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Table of Contents
REVIEW ARTICLE
Year : 2014  |  Volume : 8  |  Issue : 2  |  Page : 58-64

Diet, environmental factors and increasing incidence of colorectal cancer in Nigeria


Department of Surgery, Division of Gastrointestinal Surgery, College of Medicine, University of Ibadan, University College Hospital, Ibadan, Oyo State, Nigeria

Date of Web Publication16-Mar-2015

Correspondence Address:
David O Irabor
Department of Surgery, University College Hospital, PMB 5116, Ibadan, Oyo State
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0331-3131.153353

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   Abstract 

Colorectal cancer (CRC) in Nigeria used to be a rare disease. However, over the last 40 years it has gradually become a significant health concern. Several publications on this disease from Nigeria have documented an increase in the incidence. To suggest possible and credible pathogenesis for the observed increase in CRC incidence in Nigeria, a search through AJOL, PubMed, and Google Scholar using search items like "colon cancer in Nigeria," "rectal cancer in Nigeria," and "CRC in Nigeria" was carried out. Also, a search for known risk factors in the development of CRC such as diet, carcinogens in red meat, alcohol, and polyposis coli syndromes were also initiated. Factors responsible for the increase in CRC incidence in Nigeria include poor refrigeration facilities resulting from poor electricity services; leading to deep-fried, smoked and charcoal-grilled meat. Other risk factors include an affinity for consumption of offal, an increase in obesity, proliferation of fast food joints, and an increase in alcohol intake. It is unclear how long and large the factors that cause CRC in a patient will have to be present before developing the disease. A dietary intake of fresh, wholesome, non-processed, preservative and hydrocarbon free foods should be encouraged; while habits such as consumption of alcohol and cigarette smoking are discouraged.

Keywords: Diet, environmental factors, increased colorectal cancer incidence, Nigeria


How to cite this article:
Irabor DO. Diet, environmental factors and increasing incidence of colorectal cancer in Nigeria. Ann Nigerian Med 2014;8:58-64

How to cite this URL:
Irabor DO. Diet, environmental factors and increasing incidence of colorectal cancer in Nigeria. Ann Nigerian Med [serial online] 2014 [cited 2020 Mar 29];8:58-64. Available from: http://www.anmjournal.com/text.asp?2014/8/2/58/153353


   Introduction Top


Malignant colorectal disease in rural Africa hitherto had been reported to be rare or at least uncommon; however current data from the cancer registry of the University College Hospital Ibadan in Nigeria, show an incidence rate that triples what authors in the same center had recorded 20-40 years earlier. [1] Colorectal cancer (CRC) is at present one of the top five cancers in Nigeria. [2] The development of large bowel cancer has been reported to be linked to several factors, among which are hereditary and environmental factors. Economic development is an important environmental influence and is related to changes in dietary preferences that result from increased affluence. [3] Ordinarily, the native Nigerian diet consists of a bolus-type high fiber meal, with a vegetable-based stew assisting its swallowing. With globalization and adoption of Western diets, fewer native Nigerians still partake of their native diets, and information from available Nigerian literature reveals that as one moves away from metropolitan cities like Lagos and Ibadan, the incidence of CRC reduces [4] [Figure 1]. Thus, it may be useful to have a closer look at what is consumed in the riverine areas of Nigeria, as these could well be cancer-preventive diets. More so, it is importantly to raise a red flag, in order to avoid or modify cancer-promoting behavior in the major Nigerian cities where CRC incidence is increasing.
Figure 1: Chart showing reduction in published colorectal cancer cases in Nigeria as one moves away from the major cities

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   The Scope of the Colorectal Cancer Problem in Nigeria Top


Colorectal carcinoma hitherto was not common in the developing countries especially Africa; however, it is certainly common now, with increasing incidence. Over the years, several workers in the University College Hospital Ibadan studied this disease and remarked about the increasing rates. [5],[6],[7] The time trends in common cancers in men from the Ibadan cancer registry in Nigeria show that four decades ago, (1960-1969) the top five cancers in men did not include CRC. But by the last decade, carcinoma of the colon and rectum moved from the 10 th to the 4 th position. [8] The peak age incidence in Nigeria has constantly been within 41-50 years, thus underscoring the earlier age incidence in Nigerians since the 1960s. [9] The lower peak age incidence seen in Nigerians could be attributed to the life expectancy of Nigerians that is estimated at 47 years, buttressing the younger age structure of the Nigerian population. [10] Only in Ghana, a neighboring West African country was the seventh and eighth decades reported as ages of peak incidence (the life expectancy of Ghanaians is put at 60 years for male and 62 years for female). [11]


