The Open Infectious Diseases Journal




ISSN: 1874-2793 ― Volume 11, 2019
REVIEW ARTICLE

A Current Perspective of Schistosomiasis in Association with Colorectal Carcinogenesis



Eshtiyag Abdalla Abdalkareem1, 2, Khoo Boon Yin1, *
1 Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, 11800 Penang, Malaysia
2 Meknimer Street P.O.Box 2404, Tropical Medicine Research Institute (TMRI), Khartoum, Sudan

Abstract

Background:

Schistosomiasis is one of the parasitic infections that are often found in humans. More than approximately 200 million people are infected with Schistosomiasis in tropical and subtropical areas of Africa, South America and Asian countries. Literature has long been suggesting the correlation between Schistosomiasis and colorectal malignancy. There is a considerable directory supporting the etiological relation between Schistosoma japonicum infection and colorectal cancer in the Far East, however, the available data about the role of Schistosoma mansoni that can initiate the carcinogenesis of colorectal remain insignificant.

Objective:

As such, more studies of this disease should be conducted comprehensively for corporate social responsibility internationally.

Methods:

The present study reviewed the available data about the role of Schistosoma, including S. mansoni in association with the carcinogenesis of colorectal.

Results:

The study shows the possible evidence of epidemiology, pathology, molecules and immunopathology associated with Schistosomal infections and colorectal cancer. The infections are apparently getting little attention nor support worldwide due to the geographical barriers and some political issues because it mainly occurs in the people living in the bottom billion and happens in the endemic regions only.

Conclusion:

The in-depth study of this infectious disease will tailor early diagnosis, novel prescription drugs and cost-effective strategies for the treatment of infectious disease colorectal cancer, and hence eradicate the disease in the endemic regions.

Keywords: Schistosomiasis, Colorectal cancer, Neglected infectious disease, Schistosoma mansoni, Schistosoma japonicum, Disease eradication.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 11
First Page: 7
Last Page: 12
Publisher Id: TOIDJ-11-7
DOI: 10.2174/1874279301911010007

Article History:

Received Date: 6/10/2018
Revision Received Date: 19/12/2018
Acceptance Date: 7/1/2019
Electronic publication date: 31/1/2019
Collection year: 2019

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© 2019 Abdalkareem and Yin.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia, 11800 Penang, Malaysia; Tel: +604-6534819; E-mails: boonyin@usm.my, kboonyin@yahoo.com




1. INTRODUCTION

Schistosomiasis is a fairly predominant infectious disease that is caused by trematode of the Schistosoma genus in tropical and subtropical areas [1Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006; 368(9541): 1106-18.[http://dx.doi.org/10.1016/S0140-6736(06)69440-3] [PMID: 169976 65] , 2Elmorshedy H, Bergquist R, El-Ela NEA, Eassa SM, Elsakka EE, Barakat R. Can human schistosomiasis mansoni control be sustained in high-risk transmission foci in Egypt? Parasit Vectors 2015; 8: 372.[http://dx.doi.org/10.1186/s13071-015-0983-2] [PMID: 26174621] ]. It is the second most common parasitic infections for human after Malaria in the world. The diseases affect the health of more than 200 million people worldwide, particularly to the people living under poor and transmission-favourable conditions [1Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006; 368(9541): 1106-18.[http://dx.doi.org/10.1016/S0140-6736(06)69440-3] [PMID: 169976 65] , 3Jong EC. Schistosomiasis. Netter’s Infect Dis 2012; 516-21.]. Schistosomiasis that occurs in humans is mostly caused by three main species of Schistosoma; Schistosoma mansoni (S. mansoni) that constantly occurs in the endemic areas of South America, the Middle East and Africa, whereas Schistosoma japonicum (S. japonicum) commonly occurs in Southeast Asia, the Philippines, Southern China and Laos [4Leonardo LR, Rivera P, Saniel O, et al. Prevalence survey of schistosomiasis in Mindanao and the Visayas, The philippines. Parasitol Int 2008; 57(3): 246-51.[http://dx.doi.org/10.1016/j.parint.2008.04.006] [PMID: 18508406] , 5Leonardo L, Rivera P, Saniel O, et al. A national baseline prevalence survey of schistosomiasis in the Philippines using stratified two-step systematic cluster sampling design. J Trop Med 2012; 8 pages.[http://dx.doi.org/10.1155/2012/936128] ]. On the other hand, Schistosoma haematobium (S. haematobium) is prevalent in the Middle East and Africa [1Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006; 368(9541): 1106-18.[http://dx.doi.org/10.1016/S0140-6736(06)69440-3] [PMID: 169976 65] , 6Kali A. Schistosome infections: An Indian perspective. J Clin Diagn Res 2015; 9(2): DE01-4.[http://dx.doi.org/10.7860/JCDR/2015/10512.5521] [PMID: 25859 459] ].

