Free living Amoebae: "Trojan horses" or vectors in the dissemination of Helicobacter pylori in aquatic environments?

Authors

Keywords:

Free living Amoebae, Helicobacter pylori, antimicrobial resistance, bacterial persistence.

Abstract

Introduction: Free living amoebae are unicellular eukaryotic microorganisms that are found in different environments and that interact with bacteria, viruses and fungus. Recently, it has called the attention of the scientific community the established relation between free living amoebae and Helicobacter pylori.

Objectives: To update the role of free-living amoebae in the dissemination of Helicobacter pylori, as well as to clarify how this phenomenon can influence in the bacterial persistence, and in its possible resistance to antimicrobials.

Methods: Different search engines such as Google, PubMed, Cochrane, Google Scholar, SciELO, Redalyc, among others were used. The search was limited to the last 10 years, although some older studies, mainly classics, were taking into consideration.

Conclusions: The updating of the topic back up the fact that free living amoebae, specially Acanthamoeba spp. in the aquatic environments, intervene as Helicobacter pylori reservoir and acts as "Trojan horses” for the persistence and the dissemination of this bacteria, considered resistant to antimicrobials, specially clarithromycin and a causal agent of several gastroduodenal diseases, for instance, gastric cancer. Future investigations focused on medullar aspects of the physiopathology of this relation between both microorganisms, should be projected for a better knowledge and level of acting in front of what can be considered a serious health problem. 

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Author Biography

Amilcar Duquesne Alderete, Hospital Ortopédico Docente Fructuoso Rodríguez, La Habana

Especialista de Primer Grado en Medicina General Integral. Especialista de Segundo Grado en Microbiologia. Master en Educación Médica Superior. Master e Bacteriologia- Micología. Doctor en Ciencias Médicas. Profesor Titular. Investigador Auxiliar.

References

Real Academia Española, Diccionario de la Lengua Española, avance de la 23º ed. Ameba 2016 [acceso 24/09/2016]. Disponible en: https://dle.rae.es/?id=2Ia7rRr

Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D, Bowser SS, et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012;59(5):429-93. DOI: https://doi:10.1111/j.1550-7408.2012.00644.x

Carrero JC, Reyes López M, Serrano Luna J, Shibayama M, Unzueta J, León-Sicairos N, et al. Intestinal amoebiasis: 160 years of its first detection and still remains as a health problem in developing countries. Int J Med Microbiol. 2020;310:151358. DOI: https://doi.org/10.1016/j.ijmm .2019.151358

Anderson OR. A half-century of research on free-living amoebae (1965-2017): review of biogeographic, ecological and physiological studies. Acta Protozol. 2018;57:1-28. DOI: https://doi.org/10.4467/16890027AP.18.001.8395

Vaerewijck MJM, Baré J, Lambrecht E, Sabbe K, Houf K. Interactions of foodborne pathogens with free-living protozoa: potential consequences for food Safety. Compr Rev Food Sci Food Saf. 2014;13(5):924-44. DOI: https://doi.org/10.1111/1541-4337.12100

Siddiqui R, Abouleish MY, Khamis M, Ibrahim T, Khan NA. Dual targeting of function–structure for effective killing of pathogenic free-living amoebae. ACS Med. Chem. Lett. 2021;12(5):672-6. DOI: https://doi.org/10.1021/acsmedchemlett.1c00200

Lorenzo-Morales J, Khan NA, Walochnik J. An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite. 2015;22:10. DOI: https://doi.10.1051/parasite/2015010

Alsam S, Sissons J, Dudley R, Khan NA. Mechanisms associated with Acanthamoeba castellanii (T4) phagocytosis. Parasitol Res. 2005;96:402-9. DOI: https://doi.10.1007/s00436-005-1401-z

Lorenzo Morales J, Monteverde Miranda CA, Jiménez C, Tejedor ML, Valladares B, Ortega Rivas A. Evaluation of Acanthamoeba isolates from environmental sources in Tenerife, Canary Islands, Spain. AAEM. 2005;12:233-6.

