|Year : 2019 | Volume
| Issue : 1 | Page : 27-33
Histopathological spectrum of gastrointestinal lesions seen in university of uyo teaching hospital, South–South Nigeria
Chukwuemeka Charles Nwafor1, Nkem Nnenna Nwafor2, Emmanuel Benjamin Etuk3, Obioha Kanu4
1 Department of Pathology, University of Uyo, Uyo, Akwa Ibom, Nigeria
2 Department of Radiology, University of Uyo Teaching Hospital, Uyo, Akwa Ibom, Nigeria
3 Department of Surgery, University of Uyo, Uyo, Akwa Ibom, Nigeria
4 Department of Histopathology, University of Uyo Teaching Hospital, Uyo, Akwa Ibom, Nigeria
|Date of Web Publication||14-May-2019|
Dr. Chukwuemeka Charles Nwafor
Department of Pathology, University of Uyo, Uyo, Akwa Ibom
Source of Support: None, Conflict of Interest: None
Introduction: This is a retrospective study of all gastrointestinal tract (GIT) specimens seen in University of Uyo Teaching Hospital over a 10-year period from January 1, 2008 to December 31, 2017. Materials and Methods: Data were extracted from the departmental registers, patient request forms, and duplicate copies of histology reports of all cases seen. Results: GIT specimens accounted for 4.3% of all specimens. Majority of them were inflammatory lesions, distantly followed by malignant lesions. Inflammatory diagnoses were seen in all parts of the GIT with the appendix accounting for 76.3% of the inflammatory lesions. Appendicitis was the most common diagnosis, while negative appendix was the second most common diagnosis. In all sites except the anus, males were affected more than females in a sex ratio of 1.5:1. Age groups 10–39 years accounted for 79.9% of all appendix inflammatory lesions, with age group 20–29 contributing the highest. Age groups 40–59 had most gastritis cases. Age group 50–59 years accounted for most malignant lesions, with the majority seen in the colon. Adenocarcinomas distantly followed by squamous cell carcinomas were the most common histologic malignant diagnoses made. Conclusion: The pattern of GIT lesions seen in our institute has been documented and this will serve as a baseline data for future local studies.
Keywords: Appendix, gastrointestinal tract, inflammatory, malignant cases
|How to cite this article:|
Nwafor CC, Nwafor NN, Etuk EB, Kanu O. Histopathological spectrum of gastrointestinal lesions seen in university of uyo teaching hospital, South–South Nigeria. Ann Trop Pathol 2019;10:27-33
|How to cite this URL:|
Nwafor CC, Nwafor NN, Etuk EB, Kanu O. Histopathological spectrum of gastrointestinal lesions seen in university of uyo teaching hospital, South–South Nigeria. Ann Trop Pathol [serial online] 2019 [cited 2020 Feb 27];10:27-33. Available from: http://www.atpjournal.org/text.asp?2019/10/1/27/258158
| Introduction|| |
Extending from the oral cavity down to the anus is the hollow tube called gastrointestinal tract (GIT). It consists of anatomically distinct segments, including the esophagus, stomach, small intestine, colon, rectum, and anus. In the GIT, just as there are regional variations in structure and function, so are the diseases. Disorders of the GIT could be congenital disorders, inflammatory, or neoplastic (benign or malignant). Histopathology is regarded as the most sensitive and specific diagnostic method (gold standard) for the early detection of GIT lesions (especially malignant cases) and plays an important role in the diagnosis and therefore aids in their early management., In general, inflammatory lesions of the GIT are more common, followed by malignant lesions while benign neoplasms are rare.,, Leading the inflammatory lesions are acute appendicitis (AA) and gastritis, while the pattern of malignant GIT lesion varies from geographic location to another depending on genetic factor and environmental factors (diet and social habits).,, This study aims to describe the histopathological pattern of all GIT lesions ever seen in University of Uyo Teaching Hospital (UUTH), since there is no known encompassing histopathological study on gastrointestinal lesions published from UUTH.
| Materials and Methods|| |
This is a retrospective study of all GIT specimens that were histologically diagnosed in the Histopathology Department of UUTH over a 10-year period from January 1, 2008 to December 31, 2017. This histopathology laboratory is the only facility where histopathology services are rendered in Akwa Ibom State and as such renders services to the host hospital and many privately owned hospitals within the State. These GIT specimens included excision biopsies, incision biopsies, appendectomies, small and large intestine resections, and endoscopy and colonoscopy biopsies. These specimens were fixed in 10% buffered formalin, routinely processed, and paraffin-embedded sections were taken and stained with hematoxylin and eosin. Special stains like Giemsa stain was used when necessary, while immunohistochemistry was done in two cases (suspected cases of gastrointestinal stromal tumor).
