

“The different climates in West Africa, with regard to agro-ecological systems, can be described as semi-arid, subhumid, and humid. Thus, food grown and consumed is influenced by these climatic conditions. In this respect, two large groups of countries can be identified on the basis of food consumption:

Predominantly, cereals consumers. These include Burkina Faso, Chad, The Gambia, Guinea-Bissau, Mali, Mauritania, Niger, Senegal, and Sierra Leone. They can be further divided into those relying mostly on sorghum and millet (Burkina Faso, Chad, The Gambia, Mali, and Niger), wheat (Mauritania), and rice (Guinea-Bissau, Senegal, and Sierra Leone). These countries lean more into the Sahel regionCountries from coastal West Africa relying equally on roots, tubers, and cereals. These include Benin, Cameroun, Cote d'Ivoire, Ghana, Guinea, Liberia, Nigeria, and Togo. Cassava, yams, and plantains are consumed in these countries. Rice and maize are also consumed heartily.

Protein sources are said to be insufficient in the West African subregion despite the huge livestock sector, especially cattle. Consumption statistics of animal protein are scanty, and no reliable analyses quantifying household meat and protein consumption have been made.”[11]

Over 40–50 years ago, the age-adjusted incidence rates of CRC in the West African subregion were <3 per 100,000 population. Nigeria in the 1960s had about 3.2/100,000,[12] while the lowest was from the Gambia where 1.5/100,000 was recorded from 1986 to 1988.[5] Liver cancer is the most frequent cancer in Gambia (58%).[6] Senegal showed 2.1/100,000 from 1969 to 1974 while Mali was 2.3/100,000 between 1987 and 1988 [Table 1].[5] Mali also has a significant incidence of liver cancer; indeed, it is of the same magnitude as Senegal and Gambia.[5] The West African population has a mix of Anglophone and Francophone colonial legacies, and cursory observation shows that the Francophone countries (grain consumers) seem to have a lower incidence of CRC than the Anglophone countries (roots and tubers consumers) but a higher rate of hepatocellular carcinoma.{Table 1}

 How is it Now?



Studies that occurred more than 10 years after those earlier reported showed marginal increases in the CRC incidence in most of the countries. Mali significantly showed a big jump from the previous 2.3 in 1987/88 to 6/100,000 in 1988–1992.[6] Recent studies from Mali show an incidence averaging 16 patients per annum from 2001 to 2005.[13] Ghana also showed its earliest calculated age-adjusted incidence to be 11.8/100,000 [Table 2].[2]{Table 2}

Indeed, time trends in both Nigeria and Ghana, respectively, showed significant increases from 21 patients per year (1954–1967) to 70 patients per year (2000–2006)[1],[14],[15],[16],[17],[18],[19],[20] and 4.1 patients per year (1954) to 32.6 per year (1997–2007) [Table 3] and [Table 4].[2],[9],[21],[22]{Table 3}{Table 4}

In the Cameroun, CRC was 2.9% of all recorded cancers in both sexes, the most common being prostate cancer in men. Even with the low rate of CRC, it is on record that it (CRC) has increased in frequency over the last two decades in Cameroun.[7]

 The Concept of Nutrition Transition



Noncommunicable, nutrition-related diseases have emerged in SSA at a faster rate and a lower economic level than in industrialized countries before the battle against undernutrition has been won. The nutrition transition defined as the changes in dietary patterns and nutrient intakes when populations adopt modern lifestyles during economic and social development, urbanization, and acculturation is associated with the documented increases in noncommunicable diseases (NCDs). Most of the broad adverse changes in dietary patterns during the nutrition transition include decreases in staple foods rich in starch and dietary fiber, increases in foods from animal origin rich in total fat and saturated fatty acids, decreases in plant protein sources such as legumes, and increases in energy-dense snack foods, carbonated sweetened beverages, commercially available alcoholic beverages, as well as added sugar, fats, and oils in preparation of food. There is no doubt that the nutrition transition, accompanied by decreased physical activity, leads to increases in overweight and obesity.[23] Over the past 30 years, mean body mass index has been steadily increasing even in low- and middle-income countries, including those in West Africa. The steady increase in urbanization has resulted in the emergence and popularization of soft drinks and fast foods and many Western brand names on the continent. In many urban areas, such Western food items are regarded as desirable status symbols, rapidly inculcated by local inhabitants, and widely consumed.[24]