   Dietary etiopathogenesis of Colorectal Cancer Top


It is without doubt that countries that consume a lot of meat and animal fat have the highest rates of colon cancer, and this inversely correlates with the consumption of dietary fiber. [12],[13],[14] Current worldwide annual meat consumption per capita shows the United States having 120.2 kg meat consumed per person per year, while Nigeria has 8.80 kg per person per year [15] [Figure 2]. The United States has a high incidence of CRC, which lends credence to the fact that one dietary exposure repeatedly associated with the risk of colon cancer is meat intake, specifically red meat. Incidence rates for CRC in Nigeria have been reported as 3.4 cases/100,000; compare this with one state in the US, Connecticut, where the incidence rate for CRC is 35.8/100,000 each year. [16] Some of the compounds formed during the cooking of meat, such as the heterocyclic amines (HCAs) and the most common polycyclic aromatic hydrocarbon (PAH) compound, benzopyrene, have been identified as human carcinogens, [14],[17],[18],[19] These become capable of damaging DNA only after being bioactivated by specific enzymes in the body. This is supposedly catalyzed by the Cytochrome P450 enzymes (P450IA1 and P450IA2); [20] indeed variations in levels and activity of P450 enzymes differ among people and may explain different cancer risks associated with exposure to these compounds. [20] The dangers of HCAs and PAHs may become significant as they may be the main factors contributing to the rising incidence of CRC in Nigeria.
Figure 2: World map showing global beef consumption

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   Possibility of a Different Pathogenetic Pathway of Colorectal Cancer in Native West Africans Top


The rarity of premalignant conditions like adenomatous polyps, ulcerative colitis, and Crohn's disease in the native West African has been reported by several authors. [21],[23],[24] In fact, the finding of any adenomatous polyposis patient in Nigeria is big news and publishable. [25],[26],[27] This apparent absence of a detectable adenoma-carcinoma sequence in Africans suggests a different etiopathogenesis of CRC, and some authors have actually hypothesized that maybe the carcinoma appears de-novo in a bid to explain why there may be a rarity of adenomatous polyps in the native African. [28],[29] Hereditary nonpolyposis colon cancer (HNPCC), on the other hand, has a strong attraction as an etiological pathway in Nigerians, perhaps because of the attributes of involvement of younger patients, and increased presence of mucinous and signet ring types; [1],[30] however the drawback is that a family history remains unproven in majority of these patients. Nevertheless a study by Adebamowo et al. demonstrated germ-line mutation in MSH2 gene (microsatellite instability) in two of five Nigerian patients with CRC, suggesting that HNPCC may be more significant than hitherto known. [31] Also, Duduyemi et al. reported MSI in 23% of 26 patients with CRC; 3 of whom were <40 years. [32] It has been proposed that development of colorectal carcinoma in Africans also occurs through the adenoma-carcinoma sequence, however, carcinogenesis occurs very rapidly and possibly through sessile (serrated) adenomas that are easily missed on colonoscopy and barium enema. [33],[34] There is also growing evidence that the serrated polyp-carcinoma sequence may have a distinct natural history, and that cancers arising through this pathway may have a different prognosis and response to therapy, than cancers arising through the traditional adenoma-carcinoma sequence. [35] Not a lot of work has been done to understand and unravel the molecular and genetic factors involved in the development of CRC in native Africans; however, it is encouraging that some researchers are looking in that direction, and hopefully their contributions to the scarce literature on this issue may be helpful in reducing the health burden of CRC patients globally. [36],[37]


   Literature Review of Colorectal Cancer in Nigeria Top


In a bid to look at the time trends of CRC in Nigeria, it is pertinent to review the publications from various parts of the country over an extensive period. One of the earliest papers from Nigeria on CRC emanated in 1967 from Ibadan, where 166 cases were seen over 8 years; an average of 21 cases per year. [38] Around that time in Ilesha, a town about 80 km from Ibadan, Mulligan reported 27 patients over a period of 14 years, about two patients a year. [39] Both studies presented cases seen between 1954 and 1967. Since then, there have been several reports from Ibadan, Ife, Enugu, Jos, Zaria, Kano, and Lagos.