Lee DI, Park SH, Baek JH, Yoon JW, Jin SI, Han KE, et al. Identification of Free-Living Amoebas in Tap Water of Buildings with Storage Tanks in Korea. Korean J Parasitol. 2020;58(2):191-4. DOI: https://doi.org/10.3347/kjp.2020.58.2.191

Trabelsi H, Dendana F, Neji S, Sellami H, Cheikhrouhou F, Makni F, et al. Morphological and molecular identification of free living amoeba isolated from hospital water in Tunisia. Parasitol. Res. 2016;115(1):431-5. DOI: https://doi.10.1007/s00436-015-4788-1

Samba Louaka A, Delafont V, Rodier MH, Cateau E, Héchard Y. Free living amoebae and squatters in the wild: ecological and molecular features. FEMS Microbiol Rev. 2019;43:415-34. DOI: https://doi.org/10.1093/femsre/fuz011

Vaerewijck MJM, Sabbe K, Baré J, Houf K. Microscopic and molecular studies of the diversity of Free-Living Protozoa in meat-cutting plants. Appl Environ Microbiol. 2008;74(18):5741-9. DOI: https://doi.10.1128/AEM.00980-08

Fernández Leborans G. Epibiosis in Crustacea: an overview. Crustaceana. 2010;83(5):549-640. DOI: https://www.jstor.org/stable/27822637

Vaerewijck MJM, Sabbe K, Van Hende J, Baré J, Houf K. Sampling strategy, occurrence and diversity of free-living protozoa in domestic refrigerators: Free living protozoa in refrigerators. J Appl Microbiol. 2010;109(5):1566-78. DOI: https://doi.10.1111/j.1365-2672.2010.04783.x

Aitken D, Hay J, Kinnear FB, Kirkness CM, Lee WR, Seal DV. Amebic keratitis in a wearer of disposable contact lenses due to a mixed Vahlkampfia and Hartmannella infection. J. Ophthalmol.1996;103(3):485-94. DOI: https://doi.10.1016/s0161-6420(96)30667-2

Michel R, Schmid EN, Boker T, Hager DG, Muller KD, Hoffmann R, et al. Vannella sp. harboring microsporidia like organisms isolated from the contact lens and inflamed eye of a female keratitis patient. Parasitol Res. 2000;86(6):514-20. DOI: https://doi.10.1007/s004360050704

Grace E, Asbill S, Virga K. Naegleria fowleri: pathogenesis, diagnosis, and treatment options. Antimicrob. Agents Chemother. 2015;59(11):6677-81. DOI: https://doi.org/10.1128/AAC.01293-15

Park MK, Cho MK, Kang SA, Park HK, Kim DH, Yu HS. Acanthamoeba protease activity promotes allergic airway inflammation via protease-activated receptor 2. PloS one. 2014;9(3):e92726. DOI: https://doi.org/10.1371/journal.pone.0092726

Wagner Abuchaibe CM. Aislamiento y caracterización molecular de amebas de vida libre en Venezuela. Tesis doctoral. 2017. Disponible en: https://riull.ull.es/xmlui/handle/915/6829

Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh Navaei R, Shokri Shirvani J, et al. Systematic review with meta-analysis: The world wide prevalence of Helicobacter pylori infection. Aliment. Pharmacol. Ther. 2018;47:868-76. DOI: https://doi.org/10.1111/apt.14561

Fong I. Helicobacter pylori Infection: When Should It Be Treated? In Current Trends and Concerns in Infectious Diseases; Emerging Infectious Diseases of the 21st Century Ed.; Springer Nature: Gewerbesrasse, Switzerland, 2020; Chapter 4; pp. 81-102.