The development of molecular biology has provided guidelines to clarify the relationship between the agents of the infection of this disease in the development of cancers. Studies of the development of cancers have delivered a great deal of valuable information on the molecular basis of carcinogenesis and infectious disease [7Farid M, El-Awady S, Abdel-Moneim H, Sakr H, El-Ghafar AA, El-Desouky E. Evolution of colorectal cancer in schistosomiasis. Egypt J Surg 2006; 25(4): 206-12., 8Palumbo E. Association between schistosomiasis and cancer: A review. Infect Dis Clin Pract 2007; 15(3): 145-8.[http://dx.doi.org/10.1097/01.idc.0000269904.90155.ce] ]. The infection of this disease can initiate or enhance carcinogenesis through three main mechanisms. Firstly, the infection induces chronic inflammation that happened due to the long-term continuation of infectious agents inside the host. The release of nitrogen and reactive oxygen radicals lead to DNA damage of the host cells. Secondly, it induces active oncogene insertion into the host genome. The oncogene causes distinct changes in gene expression in infected patients, leading to cancer development. Thirdly, it induces immune-surveillance reduction as a result of immunosuppression [9Kuper H, Adami HO, Trichopoulos D. Infections as a major preventable cause of human cancer. J Intern Med 2000; 248(3): 171-83.[http://dx.doi.org/10.1046/j.1365-2796.2000.00742.x] [PMID: 10971 784] ], leading to the high tendency of an infected patient to develop cancer. With this regard, infections with Schistosomiasis can be related to the aetiology of inflammation, oncogene expression and immunosuppression of various human malignancies, including liver and bladder cancers, as well as recently colorectal cancer.

Schistosomal infections may lead to complications, e.g. chronic intestinal and hepatosplenic Schistosomiasis, which has high morbidity and mortality if the disease is not diagnosed and treated early. Many reports describe the association of S. japonicum with bowel malignancy [10Hung CS, Liang HH, Hsu W, et al. Rectal cancer in a patient infested with Schistosomiasis japonicum: Case report and literature review. Fu-Jen Journal of Medicine 2010; 8(4): 223-6.-12Peterson MR, Weidner N. Gastrointestinal neoplasia associated with bowel parasitosis: Real or imaginary? J Trop Med 2011; 8 pages.[http://dx.doi.org/10.1155/2011/234254] ] and S. hematobium in urinary bladder malignancy [13Pisani P, Parkin DM, Muñoz N, Ferlay J. Cancer and infection: Estimates of the attributable fraction in 1990. Cancer Epidemiol Biomarkers Prev 1997; 6(6): 387-400.[PMID: 9184771] ]. Considerable evidence has also supported an etiological relation between S. japonicum and colorectal carcinogenesis. Indeed, existing data demonstrated that Schistosomal colitis caused by S. mansoni is more ordinarily related to an earlier stage or beginning of multicentric colorectal carcinoma [8Palumbo E. Association between schistosomiasis and cancer: A review. Infect Dis Clin Pract 2007; 15(3): 145-8.[http://dx.doi.org/10.1097/01.idc.0000269904.90155.ce] ]. However, the precise role of S. mansoni in colorectal carcinogenesis remains meagre.

The infectious disease that commonly occurs in the tropics is probably associated with various malignant colorectal diseases [14Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] , 15van Tong H, Brindley PJ, Meyer CG, Velavan TP. Parasite infection, carcinogenesis and human malignancy. EBioMedicine 2017; 15: 12-23.[http://dx.doi.org/10.1016/j.ebiom.2016.11.034] [PMID: 27956028] ]. The precursors of colorectal carcinoma have been demonstrated to be chronic inflammatory bowel diseases, e.g. Crohn’s and ulcerative colitis diseases, though adenomatous polyps also cause colorectal cancer development. Infections of S. mansoni and S. japonicum in the intestine begin with segregated eggs in the mucosa and submucosa, inciting a severe inflammatory reaction with cellular infiltration and consequent granuloma formation in the intestine [16Ross AG, Bartley PB, Sleigh AC, et al. Schistosomiasis. N Engl J Med 2002; 346(16): 1212-20.[http://dx.doi.org/10.1056/NEJMra012396] [PMID: 11961151] -18Gu K, Li Y, Driguez P, et al. Clinical diagnostic value of viable Schistosoma japonicum eggs detected in host tissues. BMC Infect Dis 2017; 17(1): 244.[http://dx.doi.org/10.1186/s12879-017-2362-4] [PMID: 28376858] ]. This reaction, in turn, leads to the development of mucosal ulceration, microabscess formation, polyposis and neoplastic transformation that may result in the development of colorectal cancer. Inflammation due to other factors may also cause colorectal cancer, but inflammation induced by infection agents accelerates the carcinogenesis. Most of the issued data regarding this infection indicate S. japonicum and colorectal cancer, whereas the scientific data refer S. mansoni to colorectal carcinogenesis remains rare.