Data were extracted from the departmental registers, patient request forms, and duplicate copies of histology reports of all cases. Information extracted includes age, sex, duration of symptom before presentation, clinical diagnosis made by the unit consultant, type of specimen received, and histologic diagnosis. Data were analyzed using predictive analytical software, Version 17 (IBM, SPSS Inc., Chicago, IL, USA).
Simple frequencies were determined for categorical variables and mean was evaluated for continuous data. Few reports with ambiguous conclusions were excluded. Also excluded were GIT histopathology reports with any of the major identification parameters (such as sex, age and diagnosis) missing. Eight reports in all were excluded.
| Results|| |
Of 6296 specimens seen in the laboratory, 271 were GIT specimens accounting for 4.3% of all specimens. Majority of them were inflammatory lesions, distantly followed by malignant lesions as shown in [Table 1]. Inflammatory diagnoses were seen in all parts of the GIT with the appendix accounting for 76.3% of the inflammatory lesions, distantly followed by the stomach (11.1%), while the least was a case of fistula in ano as shown in [Table 2] and [Table 3]. Majority (47.6%) of chronic gastritis (CG) cases did not have sign of activity. For both small and large intestine, gangrenous lesions were the most common inflammatory lesions accounting for 69.2% and 62.5%, respectively, as shown in [Table 3]. In all sites except the anus, males were affected more than females in a sex ratio of 1.5:1. Age groups 10–39 years accounted for 79.9% of all appendix inflammatory lesions, with age group 20–29 contributing the highest. Age groups 40–59 had most gastritis cases as shown in [Table 4]. Appendicitis (including pathologies such as AA, suppurative appendicitis, gangrenous/perforated appendicitis, and lymphoid hyperplasia) is the most common diagnosis, while negative appendix is the second most common diagnosis. [Table 5] shows a comparison of various appendicitis studies in relation to the index study. The appendectomy cases in the index study are small compared to all them. The gastritis seen in this series is compared with various gastritis studies as shown in [Table 6] and had the smallest number of cases compared to the various gastritis studies. Age group 50–59 years accounted for most malignant lesions, while the lowest was seen at the extreme of ages. Most cases were seen in the colon (34.1%), followed by the anus (24.4%) and rectum (19.5%). The small intestine had the least involvement (4.9%) as seen in [Table 7]. For all the segments of the GIT except the anus, males were affected more than females as shown in [Table 8]. Adenocarcinomas (70.7%), distantly followed by squamous cell carcinomas (14.6%), were the most common histologic diagnoses made as shown in [Table 9]. Other histological diagnoses include gastrointestinal stromal tumor (4.9%), non-Hodgkin's lymphoma (4.9%), neuroendocrine tumor (2.4%), and malignant spindle cell tumor (2.4%). [Table 10] shows a comparison of the index study with various studies that focused on malignant gastrointestinal lesions.
|Table 2: Sex and site distribution of inflammatory gastrointestinal tract lesions|
Click here to view
|Table 3: Pathological diagnosis and site of inflammatory gastrointestinal tract lesions|
Click here to view
|Table 4: Age and site distribution of inflammatory gastrointestinal tract lesions|
Click here to view
|Table 7: Age and site distribution of malignant gastrointestinal tract lesions|
Click here to view
|Table 8: Sex and site distribution of malignant gastrointestinal tract lesions|
Click here to view
|Table 9: Site and histopathological diagnosis distribution of malignant cases|
Click here to view
| Discussion|| |
The vermiform appendix is a rudimentary structure with no known function that arises from the medial wall of the cecum but in which various pathologies, especially inflammatory conditions usually occur. AA is the most common acute surgical condition and is the most common inflammatory GIT pathology, while appendicectomy is the most frequently performed operation worldwide.,, The pathogenesis of AA is due to lumen obstruction (either by fecalith, foreign body, calculus, tumor in cecum, or an appendiceal tumor) leading to impaired mucosal resistance to microbial invasion, mucosal injury, ulceration, and inflammation.,, In the past, some authors have argued that routine histology for appendices was not important, especially when it looked grossly normal. Studies have shown that routine histopathological examination of the appendix must be undertaken in all cases.,,,, The index sample size of 145 cases in 10 years is too small compared to all the previous studies.,,,,,,, Reasons were mainly due to nonsubmission of all appendectomy specimens in the past. The surgeons submit what they felt looked abnormal. Furthermore, appendectomies done in peripheral hospitals even up till present are not submitted for histological examinations. The doctors in peripheral hospitals still think it is a waste of scarce resources that the incidental worrisome pathologies of appendix are very rare. Worthy of note is that results of all preoperative investigations are nonspecific and diagnosis is made only after histopathology. Histology remains the gold standard, irrespective of advances in technology and imaging modalities because apart from the common diagnosis of appendicitis, occasionally sinister findings such as neoplasms (both benign and malignant) and unusual but important incidental findings such as different types of worms and tuberculosis may also be encountered, which ultimately changes the management.,,,, Hence, histology helps to determine treatment options.
