Abstract
Free-living amoeba (FLA) group includes the potentially pathogenic genera Acanthamoeba, Naegleria, Balamuthia, Sappinia, and Vermamoeba, causative agents of human infections (encephalitis, keratitis, and disseminated diseases). In Brazil, the first report on pathogenic FLA was published in the 70s and showed meningoencephalitis caused by Naegleria spp. FLA studies are emerging, but no literature review is available to investigate this trend in Brazil critically. Thus, the present work aims to integrate and discuss these data. Scopus, PubMed, and Web of Science were searched, retrieving studies from 1974 to 2020. The screening process resulted in 178 papers, which were clustered into core and auxiliary classes and sorted into five categories: wet-bench studies, dry-bench studies, clinical reports, environmental identifications, and literature reviews. The papers dating from the last ten years account for 75% (134/178) of the total publications, indicating the FLA topic has gained Brazilian interest. Moreover, 81% (144/178) address Acanthamoeba-related matter, revealing this genus as the most prevalent in all categories. Brazil’s Southeast, South, and Midwest geographic regions accounted for 96% (171/178) of the publications studied in the present work. To the best of our knowledge, this review is the pioneer in summarising the FLA research history in Brazil.
Key words:
free-living amoeba; Brazil; literature review; Acanthamoeba; Naegleria; Balamuthia
Free-living amoeba (FLA) is a protozoan group including Excavata and Amoebozoa lineages capable of living free in the environment and alternatively proliferating within a host, therefore named amphizoic amoebas.11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.Acanthamoeba spp, Naegleria fowleri, Sappinia pedata, Balamuthia mandrillaris, and more recently Vermamoeba vermiformis, include pathogenic amoebae causative agents of human infections.11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.,22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307.,33. Schuster FL, Dunnebacke TH, Booton GC, Yagi S, Kohlmeier CK, Glaser C, et al. Environmental isolation of Balamuthia mandrillaris associated with a case of amebic encephalitis. J Clin Microbiol. 2003; 41(7): 3175-80.,44. Scheid PL. Vermamoeba vermiformis - a free-living amoeba with public health and environmental health significance. Open Parasitol J. 2019; 7(1): 40-7.
FLAs have been ubiquitously isolated around the globe from both natural and artificial environments.55. Samba-Louaka A, Delafont V, Rodier M-H, Cateau E, Héchard Y. Free-living amoebae and squatters in the wild: ecological and molecular features. FEMS Microbiol Rev. 2019; 43(4): 415-34.,66. Marciano-Cabral F. Free-living amoebae as agents of human infection. J Infect Dis. 2009; 199(8): 1104-6. These organisms share common aspects in their life cycle as the existence of a trophozoite stage able to feed, divide, and move by pseudopodium projection and constrictions of the cytoplasm. Another stage is the cyst, which can withstand adverse conditions as food scarcity, unbalance in pH, salt concentration, and temperature.66. Marciano-Cabral F. Free-living amoebae as agents of human infection. J Infect Dis. 2009; 199(8): 1104-6.Naegleria spp. possess an additional flagellate transient form that can escape from harsh environmental conditions.11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.,77. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell. 2010; 140(5): 631-42.
FLAs have attracted the interest of human health agencies due to their involvement as opportunistic and non-opportunistic infections that affect the central nervous system (CNS), the cornea, and other organs. CNS infections can be classified either as Primary Amoebic Meningoencephalitis (PAM), an acute infection, caused by N. fowleri88. Piñero JE, Chávez-Munguía B, Omaña-molina M, Lorenzo-morales J. Naegleria fowleri. Trends Parasitol. 2019; 35(10): 848-9. or Granulomatous Amoebic Encephalitis (GAE), a subacute to chronic illness caused by Acanthamoeba spp. and B. mandrillaris.22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307.,99. Lee JY, Yu IK, Kim SM, Kim JH, Kim HY. Fulminant disseminating fatal granulomatous amebic encephalitis: the first case report in an immunocompetent patient in South Korea. Yonsei Med J. 2021; 62(6): 563-7.Acanthamoeba spp. and B. mandrillaris have also been identified in skin lesions and disseminated infections that, similarly to GAE, affect predominantly debilitated or immunocompromised patients.1010. Duggal SD, Rongpharpi SR, Duggal AK, Kumar A, Biswal I. Role of Acanthamoeba in granulomatous encephalitis: a review. J Infect Dis Immune Ther. 2017; 1(1): 2. FLAs can also affect the cornea, causing a progressive, sight-threatening infection termed amoebic or Acanthamoeba keratitis (AK), which has Acanthamoeba spp as the main etiological agent.22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307.,1111. Soleimani M, Latifi A, Momenaei B, Tayebi F, Mohammadi SS, Ghahvehchian H. Management of refractory Acanthamoeba keratitis, two cases. Parasitol Res. 2021; 120(3): 1121-4.,1212. Carnt NA, Subedi D, Connor S, Kilvington S. The relationship between environmental sources and the susceptibility of Acanthamoeba keratitis in the United Kingdom. PLoS One. 2020; 15(3): 1-11.S. pedata accounts for a single case of encephalitis in humans,1313. Qvarnstrom Y, Da Silva AJ, Schuster FL, Gelman BB, Visvesvara GS. Molecular confirmation of Sappinia pedata as a causative agent of amoebic encephalitis. J Infect Dis. 2009; 199(8): 1139-42.,1414. Gelman BB, Popov V, Chaljub G, Nader R, Rauf SJ, Nauta HW, et al. Neuropathological and ultrastructural features of amebic encephalitis caused by Sappinia diploidea. J Neuropathol Exp Neurol. 2003; 62(10): 990-8. while V. vermiformis has been mainly reported in keratitis cases, most of them in co-infection with Acanthamoeba.44. Scheid PL. Vermamoeba vermiformis - a free-living amoeba with public health and environmental health significance. Open Parasitol J. 2019; 7(1): 40-7. Despite the widespread recognition of FLAs as pathogens, infections still result in several deaths or events of visual impairment. These outcomes are mainly associated with the lack of fast and reliable diagnostic methods and effective treatments.1515. Gharpure R, Bliton J, Goodman A, Ali IKM, Yoder J, Cope JR. Epidemiology and clinical characteristics of primary amebic meningoencephalitis caused by Naegleria fowleri: a global review. Clin Infect Dis. 2020; 73(1): e19-27.,1616. Król-Turminska K, Olender A. Human infections caused by free-living amoebae. Ann Agric Environ Med. 2017; 24(2): 254-60. Besides their importance as human pathogens, FLAs have been investigated in relation to their ecological interaction with the aquatic and soil microbial community. Previous analyses have shown FLA harboring intracellular organisms from the ambient, proposing the amoeba as a vehicle to bacteria, fungi, protozoan, and viruses, the so-called amoeba resistant microorganisms (ARM).1717. Scheid P. Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res. 2014; 113(7): 2407-14.,1818. Rayamajhee B, Subedi D, Peguda HK, Willcox MD, Henriquez FL, Carnt N. A systematic review of intracellular microorganisms within Acanthamoeba to understand potential impact for infection. Pathogens. 2021; 10(2): 1-26. Through lysing cells, ARMs can disseminate in the environment or a host. Therefore, FLA is referred to as Trojan horses for the microbial community,1717. Scheid P. Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res. 2014; 113(7): 2407-14.,1919. Gonçalves DS, Ferreira MS, Gomes KX, Rodríguez-de-La-Noval C, Liedke SC, Costa GCV, et al. Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose - binding proteins. Cell Microbiol. 2019; 21(10): e13066. emphasising the significance of investigating its ecological importance throughout the world.1818. Rayamajhee B, Subedi D, Peguda HK, Willcox MD, Henriquez FL, Carnt N. A systematic review of intracellular microorganisms within Acanthamoeba to understand potential impact for infection. Pathogens. 2021; 10(2): 1-26.
