Westphal A, 1937. Betrachtungen und experimentelle untersucchungen zur virulenz der Entamoeba histolytica beim menschen. Arch Schiffs Tropenhyg Leipzig 41: 262–279.
Bracha R, Kobiler D, Mirelman D, 1982. Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infect Immun 36: 396–406.
Bracha R, Mirelman D, 1983. Adherence and ingestion of Escherichia coli serotype 055 by trophozoites of Entamoeba histolytica. Infect Immun 40: 882–887.
Nixon JE, Wang A, Field J, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J, 2002. Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 1: 181–190.
Nixon JE, Field J, McArthur AG, Sogin ML, Yarlett N, Loftus BJ, Samuelson J, 2003. Iron-dependent hydrogenases of Entamoeba histolytica and Giardia lamblia: activity of the recombinant entamoebic enzyme and evidence for lateral gene transfer. Biol Bull 204: 1–9.
Field J, Rosenthal B, Samuelson J, 2000. Early lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol Microbiol 38: 446–455.
Rosenthal B, Zhiming M, Caplivski D, Ghosh S, de la Vega H, Graf T, Samuelson J, 1997. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoa parasite Entamoeba histolytica. J Bacteriol 179: 3736–3745.
Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433: 865–868.
Alsmark UC, Sicheritz-Ponten T, Foster GP, Hirt PR, Embley TM, 2009. Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol Biol 532: 489–500.
Padilla-Vaca F, Ankri S, Bracha R, Koole L, Mirelman D, 1999. Down regulation of Entamoeba histolytica virulence by monoxenic cultivation with Escherichia coli O55 is related to a decrease in expression of the light (35-kilodaltons) subunit of the Gal/GalNac lectin. Infect Immun 67: 2096–2102.
Galván-Moroyoqui JM, Domínguez-Robles MC, Franco E, Meza I, 2008. The interplay between Entamoeba and enteropathogenic bacteria modulates epithelial cell damage. PLoS Negl Trop Dis 2: e266.
Wittner M, Rosembaum RM, 1970. Role of bacteria in modifying virulence of Entamoeba histolytica. Am J Trop Med Hyg 19: 755–761.
Pimenta PF, Diamond LS, Mirelman D, 2002. Entamoeba histolytica Schaudinn, 1903 and Entamoeba dispar Brumpt, 1925: differences in their cell surfaces and in the bacteria-containing vacuoles. J Eukaryot Microbiol 49: 209–219.
Bracha R, Mirelmam D, 1984. Entamoeba histolytica trophozoites: effect of bacteria, microaerobic conditions and metronidazole. J Exp Med 160: 353–369.
Murray HW, Aley SB, Scott WA, 1981. Susceptibility of Entamoeba histolytica to oxygen intermediates. Mol Biochem Parasitol 3: 381–391.
Mirelman D, 1987. Ameba-bacterium relationship in amebiasis. Micriobiol Rev 51: 272–284.
Basu S, 2009. Klebsiella pneumoniae: an emerging pathogen of pyogenic liver abscess. Oman Med J 24: 131–133.
Bar-Shavit Z, Goldman R, Ofek I, Sharon N, Mirelman D, 1980. Mannose-binding activity of Entamoeba histolytica: a determinant of attachment and ingestion of the bacteria by macrophages. Infect Immun 29: 417–424.
Yu-Jang S, Yen-Chun L, Yu-Chia L, Yu-Hang Y, 2010. Treatment and prognosis of pyogenic liver abscess. Int J Emerg Med 3: 381–384.
Ramos F, Mora P, González E, García G, Ramiro M, Gómez A, De León M del C, Melendro EI, Valadez A, Ximénez C, 2005. High prevalence rate of Entamoeba histolytica asymptomatic infection in a rural Mexican community. Am J Trop Med Hyg 73: 87–91.
Ximénez C, Morán P, Rojas L, Valadez A, Gómez A, 2009. Reassessment of the epidemiology of amebiasis: state of the art. Infect Genet Evol 9: 1023–1032.
Lara R, Galindo E, Olarte J, Hernández G, 1974. Mixed infections by E. histolytica, Shigella and other enteropathogenic bacteria, found in children with diarrhea. Arch Invest Med (Mex) 5: 515–518.
Chatterjee BD, Thawani G, Sanyal SN, 1989. Etiology of acute childhood diarrhea in Calcutta. Trop Gastroenterol 10: 158–166.
Orlandi PP, Silva T, Magalhães GF, Alves F, de Almeida Cunha RP, Durlacher R, Pereira da Silva LH, 2001. Enteropathogens associated with diarrheal disease in infants of poor urban areas of Porto Velho, Rondônia: a preliminary study. Mem Inst Oswaldo Cruz 96: 621–625.
