Abstract
Advances in molecular biology have facilitated analyses of the oral microbiome; however, the parasites role is poorly understood. Periodontal disease is a multifactorial process involving complex interactions among microorganisms, the host, and environmental factors. At present, the precise composition of the mouth parasites microbiota is unclear. Two protozoan species have been detected in the oral microbiota: Trichomonas tenax and Entamoeba gingivalis, and a new variant, E. gingivalis-ST2-kamaktli, was recently identified by us. In this study, both E. gingivalis and the new E. gingivalis-ST2-kamaktli variant were detected in the oral cavities of people with healthy periodontium, individuals undergoing orthodontic treatment, and patients with periodontal disease. In the group with healthy periodontium, the prevalence of E. gingivalis-ST1 was 48.6% and that of E. gingivalis-ST2-kamaktli 29.5%, with a combined prevalence of 54.3%. In patients undergoing orthodontics treatment, 81.2% carried both amoebas, with 47.5% having E. gingivalis-ST1 and 73.8% E. gingivalis-ST2-kamaktli. In people with periodontal disease, the prevalence of E. gingivalis-ST1 was 57.8%, and that of E. gingivalis-ST2-kamaktli 50.0%, with a combined prevalence of 73.5%; hence, E. gingivalis-ST1 and E gingivalis-ST2-kamaktli were detected in all three groups. The question arises, what are E. gingivalis-ST1 and E. gingivalis-ST2-kamaktli doing in the oral cavity? Although, the answer remains unclear, our results suggest that each amoeba subtype is genetically distinct, and they exhibit different patterns of infectious behavior. We hypothesize that E. gingivalis-ST1 and E. gingivalis-ST2-kamaktli may represent separate species. Our data contribute to better understanding of the roles of E. gingivalis-ST1 and E. gingivalis-ST2-kamaktli in the oral microbiota.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abualqomsaan M, Töz SO, Yolasiğmaz A, Turgay N (2010) The investigation of Entamoeba gingivalis and Trichomonas tenax in a group of patients with periodontal disease. Turkiye Parazitol Derg 34(2):91–94
Bonner M, Amard V, Bar-Pinatel C, Charpentier F, Chatard JM, Desmuyck Y, Ihler S, Rochert JP, Roux de la Tribouille V, Saladin L, Verdy M, Gironès N, Fresno M, Santi-Rocca J (2014) Detection of the amoeba Entamoeba gingivalis in periodontal pockets. Parasite 21:30. https://doi.org/10.1051/parasite/2014029
Chalabi M, Rezaie F, Moghim S, Mogharehabed A, Rezaei M, Mehraban B (2010) Periodontopathic bacteria and herpesviruses in chronic periodontitis. Mol Oral Microbiol 25(3):236–240. https://doi.org/10.1111/j.2041-1014.2010.00571.x
Chanda W, Joseph TP, Wang W, Padhiar AA, Zhong M (2017) The potential management of oral candidiasis using anti-biofilm therapies. Med Hypotheses 106:15–18. https://doi.org/10.1016/j.mehy.2017.06.029
Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nuc Acids Res 16:10881–10890
Cembranelli SB, Souto FO, Ferreira-Paim K, Richinho TT, Nunes PL, Nascentes GA, Ferreira TB, Correia D, Lages-Silva E (2013) First evidence of genetic intraspecific variability and occurrence of Entamoeba gingivalis in HIV(+)/AIDS. PLoS One 8(12):e82864. https://doi.org/10.1371/journal.pone.0082864
Dao AH, Robinson DP, Wong SW (1983) Frequency of Entamoeba gingivalis in human gingival scrapings. Am J Clin Pathol 80:380–383
Darveau RP, Hajishengallis G, Curtis MA (2012) Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 91(9):816–820. https://doi.org/10.1177/0022034512453589
Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG (2010) The human oral microbiome. J Bacteriol 192(19):5002–5017. https://doi.org/10.1128/JB.00542-10
El-Dardiry AM, Shabaan SH (2016) Detection of Entamoeba gingivalis trophozoites in patients suffering from gingivitis versus healthy subjects. Adv Environ Biol 10(12):222–226
Feller L, Altini M, Khammissa RA, Chandran R, Bouckaert M, Lemmer J (2013) Oral mucosal immunity. Oral Surg Oral Med Oral Pathol Oral Radiol 116(5):576–583. https://doi.org/10.1016/j.oooo.2013.07.013
Feller L, Khammissa RA, Chandran R, Altini M, Lemmer J (2014) Oral candidosis in relation to oral immunity. J Oral Pathol Med 43(8):563–569. https://doi.org/10.1111/jop.12120
Ferreira DC, Rôças IN, Paiva SS, Carmo FL, Cavalcante FS, Rosado AS, Santos KR, Siqueira JF Jr (2011) Viral-bacterial associations in acute apical abscesses. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 112(2):264–271. https://doi.org/10.1016/j.tripleo.2011.01.029
Ghabanchi J, Zibaei M, Afkar MD, Sarbazie AH (2011) Prevalence of oral Entamoeba gingivalis and Trichomonas tenax in patients with periodontal disease and healthy population in shiraz, southern Iran. Indian J Dent Res 21(1):89–91. https://doi.org/10.4103/0970-9290.62821
García G, Ramos F, Gutierrez-Pérez R, Yáñez J, Estrada MS, Mendoza LH, Martínez-Hernández F, Gaytán P (2014) Molecular epidemiology and genetic diversity of Entamoeba species in a chelonian collection. J Med Microbiol 63(Pt2):271–283. https://doi.org/10.1099/jmm.0.061820-0
García G, Ramos F, Martínez-Hernández F, Hernández L, Yáñez J, Gaytán P (2018) A new subtype of Entamoeba gingivalis: “E. gingivalis ST2, kamaktli variant”. Parasitol Res 117:1277–1284. https://doi.org/10.1007/s00436-018-5798-6
Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, McIntosh ML, Alsam A, Kirkwood KL, Lambris JD, Darveau RP, Curtis MA (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10(5):497–506. https://doi.org/10.1016/j.chom.2011.10.006
Hajishengallis G, Moutsopoulos NM (2016) Role of bacteria in leukocyte adhesion deficiency-associated periodontitis. Microb Pathog 94:21–26. https://doi.org/10.1016/j.micpath.2015.09.003
Kandelman D, Petersen PE, Ueda H (2008) Oral health, general health, and quality of life in older people Oral and general health in older people. Spec Care Dentis 23:224–236. https://doi.org/10.1111/j.1754-4505.2008.00045.x
Klukowska M, Bader A, Erbe C, Bellamy P, White DJ, Anastasia MK, Wehrbein H (2011) Plaque levels of patients with fixed orthodontic appliances measured by digital plaque image analysis. Am J Orthod Dentofac Orthop 139(5):e463–e470. https://doi.org/10.1016/j.ajodo.2010.05.019
Lucht E, Evengård B, Skott J, Pehrson P, Nord CE (1998) Entamoeba gingivalis in human immunodeficiency virus type 1-infected patients with periodontal disease. Clin Infect Dis 27(3):471–473
Meng H, Xu L, Li Q, Han J, Zhao Y (2007) Determinants of host susceptibility in aggressive periodontitis. Periodontol 2000 43:133–159
Mukherjee PK, Wang H, Retuerto M, Zhang H, Burkey B, Ghannoum MA, Eng C (2017) Bacteriome and mycobiome associations in oral tongue cancer. Oncotarget 8(57):97273–97289. https://doi.org/10.18632/oncotarget.21921
Nocito-Mendoza I, Vasconi-Correas MD, Ponce de León-Horianski P, Zdero-Pandzich M (2003) Entamoeba gingivalis y Trichomonas tenax en pacientes diabéticos. RCOE 8(1):13–23 scielo.isciii.es/scielo.php?script=sci_arttext&pid=S1138-123X2003000100002&lng=es&tlng=e