Water-related outbreaks caused by protozoans in Latin America were revised in a survey that pointed out the Brazilian prominence accounting for 30% of the reports (20/66). Comparing the causative agents of these outbreaks, Acanthamoeba and Cyclospora shared the fourth position in the ranking.2020. Rosado-García FM, Guerrero-Flórez M, Karanis G, Hinojosa MDC, Karanis P. Water-borne protozoa parasites: the Latin American perspective. Int J Hyg Environ Health. 2017; 220(5): 783-98. Environmental isolation of FLA in the Brazilian territory relies on recent reports that call attention to the country´s potential on harboring FLAs. Efforts to address gaps in FLA knowledge include developing more reliable diagnosis,2121. Costa AO, Furst C, Rocha LO, Cirelli C, Cardoso CN, Neiva FS, et al. Molecular diagnosis of Acanthamoeba keratitis: evaluation in rat model and application in suspected human cases. Parasitol Res. 2017; 116(4): 1339-44.,2222. Barros JN, Mascaro VLD, Lowen M, Martins MC, Foronda A. Diagnosis of Acanthamoeba corneal infection by impression cytology: case report. Arq Bras Oftal. 2007; 70(2): 343-6. investigation of factors related to pathogenicity,2323. Machado ATP, Silva M, Iulek J. Expression, purification, enzymatic characterization and crystallization of glyceraldehyde-3-phosphate dehydrogenase from Naegleria gruberi, the first one from phylum Percolozoa. Protein Expr Purif. 2016; 127: 125-30.,2424. da Rocha-Azevedo B, Costa e Silva-Filho F. Biological characterization of a clinical and an environmental isolate of Acanthamoeba polyphaga: analysis of relevant parameters to decode pathogenicity. Arch Mircobiol. 2007; 188(5): 441-9. and development of therapeutic approaches.2525. Carrijo-Carvalho LC, Sant'ana VP, Foronda AS, de Freitas D, Ramos F, Carvalho DS. Therapeutic agents and biocides for ocular infections by free-living amoebae of Acanthamoeba genus. Surv Ophthalmol. 2016; 62(2): 203-18.,2626. Zorzi GK, Schuh RS, Maschio VJ, Brazil NT, Rott MB, Teixeira HF. Box Behnken design of siRNA-loaded liposomes for the treatment of a murine model of ocular keratitis caused by Acanthamoeba. Colloids Surfaces B Biointerfaces. 2019; 173: 725-32. Those are just a portion of the literature produced in Brazil on the FLA field, and controversially, there is no literature review devoted to summing up and debating these data critically. Thus, the following central question guided the present literature review: What is the Brazilian research contribution to the free-living amoeba literature until 2020?
Identification, systematic documentation, and screening of the data - The data analysis followed the general workflow as suggested by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline.2727. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. BMJ. 2009; 339: b2535. Fourteen keywords were defined [Supplementary data (Table II)] and used as queries in the databases Scopus, Web of Science, and PubMed/Medline, all accessed through the CAPES News Portal (www.periodicos.capes.gov.br) between March 22 to 24, 2021. We have defined 13 keywords (#1 to #13) and a geographical region of interest (#14) to select topics of interest [Supplementary data (Table II)].
The search entry varied according to the database, as described in the Supplementary data (Table II), providing an initial dataset composed of 1512 articles (Fig. 1). We managed the literature dataset using Mendeley version 1.17.102828. Lo Russo G, Spolveri F, Ciancio F, Mori A. Mendeley: an easy way to manage, share, and synchronize papers and citations. Plast Reconstr Surg. 2013; 131(6): 946-7. and State of the Art through Systematic Review (StArt) version 3.4 beta.2929. Hernandes E, Zamboni A, Fabbri S. Using GQM and TAM to evaluate StArt-a tool that supports Systematic Review. Clei Electron J. 2012; 15(1): 13. The StArt tool allowed to identify and subtract duplicate references, corresponding to literature overlaps intra-database and inter-databases. We designed inclusion and exclusion criteria [Supplementary data (Table II)] to accept and reject papers in the first round of data examination. The keywords listed in Supplementary data (Table II) were contrasted against the title, affiliation, and abstract sections of the 475 records selected for screening. We have withdrawn 277 of them (Fig. 1 - Screening step). Next, we examined the main text of the remaining paper according to Supplementary data (Table II - III) criteria. Study limitations included: records available in the gray literature (e.g., google scholar) are absent; the period cutoff excluding the literature made public in 2021; dissertations, letters, and protocols are also absent in this review. Following literature recommendations concerned with diminishing study bias, no language restrictions were applied.3030. Morrison A, Polisena J, Husereau D, Moulton K, Clark M, Fiander M, et al. The effect of english-language restriction on systematic review-based meta-analyses: a systematic review of empirical studies. Int J Technol Assess Health Care. 2012; 28(2): 138-44. The screening and application of inclusion/exclusion criteria resulted in 178 articles gathering the Brazilian research contribution to the free-living amoeba literature (Fig. 1).