From Ibadan, between 1971 and 1979, the incidence ranged from 12 to 14 patients annually; [40],[41] from 1980 to 2000, there was an annual average of 18-26 patients. [5],[6],[42] Ibadan in the core west showed 27 patients per year from 1995 to 2004.[9] Lagos and Sagamu accrued 402 cases over 12 years from five centers giving about 34 cases per year. [43] Ife showed an average of 10-13 cases per year between 1991 and 1994. [22],[24] Jos in the middle belt of Nigeria saw a moderate increase from nine cases a year in 1990-14, to 16 in 2003. [44],[45],[46]

Sites from the Northern parts of Nigeria showed seven cases per year in Zaria, and 12 per year in Kano. [47],[48] In Benin city, the capital of Edo state, 106 cases were encountered over a period of 20 years giving an average of <6 cases per year. [49] Enugu in the eastern part of the country saw between three and five patients yearly from 1975 to 1980. [50],[51] In the Riverine area of Nigeria, reports from Port Harcourt reveal rates of 2-4 patients per year. [52],[53] Calabar which is home to both Efik and Ibibio, showed figures of about five cases of CRC per year, indeed in the report from the Calabar cancer registry covering the period from 2004 to 2009, the top seven cancers did not include CRC. [54],[55]


   Proposed Contributory Factors in Nigeria Top


Meat and its products

Improved affluence leads to increased consumption of meat and poultry products. Unfortunately, poor electricity supply in most rural and urban areas discourages refrigeration of meat, thus many households smoke or deep-fry meat and fish for preservation and consumption. Most of the soups that are popular in Nigeria are incomplete without garnishing with smoked fish, and this has been shown (together with smoked and fried meat) to contain high levels of PAHs. [56],[57] Inhalation of aerosolized particles of HCAs may also occur during the roasting or grilling process. [58],[59] Also considering the penchant of Nigerians for throwing big parties every weekend; the caterers have to deep-fry the meat, chicken or fish a day before the event, in order to meet the deadline. Thus, most of us are exposed to HCAs every week. Indeed some authors have alluded to the carcinogenic properties of charcoal-roasted meat called "Suya" in Nigeria, [60],[61] which is a delicacy enjoyed by many. Offal, e.g., animal entrails are fatty, and there are many Nigerians who like abodi (rectum), shaki (stomach) and ifun (intestines) more than beef. Since bile is required for the digestion of fat, the more fat one consumes, the higher the production of bile. Excess bile that spills over into the colon is acted upon by colonic bacteria to form the secondary bile acids, namely deoxycholic and lithocholic acids which are carcinogenic. [62] Another delicacy that is peculiar to the Western part of Nigeria is the cowhide popularly known as "Ponmo". In a 2009 study by Okiei et al. from the University of Lagos on the dangers of flame-processed meat and hide, some serious public health concerns were voiced against ponmo; the poor man's meat. Hides processed with a flame fuelled by firewood and spent engine oil may contain toxic organic compounds such as polyaromatic hydrocarbons (PAHs), dioxins, furan, and benzene [63] [Figure 3]. For many people, this is a common dietary addition.
Figure 3: Cowhide burning in an abattoir in Lagos, Nigeria

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Alcohol consumption

Long-term alcohol use has also been linked to an increase in the probability of developing CRC. [64],[65] The World Health Organization (WHO) Global Status Report on Alcohol reveals that alcohol consumption in Nigeria has been rising steadily over the last 35 years with a significant steep rise in the last 15 years (1994/1995 to present levels). [66] One may assume that part of the increase in CRC cases may be ascribed to this. However, it should be stated that the astronomical rise in total alcohol consumption in Nigeria from 1994 onwards was due mainly to an increase in wine consumption (which is a "big" man's drink). Beer consumption only showed a slight increase, while consumption of spirits remained the same. To underscore the significant level of alcohol consumption in Nigeria, a WHO world alcohol map showed that apart from the USSR and Europe, Nigeria consumes more alcohol than the rest of the world! [Figure 4].
Figure 4: World map showing global alcohol consumption

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Tobacco consumption

There is evidence that cigarette smoking may result in a modestly increased risk of CRC in general, and specifically increased risk of tumors with microsatellite instability. [18],[67] Studies have shown that both the amount smoked and age at starting to smoke may be important etiologically. [68] This is linked to the effect of PAHs, a major carcinogen in cigarette smoke. [20] Nigeria, at present, is a high consumer of tobacco, notably through cigarette smoking, and younger persons are increasingly taking up this habit. [69] It is disheartening to know that tobacco consumption is increasing in many economically developing countries while it is decreasing in many economically developed countries. [70] Where other countries are outlawing cigarette smoking and making things difficult for cigarette manufacturers, the Nigerian government donated almost 3 acres of land for the establishment of a cigarette factory at the Ibadan end of the Lagos-Ibadan expressway.