Most of the appendices were from males in a sex ratio of 1.3:1, while the mean age was 29 ± 12.8 with age groups 20–29 years accounting for most cases. About 78.2% of cases were seen in ages less than 40. This is similar to previous studies except the observations by Omotosho et al. and Sinha et al. that reported more females.,,,, In general, appendicitis is relatively rare in infants and reaches a peak incidence in teens and early 20s. The incidence is equal among males and females before puberty. In young adults, the male:female ratio increases in favor of males. Although lymphoid hyperplasia is recognized as a cause of lumen obstruction which may eventually lead to inflammation of appendix, most studies do not recognize it as a diagnostic entity except studies by Omotosho et al. and Sinha et al. In the index study, it accounted for 27.5% of appendicitis diagnoses. There is no consensus about this diagnostic entity. Even in the same institution like ours, different pathologists differ in their opinion about this diagnostic entity. In situ ations like this, what settles/resolves the argument is that neither lymphoid hyperplasia nor negative appendicitis which will be the other diagnosis, means no harm to the patient and will probably not change the treatment plan.
Negative appendectomy (NA) or normal appendix following appendectomy or false-positive appendectomy is defined as postoperative appendix specimen for suspected appendicitis that was however microscopically normal on histopathological examination without evidence of inflammation, tumors, and parasitic infestation.,, All studies except Sinha et al. and Priavadhana reported NA which had a range of 3%–21.2%.,,,,,, A rate of 11.2% was observed in this study, which is within the acceptable range of 10%–20%., The high rates of 10%–20% for NA is acceptable internationally, so as to avoid missing cases of appendicitis and its possible complications (such as perforation, peritonitis, abscess formation, peritonitis, and sepsis) which causes more morbidity and mortality. It was observed that studies that had high rate of lymphoid hyperplasia, reported a lower rate of NA or none., It could be deduced that if not for lymphoid hyperplasia as a diagnostic entity, the rate of NA would be higher. About 72% of the NA group were female, aged between 10 and 40 years (though not statistically significant) which is similar to previous documentations.,,,, Right iliac fossa pain with rebound tenderness is the major clinical suggestion of appendicitis. Mimickers of appendicitis clinically that usually lead to NA include gynecologic lesions (ovarian cysts, leiomyoma, endometriosis, benign ovarian neoplasms, malignant ovarian disease, pelvic adhesions, and pelvic inflammatory diseases), Merkel diverticulitis, omental infarction, mesenteric lymphadenitis, and chemotherapy-induced typhlitis.,,, Recently, to reduce the rate of NA, in addition to the previously well-known clinical assessment (detailed history taking, examination, and investigations to show the presence of infection), selective diagnostic imaging modalities (including plain abdominal radiographs, ultrasound scan (USS), and computerized tomography (CT scan) have been introduced). Of the three radiologic modalities, CT is the best and is highly accurate for confirming or excluding AA. It has a sensitivity of 90%–100%, specificity of 91%–99%, and positive predictive value of 95%–97%. In our setting, almost all appendectomies were done as emergency cases, usually based on high index of suspicion. Very few had USS done before surgery and none had a CT scan done before the surgery.