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow chart describing the protocol employed in the systematic review and the number of citations (n) retrieved in each step.
Data analysis considered (1) the geographic scope and (2) research domains of the Brazilian literature on FLA topics. A primary analysis exposed a need for two clustering levels concerning the research domain. Based on the central research question addressed in each study we divided the first level into core and auxiliary classes. We settled as core the investigations with FLAs as the major topic addressed in all sections of the paper. We sorted some studies including FLAs in any part of the main text, but as a complement to other topics, as auxiliary. The second level of clustering consisted of five research domains in which both core/auxiliary papers were categorised: dry-bench, wet-bench, clinical, environmental and review.
Publications categorised as wet-bench included in vitro or in vivo procedures conducted with isolates or cultures without a primary intention of prospecting the environment (environmental) or describing cases (clinical). Dry-bench grouped the bioinformatics-based research whose experimental approach is in silico. And review account to literature reviews. We assessed the main text of each paper, and we added the additional two layers of clustering to the data extraction forms. Two researchers have conducted the eligibility checking and data extraction processes to reinforce decisions taken during both steps. We have solved in consensus any uncertainty related to studies inclusion, exclusion, and clustering.
The first and second levels of clustering were displayed in the number or percentage of papers and sorted according to date of publication, federative unit, and FLA species. Occasionally, papers encompassing multiple federative units’ affiliation were scored numerous times and obtained percentages exceeding 100%. However, regardless of the number of authors from the same federative unit, we gave the “1” score.
FLA research in Brazil had an expansion in the last ten years, and the Southern, South, and Midwest regions lead the contribution - The FLA topic is an emerging field in Brazil, in which 134 papers from a total of 178 papers (~ 75%) were published in the last ten years of the 1974 to 2020 period (Fig. 2A). The remaining 44 papers (~ 25%) are dated in a time window of 37 years from this period. The data indicate that after 2008, FLA knowledge increased progressively.
Papers classified as the core class accounted for 120 articles predominantly originating from Brazilian scientific institutions in the Southeast (SP, MG, ES, RJ), South (SC, PR, RS), and the Midwest (GO, DF, MS) regions, named here with the acronym SSM (Fig. 2B). Although the Southeast region leads the ranking, with ~ 64% of the total reports, the state of Rio Grande do Sul (RS) represents the federative unit with more contributions. The map has also shown studies from the North (PA) and Northeast (PB, and SE) regions with lower frequencies. Overall, it depicts half of the country (13 out of 26 federative unities) contributing on FLA topics sorted as core (Fig. 2B).
progression and distribution of free-living amoeba (FLA) studies in Brazil. A - Bar graph with the number of core and auxiliary classes of publications per year representing the first level of clustering. Geographical distribution of core (B) and auxiliary (C) classes of papers according to federative units declared in the affiliations. A single paper with multiple federative unities affiliation was scored once per federative unit so that the total percentage resulted higher than 100% in both B and C panels.
A total of 58 articles were classified in the auxiliary class (Fig. 2C). Most of them were originated in universities in the Southeast region, resembling the tendency perceived for the core class of papers (Fig. 2B). Altogether, FLA studies in Brazil have a predominant origin in centres from the SSM region (96% - 171/178). Factors explaining this regional concentration are the heterogeneous funding distributions3131. McManus C, Baeta Neves AA. Funding research in Brazil. Scientometrics. 2021; 126(1): 801-23. and spatial distributions of universities through the country.3232. Chiarini T, Oliveira VP, Neto FC. Spatial distribution of scientific activities: an exploratory analysis of Brazil, 2000-10. Sci Public Policy. 2014; 41(5): 625-40. Regardless of this trend, the overall landscape of FLA research in Brazil has highlighted half of the federative unities being committed to expanding the knowledge on FLA, therefore reinforcing the country’s relevance as a thriving contributor to the field.
Wet-bench research predominates in Brazilian FLA literature - Five research domains composed the second level of clustering in the core and auxiliary classes of papers, as shown in Fig. 3. The research domain classified as wet-bench represents 58 out of 120 core class papers (Fig. 3A), mainly with studies addressing the biochemical characterisation of FLA strains isolated by the authors and commercial lineages (e.g., ATCC strains). Regarding the territorial distribution, wet-bench investigations reproduced the prevalence of the SSM region, in which Rio Grande do Sul (RS) and São Paulo (SP) occupied the first and second positions in the ranking with 40.7% and 22% of the published papers, respectively (Fig. 3B).
discriminative free-living amoeba (FLA) literature that has FLAs as the central topic (core) in Brazil according to five categories: clinical, environmental, review, dry, and wet-bench. (A) Stacked bar graph comparing the number of papers published per year per category. (B) Territorial scope depicting the percentage of papers per federative unit.
The higher occurrence of clinical assigned reports is on papers describing keratitis (18/29), followed by encephalitis (7/29). Fewer reporting cases of disseminated diseases (1/29), skin infections (1/29), besides the presence of FLA in urine and feces (2/29), were reported. Summarising the Brazilian publications on FLA distribution, the environmental category identified 25 out of 120 papers in the core class.
The remaining 58 papers sorted in the auxiliary class included 60% (n = 34) of wet-bench research [Supplementary data (Figure)], reinforcing the predominance of this research domain in FLA national studies. Review, clinical and environmental tags account for 13, 6, and 5 papers, respectively, out of the 58 in this class, while no study was classified as dry-bench. Once again, the Southeast region leads the number of studies, covering topics ranging from waterborne protozoa to more specific issues as virus replication.
Acanthamoeba leads the ranking of FLA studies in Brazil - The Acanthamoeba genus was predominant in 81% (144/178) of papers [Supplementary data (Table I)], a tendency depicted in clinical, environmental, wet-bench and review categories of both the core and auxiliary classes (Fig. 4). For the dry-bench category, both Acanthamoeba and Naegleria shared the same number of publications (one paper each) in the core class.
the diversity of the free-living amoeba (FLA) genus per category and class of references. From intense to pale shades, the color spectrum, indicates the prevalence of FLA genera per number of papers. A, N, V, B, and S are Acanthamoeba, Naegleria, Vermamoeba, Balamuthia, and Sappinia, respectively. M: multiple topics (two or more FLA genera included in the main scope).