Onyido AE, Amadi ES, Olofin I, Onwumma AA, Okoh IC, Chikwendu CI (2011) Prevalence of Entamoeba gingivalis and Trichomonas tenax among dental patients attending Federal School of Dental Technology and Therapy clinic, Enugu, Nigeria. Nat Sci 9(9):59–62
Peng Y, Wu R, Qu W, Wu W, Chen J, Fang J, Chen Y, Farella M, Mei L (2014) Effect of visual method vs plaque disclosure in enhancing oral hygiene in adolescents and young adults: a single-blind randomized controlled trial. Am J Orthod Dentofac Orthop 145:280–286
Peters BA, Wu J, Hayes RB, Ahn J (2017) The oral fungal mycobiome: characteristics and relation to periodontitis in a pilot study. BMC Microbiol 17(1):157. https://doi.org/10.1186/s12866-017-1064-9
Ramsey MM, Rumbaugh KP, Whiteley M (2011) Metabolite cross-feeding enhances virulence in a model Polymicrobial infection. PLoS Pathog 7(3):e1002012. https://doi.org/10.1371/journal.ppat.1002012
Slots J (2011) Herpesvirus periodontitis: infection beyond biofilm. J Calif Dent Assoc 39(6):393–399 Social Scientific Statistical package on line. http://www.socscistatistics.com/Default.aspx
Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25(2):134–144
Tanner AC, Izard J (2006) Tannerella forsythia, a periodontal pathogen entering the genomic era. Periodontol 2000 42:88–113
Trim RD, Skinner MA, Farone MB, DuBois JD, Newsome AL (2011) Use of PCR to detect Entamoeba gingivalis in diseased gingival pockets and demonstrate its absence in healthy gingival sites. Parasitol Res 109(3):857–864
Verweij JJ, Polderman AM, Clark CG (2001) Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. J Clin Microbiol 39(4):1644–1646. https://doi.org/10.1128/JCM.39.4.1644-1646.2001
Yamamoto A, Kikuta N, Hashimoto T, Oyaizu H, Goto N (1995) Nucleotide sequence of the SrRNA gene of Entamoeba gingivalis: applications for construction of a species-specific DNA probe and phylogenetic analysis. Microbiol Immunol 39(3):185–192
Zhu L, Kreth J (2012) The role of hydrogen peroxide in environmental adaptation of oral microbial communities. Oxidative Med Cell Longev 717843:10. https://doi.org/10.1155/2012/717843
Acknowledgments
We thank the students in our lab, Eric López Huerta and Brenda Esmeralda Roldán Chávez, for the technical help with this project. We would like to thank Editage (www.editage.com) for the English language editing.
Funding
This research was carried out thanks to support from the Medicine Faculty (151/2014, 008/2016, and FM-DI/025/2018), and was approved by the Scientific and Ethics Committees at the Universidad Nacional Autónoma de México (UNAM).
Author information
Authors and Affiliations
Contributions
GG and RF conceived and designed the experiments; MJ and LA collected the oral samples and were responsible for approaching patients, and obtaining informed consent and questionnaires; GG and LH for the coordination of patient samples; RF organized the database; GG, RF, YJ, and GP performed the experiments; GG and RF performed the statistical analyses; and GG and RF wrote the entire manuscript. All authors contributed to manuscript revision, and read and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Panagiotis Karanis
Rights and permissions
About this article
Cite this article
Garcia, G., Ramos, F., Maldonado, J. et al. Prevalence of two Entamoeba gingivalis ST1 and ST2-kamaktli subtypes in the human oral cavity under various conditions. Parasitol Res 117, 2941–2948 (2018). https://doi.org/10.1007/s00436-018-5990-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-5990-8