   Increased Affluence Leads to Obesity Top


Increased caloric intake and reduced physical activity seems to be a sign of development and civilization, and this leads to obesity, which is a common ailment in the United States. Everything is now automatic; designed to remove the word "manual" from our lives. There are machines to wash clothes, plates, floors, etc. They call them labor-saving machines. Overindulgence in high-calorie containing meals, with lack of exercise leads to obesity; and obesity is a major risk factor for colon cancer. [71] According to previous research, people who are obese are 7-60% more likely to develop colon cancer than their leaner counterparts. [72] Until recently scientists were at a loss to explain why. Recent studies have now focused on the hypothesis that involves two hormonal systems; the insulin/insulin-like growth factor (IGF) and adipokines (adiponectin and leptin) systems. [18] Obese persons often have increased levels of insulin and IGF-1, which may promote the development of CRC. [73],[74] The hormone leptin is released by adipocytes, and the higher the body fat content, the higher the concentration of leptin in the blood stream. It has been demonstrated that the "fat hormone" leptin may enhance the growth of colonic cancer cells. [75] Previously in developing countries, the level of poverty precluded the luxury of over-indulgence in food and ensured continuous physical activity either from farming, manual labor or self-employment. Unfortunately, no one wants to work with his/her hands anymore. The farms are dying gradually in this country; everyone knows the fastest way to wealth is to join a political party. Obesity has been reported to be the silent global epidemic of the last 30 years, with almost every country recording an increase. [76] Apparently, Nigeria has recorded a modest increase in the incidence of obesity over the last 7 years with a prevalence of overweight individuals ranging from 20.3% to 35.1%, while the prevalence of obesity ranged from 8.1% to 22.2%. [77],[78],[79]


   Adoption of Western Dietary Lifestyle in Emergence of Fast-food Establishments Top


Consider the widespread emergence of fast-food establishments in Nigeria; these attract big-spenders eager to advertise their status by patronizing such establishments. These establishments offer grilled meat, deep-fried chicken, refined carbohydrate (pastry) and carbonated sugared drinks. There exists a direct correlation between the rates of CRC and per capita consumption of calories, dietary fat and meat protein. [80],[81],[82] Consumption of fast food by Nigerians could compromise a healthy diet. The fast-food revolution in Nigeria has, unfortunately, been fully embraced by the young and old, poor and rich, without recourse to the health dangers it poses. [83],[84] The dangers of fast food consumption can be summarized thus: Exposure to HCAs and PAHs from roasted, grilled and deep-fried meat, chicken or fish; increased carbohydrate consumption from pastry snacks which lead to obesity, with increase in leptin and adiponectin levels, and last but not least, an increased sugar consumption from carbonated soft drinks which lead to hyperinsulinism and the elaboration of IGF-1.


   Environmental Pollution Top


This is an inevitable sequel of civilization, industrialization and urbanization. Increase in rural to urban shifts has ensured that most of the established cities in Nigeria are overcrowded, notably Lagos, where traffic jams and gridlocks are legendary. PAHs and toxic quinones are present in vehicle exhausts, and diesel-generator exhaust fumes; [85],[86] and these are known carcinogens for CRC. Poor electricity has led to more households purchasing electricity generators. Thus, more people are exposed to these carcinogens. Nigeria may well be the only country where poor electricity may be marked as a risk factor for the development and increased rates of CRC.

It is possible that the levels and/or activities of the P450 enzymes are increasing in Nigerians leading to more hepatic bioactivation of carcinogens like HCAs and PAHs; and there is also no doubt that there is more exposure to greater levels of HCAs/PAHs than hitherto. Poor dietary choices like consumption of fast-foods ensure reduction of the ingestion of dietary components that previously inhibited the mutagenicity of HCAs/PAHs.

In summary, reasons for increased CRC incidence in Nigeria may include poor refrigeration facilities from poor electricity services, leading to deep-fried, smoked and charcoal-grilled animal protein; and too many generators. Also, an affinity for consumption of offal, an increase in obesity, proliferation of fast food joints, and an increase in alcohol intake may also be associated with an increased incidence of CRC. However, it is not yet clear how large a load of the contributing factors will lead to CRC or how much of the protective factors will ensure total abeyance of CRC. Yet one will not be too wrong to encourage a back-to-the-basics dietary intake of fresh, wholesome nonprocessed, preservative-free and hydrocarbon-free foods.


   Acknowledgements Top


[Figure 2]: Adopted from Scientific American: How Meat Contributes to Global Warming. [Online]. Available form: http://www.scientificamerican.com/slideshow/the-greenhouse-hamburger/ (Accessed 27th June, 2014).

[Figure 3]: Adopted from Google Images (Accessed 27th June, 2014).

[Figure 4]: The Economist Online: Global alcohol consumption - Drinking habits. [Online]. Available form: http://www.economist.com/blogs/dailychart/2011/02/global_alcohol_consumption (Accessed 27th June, 2014).