2. EVIDENCE ACQUISITION

There are considerable directory and evidence supporting the etiological relation between S. japonicum infection and colorectal cancer in the Far East, however, the available data about the role of S. mansoni that initiate the carcinogenesis of colorectal more ordinarily remain insignificant. Work of literature have long been suggesting the correlation between Schistosomiasis and colorectal malignancy. As such, this review aims to shed light on the evidence that supports the relation between Schistosomiasis, including S. mansoni infection and colorectal carcinogenesis to prove that studying S. mansoni is as important as studying other species of Schistosoma.

3. RESULTS

3.1. Epidemiological Evidence

A few epidemiological studies have reported the possible association between the infection of S. mansoni and colorectal cancer. The previous study noted that there was a significant variance in the geographical distribution of infection with S. mansoni, where the colorectal cancer was clearly shown to be associated with S. mansoni in the African continents [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] ]. Moreover, this infection is associated with inflammation. Any infection, including with S. mansoni that showed a strong effect on inflammation is related to chronic infections of the gastrointestinal tract and is likely to lead to tumour development. For example, a recent study in Uganda and Zimbabwe that compared 950 cases of the infective gastrointestinal disease found that 34 of the patients with the colorectal disease had chronic Schistosomiasis or Amebiasis [19Waku M, Napolitano L, Clementini E, et al. Risk of cancer onset in sub-Saharan Africans affected with chronic gastrointestinal parasitic diseases. Int J Immunopathol Pharmacol 2005; 18(3): 503-11.[http://dx.doi.org/10.1177/039463200501800310] [PMID: 16164831] ]. Therefore, it concludes that large bowel cancer is possibly correlated with chronic infections and gastrointestinal diseases that are possibly associated with Schistosomal infections, including S. mansoni.

Another study that recruited 93 patients with colorectal cancer with or without S. mansoni infection in Sudan reported that 40-43% of the patients diagnosed with malignant colorectal cancer by colonoscopy and histopathology were infected with S. mansoni [20Abdelkareem EA, Tan GC, Sharief AH, Lim BH, Khoo BY. Identification of specific proteins in colorectal cancer patients with Schistosoma mansoni infection as a possible biomarker for the treatment of this infection. Asian Pac J Trop Dis 2014; 4(2): 720-4.[http://dx.doi.org/10.1016/S2222-1808(14)60714-3] ]. Furthermore, 40% of the colorectal cancer patients infected with S. mansoni were younger than 40 years [21Abou-Zeid AA, Khafagy W, Marzouk DM, Alaa A, Mostafa I, Ela MA. Colorectal cancer in Egypt. Dis Colon Rectum 2002; 45(9): 1255-60.[http://dx.doi.org/10.1007/s10350-004-6401-z] [PMID: 12352245] , 22Mansoor I, Zahrani IH, Abdul Aziz S. Colorectal cancers in Saudi Arabia. Saudi Med J 2002; 23(3): 322-7.[PMID: 11938426] ] and as much as 21% of young children were infected with S. mansoni in the country [23Curtale F, Nabil M, el Wakeel A, Shamy MY. Anaemia and intestinal parasitic infections among school age children in Behera Governorate, Egypt. J Trop Pediatr 1998; 44(6): 323-8.[http://dx.doi.org/10.1093/tropej/44.6.323] [PMID: 9972072] , 24Ibrahim AM, Ibrahim ME. Evaluation of microscopical and serological techniques in the diagnosis of Schistosoma mansoni infection at Sennar State, Central Sudan. Asian Pac J Trop Dis 2014; 4(1): 8-13.[http://dx.doi.org/10.1016/S2222-1808(14)60305-4] ]. Studies have also shown that 90% of colorectal cancers are affected by environmental factors and only 10% are due to genetics [25Anand P, Kunnumakkara AB, Sundaram C, et al. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res 2008; 25(9): 2097-116.[http://dx.doi.org/10.1007/s11095-008-9661-9] [PMID: 18626751] ]. The factors of genetic include uncommon gene mutations that reduce the penetration defence and inherited gene expression in the family group are unusual. The factors associated with exposure to Schistosoma in young people and children include a contaminated environment, swimming pool water [26Grimes JET, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR. The roles of water, sanitation and hygiene in reducing schistosomiasis: A review. Parasit Vectors 2015; 8: 156.[http://dx.doi.org/10.1186/s13071-015-0766-9] [PMID: 25884172] , 27Magaisa K, Taylor M, Kjetland EF, Naidoo IPJ. A review of the control of schistosomiasis in South Africa. S Afr J Sci 2015; 111: 11-2.[http://dx.doi.org/10.17159/sajs.2015/20140427] ] and the westernization of their diet [28Evan Secor W. Water-based interventions for schistosomiasis control. Pathog Glob Health 2014; 108(5): 246-54.[http://dx.doi.org/10.1179/2047773214Y.0000000149] [PMID: 2517 5875] ]. Processed western foods are often contaminated with chemical substances and microorganisms because of multiple handling processes that are not hygienic.