To a lesser extent, some papers addressed two FLA genera in a single research, as revealed by combinations of Vermamoeba and Acanthamoeba in the clinical category, as well as Naegleria and Acanthamoeba in the environmental category, both within the core class (Fig. 4). Multiple emphases occurred in papers discussing more than two FLA genera in a single paper, for example, Naegleria, Acanthamoeba, and Balamuthia identified in clinical publications of the auxiliary class (Fig. 4). Regardless of the single or multiple FLA genus in the same article, those classified in the environmental category accounted for Acanthamoeba, Vermamoeba, Balamuthia, and Naegleria reports in the Brazilian territory (Fig. 4). Sappinia was mentioned only in two papers classified as reviews in the auxiliary class.3333. Sullivan KE, Bassiri H, Bousfiha AA, Costa-Carvalho BT, Freeman AF, Hagin D, et al. Emerging infections and pertinent infections related to travel for patients with primary immunodeficiencies. J Clin Immunol. 2017; 37: 650-92.,3434. Chimelli L. A morphological approach to the diagnosis of protozoal infections of the central nervous system. Patholog Res Int. 2011; 2011: 29085. The predominance of Acanthamoeba-related investigations is an expected finding considering that this species is the most frequent FLA in the environment22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307. and presents higher viability than Naegleria in dust samples.3535. Carlesso AM, Simonetti AB, Artuso GL, Rott MB. Isolation and identification of potentially pathogenic free-living amoebae in samples from environments in a public hospital in the City of Porto Alegre, Rio Grande do Sul. Rev Soc Bras Med Trop. 2007; 40(3): 316-20. In addition, while other pathogenic species of FLAs are involved in rare brain infections, Acanthamoeba can cause both cerebral and corneal AK infections, the latter showing an increasing number of cases in recent years.22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307.
Diversity of approaches in wet-bench references - The wet-bench category included approaches that varied from morphological characterisation to the development of diagnostic and therapeutic tools. Biochemical assays aiming to isolate and characterise nuclear and mitochondrial DNA of Acanthamoeba were the pioneer reports on FLA in Brazil, being published in 1974 and 1975.3636. Marzzoco A, Colli W. Characterization of the genome of the small free-living amoeba Acanthamoeba castellanii. Biochim Biophys Acta. 1975; 395(4): 525-34.,3737. Marzzoco A, Colli W. Isolation of nuclei and characterization of nuclear DNA of Acanthamoeba castellanii. Biochim Biophys Acta. 1974; 374(3): 292-303. A long gap of reports on wet-bench research occurred until 1992 when a study reported an isoenzymatic and antigenic assessment towards classifying Acanthamoeba isolates in groups I, II and III.3838. Moura H, Wallace S, Visvesvara GS. Acanthamoeba healyi N. sp. and the isoenzyme and immunoblot profiles of Acanthamoeba spp., groups 1 and 3. J Protozool. 1992; 39(5): 573-83. Further, the randomly amplified polymorphic DNA (RAPD) technique was indicated as a suitable strategy to rapid genotyping new isolates.3939. Alves JM, Gusmão CX, Teixeira MMG, Freitas D, Foronda AS, Affonso HT. Random amplified polymorphic DNA profiles as a tool for the characterization of Brazilian keratitis isolates of the genus Acanthamoeba. Braz J Med Biol Res. 2000; 33(1): 19-26. More recent studies adopted high throughput sequencing with bioinformatics pipelines to decipher nuclear and mitochondrial DNA of Acanthamoeba and Vermamoeba strains.4040. Fuciková K, Lahr DJG. Uncovering cryptic diversity in two amoebozoan species using complete mitochondrial genome sequences. J Eukaryot Microbiol. 2016; 63(1): 112-22. Proteomics and metabolomics analysis are also represented by studies devoted to characterising Acanthamoeba, which provided informative molecular elements with the potential to be investigated as drug targets or as epitopes for antibodies in diagnostic tools.4141. Caumo KS, Monteiro KM, Ott TR, Maschio VJ, Wagner G, Ferreira HB, et al. Proteomic profiling of the infective trophozoite stage of Acanthamoeba polyphaga. Acta Trop. 2014; 140: 166-72.,4242. Maschio JV, Virgínio VG, Ferreira HB, Rott MB. Comparative proteomic analysis of soluble and surface-enriched proteins from Acanthamoeba castellanii trophozoites. Mol Biochem Parasitol. 2018; 225: 47-53.,4343. Alves DSMM, Alves LM, da Costa TL, de Castro AM, Vinaud MC. Anaerobic metabolism in T4 Acanthamoeba genotype. Curr Microbiol. 2017; 74(6): 685-90. Additional targets for detection purposes are cation:proton antiporter protein family (CPA) and a calreticulin extracellular domain.4444. Sánchez AGC, Virginio VG, Maschio VJ, Ferreira HB, Rott MB. Evaluation of the immunodiagnostic potential of a recombinant surface protein domain from Acanthamoeba castellanii. Parasitology. 2021; 143(12): 1656-64.,4545. Weber-Lima MM, Prado-Costa B, Becker-Finco A, Costa AO, Billilad P, Furst C, et al. Acanthamoeba spp. monoclonal antibody against a CPA2 transporter : a promising molecular tool for acanthamoebiasis diagnosis and encystment study. Parasitology. 2020; 147(14): 1678-88. The former was identified through the monoclonal antibody mAb3, which positively reacted with several Acanthamoeba pathogenic strains.4444. Sánchez AGC, Virginio VG, Maschio VJ, Ferreira HB, Rott MB. Evaluation of the immunodiagnostic potential of a recombinant surface protein domain from Acanthamoeba castellanii. Parasitology. 