Mladenova I. Clinical Relevance of Helicobacter pylori Infection. J Clin Med. 2021;10(6):3473. DOI: https://doi.org/10.3390/jcm10163473

Willyard C. The drug-resistant bacteria that pose the greatest health threats. Nature. 2017;543:15. DOI: https://doi.org/10.1038/nature.2017.21550

Lee YC, Dore MP, Graham DY. Diagnosis and Treatment of Helicobacter pylori Infection. Annu. Rev. Med. 2022;73:183-95. DOI: https://doi.org/10.1146/annurev-med-042220-020814

Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology. 2017;153:420-9. DOI: https://doi.10.1053/jgastro.2017.04.022.

Llanes R, Feliciano O, Gutiérrez O, Gala A, Valdés L, Capó V, et al. Nuevos conocimientos sobre el diagnóstico y la resistencia antimicrobiana de Helicobacter pylori en Cuba. Rev. Ann. Acad. Cienc. Cuba. 2014 [acceso 17/02/2023];4:1-9. Disponible en: http://www.revistaccuba.cu ISSN:2304-0106.

Galbán E, Arús E, Periles U. Endoscopic findings and associated risk factors in primary health care settings in Havana, Cuba. Medicc Rev. 2012;14(1):30-7. DOI: https://doi.org/10.37757/MR2012V14.N1.7

Rodríguez A, Llanes R, Bello M, Langaney J, Verdasquera D, Argüez A, et al. Infección por Helicobacter pylori en pacientes atendidos en el Hospital General Docente Iván Portuondo. Panorama. Cuba y Salud. 2014 [acceso 17/02/2023];8:26-30. Disponible en: https://revpanorama.sld.cu/index.php/panorama/article/view/16

Gutiérrez B, Vidal T, Valmaña CE, Camou Juncas C, Santos A, Mégraud F, et al. Helicobacter pylori infection in Havana, Cuba. Prevalence and cagA status of the strains. Vaccimonitor. 2005 [acceso 17/02/2023];14:15-19. Disponible en: https://researchonline.nd.edu.au/med_article/151/

Anuario Estadístico de Salud. República de Cuba. 2020 [acceso 17/02/2023];1-192. Disponible en: https://temas.sld.cu/estadisticassalud/2021/0 8/11/anuario-estadistico-de-salud-2020/

Allen LA. Phagocytosis and persistence of Helicobacter pylori. Cell Microbiol. 2007;9(4):817-28. DOI: https://doi.org/10.1111/j.1462-5822.2007.00906.x

Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu JY, et al. The peopling of the Pacific from a bacterial perspective. Science. 2009;323:527-30. DOI: https://doi.10.1126/science.1166083

Beswick EJ, Bland DA, Suarez G, Barrera CA, Fan X, Reyes VE. Helicobacter pylori binds to CD74 on gastric epithelial cells and stimulates interleukin-8 production. Infect Immun. 2005;73:2736-43. DOI: https://doi.10.1128/IAI.73.5.2736-2743.2005

Percival SL, Thomas JG. Transmission of Helicobacter pylori and the role of water and biofilms. J Water Health. 2009;7(3):469-77. DOI: https://doi.10.2166/wh.2009.070

Aziz RK, Khalifa MM, Sharaf RR. Contaminated water as a source of Helicobacter pylori infection: A review. J Adv Res. 2015;6(4):539-47. DOI: https://doi.10.1016/j.jare.2013.07.007

Ashbolt NJ. Microbial contamination of drinking water and human health from community water systems. Curr Environ Health Rep. 2015;2(1):95-106. DOI: https://doi.10.1007/s40572-014-0037-5

Moreno-Mesonero L, Moreno Y, Alonso JL, Ferrús MA. Detection of viable Helicobacter pylori inside free-living amoebae in wastewater and drinking water samples from Eastern Spain. Environ Microbiol. 2017;19(10):4103-12. DOI: https://doi.org/10.1111/1462-2920.13856

Moreno Mesonero L, Moreno Trigos MY, Alonso Molina JL, Ferrús Pérez MA. DVC-FISH and PMA-qPCR techniques to assess the survival of Helicobacter pylori inside Acanthamoeba castellanii. Res. Microbiol. 2016;167(1):29-34. DOI: https://doi.org/10.1016/j.resmic.2015.08.002