Studying the correlation of Schistosomal infections with colorectal cancer revealed that men have a higher tendency to develop the infections than women [29Hammam HM, Zarzour AH, Moftah FM, et al. The epidemiology of schistosomiasis in Egypt: Qena governorate. Am J Trop Med Hyg 2000; 62(2)(Suppl.): 80-7.[http://dx.doi.org/10.4269/ajtmh.2000.62.80] [PMID: 10813504] -32Shati A. Factors affecting the prevalence of human schistosomiasis in Aseer Region, Saudi Arabia. J Biol Sci 2009; 9(8): 815-9.[http://dx.doi.org/10.3923/jbs.2009.815.819] ], although McDermott found an equal sex distribution [33McDermott FT. Carcinoma of the rectum.Colorectal surgery 1999; 336.] and age groups [34Worku L, Damte D, Endris M, Tesfa H, Aemero M. Schistosoma mansoni infection and associated determinant factors among school children in Sanja Town, Northwest Ethiopia. J Parasitol Res 2014; 7 pages.[http://dx.doi.org/10.1155/2014/792536] ] of the infections. The tendency may also be due to the influence of male hormones [35Bernin H, Lotter H. Sex bias in the outcome of human tropical infectious diseases: Influence of steroid hormones. J Infect Dis 2014; 209(3)(Suppl. 3): S107-13.[http://dx.doi.org/10.1093/infdis/jit610] [PMID: 24966190] ]. Speculation suggested that the spread of Schistosomal infections in men is caused by more exposure to this infection. Most men work or seek work in agricultural areas that may be exposed to a contaminated environment, in which this infection occurs in the areas rapidly. As a result, men have a higher tendency to develop more Schistosomal infections, including S. mansoni infection. This high male tendency to develop an infection is also not fully hormone-dependent [36dos Santos Silva I, Swerdlow AJ. Sex differences in time trends of colorectal cancer in England and Wales: The possible effect of female hormonal factors. Br J Cancer 1996; 73(5): 692-7.[http://dx.doi.org/10.1038/bjc.1996.120] [PMID: 8605109] , 37Franceschi S, La Vecchia C. Colorectal cancer and hormone replacement therapy: An unexpected finding. Eur J Cancer Prev 1998; 7(6): 427-38.[http://dx.doi.org/10.1097/00008469-199812000-00002] [PMID: 992 6290] ]. Indeed, women with Schistosomal infections had a 3-4 fold increased risk of getting the Human Immunodeficiency Virus (HIV) compared to women without Schistosomal infections, increasing the ease of transmitting the HIV to their sexual partners [38Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA. Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis 2011; 5(12): e1396.[http://dx.doi.org/10.1371/journal.pntd.0001396] [PMID: 22163056] , 39Downs JA, Dupnik KM, van Dam GJ, et al. Effects of schistosomiasis on susceptibility to HIV-1 infection and HIV-1 viral load at HIV-1 seroconversion: A nested case-control study. PLoS Negl Trop Dis 2017; 11(9): e0005968.[http://dx.doi.org/10.1371/journal.pntd.0005968] [PMID: 28945756] ].

3.2. Pathological Evidence

The pathological changes of Schistosomiasis with colorectal carcinoma that have been described may, partially, play an aetiological role in bowel carcinogenesis [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] , 40Liu W, Zeng HZ, Wang QM, et al. Schistosomiasis combined with colorectal carcinoma diagnosed based on endoscopic findings and clinicopathological characteristics: A report on 32 cases. Asian Pac J Cancer Prev 2013; 14(8): 4839-42.[http://dx.doi.org/10.7314/APJCP.2013.14.8.4839] [PMID: 24083755] ]. Of the cases studied, around 60 cases of Schistosoma granulomatous disease of the large intestine were identified without carcinoma and 36 patients were found to have mild to severe dysplasia. The changes of dysplastic are considered as the pathological basis for the malignant probability of Schistosomal colitis and these changes are found in long-term ulcerative colitis [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] , 41Kim ER, Chang DK. Colorectal cancer in inflammatory bowel disease: The risk, pathogenesis, prevention and diagnosis. World J Gastroenterol 2014; 20(29): 9872-81.[http://dx.doi.org/10.3748/wjg.v20.i29.9872] [PMID: 25110418] ]. Chronic intestinal Schistosomiasis is noted as potentially a pre-cancerous condition [42Helmstädter V, Ostertag-Körner D, Wysocki S, Waldherr R. Schistosomiasis and signet ring cell carcinoma of the ileocecal valve. Dtsch Med Wochenschr 1994; 119(9): 301-4.[http://dx.doi.org/10.1055/s-2008-1058695] [PMID: 8119110] , 43Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] ] and many investigators believe that the mechanism of injury caused by Schistosoma is due to the endogenous production of toxins by eggs rather than a direct carcinogenic action of the eggs [43Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] ]. On the other hand, Matsuda believed that Schistosomal ova also displayed some effects on carcinogenesis [17Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: Review. J Adv Res 2013; 4(5): 445-52. [Review].[http://dx.doi.org/10.1016/j.jare.2012.12.001] [PMID: 25685451] , 44Matsuda K, Masaki T, Ishii S, et al. Possible associations of rectal carcinoma with Schistosoma japonicum infection and membranous nephropathy: A case report with a review. Jpn J Clin Oncol 1999; 29(11): 576-81.[http://dx.doi.org/10.1093/jjco/29.11.576] [PMID: 10678562] ].