2021; 143(12): 1656-64. The latter study described the use of a recombinant polypeptide, produced from a predicted sequence of A. castellanii calreticulin, which was recognised by sera from rats with GAE in the ELISA test.4444. Sánchez AGC, Virginio VG, Maschio VJ, Ferreira HB, Rott MB. Evaluation of the immunodiagnostic potential of a recombinant surface protein domain from Acanthamoeba castellanii. Parasitology. 2021; 143(12): 1656-64. These contributions meet the urgent demand for faster detection techniques since late diagnosis is a factor contributing for the high mortality or visual sequelae of FLA infections.11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.,22. Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003; 16(2): 273-307.,66. Marciano-Cabral F. Free-living amoebae as agents of human infection. J Infect Dis. 2009; 199(8): 1104-6.,88. Piñero JE, Chávez-Munguía B, Omaña-molina M, Lorenzo-morales J. Naegleria fowleri. Trends Parasitol. 2019; 35(10): 848-9.Other Acanthamoeba wet-bench research is concerned with culture manipulation, as the proposal of strategies for prolonging culture storage4646. Pens CJ, Rott MB. Acanthamoeba spp. cysts storage in filter paper. Parasitol Res. 2008; 103(5): 1229-30. and removing contaminants from cultures.4747. Alves DSMM, Gurgel-Gonçalves R, Albuquerque P, Cuba-Cuba CA, Muniz-Junqueira MI, Kuckelhaus SAS. A method for microbial decontamination of Acanthamoeba cultures using the peritoneal cavity of mice. Asian Pac J Trop Biomed. 2015; 5(10): 796-800. Additional approaches included investigating the role of phosphate transporters in metabolism,4848. Carvalho-Kelly LF, Pralon CF, Rocco-Machado N, Nascimento MT, Carvalho-de-Araújo AD, Meyer-Fernandes JR. Acanthamoeba castellanii phosphate transporter (AcPHS) is important to maintain inorganic phosphate influx and is related to trophozoite metabolic processes. J Bioenerg Biomembr. 2020; 52(2): 93-102. description of ultrastructural cyst wall morphology,4949. Lemgruber L, Lupetti P, De Souza W, Vommaro RC, Da Rocha-Azevedo B. The fine structure of the Acanthamoeba polyphaga cyst wall. FEMS Microbiol Lett. 2010; 305(2): 170-6. and genomic features.5050. Corsaro D, Köhsler M, Venditti D, Rott MB, Walochnik J. Recovery of an Acanthamoeba strain with two group I introns in the nuclear 18S rRNA gene. Eur J Protistol. 2019; 68: 88-98.,5151. Corsaro D, Walochnik J, Köhsler M, Rott MB. Acanthamoeba misidentification and multiple labels: redefining genotypes T16, T19, and T20 and proposal for Acanthamoeba micheli sp. nov. (genotype T19). Parasitol Res. 2015; 114(7): 2481-90. Once the primary status of FLAs is not parasitic, a relevant issue in the research field is understanding factors associated with the pathogenic behavior. Brazilian studies explored in vitro Acanthamoeba properties, such as the interaction of trophozoites with the host cell or the extracellular matrix.2424. da Rocha-Azevedo B, Costa e Silva-Filho F. Biological characterization of a clinical and an environmental isolate of Acanthamoeba polyphaga: analysis of relevant parameters to decode pathogenicity. Arch Mircobiol. 2007; 188(5): 441-9.,5252. da Rocha-Azevedo B, Menezes GC, Costa e Silva-Filho F. The interaction between Acanthamoeba polyphaga and human osteoblastic cells in vitro. Microb Pathog. 2006; 40(1): 8-14.,5353. da Rocha-Azevedo B, Jamerson M, Cabral GA, Costa e Silva-Filho F, Marciano-Cabral F. Acanthamoeba interaction with extracellular matrix glycoproteins: biological and biochemical characterization and role in cytotoxicity and invasiveness. J Eukaryot Microbiol. 2009; 56(3): 270-8.,5454. Alves DSMM, Moraes AS, Alves LM, Gurgel-Gonçalves R, Lino Jr RS, Cuba-Cuba CA, et al. Experimental infection of T4 Acanthamoeba genotype determines the pathogenic potential. Parasitol Res. 2016; 115(9): 3435-40. Contact-independent elements were also included, with contributions that described released proteases through the zymographic technique, indicating the serine protease class as the predominant type produced by Acanthamoeba.5555. Ferreira GA, Magliano ACM, Pral EMF, Alfieri SC. Elastase secretion in Acanthamoeba polyphaga. Acta Trop. 2009; 112(2): 156-63.,5656. Cirelli C, Mesquita EIS, Chagas IAR, Furst C, Possamai CO, Abrahão JS, et al. Extracellular protease profile of Acanthamoeba after prolonged axenic culture and after interaction with MDCK cells. Parasitol Res. 2020; 119(2): 659-66.,5757. Sant'ana VP, Carrijo-Carvalho LC, Foronda AS, Chudzinski-Tavassi AM, de Freitas D, Ramos F, et al. Cytotoxic activity and degradation patterns of structural proteins by corneal isolates of Acanthamoeba spp. Graefes Arch Clin Exp Ophtalmol. 2015; 253(1): 65-75.,5858. Alfieri SC, Correia CEB, Motegi SA, Pral EMF. Proteinase activities in total extracts and in medium conditioned by Acanthamoeba polyhaga trophozoites. J Parasitol. 2000; 86(2): 220-7. Of note, an additional contribution showed for the first time that Acanthamoeba produces and releases extracellular vesicles (EVs) that carry proteases and can be/are taken up by target cells, causing cytotoxicity.5959. Gonçalves DS, Ferreira MS, Liedke SC, Gomes KX, de Oliveira GA, Leão PEL, et al. Extracellular vesicles and vesicle-free secretome of the protozoa Acanthamoeba castellanii under homeostasis and nutritional stress and their damaging potential to host cells. Virulence. 2018; 9(1): 818-36. Apart from the entirely in vitro investigations aforementioned, a study adopted a rat model to induce systemic and cerebral acanthamoebiasis as a strategy to reactivate the virulence of Acanthamoeba cultures.6060. Veríssimo CM, Maschio VJ, Correa APF, Brandelli A, Rott MB. Infection in a rat model reactivates attenuated virulence after long-term axenic culture of Acanthamoeba spp. Mem Inst Oswaldo Cruz. 2013; 108(7): 832-5.