Unhealthy diets, physical inactivity, and obesity have been linked with increased risk of several cancers such as endometrial, colon, breast, renal cell, pancreatic, and esophageal (adenocarcinoma). Despite this increasing cancer burden, cancer continues to receive a relatively low public health priority in Africa. This may be explained by limited resources and probably other more immediate problems such as HIV/AIDS, malaria, and tuberculosis.[25]

 What Was it Like Before?



There was in Africa generally, among native Africans, a rarity of premalignant colonic lesions such as colonic polyps, ulcerative colitis, and Crohn's disease.[26],[27],[28] The native diet in the Sub-Saharan region was rich in resistant starch, fiber, fruits and nuts, and pepper, which were naturally occurring antioxidants and chemopreventives against CRC.[27],[29],[30],[31]

 Why is it Like it is Now?



Increased longevity, intake of red and processed meat, cigarette smoking, alcohol ingestion, environmental pollution, westernization of diet, and obesity are the contributory factors toward the emergence and entrenchment of CRC in West Africa in contemporary times. The burden of all forms of cancer is increasing in Africa because the population is now aging and increasing bringing with it an increased prevalence of risk factors associated with economic transition which includes smoking, obesity, physical inactivity, and reproductive behaviors. In most urban African populations, there have been changes in diet toward high-saturated fat intake.[25],[32],[33] At present, Nigerians consume the most alcohol in West Africa, and Sierra Leone and the Gambia are the top cigarette-smoking nations in West Africa.[34],[35]

 Emergence of Polyps in West Africa: from Very Rare to Quite a Few to Maybe More Than We Thought



From rarity of polyps…

In a study on resected colon specimens at the University College Hospital, Ibadan, Nigeria, between 1960 and 1969, only forty histologically confirmed cases of colonic polyps were encountered over that 10-year period. Analysis of these cases revealed a preponderance (60%) of the nonneoplastic juvenile type of polyp. Neoplastic polyps, which accounted for <10% of all the specimens, were not encountered in any female patient. All but one of the polyps were reported as solitary on clinical and radiological examination.[36] Experiences like this led many researchers at the time to believe that familial or multiple polyposis of the colon is distinctly rare in the African.[14],[28],[37]

To quite a few…

The status quo was maintained with respect to colonic polyps in Nigeria until the early 1990s when reports were emanating from parts of the country of patients with colonic polyps that had neoplastic potential. From 1992 to 2010, at least five reports were published in some peer-reviewed journals of patients who had features of multiple adenomatous polyposis.[38],[39],[40],[41],[42]

To more than we thought…

With the improvement in hospital infrastructure, diagnostic imaging, health workforce, and training of relevant personnel across West Africa, diagnoses of hitherto rare lesions are being seen. Even though there still seems to be no government-powered CRC screening programs in SSA, many tertiary health centers now have access to flexible fiberoptic endoscopes. The results of some colonoscopy studies show that colonic polyps are not as rare in Africans in the present day; however, those with malignant potential still have a low incidence with the percentage of histopathologically confirmed adenomatous polyps at 6.75% in Ile-Ife, Nigeria, and 2.85% in Accra, Ghana [Table 5].[43],[44],[45],[46],[47]{Table 5}