In line with the above phenomenon, two cases were reported regarding this phenomenon by Al-Mashat in Saudi Arabia [43Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] ]. The first case presented a 46-year-old Saudi male patient with a two-month history of constipation and faecal soiling, whereby S. mansoni eggs were found in faecal. The case was also reported to be associated with rectal bleeding, anal pain, loss of weight and appetite. No previous similar symptoms and no family history of colorectal polyps or malignancies were found in the patient. The history before Schistosomiasis was not clear, but the results of rectal biopsy could moderately distinguish between adenocarcinoma and Schistosomal colitis. On the other hand, the second case presented a 55-year-old male patient, who lost 8 kg over four months and was under medications for diabetic and hypertensive, without the family history of ulcerative colitis or history of colorectal neoplasms or Schistosomiasis. The patient looked well upon examination, whereby the systemic review and abdominal examination were unremarkable; the rectal mass was extending down to the anal verge as observed by rectal examination and invasive moderately differentiated adenocarcinoma with many S. mansoni ova was shown in the biopsy.

In addition, other cases have also been reported in Sudan [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] ]. For example, an elderly man, who aged 35 years presented with a history of stomach cramps in the lower left stomach for four years. He suffered from abdominal pain, bleeding at rectal frequently and almost constant in the last two months of his medical history. This patient, who came from Al-Gezira province, was suffering from anorexia with frequent weight loss. Another reported case was that of a patient from the Al-Gezira state, an area of high endemicity of Schistosomiasis in Sudan, at the age of 20 was infected with S. mansoni. This patient, who had later received anti-Schistosoma treatment and the abdominal sonography, did not reveal significant periportal fibrosis or splenomegaly. The overall examination of the specimen showed an ulcerated tumour, S. mansoni ova in a cancerous tumour and colonic submucosa, where eggs were seen more in tumour tissue than in normal tissue. This case is consistent with the conditions of the infection, whereby intestinal Schistosomiasis induces various pathologic conditions, including carcinoma [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] , 15van Tong H, Brindley PJ, Meyer CG, Velavan TP. Parasite infection, carcinogenesis and human malignancy. EBioMedicine 2017; 15: 12-23.[http://dx.doi.org/10.1016/j.ebiom.2016.11.034] [PMID: 27956028] , 17Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: Review. J Adv Res 2013; 4(5): 445-52. [Review].[http://dx.doi.org/10.1016/j.jare.2012.12.001] [PMID: 25685451] , 42Helmstädter V, Ostertag-Körner D, Wysocki S, Waldherr R. Schistosomiasis and signet ring cell carcinoma of the ileocecal valve. Dtsch Med Wochenschr 1994; 119(9): 301-4.[http://dx.doi.org/10.1055/s-2008-1058695] [PMID: 8119110] , 45Ojo OS, Odesanmi WO, Akinola OO. The surgical pathology of colorectal carcinomas in Nigerians. Trop Gastroenterol 1991; 12(4): 180-4.[PMID: 1667558] , 46Jatzko G, Kleinert R, Denk H. Intestinal schistosomiasis, a facultative precancerous condition? Review of the literature with reference to Schistosoma japonicum associated rectum carcinoma. Chirurg 1997; 68(7): 727-31.[http://dx.doi.org/10.1007/s001040050261] [PMID: 9340240] ], lymphoma [15van Tong H, Brindley PJ, Meyer CG, Velavan TP. Parasite infection, carcinogenesis and human malignancy. EBioMedicine 2017; 15: 12-23.[http://dx.doi.org/10.1016/j.ebiom.2016.11.034] [PMID: 27956028] , 47Chirimwami B, Okonda L, Nelson AM. Lymphoma and Schistosoma mansoni schistosomiasis. Report of 1 case. Arch Anat Cytol Pathol 1991; 39(1-2): 59-61.[PMID: 1905526] ] polyps [17Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: Review. J Adv Res 2013; 4(5): 445-52. [Review].[http://dx.doi.org/10.1016/j.jare.2012.12.001] [PMID: 25685451] , 48King CL, Malhotra I, Mungai P, et al. Schistosoma haematobium-induced urinary tract morbidity correlates with increased tumor necrosis factor-alpha and diminished interleukin-10 production. J Infect Dis 2001; 184(9): 1176-82.[http://dx.doi.org/10.1086/323802] [PMID: 11598841] , 49Swe T, Baqui A, Naing AT, Baqui T, Sherigar J, Mansour M. Non-necrotizing colonic granuloma induced by schistosomiasis. J Community Hosp Intern Med Perspect 2016; 6(6): 33114.[http://dx.doi.org/10.3402/jchimp.v6.33114] [PMID: 27987283] ], carcinoid [43Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] ] and pedunculated teratoma [43Al-Mashat F, Sibiany A, Radwi A, et al. Rectal cancer associated with schistosomiasis: Report of two cases and review of the literature. Ann Saudi Med 2001; 21(1-2): 65-7.[http://dx.doi.org/10.5144/0256-4947.2001.65] [PMID: 17264594] ].