 
   References Top

1.
Irabor DO, Arowolo A, Afolabi AA. Colon and rectal cancer in Ibadan, Nigeria: An update. Colorectal Dis 2010;12:e43-9.  Back to cited text no. 1
    
2.
Irabor DO. Colorectal carcinoma: Why is there a lower incidence in Nigerians when compared to Caucasians? J Cancer Epidemiol 2011;2011:675154.  Back to cited text no. 2
    
3.
Burkitt DP. Epidemiology of cancer of the colon and rectum. Cancer 1971;28:3-13.  Back to cited text no. 3
    
4.
Irabor DO. Ethnic differences in colon and rectal cancer incidence in Nigeria: A case of dietary determinants? Ann Niger Med 2012;6:71-4.  Back to cited text no. 4
    
5.
Adekunle OO, Abioye AA. Adenocarcinoma of the large bowel in Nigerians: A clinicopathologic study. Dis Colon Rectum 1980;23:559-63.  Back to cited text no. 5
    
6.
Akute OO. Colorectal carcinoma in Ibadan, Nigeria: A 20-year survey-1971 to 1990. Hepatogastroenterology 2000;47:709-13.  Back to cited text no. 6
    
7.
Adesanya AA. Colorectal cancer in Nigeria. Abu Dhabi proceedings. Available from: http://www.cancerworld.org/cancerworld/moduleStaticPage. [Last accessed on 2014 Oct].  Back to cited text no. 7
    
8.
Ogunbiyi JO, Shittu OB. Increased incidence of prostate cancer in Nigerians. J Natl Med Assoc 1999;91:159-64.  Back to cited text no. 8
    
9.
Irabor D, Adedeji OA. Colorectal cancer in Nigeria: 40 years on. A review. Eur J Cancer Care (Engl) 2009;18:110-5.  Back to cited text no. 9
    
10.
UNICEF. At a glance: Nigeria. Available from: http://www.unicef.org/infobycountry/nigeria_statistics.html. [Last accessed on 2014 Oct].   Back to cited text no. 10
    
11.
Naaeder SB, Archampong EQ. Cancer of the colon and rectum in Ghana: A 5-year prospective study. Br J Surg 1994;81:456-9.  Back to cited text no. 11
    
12.
Kampman E, Slattery ML, Bigler J, Leppert M, Samowitz W, Caan BJ, et al. Meat consumption, genetic susceptibility, and colon cancer risk: A United States multicenter case-control study. Cancer Epidemiol Biomarkers Prev 1999;8:15-24.  Back to cited text no. 12
    
13.
Giovannucci E, Willett WC. Dietary factors and risk of colon cancer. Ann Med 1994;26:443-52.  Back to cited text no. 13
    
14.
Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Gammon MD, et al. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 2003;157:434-45.  Back to cited text no. 14
    
15.
Current worldwide annual meat consumption per capita. Chartsbin. Available from: http://www.com/view/12730. [Last accessed on 2014 Apr].  Back to cited text no. 15
    
16.
DuBois RN. COX-2 in large bowel cancer: A one-sided story. Gut 1999;45:636-7.  Back to cited text no. 16
    
17.
Schut HA, Snyderwine EG. DNA adducts of heterocyclic amine food mutagens: Implications for mutagenesis and carcinogenesis. Carcinogenesis 1999;20:353-68.  Back to cited text no. 17
    
18.
Wu AH, Shibata D, Yu MC, Lai MY, Ross RK. Dietary heterocyclic amines and microsatellite instability in colon adenocarcinomas. Carcinogenesis 2001;22:1681-4.  Back to cited text no. 18
    
19.
Pratt MM, John K, MacLean AB, Afework S, Phillips DH, Poirier MC. Polycyclic aromatic hydrocarbon (PAH) exposure and DNA adduct semi-quantitation in archived human tissues. Int J Environ Res Public Health 2011;8:2675-91.  Back to cited text no. 19
    
20.
Hammons GJ, Milton D, Stepps K, Guengerich FP, Tukey RH, Kadlubar FF. Metabolism of carcinogenic heterocyclic and aromatic amines by recombinant human cytochrome P450 enzymes. Carcinogenesis 1997;18:851-4.  Back to cited text no. 20
    
21.
Adekunle OO, Lawani JA. Clinical aspects and management of carcinoma of the rectum in Nigerians. East Afr Med J 1982;59:206-13.  Back to cited text no. 21
    
22.
Ojo OS, Odesanmi WO, Akinola OO. The surgical pathology of colorectal carcinomas in Nigerians. Trop Gastroenterol 1991;12:180-4.  Back to cited text no. 22
    