 Peculiarities of West African Colorectal Cancer



West African patients usually have a higher percentage of rectal than colon cancer,[10],[48],[49],[50] except a paper from Mali that showed 56% colon to 44% rectum proportion.[13] No definite explanation has been put forward for this topographical peculiarity, and this has led some authors to consider the possibility of the etiopathogenesis of rectal cancer as being separate from colon cancer.[51],[52] It is well-known that many patients with CRC in SSA present with advanced diseases;[53] however, late presentation, which is a significant problem,[54],[55] cannot be the sole reason for this because it has been shown that West African CRC shows evidence of unfavorable and/or aggressive tumor biology by the presence of increased mucinous and signet ring types and also the significant affectation of younger patients under 40 years.[1],[13],[48],[49]

 Challenges in West Africa



Lack of government support and framework. It is known that most Sub-Saharan governments have no structured cancer-prevention programs and this makes it difficult to promote cancer awareness and institute advocacy.[56] The reliance on outside funding for control of communicable diseases, for example, malaria, HIV/AIDS, and tuberculosis, has made many governments complacent and unwilling to rise to the challenges which NCDs such as cancer present with respect to funding for adequate control [25]Prevailing nutrition transition with strong attraction to western diet and lifestyle. It seems like there is no way back from this. The pull of fast foods, highly-sugared carbonated drinks, cigarette smoking, and alcohol ingestion is too strong that it is unlikely that this development can be halted or moderated.[23],[24],[25] The effect of this nutrition transition superimposed on the burden of malnutrition may actually directly contribute to the increasing incidence of CRC in SSA because it appears that stunted children showed a greater susceptibility to a high fat diet, lower fat oxidation, and higher fat gain.[24] Obesity is a risk factor for the development of CRC [25],[33]High cost of treatment: Screening, surgery, chemotherapy, and radiotherapy. In the low-economic countries of SSA, the complete treatment for CRC will still be in bits and pieces, stops and starts, with financial challenges of individual patients determining which of the modalities for adequate cancer treatment they can afford at any given time [48]Dearth of radiotherapy centers. Basically, in Africa, there is a shortfall of radiotherapy centers even for basic radiation services. West Africa is the worst hit, where out of 16 countries only 4 countries (Ghana, Mauritania, Nigeria, and Togo) have existing radiotherapy machines.[57] Whether they are functioning optimally is another matter entirely which is beyond the scope of this paperScarcity of literature on molecular biology of West African CRC. In a pilot study in Ibadan, five randomly picked CRC tumors were subjected to microsatellite analysis; two were found to be microsatellite unstable.[58] Another study aimed to determine KRAS and BRAF mutations of Nigerian CRC using CRC tissue from Lagos patients. They showed that 21% of Nigerian CRC patients carry a KRAS mutation (half the rate in Caucasians) and 4.5% BRAF V600E mutation.[59] Other authors tried to determine the MSI status using IHC to detect defects in MMR gene among CRC cases in Ibadan. There was a loss of MMR gene protein (MLH1 and MSH2), indicating MSI in 23% of the cases.[60] A study from Accra, Ghana, analyzed MMR by IHC and sequenced exons 2 and 3 of KRAS and exon 15 of BRAF from ninety paraffin blocks of CRC. The study found 41% of MSI-H, 32% of KRAS, and no BRAF mutations.[49]

 Conclusion



The world is now referred to as a global village given the rapid technological advances in communication, travel, and medical care. Western culture has pervaded the whole of Africa; western modes of dressing, music, electronic devices, and diet are seen as most desirable. Native Africans are turning their backs on native diets because one is seen as more “developed” or “civilized” if a taste for western diet has been acquired. Can we hope for a turn-around to the wholesome, healthy, antioxidant, and chemopreventive property that native African diet offers?[31],[33] This will probably be difficult and too late now.