Haque R, Mondal D, Kirkpatrick BD, Akther S, Farr BM, Sack RB, Petri WA, 2003. Epidemiologic and clinical characteristics of acute diarrhea with emphasis on Entamoeba histolytica infections in preschool children in an urban slum of Dhaka, Bangladesh. Am J Trop Med Hyg 69: 398–405.
Lagier JC, Million M, Hugon P, Armougom F, Raoult D, 2012. Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2: 136.
Ximénez C, Cerritos R, Rojas L, Dolabella S, Morán P, Shibayama M, González E, Valadez A, Hernández E, Valenzuela O, Limón A, Partida O, Silva EF, 2010. Human amebiasis: breaking the paradigm? Int J Environ Res Public Health 7: 1105–1120.
Graffeo R, Archibusacci CM, Soldini S, Romano L, Masucci L, 2014. Entamoeba dispar: a rare case of enteritis in a patient living in a nonendemic area. Case Rep Gastrointest Med 2014: 498058.
Lane DJ, 1991. 16S/23S rRNA sequencing. Stackebrandt E, Goodfellow M, eds. Nucleic Acid Techniques in Bacterial Systematics. New York, NY: Wiley, 115–175.
Ali IKM, Zaki M, Clark CG, 2005. Use of PCR amplification of tRNA gene-linked short tandem repeats for genotyping Entamoeba histolytica. J Clin Microbiol 43: 5842–5847.
Zermeño V, Ximénez C, Morán P, Valadez A, Valenzuela O, Rascón E, Diaz D, Cerritos R, 2013. Worldwide genealogy of Entamoeba histolytica. An overview to understand haplotype distribution and infection outcome. Infect Genet Evol 17: 243–252.
Hall TA, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
Ronquist F, Huelsenbeck JP, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Costa PS, Santos CN, Cunha P, Cotter J, Sousa N, 2013. The use of multiple correspondence analysis to explore associations between categories of qualitative variables in healthy ageing. J Aging Res 2013: 302163.
Morán P, Gómez A, Valadez A, Ramos F, González E, García G, Limón A, Valenzuela O, Ramiro M, Hidalgo H, Melendro EI, Ximénez C, 2007. Amebic and Pyogenic Liver Abscess: Importance of Differential Diagnosis in Endemic Areas of Amebiasis. International Proceedings of the 5th European Congress on Tropical Medicine and International Health, Amsterdam, The Netherlands, 57–64.
Ali IKM, Solaymani-Mohammadi S, Akhter J, Roy S, Gorrini C, Calderaro A, Parker SK, Haque R, Petri WA, Clark CG, 2008. Tissue invasion by Entamoeba histolytica: evidence of genetic selection and/or DNA reorganization events in organ tropism. PLoS Negl Trop Dis 2: e219.
Sachdev DD, Yin MT, Horowitz JD, Mukkamala SK, Lee SE, Ratnerc AJ, 2013. Klebsiella pneumoniae K1 liver abscess and septic endophthalmitis in a U.S. resident. J Clin Microbiol 51: 1049–1051.
Liu Y, Wang J, Jiang W, 2013. An increasing prominent disease of Klebsiella pneumoniae liver abscess: etiology, diagnosis, and treatment. Gastroenterol Res Pract 2013: 258514.
Benazzouz M, Afifi R, Ibrahimi A, Essaid FA, Sebti MF, 1996. Liver abscess: diagnosis and treatment. Study of a series of 22 cases. Ann Gastroenterol Hepatol (Paris) 31: 333–336.
Tazawa J, Sakai Y, Maekawa S, Ishida Y, Maeda M, Marumo F, Sato C, 1997. Solitary and multiple pyogenic liver abscesses: characteristics of the patients and efficacy of percutaneous drainage. Am J Gastroenterol 92: 271–274.
Jamil B, Hamid SS, 2002. Abscesses in the liver: amebic or pyogenic? J Pak Med Assoc 52: 495–496.
Ahsan T, Jehangir MU, Mahmood T, Ahmed N, Saleem M, Shahid M, Shaheer A, Anwer A, 2002. Amebic versus pyogenic liver abscess. J Pak Med Assoc 52: 497–501.
Lodhi S, Sarwari AR, Muzammil M, Salam A, Smego RA, 2004. Features distinguishing amebic from pyogenic liver abscess: a review of 577 adult cases. Trop Med Int Health 9: 718–723.
Valenzuela O, Ramos F, Moran P, Gonzalez E, Valadez A, Gómez A, Melendro EI, Ramiro M, Muñoz O, Ximénez C, 2001. Persistence of secretory antiamoebic antibodies in patients with past invasive intestinal or hepatic amebiasis. Parasitol Res 87: 849–852.
Alam MA, Maqboo A, Nazir MM, Lateef M, Khan MS, Ahmed AN, Mughal Z, Lindsay DS, 2014. Prevalence of Entamoeba histolytica-like cysts compared to E. histolytica antigens detected by ELISA in the stools of 600 patients from three socioeconomic communities in the metropolitan city of Lahore, Pakistan. J Parasitol 101: 236–239.