Efforts to develop novel and improve existing therapies to combat FLA infections have been performed in Brazil, including tests with both first-line options and novel compounds. Polyhexamethylene biguanide and chlorhexidine digluconate were evaluated alone or combined against Acanthamoeba cysts.6161. Mafra CSP, Carrijo-Carvalho LC, Chudzinski-Tavassi AM, Taguchi FMC, Foronda AS, Carvalho FRS, et al. Antimicrobial action of biguanides on the viability of Acanthamoeba cysts and assessment of cell toxicity. Invest Ophthalmol Vis Sci. 2013; 54(9): 6363-72. Those biguanides and diamidines (e.g., propamidine and hexamidine isethionate), are currently the main therapeutic lines for Acanthamoeba keratitis.6262. Lorenzo-Morales J, Khan NA, Walochnik J. An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite. 2015; 22(10): 1-20. As they exert cytotoxicity to the cornea, searching for new amoebicidal products is still necessary. Thirteen studies proposed in Brazil included dose-response assays with natural and synthetic substances in this direction. Examples are bacteriocin-like compounds,6363. Benitez LB, Caumo K, Brandelli A, Rott MB. Bacteriocin-like substance from Bacillus amyloliquefaciens shows remarkable inhibition of Acanthamoeba polyphaga. Parasitol Res. 2011; 108(3): 687-91. alpha-helical and beta-hairpin antimicrobial peptides,6464. Sacramento RS, Martins RM, Miranda A, Dobroff ASS, Daffre S, Foronda AS, et al. Differential effects of alpha-helical and beta-hairpin antimicrobial peptides against Acanthamoeba castellanii. Parasitology. 2009; 136(8): 813-21. S-nitrosothiols,6565. Cariello AJ, de Souza GFP, Foronda AS, Yu MCZ, Hofling-Lima AL, de Oliveira MG. In vitro amoebicidal activity of S-nitrosoglutathione and S-nitroso-N-acetylcysteine against trophozoites of Acanthamoeba castellanii. J Antimicrob Chemother. 2010; 65(3): 588-91. silver nanoparticles,6666. Borase HP, Patil CD, Sauter IP, Rott MB, Patil SV. Amoebicidal activity of phytosynthesized silver nanoparticles and their in vitro cytotoxicity to human cells. FEMS Microbiol Lett. 2013; 345(2): 127-31. plant extract, or essential oils directly assayed.6767. Santos IGA, Scher R, Rott MB, Menezes LR, Costa EV, Cavalcanti SCH, et al. Amoebicidal activity of the essential oils of Lippia spp. (Verbenaceae) against Acanthamoeba polyphaga trophozoites. Parasitol Res. 2016; 115(2): 535-40.
68. Sauter IP, dos Santos JC, Apel MA, Cibulski SP, Roehe PM, von Poser GL, et al. Amebicidal activity and chemical composition of Pterocaulon polystachyum (Asteraceae) essential oil. Parasitol Res. 2011; 109(5): 1367-71.
69. Vunda SLL, Sauter IP, Cibulski SP, Roehe PM, Bordignon SAL, Rott MB, et al. Chemical composition and amoebicidal activity of Croton pallidulus, Croton ericoides, and Croton isabelli (Euphorbiaceae) essential oils. Parasitol Res. 2012; 111(3): 961-6.
70. Sauter IP, Rossa GE, Lucas AM, Cibulski SP, Roehe PM, Silva LAA, et al. Chemical composition and amoebicidal activity of Piper hispidinervum (Piperaceae) essential oil. Ind Crop Prod. 2012; 40: 292-5.
71. Ródio C, Vianna DR, Kowalski KP, Panatiere LF, von Poser G, Rott MB. In vitro evaluation of the amebicidal activity of Pterocaulon polystachyum (Asteraceae) against trophozoites of Acanthamoeba castellanii. Parasitol Res. 2008; 104(1): 191-4.
72. Castro LC, Sauter IP, Ethur EM, Kauffmann C, Dall'agnol R, Souza J, et al. In vitro effect of Acanthospermum australe (Asteraceae) extracts on Acanthamoeba polyphaga trophozoites. Rev Bras Plantas Med. 2013; 15(4): 589-94.-7373. Panatieri LF, Brazil NT, Faber K, Medeiros-Neves B, von Poser GL, Rott MB, et al. Nanoemulsions containing a coumarin-rich extract from Pterocaulon balansae (Asteraceae) for the treatment of ocular Acanthamoeba keratitis. AAPS PharmSciTech. 2017; 18(3): 721-8. Two studies have explored alternatives such as photodynamic therapy by using riboflavin and curcuminoids as photosensitisers for treating Acanthamoeba keratitis.7474. Kashiwabuchi RT, Carvalho FRS, Khan YA, de Freitas D, Foronda AS, Hirai FE, et al. Assessing efficacy of combined riboflavin and UV-A Light (365 nm) treatment of Acanthamoeba trophozoites. Invest Ophthalmol Vis Sci. 2011; 52(13): 9333-8.,7575. Corrêa TQ, Geralde MC, Carvalho MT, Bagnato VS, Kurachi C, Souza CWO. Photodynamic inactivation of Acanthamoeba polyphaga with curcuminoids: an in vitro study. Opt Methods Tumor Treat Detect Mech Tech Photodyn Ther XXV. 2016; 9694: 1-7. The effectiveness of contact lens multipurpose solutions against Acanthamoeba, a topic debated by the FLA community,7676. Hendiger EB, Padzik M, Sifaoui I, Reyes-Batlle M, López-Arencibia A, Zyskowska D, et al. Silver nanoparticles conjugated with contact lens solutions may reduce the risk of Acanthamoeba keratitis. Pathogens. 2021; 10(5): 583. has been also investigated in Brazil,7777. de Aguiar APC, Silveira CO, Winck MAT, Rott MB. Susceptibility of Acanthamoeba to multipurpose lens-cleaning solutions. Acta Parasitol. 2013; 58(3): 304-8.,7878. Ludwig IH, Meisler DM, Rutherford I, Bican FE, Langston RH, Visvesvara GS. Susceptibility of Acanthamoeba to soft contact lens disinfection systems. Investig Ophthalmol Vis Sci. 1986; 27(4): 626-8. including the suggestion of imidazolium salt, an anti-amoebic substance, as a suitable option for lens storage.7979. Fabres LF, Gonçalves FC, Duarte EOS, Berté FK, da Conceição DKSL, Ferreira LA, et al. In vitro amoebicidal activity of imidazolium salts against trophozoites. Acta Parasitol. 2020; 65(2): 317-26. Alternatively, therapeutic strategies were concerned with molecules essential to cell division, energy production, cell differentiation, or movement. Examples consist of two Brazilian studies testing the role of small interfering RNA (siRNA) carried in liposomes as an anti-amoebic agent by in vitro and in vivo assays.2626. Zorzi GK, Schuh RS, Maschio VJ, Brazil NT, Rott MB, Teixeira HF. Box Behnken design of siRNA-loaded liposomes for the treatment of a murine model of ocular keratitis caused by Acanthamoeba. Colloids Surfaces B Biointerfaces. 