We must then gear up for the next round of battles against disease in West Africa; the fight against communicable diseases has not been totally won, and now, we are exposing ourselves to factors that will increase cancer. A change in mindset will be the means to winning this battle.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Irabor D, Adedeji OA. Colorectal cancer in Nigeria: 40 years on. A review. Eur J Cancer Care (Engl) 2009;18:110-5.
2Dakubo JC, Naaeder SB, Tettey Y, Gyasi RK. Colorectal carcinoma: An update of current trends in Accra. West Afr J Med 2010;29:178-83.
3Graham A, Adeloye D, Grant L, Theodoratou E, Campbell H. Estimating the incidence of colorectal cancer in Sub-Saharan Africa: A systematic analysis. J Glob Health 2012;2:1-14.
4Jedy-Agba E, Curado MP, Ogunbiyi O, Oga E, Fabowale T, Igbinoba F, et al. Cancer incidence in Nigeria: A report from population-based cancer registries. Cancer Epidemiol 2012;36:e271-8.
5Bayo S, Parkin DM, Koumaré AK, Diallo AN, Ba T, Soumaré S, et al. Cancer in Mali, 1987-1988. Int J Cancer 1990;45:679-84.
6Bah E, Parkin DM, Hall AJ, Jack AD, Whittle H. Cancer in the Gambia: 1988-97. Br J Cancer 2001;84:1207-14.
7Enow Orock GE, Ndom P, Doh AS. Current cancer incidence and trends in Yaounde Cameroun. Oncol Gastroenterol Hepatol Rep 2012;1:58-63.
8Echimane AK, Ahnoux AA, Adoubi I, Hien S, M'Bra K, D'Horpock A, et al. Cancer incidence in Abidjan, Ivory Coast:First results from the cancer registry, 1995-1997. Cancer 2000;89:653-63.
9Naaeder SB, Archampong EQ. Cancer of the colon and rectum in Ghana: A 5-year prospective study. Br J Surg 1994;81:456-9.
10Amegbor K, Napo-Koura GA, Songne-Gnamkoulamba B, Redah D, Tekou A. Epidemiological and pathological aspects of gastrointestinal tumors in Togo. Gastroenterol Clin Biol 2008;32:430-4.
11Elbehri A, Kaminski J, Koroma S, Lafrate M, Benali M. West Africa food systems: An overview of trends and indicators of demand, supply and competitiveness of staple food value chains. In: Elbehri A, editor. Rebuilding West Africa's Food Potential. Rome: FAO/IFAD; 2013.
12Irabor DO, Arowolo A, Afolabi AA. Colon and rectal cancer in Ibadan, Nigeria: An update. Colorectal Dis 2010;12:e43-9.
13Gaudre N, Ly M, Badiaga Y, Dembele AK, Bathily M, Kone A, et al. Epidemiological and clinical features of colorectal cancer at the hematology and oncology ward of Point G in Bamako, Mali from 2005-2001: 113 cases. Mali Med 2013;28:32-6.
14Williams AO, Edington GM. Malignant disease of the colon, rectum and anal canal in Ibadan, Western Nigeria. Dis Colon Rectum 1967;10:301-8.
15Grillo IA, Bond LF, Ebong WW. Cancer of the colon in Nigerians and American Negroes. J Natl Med Assoc 1971;63:357-61.
16Ajao OG. Colon and anorectal neoplasms in a tropical African population. Int Surg 1979;64:47-52.
17Adekunle OO, Abioye AA. Adenocarcinoma of the large bowel in Nigerians: A clinicopathologic study. Dis Colon Rectum 1980;23:559-63.
18Iliyasu Y, Ladipo JK, Akang EE, Adebamowo CA, Ajao OG, Aghadiuno PU. A twenty-year review of malignant colorectal neoplasms at University College Hospital, Ibadan, Nigeria. Dis Colon Rectum 1996;39:536-40.
19Akute OO. Colorectal carcinoma in Ibadan, Nigeria: A 20-year survey-1971 to 1990. Hepatogastroenterology 2000;47:709-13.