3.3. Molecular Evidence

Parasitism is highly correlated with defective in DNA repair, which is known as microsatellite instability [50Soliman AS, Bondy ML, El-Badawy SA, et al. Contrasting molecular pathology of colorectal carcinoma in Egyptian and Western patients. Br J Cancer 2001; 85(7): 1037-46.[http://dx.doi.org/10.1054/bjoc.2001.1838] [PMID: 11592777] ]. This errors of DNA replication can affect the target genes in cell replication, e.g. transforming growth factor-bRII and insulin-like growth factor-2R. This phenomenon renders cells unable of normal colonocyte homeostasis that can lead to abnormal growth [51Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: The role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004; 287(1): G7-G17.[http://dx.doi.org/10.1152/ajpgi.00079.2004] [PMID: 15194558] ]. Farid and his colleagues found a strong association between the Transformation-related Protein 53 (TP53) mutation and S. mansoni in colorectal cancer [7Farid M, El-Awady S, Abdel-Moneim H, Sakr H, El-Ghafar AA, El-Desouky E. Evolution of colorectal cancer in schistosomiasis. Egypt J Surg 2006; 25(4): 206-12.]. This close association supports the idea that Schistosoma colorectal cancer and harmful biological behaviour are related to the TP53 mutation [52Watson NF, Madjd Z, Scrimegour D, et al. Evidence that the p53 negative / Bcl-2 positive phenotype is an independent indicator of good prognosis in colorectal cancer: A tissue microarray study of 460 patients. World J Surg Oncol 2005; 3: 47.[http://dx.doi.org/10.1186/1477-7819-3-47] [PMID: 16029489] ]. Furthermore, Zhang and his colleagues suggested that the clastogen of TP53 was derived from S. japonicum, subsequently, others had found cross-reactivity and antigenic communities in different Schistosomiasis species [53Zhang R, Takahashi S, Orita S, et al. p53 gene mutations in rectal cancer associated with schistosomiasis japonica in chinese patients. Cancer Lett 1998; 131(2): 215-21.[http://dx.doi.org/10.1016/S0304-3835(98)00154-2] [PMID: 9851256] , 54Losada S, Chacón N, Colmenares C, et al. Schistosoma: Cross-reactivity and antigenic community among different species. Exp Parasitol 2005; 111(3): 182-90.[http://dx.doi.org/10.1016/j.exppara.2005.07.007] [PMID: 16165128] ]. Consequently, the molecules derived from S. mansoni inactivated TP53 resulting in the progression of Schistosoma associated colorectal cancer. Hence, S. mansoni is believed to be indirectly implicated in the progression of colorectal cancer.

On the other hand, a report denied the statements that the worms and egg extracts were mutagenic [55Osada Y, Kumagai T, Masuda K, Suzuki T, Kanazawa T. Mutagenicity evaluation of Schistosoma spp. extracts by the umu-test and V79/HGPRT gene mutation assay. Parasitol Int 2005; 54(1): 29-34.[http://dx.doi.org/10.1016/j.parint.2004.08.004] [PMID: 15710547] ], but colorectal cancer was a special clinical entity with a young age predilection, male predominance, distal colorectal prevalence and advanced-stage presentation. A more comprehensive study was developed by Zalata of the expression pattern of B-cell lymphoma 2 (Bcl-2), MYC proto-oncogene (c-myc) and protein 53 (p53) in 75 colorectal cancer cases, in which 24 of the cases were pathologically associated with S. mansoni infection [56Zalata KR, Nasif WA, Ming SC, et al. p53, Bcl-2 and C-Myc expressions in colorectal carcinoma associated with schistosomiasis in Egypt. Cell Oncol 2005; 27(4): 245-53.[PMID: 16308474] ]. The results showed a significant association between S. mansoni and colorectal cancer characterized by overexpression of Bcl-2 with less apoptotic activity than seen commonly in colorectal cancer, whereas the results did not show an association between p53 and c-myc expression with parasitism. This evasion of apoptosis phenomenon through a change in Bcl-2 expression may be due to an alternative molecular pathway, which induces carcinogenesis in intestinal Schistosomiasis. It is indicated that many genetic changes occur during the S. mansoni colorectal carcinogenesis that plays a significant role in the development and progression of the tumour. The molecular profile of S. mansoni colorectal carcinoma is believed to be different than the profile that has been demonstrated in colitis induced carcinomas, indicating that other factors than inflammation are also implicated in the carcinogenic process.