2019; 173: 725-32.,8080. Faber K, Zorzi GK, Brazil NT, Rott MB, Teixeira HF. siRNA-loaded liposomes: inhibition of encystment of Acanthamoeba and toxicity on the eye surface. Chem Biol Drug Des. 2017; 90(3): 406-16. Even though mentions of other FLA species were less frequent than Acanthamoeba, B. mandrillaris is represented in a study describing the amoeba-host cell interaction.8181. da Rocha-Azevedo B, Jamerson M, Cabral GA, Costa e Silva-Filho F, Marciano-Cabral F. The interaction between the amoeba Balamuthia mandrillaris and extracellular matrix glycoproteins in vitro. Parasitology. 2007; 134(Pt 1): 51-8.Naegleria was the focus of three reports; in one of them, mass spectrometry (MALDI-TOF MS) was proposed as a tool to discriminate N. fowleri from non-pathogenic species (e.g., N. italica, N. jadini, N. gruberi).8282. Moura H, Izquierdo F, Woolfitt AR, Wagner G, Pinto T, Del Aguila C, et al. Detection of biomarkers of pathogenic Naegleria fowleri through mass spectrometry and proteomics. J Eukaryot Microbiol. 2015; 62(1): 12-20. In two papers, proteins of Naegleria were characterised by biophysical approaches, providing insights about its metabolism.8383. Da Silva MTA, Caldas VEA, Costa FC, Silvestre DAMM, Thiemann OH. Selenocysteine biosynthesis and insertion machinery in Naegleria gruberi. Mol Biochem Parasitol. 2013; 188(2): 87-90.,8484. Penteado RF, Martini VP, Iulek J. Crystallization and crystallographic analyses of triosephosphate isomerase from Naegleria gruberi. Rev Virtual Quim. 2016; 8(6): 1835-41.
Wet-bench Brazilian research also included ecological information on FLA and amoebic resistant microorganisms (ARMs). Some reports discuss interactions of FLAs with fungi and bacteria, addressing both endosymbionts and pathogens of concern in human health.1919. Gonçalves DS, Ferreira MS, Gomes KX, Rodríguez-de-La-Noval C, Liedke SC, Costa GCV, et al. Unravelling the interactions of the environmental host Acanthamoeba castellanii with fungi through the recognition by mannose - binding proteins. Cell Microbiol. 2019; 21(10): e13066.,8585. Nunes TET, Brazil NT, Fuentefria AM, Rott MB. Acanthamoeba and Fusarium interactions: a possible problem in keratitis. Acta Trop. 2016; 157: 102-7.
86. Maschio VJ, Corção G, Rott MB. Identification of Pseudomonas spp. as amoeba-resistant microorganisms in isolates of Acanthamoeba. Rev Inst Med Trop São Paulo. 2015; 57(1): 81-3.
87. Sticca MP, Carrijo-Carvalho LC, Silva IMB, Vieira LA, Souza LB, Belfort Jr R, et al. Acanthamoeba keratitis in patients wearing scleral contact lenses. Cont Lens Anterior Eye. 2018; 41(3): 307-10.
88. Medina G, Neves P, Flores-Martin S, Manosalva C, Andaur M, Otth C, et al. Transcriptional analysis of flagellar and putative virulence genes of Arcobacter butzleri as an endocytobiont of Acanthamoeba castellanii. Arch Microbiol. 2019; 201(8): 1075-83.
89. Medina G, Leýan P, Silva CV, Flores-Martin S, Manosalva C, Fernández H. Intra-amoebic localization of Arcobacter butzleri as an endocytobiont of Acanthamoeba castellanii. Arch Microbiol. 2019; 201(10): 1447-52.-9090. de Faria LV, do Carmo PHF, da Costa MC, Peres NTA, Chagas IAR, Furst C, et al. Acanthamoeba castellanii as an alternative interaction model for the dermatophyte Trichophyton rubrum. Mycoses. 2020; 63(12): 1331-40. Another type of ARMs studied in Brazil comprises human adenovirus9191. Staggemeier R, Arantes T, Caumo KS. Detection and quantification of human adenovirus genomes in Acanthamoeba isolated from swimming pools. An Acad Bras Cienc. 2016; 88: 635-41. and giant viruses such as the Tupanvirus, isolated from V. vermiformis and A. polyphaga mimivirus.9292. Silva LCF, Almeida GMF, Assis FL, Albarnaz JD, Boratto PVM, Dornas FP, et al. Modulation of the expression of mimivirus-encoded translation-related genes in response to nutrient availability during Acanthamoeba castellanii infection. Front Microbiol. 2015; 6(6): 539.,9393. Boratto P, Albarnaz JD, Almeida GMDF, Botelho L, Fontes ACL, Costa AO, et al. Acanthamoeba polyphaga mimivirus prevents amoebal encystment-mediating serine proteinase expression and circumvents cell encystment. J Virol. 2015; 89(5): 2962-5. We discussed below other reports on giant virus classified in the auxiliary class. Apart from intra-amoebic microorganisms, a wet-bench study investigated the ecological relation between amoeba and mosquitoes, demonstrating for the first time that A. polyphaga can infect Aedes aegypti.9494. Rott M, Caumo K, Sauter I, Eckert J, da Rosa L, da Silva O. Susceptibility of Aedes aegypti (Diptera:Culicidae) to Acanthamoeba polyphaga (Sarcomastigophora:Acanthamoebidae ). Parasitol Res. 2010; 107(1): 195-8. Moreover, the role of FLA as vehicles of pathogenic microorganisms debated worldwide9595. Scheid PL. Amoebophagous fungi as predators and parasites of potentially pathogenic free-living amoebae. Open Parasitol J. 2018; 6(1): 75-86.,9696. Scheid PL, Schwarzenberger R. Free-living amoebae as vectors of cryptosporidia. Parasitol Res. 2011; 109(2): 499-504.,9797. Lorenzo-Morales J, Coronado-Álvarez N, Martínez-Carretero E, Maciver SK, Valladares B. Detection of four adenovirus serotypes within water-isolated strains of Acanthamoeba in the Canary Islands, Spain. Am J Trop Med Hyg. 2007; 77(4): 753-6. and also present in Brazilian surveys8585. Nunes TET, Brazil NT, Fuentefria AM, Rott MB. Acanthamoeba and Fusarium interactions: a possible problem in keratitis. Acta Trop. 2016; 157: 102-7.,8888. Medina G, Neves P, Flores-Martin S, Manosalva C, Andaur M, Otth C, et al. Transcriptional analysis of flagellar and putative virulence genes of Arcobacter butzleri as an endocytobiont of Acanthamoeba castellanii. Arch Microbiol. 2019; 201(8): 1075-83.,9191. Staggemeier R, Arantes T, Caumo KS. Detection and quantification of human adenovirus genomes in Acanthamoeba isolated from swimming pools. An Acad Bras Cienc. 2016; 88: 635-41.,9898. Maschio VJ, Corção G, Bücker F, Caumo K, Rott MB. Identification of Paenibacillus as a symbiont in Acanthamoeba. Curr Microbiol. 2015; 71(3): 415-20. reinforce the need of monitoring FLA presence in the environment.