20Ibadan Cancer Registry Data. Available from: http://www.uch-ibadan.org.ng/sites/default/files/Ibadan_Cancer_Registry.pdf. [Last accessed on 2014 Dec].
21Badoe EA. Malignant disease of gastrointestinal tract in Korle Bu Hospital, Accra, Ghana, 1956-65. West Afr Med J 1966;15:181-4.
22Badoe EA. Malignant tumours of the large bowel (Including Rectum) in Korle-Bu Hospital Accra 1970-1975. Ghana Med J 1977;16:157-9.
23Vorster HH, Kruger A, Margetts BM. The nutrition transition in Africa: Can it be steered into a more positive direction? Nutrients 2011;3:429-41.
24Steyn NP, McHiza ZJ. Obesity and the nutrition transition in Sub-Saharan Africa. Ann N Y Acad Sci 2014;1311:88-101.
25Jemal A, Bray F, Forman D, O'Brien M, Ferlay J, Center M, et al. Cancer burden in Africa and opportunities for prevention. Cancer 2012;118:4372-84.
26Burkitt DP. Epidemiology of cancer of the colon and rectum. Cancer 1971;28:3-13.
27Stewart HL. Geographic pathology of cancer of the colon and rectum. Cancer 1971;28:25-8.
28Segal I. Rarity of colorectal adenomas in the African black population. Eur J Cancer Prev 1998;7:387-91.
29Segal I, Edwards CA, Walker AR. Continuing low colon cancer incidence in African populations. Am J Gastroenterol 2000;95:859-60.
30Segal I. Physiological small bowel malabsorption of carbohydrates protects against large bowel diseases in Africans. J Gastroenterol Hepatol 2002;17:249-52.
31Irabor DO. Colorectal carcinoma: Why is there a lower incidence in Nigerians when compared to Caucasians? J Cancer Epidemiol 2011;2011:675154.
32CanTreat International. Scaling up cancer diagnosis and treatment in developing countries: What can we learn from the HIV/AIDS epidemic? Ann Oncol 2010;21:680-2.
33Irabor DO. Diet, environmental factors and increasing colorectal cancer in Nigeria. Ann Niger Med 2014;8:58-64.
34The Economist Online: Global Alcohol Consumption-Drinking Habits. Available from: http://www.economist.com/blogs/dailychart/2011/02/global_alcohol_consumption. [Last accessed on 2011 Sep].
35Winkler V, Lan Y, Becher H. Tobacco prevention policies in west-African countries and their effects on smoking prevalence. BMC Public Health 2015;15:1216.
36Williams AO, Prince DL. Intestinal polyps in the Nigerian African. J Clin Pathol 1975;28:367-71.
37Hutt MS, Templeton AC. The georgraphical pathology of bowel cancer and some related diseases. Proc R Soc Med 1971;64:962-4.
38Udofot SU, Ekpo MD, Khalil MI. Familial polyposis coli: An unusual case in West Africa. Cent Afr J Med 1992;38:44-8.
39Olasode BJ, Olasode OA. Missed diagnosis – Adenomatous polyposis coli. Cent Afr J Med 1997;43:339.
40Nzegwu MA, Osuagwu CC, Machembarrena JM, Ezeofor S, Picardo NG, Emegakor C, et al. Familial adenomatous polyposis complicated with an invasive colo-rectal adenocarcinoma in a 26-year-old Nigerian male – A rare finding. Eur J Cancer Care (Engl) 2007;16:198-200.
41Alese OB, Irabor DO. Adenomatous polyposis coli in an elderly female Nigerian. Ghana Med J 2009;43:139-41.
42Osuagwu CC, Okafor OC, Ezeome ER, Uche CE, Ememonu C, Kesieme E. Familial adenomatous polyposis with synchronous invasive colonic carcinomas and metastatic jejunal adenocarcinoma in a Nigerian male. Rare Tumors 2010;2:e66.