Other unusual inflammatory diseases of the appendix (associated with specific causes) include oxyuriasis, eosinophilic appendicitis, schistosomiasis, Helicobacter pylori, measles, infectious mononucleosis, Crohn's disease, ulcerative colitis, sarcoidosis, yersiniosis, Rosai–Dorfman disease, invasive candidiasis, amebiasis, cryptosporidiosis, and cytomegalovirus appendicitis. It accounted for 3% of cases seen in this study which is within the range of 1%–8.6% seen in previous studies.,,, Sinha et al. in West Bengal, India, reported a rate of 22.8%, though no reasons were given for this high occurrence. The importance of making these diagnoses is that appendectomy alone does not solve the problem in these cases and the patients have to be treated specifically for the various disease entities diagnosed histopathologically. Neoplasms of the appendix are rare. Although the total number of appendices seen in this study is small, the none occurrence of even one neoplasm could mean that they are very rare in our setting.
Only 21 (11.1%) cases of CG and its complications were seen in 10 years in our study. This is too small compared to most previous studies.,,,,,,,, The reasons were mainly due to nonavailability of a gastroenterologist in UUTH until 5 years ago and nonavailability of endoscopy instruments and other trained personnel until few months ago. Only 9 (42.9%) of these gastric biopsies were from endoscopies. The others were from cases that presented to the surgery department. This obviously underrepresents the magnitude CG and H. pylori (HP) infection in our environment. Although small sized, the noting of the pattern seen in our center is still important. The mean age and sex ratio is same with previous studies from other parts of the world.,,, The HP infection rate of 33.3% is also within the range of 22.4%–61% seen in previous Nigerian studies.,,
Causes of CG include HP infection, abuse of nonsteroidal anti-inflammatory drugs, alcohol, radiation, chronic bile reflux, mechanical injury (e.g., indwelling nasogastric tube), and systemic diseases (amyloidosis, Crohn's disease and graft vs. host disease). CG due to HP infection is the most common. In about 90% of CG cases, HP organisms are present. Known risk factors for HP include poverty, household crowding, limited education, African American and Mexican America ethnicity, and residence in rural areas. Morphologically, HP organism is mainly seen within the surface mucus overlying epithelial cells in the surface and neck regions, mostly in the antrum and less common in acid producing (oxyntic) mucosa of the fundus and body. Common histologic findings include intraepithelial neutrophils, subepithelial plasma cells, and lymphoid follicles. Major complications are peptic ulcer disease, mucosal atrophy, and intestinal metaplasia.
Over time, especially in populations that are more genetically susceptible, HP-induced gastritis may progress through a series of stages (nonatrophic CG, multifocal atrophic gastritis, intestinal metaplasia, low-grade dysplasia, and high-grade dysplasia) to form an invasive adenocarcinoma. The low rate of glandular atrophy and metaplasia we observed and a single case of gastric adenocarcinoma reconfirms the known pattern in Nigeria and other African Countries.,,
In this series, the most common inflammatory lesion of both the small and large intestine is gangrenous necrosis and the causes ranged from bands/adhesions to herniation to volvulus and rarely due to tumors. Microscopically, depending on the stage of the lesion, it usually appears as nonspecific transmural inflammation with extensive areas of necrosis in severe cases.
The number of cases of small intestine malignancies in the present study was too small (only two cases) to draw any conclusion except that malignant lesions of the small intestine were rare in occurrence.
Worldwide GIT cancers constitute about 15%–25% of all cancer burdens. It shows very remarkable and striking differences in its occurrence in different regions and different races of the world. The incidence of GIT malignancies varies from country to country and also in different parts of the same country.,
Only 41 malignant cases were seen during the period of study, which is small compared to the previous studies.,,,, Although these are all the malignant GIT lesions seen in our hospital laboratory register, this may be an underestimation of the malignant GIT lesions in our environment. The low rate is similar to a previous observation from this center. The low rate was attributed to the high fiber and vegetable-based diet that is very common in Akwa Ibom State. A repeat study of colorectal cancers in Ibadan showed a significant increase in rate of over 80% and this was attributed to diet Westernization and the recent increase in hospital visitation. A repeat future study in our center will help to identify such if it exists.