3.4. Immunopathology Evidence

Many explanations to clarify the potential role of Schistosomiasis that induces colorectal tumorigenesis have been mentioned in previous studies, where the existence of parasites endogenously generated carcinogens [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] , 57Rosin MP, Anwar WA, Ward AJ. Inflammation, chromosomal instability, and cancer: The schistosomiasis model. Cancer Res 1994; 54(7)(Suppl.): 1929s-33s.[PMID: 8137314] , 58Machicado C, Marcos LA. Carcinogenesis associated with parasites other than Schistosoma, Opisthorchis and Clonorchis: A systematic review. Int J Cancer 2016; 138(12): 2915-21.[http://dx.doi.org/10.1002/ijc.30028] [PMID: 26840624] ]. Therefore, the presence of Schistosomal toxins [59Long XC, Bahgat M, Chlichlia K, Ruppel A, Li YL. Detection of inducible nitric oxide synthase in Schistosoma japonicum and S. mansoni. J Helminthol 2004; 78(1): 47-50.[http://dx.doi.org/10.1079/JOH2003202] [PMID: 14972036] ], chronic immune-modulation that results in the impairment of immunological surveillance [60van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodulation: Consequences and mechanisms. Immunobiology 2007; 212(6): 475-90.[http://dx.doi.org/10.1016/j.imbio.2007.03.009] [PMID: 17544832] ] and symbiotic action of other infective agents [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] , 59Long XC, Bahgat M, Chlichlia K, Ruppel A, Li YL. Detection of inducible nitric oxide synthase in Schistosoma japonicum and S. mansoni. J Helminthol 2004; 78(1): 47-50.[http://dx.doi.org/10.1079/JOH2003202] [PMID: 14972036] , 61Ye C, Tan S, Jiang L, et al. Endoscopic characteristics and causes of misdiagnosis of intestinal schistosomiasis. Mol Med Rep 2013; 8(4): 1089-93.[http://dx.doi.org/10.3892/mmr.2013.1648] [PMID: 23969514] , 62Soliman NA, Keshk WA, Shoheib ZS, Ashour DS, Shamloula MM. Inflammation, oxidative stress and L-fucose as indispensable participants in schistosomiasis-associated colonic dysplasia. Asian Pac J Cancer Prev 2014; 15(3): 1125-31.[http://dx.doi.org/10.7314/APJCP.2014.15.3.1125] [PMID: 24606429] ] in Schistosomiasis are believed to induce tumourigenesis. All of these factors might interact to induce chronic inflammation and carcinogenesis. Schistosomal infections affect the host immune response in two ways that extend the carrier state of the parasite. Firstly, by anti-idiotype antibodies produced in patients with chronic Schistosomiasis to down-regulate specific immune responses and suppress non-specific immune responses [63van Den Biggelaar AH, Grogan JL, Filié Y, et al. Chronic schistosomiasis: Dendritic cells generated from patients can overcome antigen-specific T cell hyporesponsiveness. J Infect Dis 2000; 182(1): 260-5.[http://dx.doi.org/10.1086/315662] [PMID: 10882605] -65Naveed A, Rahman SU, Arshad MI, Aslam B. Recapitulation of the anti-idiotype antibodies as vaccine candidate. Transl Med Comm 2018; 3: 1.[http://dx.doi.org/10.1186/s41231-018-0021-4] ]. Secondly, by modifying the subpopulations of thymus helper cells to lower immune surveillance of infected organism and human [66Khurana S, Dubey ML, Malla N. Association of parasitic infections and cancers. Indian J Med Microbiol 2005; 23(2): 74-9.[http://dx.doi.org/10.4103/0255-0857.16044] [PMID: 15928434] , 67Ponnappan S, Ponnappan U. Aging and immune function: Molecular mechanisms to interventions. Antioxid Redox Signal 2011; 14(8): 1551-85.[http://dx.doi.org/10.1089/ars.2010.3228] [PMID: 20812785] ].

Inflammatory cells produce potential genotoxic mediators, e.g. reactive oxygen, nitrogen and pro-inflammatory cytokines that may induce genomic instability and the dysregulation of oncogenes and oncosuppressor genes during Schistosomal infections [68Herrera LA, Benítez-Bribiesca L, Mohar A, Ostrosky-Wegman P. Role of infectious diseases in human carcinogenesis. Environ Mol Mutagen 2005; 45(2-3): 284-303.[http://dx.doi.org/10.1002/em.20122] [PMID: 15744742] , 69Trakatelli C, Frydas S, Hatzistilianou M, et al. Chemokines as markers for parasite-induced inflammation and tumors. Int J Biol Markers 2005; 20(4): 197-203.[http://dx.doi.org/10.1177/172460080502000401] [PMID: 16398400] ], whereas the mutation of these molecular disorder leads to the development of carcinoma. The existence of concomitant enterobacterial infections in the host might play a significant role in the colorectal carcinogenesis of Schistosomiasis patients. Different strains of enteric bacteriaceae have been described in association with Schistosomal infections, granting a survival advantage to bacteria by inducing immune suppression [70Chieffi PP. Interrelationship between schistosomiasis and concomitant diseases. Mem Inst Oswaldo Cruz 1992; 87(4)(Suppl. 4): 291-6.[http://dx.doi.org/10.1590/S0074-02761992000800045] [PMID: 134 3911] ]. Part of these organisms is capable of stimulating colorectal carcinogenesis during various pathways, e.g. production of reactive oxygen intermediates, dysregulation in the T-cell response and modification the epithelial carbohydrate expression in the host [71Hope ME, Hold GL, Kain R, El-Omar EM. Sporadic colorectal cancer: Role of the commensal microbiota. FEMS Microbiol Lett 2005; 244(1): 1-7.[http://dx.doi.org/10.1016/j.femsle.2005.01.029] [PMID: 15727814] ]. Pathologically, Schistosomiasis leading to colorectal cancer is demonstrated by dysplastic morphological changes, aggressiveness in both pathologic variants and the tumour microenvironment, as well as elicitation of a poor host immune response.