Jeon KW, Lorch IJ. Unusual intra-cellular bacterial infection in large, free living amoebae. Exp. Cell Res. 1967;48(1):236-40. DOI: https://doi.org/10.1016/0014-4827(67)90313-8

Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev. 2004;17:413-33. DOI: https://doi.org/10.1128/CMR.17.2.413-433.2004

Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RH. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol Res. 2016;193:30-8. DOI: https://doi.org/10.1016/j.micres.2016.08.001

Balczun C, Scheid PL. Free-Living Amoebae as Hosts for and Vectors of Intracellular Microorganisms with Public Health Significance. Viruses. 2017;9. DOI: https://doi.org/10.3390/v9040065

Kofman A, Guarner J. Infections Caused by Free-Living Amoebae. J. Clin Microbiol. 2022;60(1):e0022821. DOI: https://doi.org/10.1128/JCM.00228-21

Potgieter N, van der Loo C, Barnard TG. Co-Existence of Free-Living Amoebae and Potential Human Pathogenic Bacteria Isolated from Rural Household Water Storage Containers. Biology. 2021;10(12):1228. DOI: https://doi.org/10.3390/biology10121228

Moreno Mesonero L, Hortelano I, Moreno Y, Ferrús MA. Evidence of viable Helicobacter pylori and other bacteria of public health interest associated with free-living amoebae in lettuce samples by next generation sequencing and other molecular techniques. Int J Food Microbiol. 2020;3318:108477. DOI: https://doi.org/10.1016/j.ifoodmicro.2019.108477

Cosson P, Lima WC. Intracellular killing of bacteria: is Dictyostelium a model macrophage or an alien? Cell Microbiol. 2014;16(6):816-23. DOI: https://doi.org/10.1111/cmi.12291

Delafont V, Brouke A, Bouchon D, Moulin L, Héchard Y. Microbiome of free-living amoebae isolated from drinking water. Water Res. 2013;47(19):6958-65. DOI: https://doi.10.1016/jwaters.2013.07.047

Moreno Mesonero L, Ferrús MA, Moreno Y. Determination of the bacterial microbiome of free-living amoebae isolated from wastewater by 16S rRNA amplicon-based sequencing. Environ Res. 2020;190:109987. DOI: https://doi.10.1016/j.envres.2020.109987

Lovieno A, Ledee DR, Miller D, Alfonso EC. Detection of bacterial endosymbionts in clinical Acanthamoeba isolates. Ophthalmology. 2010;117:445-52. DOI: https://doi.org/10.1016/j.ophtha.2009.08.033

Shi Y, Queller DC, Tian Y, Zhang S, Yan Q, HeZ Wu, et al. The ecology and evolution of amoeba-bacterium interactions. Appl Environ Microbiol. 2021;87:e01866-20. DOI: https://doi.org/10.1128/AEM.01866-20

Pernthaler J. Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol. 2005;3:537-46. DOI: https://doi.org/10.1038/nrmicro1180

Cateau E, Delafont V, Hechard Y, Rodier MH. Free-living amoebae: what part do they play in healthcare-associated infections? J Hosp Infect. 2014;87:131-40. DOI: https://doi.org/10.1016/j.jhin.2014.05.001

Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y. Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol. 2005;71:20-8. DOI: https://doi.org/10.1128/AEM.71.1.20-28.2005

Mungroo MR, Siddiqui R, Khan NA. War of the microbial world: Acanthamoeba spp. interactions with microorganisms. Folia Microbiol. 2021;66:689-99. DOI: https://doi.org/10.1007/s12223-021-00889-7

López García P, Eme L, Moreira D. Symbiosis in eukaryotic evolution. J Theor Biol. 2017;434:20-33. DOI: https://doi.10.1016/j.jtbi.2017.02.031

Thewes S, Soldati T, Eichinger L. Amoebae as host models to study the interaction with pathogens. Front Cell Infect Microbiol. 2019;9:47. DOI: https://doi.org/10.3389/fcimb.2019.00047