The small number observed in relation to previous studies may be because some previous studies included accessory GIT organs such as the liver and pancreas.,, Some of these studies also were multicenter studies.,, For GIT cancer cases, the demographic factors such as age incidence, male preponderance, and histological characteristics observed in the index study are similar to reports in previous studies.,,, Reason for male sex predominance is not clear. Colorectal adenocarcinomas were the most common malignancies, which is similar to observations in Southwest Nigeria, Zaria and Dhule, India. However, in Sudan and Saudi Arabia, pancreatic cancer and liver cancer, respectively, were identified., No definite causative reason was given for the high rate of pancreatic cancers in Sudan except for recent availability of hi-tech equipment. In Saudi Arabia, high rate of hepatitis B and C viral infections were stated to be possible reasons., In Pakistan, esophageal cancers are the commonest GIT cancers with female preponderance. Factors such as genetic factors, malnutrition, alcohol consumption, cigarette smoking, areca nuts consumption, thermal injury from scalding and hot beverages, physical injury caused by ingesting coarse food and deficiencies of riboflavin, Vitamin A and zinc, and low consumption of raw vegetables and fruits are the major risk factors.,,
Recent studies (molecular pathological classification) have shown that there are about four molecular subtypes of colorectal carcinoma based on chromosomal and microsatellite instability. This grouping is both for clinical trial designs and future postsurgical adjuvant treatment decisions, especially for tumors with aggressive features. It is no longer enough for a pathologist to give light microscopic diagnosis without a few immunohistochemistry markers when needed.
A major limitation of this study is that it was conducted in a hospital setting and more so it was carried out in one center. A community study is therefore desirable as this is usually more representative. The small sample size, especially with reference to the number of gastric biopsies done in UUTH also contributed to its limitation.
| Conclusion|| |
Our study of analysis of GIT lesions throws light on the pattern of GI lesions seen in our institute and we believe that our findings will create a baseline data for future local studies. The awareness on the need to submit all appendectomy specimens should be increased among doctors, especially the private practitioners.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Turner JR. The gastrointestinal tract. In: Kumar V, Abbas AK, Fausto N, Aster JC, editors. Robbins and Cotran Pathologic Basis of Diseases. 9th
ed. Canada: Elsevier; 2015. p. 749-819.
Prasaad PR, Rao B. Histo-pathological spectrum of gastrointestinal lesions-an experience in a tertiary care centre in South India. Int J Res Med Sci 2016;4:3407-12.
Thakur RY, Nikumbh DB, Swami SY. Clinico histopathological overview of git lesions in a rural hospital. Indian J Pathol Oncol 2016;3:305-14.
Ahmad Z, Arshad H, Fatima S, Idrees R, Ud-Din N, Ahmed R, et al.
Gastrointestinal, liver and biliary tract pathology: A histopathological and epidemiological perspective from Pakistan with a review of the literature. Asian Pac J Cancer Prev 2013;14:6997-7005.
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A, et al.
Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87-108.
Omotoso AJ, Nnoli MA, Bassey IE, Akintomide AO, Ngim OE, Ekanem IA. Histopathological analysis of appendectomy specimens in Calabar, South – Southern Nigeria. IOSR J VLSI Signal Proc 2013;2:42-6.
Chamisa I. A clinicopathological review of 324 appendices removed for acute appendicitis in Durban, South Africa: A retrospective analysis. Ann R Coll Surg Engl 2009;91:688-92.
Sinha RT, Dey A. A retrospective study of histopathological features of appendectomy specimens – What all can expect? J Med Sci Health 2016;2:6-12.
Jat MA, Al-Swailmi FK, Mehmood Y, Alrowaili M, Alanazi S. Histopathological examination of appendicectomy specimens at a district hospital of Saudi Arabia. Pak J Med Sci 2015;31:891-4.
Omiyale AO, Adjepong S. Histopathological correlations of appendectomies: A clinical audit of a single center. Ann Transl Med 2015;3:119.
Udoh MO, Obaseki DE. Histopathological evaluation of h. Pylori associated gastric lesions in Benin City, Nigeria. East Afr Med J 2012;89:408-13.
Oluwasola AO, Ogunbiyi JO. Chronic gastritis and Helicobacter pylori
infection in university college hospital Ibadan, Nigeria – A study of 85 fibre optic gastric biopsies. Niger J Med 2004;13:372-8.
Kalebi A, Rana F, Mwanda W, Lule G, Hale M. Histopathological profi le of gastritis in adult patients seen at a referral hospital in Kenya. World J Gastroenterol 2007;13:4117-21.
Carrilho C, Modcoicar P, Cunha L, Ismail M, Guisseve A, Lorenzoni C, et al.
Prevalence of Helicobacter pylori
infection, chronic gastritis, and intestinal metaplasia in Mozambican dyspeptic patients. Virchows Arch 2009;454:153-60.