23.
Segal I. Rarity of colorectal adenomas in the African black population. Eur J Cancer Prev 1998;7:387-91.  Back to cited text no. 23
    
24.
Akinola DO, Arigbabu AO. Pattern and presentation of large bowel neoplasms in Nigerians. Cent Afr J Med 1994;40:98-102.  Back to cited text no. 24
    
25.
Alese OB, Irabor DO. Adenomatous polyposis coli in an elderly female Nigerian. Ghana Med J 2009;43:139-41.  Back to cited text no. 25
    
26.
Olasode BJ, Olasode OA. Missed diagnosis - adenomatous polyposis coli. Cent Afr J Med 1997;43:339.  Back to cited text no. 26
    
27.
Udofot SU, Ekpo MD, Khalil MI. Familial polyposis coli: An unusual case in West Africa. Cent Afr J Med 1992;38:44-8.  Back to cited text no. 27
    
28.
Jaskiewicz K, Lancaster E, Banach L, Karmolinski A. Proliferative activity of normal and neoplastic colonic mucosa in population groups with high and low risk for colorectal carcinoma. Anticancer Res 1998;18:4641-4.  Back to cited text no. 28
    
29.
van′t Hof A, Gilissen K, Cohen RJ, Taylor L, Haffajee Z, Thornley AL, et al. Colonic cell proliferation in two different ethnic groups with contrasting incidence of colon cancer: Is there a difference in carcinogenesis? Gut 1995;36:691-5.  Back to cited text no. 29
    
30.
Anderson WF, Umar A, Brawley OW. Colorectal carcinoma in black and white race. Cancer Metastasis Rev 2003;22:67-82.  Back to cited text no. 30
    
31.
Adebamowo 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.  Back to cited text no. 31
    
32.
Duduyemi BM, Akang EE, Adegboyega PA, Thomas JA. Significance of DNA mismatch repair genes and microsatellite instability in colorectal carcinoma in Ibadan, Nigeria. Am J Med Biol Res 2013;1:145-8.  Back to cited text no. 32
    
33.
Makkar R, Pai RK, Burke CA. Sessile serrated polyps: Cancer risk and appropriate surveillance. Cleve Clin J Med 2012;79:865-71.  Back to cited text no. 33
    
34.
Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011;42:1-10.  Back to cited text no. 34
    
35.
Groff RJ, Nash R, Ahnen DJ. Significance of serrated polyps of the colon. Curr Gastroenterol Rep 2008;10:490-8.  Back to cited text no. 35
    
36.
Abdulkareem 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.  Back to cited text no. 36
    
37.
Raskin L, Dakubo JC, Palaski N, Greenson JK, Gruber SB. Distinct molecular features of colorectal cancer in Ghana. Cancer Epidemiol 2013;37:556-61.  Back to cited text no. 37
    
38.
Williams AO, Edington GM. Malignant disease of the colon, rectum and anal canal in Ibadan, Western Nigeria. Dis Colon Rectum 1967;10:301-8.  Back to cited text no. 38
    
39.
Mulligan TO. The pattern of malignant disease in Ilesha, Western Nigeria. Br J Cancer 1970;24:1-10.  Back to cited text no. 39
    
40.
Grillo IA, Bond LF, Ebong WW. Cancer of the colon in Nigerians and American Negroes. J Natl Med Assoc 1971;63:357-61.  Back to cited text no. 40
    
41.
Ajao OG. Colon and anorectal neoplasms in a tropical African population. Int Surg 1979;64:47-52.  Back to cited text no. 41
    
42.
Iliyasu 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.  Back to cited text no. 42
    
43.
Abdulkareem FB, Abudu EK, Awolola NA, Elesha SO, Rotimi O, Akinde OR, et al. Colorectal carcinoma in Lagos and Sagamu, Southwest Nigeria: A histopathological review. World J Gastroenterol 2008;14:6531-5.  Back to cited text no. 43
    
44.
Obafunwa JO. Pattern of alimentary tract tumours in Plateau State: A middle belt area of Nigeria. J Trop Med Hyg 1990;93:351-4.  Back to cited text no. 44
    
45.
Sule AZ, Mandong BM, Iya D. Malignant colorectal tumours: A ten year review in Jos, Nigeria. West Afr J Med 2001;20:251-5.  Back to cited text no. 45
    
46.
Mandong BM, Sule AZ. Description of age, sex and site distribution of large bowel cancer in the middle belt of Nigeria. Niger J Surg Res 2003;5:80-4.  Back to cited text no. 46
    