Post S. mansoni infection, the T-helper 2 cell activity and cytokines involved in eosinophilia and immunoglobulin E secretion are stimulated [72Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, Berzofsky JA. Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci USA 1993; 90(3): 948-52.[http://dx.doi.org/10.1073/pnas.90.3.948] [PMID: 8094248] ]. On the other hand, the cytokines of T-helper 1 cell activity, e.g. Interleukin-2, interferon-gamma and cytotoxic CD8+ T-cells are demonstrated to be down-regulated in BALB/C mice post infected with S. mansoni. Other studies have shown that colorectal cancer is usually found in patients with a history of 10 years or more of Schistosomiasis and in whom the large bowel is wholly involved [11H Salim OE, Hamid HKS, Mekki SO, Suleiman SH, Ibrahim SZ. Colorectal carcinoma associated with Schistosomiasis: A possible causal relationship. World J Surg Oncol 2010; 8: 68.[http://dx.doi.org/10.1186/1477-7819-8-68] [PMID: 20704754] ]. There is a high rate of synchronous tumours in patients with Schistosoma colorectal cancer than in patients with spontaneous colorectal cancer [73Madbouly KM, Senagore AJ, Mukerjee A, et al. Colorectal cancer in a population with endemic Schistosoma mansoni: Is this an at-risk population? Int J Colorectal Dis 2007; 22(2): 175-81.[http://dx.doi.org/10.1007/s00384-006-0144-3] [PMID: 16786317] ]. This phenomenon can be due to the infection that is caused by chronic Schistosomal inflammation throughout the colon and rectum, an event that is similar to that described in the case of colitis-associated cancers. Chronic intestinal inflammation, on the other hand, is a well-known risk factor for colorectal cancer progression [74Jess T, Simonsen J, Jørgensen KT, Pedersen BV, Nielsen NM, Frisch M. Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology 2012; 143(2): 375-81.e1.[http://dx.doi.org/10.1053/j.gastro.2012.04.016] [PMID: 22522090] ]. The chronic inflammatory response induced by Schistosome antigens provides the proliferative motivation that is indispensable to enhance the cancer growth from potentially malignant foci. The increase in the epithelial cell proliferation post infection probably participates in cancers, but it is not sufficient to cause carcinogenesis.

CONCLUSION

The compelling epidemiological and molecular data, as well as the immunopathological features of Schistosomiasis colorectal cancer, describe a potential role for chronic Schistosomiasis in enhancing carcinogenesis of colorectal cancer and the inflammation represents the most important factor in the carcinogenic process. We believe there is more to explain the association between Schistosomiasis and colorectal cancer, particularly in the cases infected with S. mansoni, but yet to be fully elucidated. Many countries in South East Asia, including Malaysia, the Philippines and other tropical countries that are heavily burdened with the float season and tends to get contaminated river water and other sources of water, have not eliminated these parasites. As the published data linking S. mansoni to colorectal cancer occurrence remain rare, we adapted the success stories of Japan and the coastal plain of the People’s Republic of China, which have been successfully free from Schistosoma over the last two decades, as the role model to eradicate the diseases. Studying this topic in depth may help to tailor early diagnosis, novel prescription drugs and cost-effective strategies for treatment of infectious disease colorectal cancer, and hence eradicate the disease in the endemic regions in the near future.

LIST OF ABBREVIATIONS

HIV = Human Immunodeficiency Virus
TP53 = Transformation-related Protein 53
Bcl-2 = B-cell lymphoma 2
c-myc = MYC proto-oncogene
p53 = Protein 53

CONSENT FOR PUBLICATION

Not applicable.

CONFLICT OF INTEREST

We declare that we have no conflict of interest in the authorship or publication of this contribution.

ACKNOWLEDGEMENTS

The authors would like to thank USM-TWAS Fellowship and Tropical Medicine Research Institute (TMRI), Sudan for giving the supports to the first author of the study. This study was also supported by the Fundamental Research Grant Scheme (FRGS) Fasa 1/2017 (Grant No. 203/CIPPM/67115 99).

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