43Alatise OI, Arigbabu AO, Agbakwuru AE, Lawal OO, Sowande OA, Odujoko OO, et al. Polyp prevalence at colonoscopy among Nigerians: A prospective observational study. Niger J Clin Pract 2014;17:756-62.
44Ajayi AO, Ajayi EA, Solomon OA, Udo E. Lower gastrointestinal bleeding: Spectrum of colonoscopy findings in Ado-Ekiti, Nigeria. Int J Med Med Sci 2014;6:128-33.
45Anoukane Andulo F, Kowo M, Ngo Nonga B, Djapa R, Tagni-Sartre M, Njoya O, et al. Indications, Results and yield of Colonoscopy in a Difficult Economic Environment: The Case of Cameroun: Le cas du cameroun. Health Sci Dis 2013;144:1-6.
46Olokoba AB, Obateru OA, Bojuwoye MO, Olatoke SA, Bolarinwa OA, Olokoba LB. Indications and findings at colonoscopy in Ilorin, Nigeria. Niger Med J 2013;54:111-4.
47Dakubo J, Kumoji R, Naaeder S, Clegg-Lamptey J. Endoscopic evaluation of the colorectum in patients presenting with haematochezia at korle-bu teaching hospital Accra. Ghana Med J 2008;42:33-7.
48Irabor DO, Afuwape OO, Ayandipo OO. The present status of the management of colorectal cancer in Nigeria. J Cancer Res 2014;2014:267190.
49Raskin L, Dakubo JC, Palaski N, Greenson JK, Gruber SB. Distinct molecular features of colorectal cancer in Ghana. Cancer Epidemiol 2013;37:556-61.
50Saluja S, Alatise OI, Adewale A, Misholy J, Chou J, Gonen M, et al. A comparison of colorectal cancer in Nigerian and North American patients: Is the cancer biology different? Surgery 2014;156:305-10.
51Faivre J, Bédenne L, Boutron MC, Milan C, Collonges R, Arveux P. Epidemiological evidence for distinguishing subsites of colorectal cancer. J Epidemiol Community Health 1989;43:356-61.
52Mohandas KM, Desai DC. Epidemiology of digestive tract cancers in India. V. Large and small bowel. Indian J Gastroenterol 1999;18:118-21.
53Kingham TP, Alatise OI, Vanderpuye V, Casper C, Abantanga FA, Kamara TB, et al. Treatment of cancer in Sub-Saharan Africa. Lancet Oncol 2013;14:e158-67.
54Adekunle OO, Lawani JA. Clinical aspects and management of carcinoma of the rectum in Nigerians. East Afr Med J 1982;59:206-13.
55Akinola DO, Arigbabu AO. Pattern and presentation of large bowel neoplasms in Nigerians. Cent Afr J Med 1994;40:98-102.
56Morhason-Bello IO, Odedina F, Rebbeck TR, Harford J, Dangou JM, Denny L, et al. Challenges and opportunities in cancer control in Africa: A perspective from the African Organisation for Research and Training in Cancer. Lancet Oncol 2013;14:e142-51.
57Abdel-Wahab M, Bourque JM, Pynda Y, Izewska J, Van der Merwe D, Zubizarreta E, et al. Status of radiotherapy resources in Africa: An International Atomic Energy Agency analysis. Lancet Oncol 2013;14:e168-75.
58Adebamowo CA, Adeyi O, Pyatt R, Prior TW, Chadwick RB, de la Chapelle A. Case report on hereditary non-polyposis colon cancer (HNPCC) in Nigeria. Afr J Med Med Sci 2000;29:71-3.
59Abdulkareem FB, Sanni LA, Richman SD, Chambers P, Hemmings G, Grabsch H, et al. KRAS and BRAF mutations in Nigerian colorectal cancers. West Afr J Med 2012;31:198-203.
60Duduyemi BM, Akang EE, Adegboyega PA, Thomas JO. Significance of DNA mismatch repair genes and microsatellite instability in colorectal carcinoma in Ibadan Nigeria. Am J Med Biol Res 2013;1:145-8.