47.
Mabogunje OA. Management of carcinoma of the colon and rectum in Nigeria: A review. East Afr Med J 1988;65:423-30.  Back to cited text no. 47
    
48.
Edino ST, Mohammed AZ, Ochicha O. Characteristics of colorectal carcinoma in Kano, Nigeria: An analysis of 50 cases. Niger J Med 2005;14:161-6.  Back to cited text no. 48
    
49.
Eze GI, Igbe AP, Obaseki DE, Akhiwu WO, Aligbe JU, Akang EEU et al. Presentation of colorectal cancers in Benin city, Nigeria. Sahel Med J 2010;13:24-8.  Back to cited text no. 49
  Medknow Journal  
50.
Onuigbo WI. Alimentary tract carcinomas in Nigerian Igbos. Arch Surg 1975;110:349.  Back to cited text no. 50
    
51.
Nwafo DC, Ojukwu JO. Malignant disease of the colon, rectum, and anus in Nigerian Igbos. Ann R Coll Surg Engl 1980;62:133-5.  Back to cited text no. 51
    
52.
Seleye-Fubara D, Gbobo I. Pathological study of colorectal carcinoma in adult Nigerians: A study of 45 cases. Niger J Med 2005;14:167-72.  Back to cited text no. 52
    
53.
Adotey JM, Jebbin NJ, Jebbin NJ. Colorectal cancer in Port Harcourt. Port Harcourt Med J 2008;2:198-203.  Back to cited text no. 53
    
54.
Essiet A, Iwatt AR. Surgical management of large bowel cancer 1983-1988, University of Calabar Teaching Hospital audit. Cent Afr J Med 1994;40:8-13.  Back to cited text no. 54
    
55.
Calabar cancer registry. Available from: http://www.calcanreg.org/index.htm. [Last accessed on 2014 Apr]  Back to cited text no. 55
    
56.
Palm LM, Carboo D, Yeboah PO, Quasie WJ, Gorleku MA, Darko A. Characterization of polycyclic aromatic hydrocarbons (PAHs) present in smoked fish from Ghana. Adv J Food Sci Technol 2011;3:332-8.  Back to cited text no. 56
    
57.
Silva BO, Adetunde TO, Oluseyi TO, Olayinka KO, Alo BI. Effects of the methods of smoking on the levels of polycyclic aromatic hydrocarbons (PAHs) in some locally consumed fishes in Nigeria. Afr J Food Sci 2011;5:384-91.  Back to cited text no. 57
    
58.
Hampikyan H, Colak H. Investigation of polycyclic aromatic hydrocarbons in food. Asian J Chem 2010;22:5797-807.  Back to cited text no. 58
    
59.
Kim H, Lee S. Charcoal grill restaurants deteriorate outdoor air quality by emitting volatile organic compounds. Pol J Environ Stud 2012;21:1667-73.  Back to cited text no. 59
    
60.
Emerole GO. Carcinogenic polycyclic aromatic hydrocarbons in some Nigerian foods. Bull Environ Contam Toxicol 1980;24:641-6.  Back to cited text no. 60
    
61.
Farombi EO. Diet-related cancer and prevention using anticarcinogens. Afr J Biotechnol 2004;3:651-61.  Back to cited text no. 61
    
62.
Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006;47:241-59.  Back to cited text no. 62
    
63.
Okiei W, Ogunlesi M, Alabi F, Osiughwu B, Sojinrin A. Determination of toxic metal concentrations in flame-treated meat products, ponmo. Afr J Biochem Res 2009;3:332-9.  Back to cited text no. 63
    
64.
Meyer F, White E. Alcohol and nutrients in relation to colon cancer in middle-aged adults. Am J Epidemiol 1993;138:225-36.  Back to cited text no. 64
    
65.
Cho E, Lee JE, Rimm EB, Fuchs CS, Giovannucci EL. Alcohol consumption and the risk of colon cancer by family history of colorectal cancer. Am J Clin Nutr 2012;95:413-9.  Back to cited text no. 65
    
66.
WHO Global status on Alcohol 2004. Country profiles. Nigeria. Available from: http://www.who.int/substance_abuse/publications/en/nigeria.pdf.  Back to cited text no. 66
    
67.
Giovannucci E. An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 2001;10:725-31.  Back to cited text no. 67
    
68.
Voutsinas J, Wilkens LR, Franke A, Vogt TM, Yokochi LA, Decker R, et al. Heterocyclic amine intake, smoking, cytochrome P450 1A2 and N-acetylation phenotypes, and risk of colorectal adenoma in a multiethnic population. Gut 2013;62:416-22.  Back to cited text no. 68
    