Tengku SA, Norhayati M, 2011. Public health and clinical importance of amebiasis in Malaysia: a review. Trop Biomed 28: 194–222.
Nathaniel CVC, Sarah NB, William AP Jr, 2012. Common pathways for receptor-mediated ingestion of Escherichia coli and LDL cholesterol by Entamoeba histolytica regulated in part by transmembrane kinase 39. Int J Parasitol 42: 393–400.
Talamaìs-Lara D, Chaìvez-Munguiìa B, Gonzaìlez-Robles A, Talamaìs-Rohana P, Salazar-Villatoro L, Duraìn-Diìaz A, Martiìnez-Palomo A, 2014. Erythrophagocytosis in Entamoeba histolytica and Entamoeba dispar: a comparative study. BioMed Res Int 2014: 626259.
Ilan Y, 2012. Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis. World J Gastroenterol 18: 2609–2618.
Kim JK, Chung DR, Wie SH, Lin YT, Wang FD, Wu PF, Fung CP, 2013. Klebsiella pneumoniae liver abscess in diabetic patients: association of glycemic control with the clinical characteristics. BMC Infect Dis 13: 56.
Fang CT, Chuang YP, Shun CT, Chang SC, Wang JT, 2004. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. J Exp Med 199: 697–705.
Fung CP, Lin YT, Lin JC, Chen TL, Yeh KM, Chang FY, Chuang HC, Wu HS, Tseng CP, Siu LK, 2012. Klebsiella pneumoniae in gastrointestinal tract and pyogenic liver abscess. Emerg Infect Dis 18: 1322–1325.
Rahimian J, Wilson T, Oram V, Holzman RS, 2004. Pyogenic liver abscess: recent trends in etiology and mortality. Clin Infect Dis 39: 1654–1659.
Lok KH, Li KF, Szero ML, 2008. Pyogenic liver abscess: clinical profile, microbiological characteristics, and management in a Hong Kong hospital. J Microbiol Immunol Infect 41: 483–490.
Brook I, Frazier EH, 1998. Microbiology of liver and spleen abscesses. J Med Microbiol 47: 1075–1080.
Cosme A, Ojeda E, Zamarreño I, Bujanda L, Garmendia G, Echeverría MJ, Benavente J, 2010. Pyogenic versus amebic liver abscesses. A comparative clinical study in a series of 58 patients. Rev Esp Enferm Dig 102: 90–99.
Sheh A, Fox JG, 2013. The role of the gastrointestinal microbiome in Helicobacter pylori pathogenesis. Gut Microbes 4: 505–531.
Halliez MC, Buret AG, 2013. Extra-intestinal and long term consequences of Giardia duodenalis infections. World J Gastroenterol 19: 8974–8985.
|Past two years||Past Year||Past 30 Days|
|Full Text Views||420||143||2|
Several recent studies have demonstrated that virulence in Entamoeba histolytica is triggered in the presence of both pathogenic and nonpathogenic bacteria species using in vitro and in vivo experimental animal models. In this study, we examined samples aspirated from abscess material obtained from patients who were clinically diagnosed with amebic liver abscess (ALA) or pyogenic liver abscess (PLA). To determine the diversity of bacterial species in the abscesses, we performed partial 16S rRNA gene sequencing. In addition, the E. histolytica and Entamoeba dispar species were genotyped using tRNA-linked short tandem repeats as specific molecular markers. The association between clinical data and bacterial and parasite genotypes were examined through a correspondence analysis. The results showed the presence of numerous bacterial groups. These taxonomic groups constitute common members of the gut microbiota, although all of the detected bacterial species have a close phylogenetic relationship with bacterial pathogens. Furthermore, some patients clinically diagnosed with PLA and ALA were coinfected with E. dispar or E. histolytica, which suggests that the virulence of these parasites increased in the presence of bacteria. However, no specific bacterial groups were associated with this effect. Together, our results suggest a nonspecific mechanism of virulence modulation by bacteria in Entamoeba.
Financial support: This work was partially supported by the Grant IN218214 and IN226511 from the Support Program to Research and Technological Development Projects (PAPIIT) from the National University of Mexico and Grant number 210-COI-140990 from the National Council of Science and Technology in Mexico.
Authors' addresses: Miriam E. Reyna-Fabián, Valeria Zermeño, Cecilia Ximénez, Janin Flores, Jesús Argueta, Patricia Moran, Alicia Valadez, and René Cerritos, Departamento de Medicina Experimental, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), México City, México, E-mails: firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, and email@example.com. Miguel F. Romero and Daniel Diaz, Departamento de Biología Celular y Fisiología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México (UNAM), México City, México, E-mails: firstname.lastname@example.org and email@example.com.