Allen LA. Modulating phagocyte activation: the pros and cons of Helicobacter pylori virulence factors. J Exp Med. 2000;191(9):1451-4. DOI: https://doi.org/10.1084/jem.191.9.1451

Mehlhorn H, Klimpel S. Parasite and Disease Spread by Major Rivers on Earth. Parasitol Res. 2019. https://doi.org/10.1007/978-3-030-29061-0

Allen LA, Schlesinger LS, Kang B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J Exp Med. 2000;191(1):115-28. DOI: https://doi.org/10.1084/jem.191.1.115

Allen LA, Allgood JA. Atypical protein kinase C-f is essential for delayed phagocytosis of Helicobacter pylori. Curr Biol. 2002;12(20):1762-6. DOI: https://doi.org/10.1016/s0960-9822(02)01216-2

Zheng PY, Jones NL. Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein, Cell. Microbiol. 2003;5(1):25-40. DOI: https://doi.org/10.1046/j.1462-5822.2003.00250.x

Tegtmeyer N, Wessler S, Necchi V, Rohde M, Harrer A, Rau TT, et al. Helicobacter pylori employs a unique basolateral type IV secretion mechanism for CagA delivery. Cell Host Microbe. 2017;22:552-60.e5. DOI: https://doi.org/10.1016/j.chom.2017.09.005

Smith CD, Ashbolt NJ. The fate of Helicobacter pylori phagocytised by Acanthamoeba polyphaga demonstrated by fluorescent in situ hybridization and quantitative polymerization chain reaction tests. Curr Microbiol. 2012;65(6):805-12. DOI: https://doi.org/10.1007/s00284-012-0232-2

Winiecka Krusnell J, Wreiber K, Euler A, Engstrand L, Linder E. Free living amoebae promote growth and survival of Helicobacter pylori. Scand J Infect Dis. 2002;34(4):253-6. DOI: https://doi.org/10.1080/00365540110080052

Chatton E, Lalung Bonnaire P. Amibe limax (Vahlkampfia n. gen.) dans l’intestin humaine. Son importance pour l’interpretation des amibes de culture. Bull Soc path exot. 1912 [acceso 17/02/2023];5:135-43. DOI: https://www.algaebase.org/search/genus/detail/?genus_id=50534

Dey R, Rieger A, Banting G, Ashbolt N J. Role of amoebae for survival and recovery of ‘non-culturable’ Helicobacter pylori cells in aquatic environments. FEMS Microbiol. Ecol. 2020;96(10):182. DOI: https://doi.org/10.1093/femsec/fiaa182

Giono Cerezo S, Santos Preciado JI, Morfín Otero MR, Torres López FJ, Alcántar Curiel MD. Resistencia antimicrobiana. Importancia y esfuerzos por contenerla. Gac Med Mex. 2020;156:172-80. DOI: https://doi.10.24875/GMM.20005624

O’Neill CB. The review on antimicrobial resistence. Suiza: World Intellectual Property Organization; 2016.

Suclupe Campos DO, Aguilar Gamboa FR. Persistencia bacteriana: un fenotipo celular de importancia clínica en infecciones crónicas y recurrentes. Horiz Med (Lima). 2020;20(1):77-87. DOI: http://dx.doi.org/10.24265/horizmed.2020.v20n1.11

Van Den Bergh B, Fauvart M, Michiels J. Formation, physiology, ecology, evolution and clinical importance of bacterial persisters. FEMS Microbiol Rev. 2017;41(3):219-51. DOI: https://doi.org/10.1093/femsre/fux001

Kim JS, Wood TK. Tolerant, growing cells from nutrient shifts are not persister cells. MBio. 2017;8(2):e00354-17. DOI: https://doi.org/10.1128/mBio.00354-17

Fisher RA, Gollan B, Helaine S. Persistent bacterial infections and persister cells. Nat Rev Microbiol. 2017;15(8):453-64. DOI: https://doi.org/10.1038/nrmicro.2017.42