69.
Salawu FK, Danburam A, Desalu OO, Olokoba AB, Agbo J, Midala JK, et al. Cigarette smoking habits among adolescents in northeast Nigeria. Mera Afr J Respir Med 2009;1:9-11.  Back to cited text no. 69
    
70.
Brawley OW. Avoidable cancer deaths globally. CA Cancer J Clin 2011;61:67-8.  Back to cited text no. 70
    
71.
Giovannucci E. Obesity, insulin and colon cancer. Proc Am Assoc Cancer Res 2004;45:1319-20.  Back to cited text no. 71
    
72.
Ma Y, Yang Y, Wang F, Zhang P, Shi C, Zou Y, et al. Obesity and risk of colorectal cancer: A systematic review of prospective studies. PLoS One 2013;8:e53916.  Back to cited text no. 72
    
73.
Ollberding NJ, Cheng I, Wilkens LR, Henderson BE, Pollak MN, Kolonel LN, et al. Genetic variants, prediagnostic circulating levels of insulin-like growth factors, insulin, and glucose and the risk of colorectal cancer: The Multiethnic Cohort study. Cancer Epidemiol Biomarkers Prev 2012;21:810-20.  Back to cited text no. 73
    
74.
Shiratsuchi I, Akagi Y, Kawahara A, Kinugasa T, Romeo K, Yoshida T, et al. Expression of IGF-1 and IGF-1R and their relation to clinicopathological factors in colorectal cancer. Anticancer Res 2011;31:2541-5.  Back to cited text no. 74
    
75.
Koda M, Sulkowska M, Kanczuga-Koda L, Surmacz E, Sulkowski S. Overexpression of the obesity hormone leptin in human colorectal cancer. J Clin Pathol 2007;60:902-6.  Back to cited text no. 75
    
76.
Durazo-Arvizu RA, Luke A, Cooper RS, Cao G, Dugas L, Adeyemo A, et al. Rapid increases in obesity in Jamaica, compared to Nigeria and the United States. BMC Public Health 2008;8:133.  Back to cited text no. 76
    
77.
Chukwuonye II, Chuku A, John C, Ohagwu KA, Imoh ME, Isa SE, et al. Prevalence of overweight and obesity in adult Nigerians - A systematic review. Diabetes Metab Syndr Obes 2013;6:43-7.  Back to cited text no. 77
    
78.
Iloh G, Amadi AN, Nwankwo BO, Ugwu VC. Obesity in adult Nigerians: A study of its pattern and common primary co-morbidities in a rural Mission General Hospital in Imo state, South-Eastern Nigeria. Niger J Clin Pract 2011;14:212-8.  Back to cited text no. 78
[PUBMED]  Medknow Journal  
79.
Bakari AG, Onyemelukwe GC, Sani BG, Aliyu IS, Hassan SS, Aliyu TM, et al. Obesity, overweight and underweight in suburban Northern Nigeria. Int J Diabetes Metab 2007;15:68-9.  Back to cited text no. 79
    
80.
Popkin BM. Understanding global nutrition dynamics as a step towards controlling cancer incidence. Nat Rev Cancer 2007;7:61-7.  Back to cited text no. 80
    
81.
Spencer EH, Frank E, McIntosh NF. Potential effects of the next 100 billion hamburgers sold by McDonald′s. Am J Prev Med 2005;28:379-81.  Back to cited text no. 81
    
82.
Slattery ML, Boucher KM, Caan BJ, Potter JD, Ma KN. Eating patterns and risk of colon cancer. Am J Epidemiol 1998;148:4-16.  Back to cited text no. 82
    
83.
Otemuyiwa IO, Adewusi SR. Effects of fast food consumption on nutrient intake among Nigerian elite in Lagos, Nigeria. Int J Health Nutr 2012;3:12-9.  Back to cited text no. 83
    
84.
Arulogun OS, Owolabi MO. Fast food consumption pattern among undergraduates of the University of Ibadan, Nigeria: Implications for nutrition education. J Agric Food Technol 2011;1:89-93.  Back to cited text no. 84
    
85.
Krivoshto IN, Richards JR, Albertson TE, Derlet RW. The toxicity of diesel exhaust: Implications for primary care. J Am Board Fam Med 2008;21:55-62.  Back to cited text no. 85
    
86.
Lafuente MJ, Casterad X, Trias M, Ascaso C, Molina R, Ballesta A, et al. NAD(P)H:quinone oxidoreductase-dependent risk for colorectal cancer and its association with the presence of K-ras mutations in tumors. Carcinogenesis 2000;21:1813-9.  Back to cited text no. 86
    


    Figures

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