Sharma P, Kumar KK, Mahajan M, Chandail VS, Goswami K, Gupta P. Histopathological changes in gastric mucosal biopsies in chronic gastritis and correlation of pathological features with Helicobacter pylori
infection. Trop J Path Micro 2015;1:8-15.
Shafii M, Nikzad SE, Kasiri H, Naghipour M. Histopathological evaluation of chronic gastritis with and without Helicobacter pylori
colonization: A study from Iran. Malays J Pathol 2008;30:27-30.
Desmet VJ, Rosai J. Liver non neoplastic diseases, tumors and tumorlike conditions. In: Rosai J, editor. Rosai and Akerman's Surgical Pathology. 10th
ed., Vol. 1. China: Elsevier; 2011. p. 857-980.
Gray GF Jr., Wackym PA. Surgical pathology of the vermiform appendix. Pathol Annu 1986;21 Pt 2:111-44.
Sisson RG, Ahlvin RC, Harlow MC. Superficial mucosal ulceration and the pathogenesis of acute appendicitis in childhood. Am J Surg 1971;122:378-80.
Matthyssens LE, Ziol M, Barrat C, Champault GG. Routine surgical pathology in general surgery. Br J Surg 2006;93:362-8.
Raja AS, Wright C, Sodickson AD, Zane RD, Schiff GD, Hanson R, et al.
Negative appendectomy rate in the era of CT: An 18-year perspective. Radiology 2010;256:460-5.
Webb EM, Nguyen A, Wang ZJ, Stengel JW, Westphalen AC, Coakley FV, et al.
The negative appendectomy rate: Who benefits from preoperative CT? AJR Am J Roentgenol 2011;197:861-6.
Seetahal SA, Bolorunduro OB, Sookdeo TC, Oyetunji TA, Greene WR, Frederick W, et al.
Negative appendectomy: A 10-year review of a nationally representative sample. Am J Surg 2011;201:433-7.
Gilmore OJ, Browett JP, Griffin PH, Ross IK, Brodribb AJ, Cooke TJ, et al.
Appendicitis and mimicking conditions. A prospective study. Lancet 1975;2:421-4.
Zoarets I, Poluksht N, Halevy A. Does selective use of computed tomography scan reduce the rate of “white” (negative) appendectomy? Isr Med Assoc J 2014;16:335-7.
Duduyemi BM, Ojo BA, Olaomi OO, Atiba AS. Histopathological pattern of endoscopic gastric biopsy in a district hospital in Nigeria: A review of 118 consecutive cases. Am J Med Biol Res 2014;2:83-6.
Correa P. Chronic gastritis: A clinico-pathological classification. Am J Gastroenterol 1988;83:504-9.
Abdulkareem FB, Faduyile FA, Daramola AO, Rotimi O, Banjo AA, Elesha SO, et al.
Malignant gastrointestinal Tumours in South Western Nigeria: A histopathologic analysis of 713 cases. West Afr J Med 2009;28:173-6.
Mbuk EU, Amber EI. Retrospective study on gastrointestinal tract tumors in humans in Zaria, Kaduna State, Nigeria. J Cancer Res Exp Oncol 2017;9:1-6.
Mahmoud K, Musaad A, Alawad MA. Pattern of primary gastrointestinal tract cancer in a Tertiary central hospital in Sudan: A prospective study. Med J 2014;1:34-7.
Ajarim DS. Pattern of primary gastrointestinal cancer: King Khalid university hospital experience and review of published national data. Ann Saudi Med 1996;16:386-91.
Nwafor CC, Nwafor NN. The pattern and distribution of cancers in Akwa Ibom state, Nigeria. Niger J Clin Pract 2018;21:603-8.
] [Full text]
Iliyasu Y, Ladipo JK, Akang EE, Adebamowo CA, Ajao OG, Aghadiuno PU, et al.
Atwenty-year review of malignant colorectal neoplasms at university college hospital, Ibadan, Nigeria. Dis Colon Rectum 1996;39:536-40.
Bhurgri Y, Faridi N, Kazi LA, Ali SK, Bhurgri H, Usman A, et al.
Cancer esophagus Karachi 1995-2002: Epidemiology, risk factors and trends. J Pak Med Assoc 2004;54:345-8.
Mike F. Müller MF, Ibrahim EK, Arends MJ. Molecular pathological classification of colorectal cancer. Virchows Arch 2016;469:125-34.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10]