Kussell E, Kishony R, Balaban NQ, Leibler S. Bacterial persistence: a model of survival in changing environments. Genetics. 2005 [acceso 17/02/2023];169(4):1807-14. Disponible en: https://10.1534/genetics.104.035352

Orman MA, Brynildsen MP. Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother. 2013;57(7):3230-9. DOI: https://doi.org/10.1128/AAC.00243-13

Trastoy R, Manso T, Fernández García L, Blasco L, Ambroa A, Pérez del Molino ML, et al. Mechanisms of bacterial tolerance and persistence in the gastrointestinal and respiratory environments. Clin Microbiol Rev. 2018;31(4):e00023-18. DOI: https://doi.org/10.1128/CMR.00023-18

Torrey HL, Keren I, Via LE, Lee JS, Lewis K. High persister mutants in Mycobacterium tuberculosis. PLoS One. 2016;11(5):1-28. DOI: https://doi.org/10.1371/journal.pone.0155127

Helaine S, Kugelberg E. Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol. 2014;22(7):417-24. DOI: https://doi.10.1016/j.tim.2014.03.008

Pu Y, Zhao Z, Li Y, Zou J, Ma Q, Zhao Y, et al. Enhanced efflux activity facilitates drug tolerance in dormant bacterial cells. Mol Cell. 2016;62(2):284-94. DOI: https://doi.org/10.1016/j.molcel.2016.03.035

Patricelli P, Ramirez E, Presa RC, Dell’Elce A, Formentini E. Efecto de la persistencia bacteriana sobre la eficacia de la enrofloxacina y ciprofloxacina frente a una cepa de Escherichia coli. FAVE- Ciencias Vet. 2017;16(2017):30-8. DOI: https://doi.org/10.14409/favecv.v16i1.6648

Wood TK, Knabel SJ, Kwan BW. Bacterial persister cell formation and dormancy. Appl Environ Microbiol. 2013;79(23):7116-21. DOI: https://doi.org/10.1128/AEM.02636-13

Van den Bergh B, Michiels JE, Wenseleers T, Windels EM, Boer PV, Kestemont D, et al. Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence. Nat Microbiol. 2016;1(5):1-7. DOI: https://doi.org/10.1038/nmicrobiol.2016.20

Zhang Y. Persisters, persistent infections and the Yin-Yang model. Emerg Microbes Infect. 2014;3(1):e3. DOI: https://doi.org/10.1038/emi.2014.3

Wang T, El Meouche I, Dunlop MJ. Bacterial persistence induced by salicylate via reactive oxygen species. Sci Rep. 2017;7(43839):1-7. DOI: https://doi.org/10.1038/srep43839

Xu T, Wang XY, Cui P, Zhang YM, Zhang WH, Zhang Y. The Agr quorum sensing system represses persister formation through regulation of phenol soluble modulins in Staphylococcus aureus. Front Microbiol. 2017;8(2189):1-13. DOI: https://doi.org/10.3389/fmicb.2017.02189

Zhang Y, Yew WW, Barer MR. Targeting persisters for tuberculosis control. Antimicrob Agents Chemother. 2012;56(5):2223-30. DOI: https://doi.org/10.1128/AAC.06288-11

Loret JF, Greub G. Free-living amoebae: biological by-passes in water treatment. Int J of Hyg Environ Health. 2010;213(3):167-75. DOI: https://doi.org/10.1016/j.ijheh.2010.03.004

Published

2024-12-27

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1.
Duquesne Alderete A, Falcón Márquez R, Jerez Puebla LE, Ginorio Gavito D, Sanler Wong E, Llanes Caballero R, et al. Free living Amoebae: "Trojan horses" or vectors in the dissemination of Helicobacter pylori in aquatic environments?. Rev Cuba Med Tropical [Internet]. 2024 Dec. 27 [cited 2025 Feb. 22];76. Available from: https://revmedtropical.sld.cu/index.php/medtropical/article/view/1098

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