Clinical references and the risks of FLA infections for human health in Brazil - As shown in Fig. 3, 29 out of 178 references were classified in the clinical category, including mainly Acanthamoeba keratitis,9999. Forseto AS, Nosé W. Diagnosis of Acanthamoeba keratitis with confocal microscopy. Rev Bras de Oftalmol. 2003; 62: 220-8.
100. Nakano E, Oliveira M, Portellinha W, de Freitas D, Nakano K. Confocal microscopy in early diagnosis of Acanthamoeba keratitis. J Refract Surg. 2004; 20(5): S737-41.
101. Kashiwabuchi RT, de Freitas D, Alvarenga LS, Vieira L, Contarini P, Sato E, et al. Corneal graft survival after therapeutic keratoplasty for Acanthamoeba keratitis. Acta Ophthalmol. 2008; 86(6): 666-9.
102. Carvalho FRS, Foronda AS, Mannis MJ, Hofling-Lima AL, Belfort Jr R, de Freitas D. Twenty years of Acanthamoeba keratitis. Cornea. 2009; 28(5): 516-9.
103. Duarte JL, Furst C, Klisiowicz DR, Klassen G, Costa AO. Morphological, genotypic, and physiological characterization of Acanthamoeba isolates from keratitis patients and the domestic environment in Vitoria, Espírito Santo, Brazil. Exp Parasitol. 2013; 135(1): 9-14.-104104. Sant'ana VP, Foronda AS, de Freitas D, Carrijo-Carvalho LC, Carvalho FRS. Sensitivity of enzymatic toxins from corneal isolate of Acanthamoeba protozoan to physicochemical parameters. Curr Microbiol. 2017; 74(11): 1316-23. PAM,105105. Pimentel LA, Dantas AFM, Uzal F, Riet-Correa F. Meningoencephalitis caused by Naegleria fowleri in cattle of northeast Brazil. Res Vet Sci. 2012; 93(2): 811-2. and GAE,106106. Campos R, Gomes MCO, Prigenzi LS, Stecca J. Meningencefalite por ameba de vida livre apresentação do primeiro caso latino-americano. Rev Inst Med Trop São Paulo. 1977; 19(5): 349-51. reports (Table I).
FLA infections reported in Brazil present the occurrence of Naegleria spp. in encephalitis cases,105105. Pimentel LA, Dantas AFM, Uzal F, Riet-Correa F. Meningoencephalitis caused by Naegleria fowleri in cattle of northeast Brazil. Res Vet Sci. 2012; 93(2): 811-2.,107107. Henker LC, Cruz RAS, Silva FS, Driemeier D, Sonne L, Uzal FA, et al. Meningoencephalitis due to Naegleria fowleri in cattle in southern Brazil. Rev Bras Parasitol Vet. 2019; 28(3): 514-7. and Acanthamoeba spp. as the commonest genus of keratitis,108108. Fabres LF, Maschio VJ, Santos DL, Kwitko S, Marinho DR, Araújo BS, et al. Virulent T4 Acanthamoeba causing keratitis in a patient after swimming while wearing contact lenses in Southern Brazil. Acta Parasitol. 2018; 63(2): 428-32.
109. Buchele MLC, Wopereis DB, Casara F, Macedo JP, Rott MB, Monteiro FBF, et al. Contact lens-related polymicrobial keratitis : Acanthamoeba spp. genotype T4 and Candida albicans. Parasitol Res. 2018; 117(11): 3431-6.
110. Alves DSMM, Gonçalves GS, Moraes AS, Alves LM, Carmo Neto JR, Hecht MM, et al. The first Acanthamoeba keratitis case in the Midwest region of Brazil: diagnosis, genotyping of the parasite and disease outcome. Rev Soc Bras Med Trop. 2018; 51(5): 716-9.-111111. Carlesso AM, Mentz MB, Machado MLS, Carvalho A, Nunes TET, Maschio VJ, et al. Characterization of isolates of Acanthamoeba from the nasal mucosa and cutaneous lesions of dogs. Curr Microbiol. 2014; 68(6): 702-7. skin infections, disseminated disease, and even encountered in human feces112112. Frade MTS, Melo LF, Pessoa CRM, Araújo JL, Fighera RA, Souza AP, et al. Systemic acanthamoebiasis associated with canine distemper in dogs in the semiarid region of Paraíba, Brazil. Pesq Vet Bras. 2015; 35(2): 160-4. and urine.113113. Santos LC, Oliveira MS, Lobo RD, Higashino HR, Costa SF, Van Der Heijden IM, et al. Acanthamoeba spp. in urine of critically ill patients. Emerg Infect Dis. 2009; 15(7): 1144-6.Vermamoeba and Balamuthia were reported in two records, and no Sappinia cases were described (Table I). Of seven encephalitis cases, only one describes the recovery of the patient.114114. Salles-Gomes Jr CE, Barbosa ER, Nóbrega JP, Scaff M, Spina-França A. Primary amebic meningoencephalomyelitis. Report of a case. Arq Neuropsiquiatr. 1978; 36(2): 139-42. It is dated from 1978, reporting the recovery of a 14-year-old boy with a habit of bathing in lagoons. Water samples were collected, confirming the presence of N. fowleri.114114. Salles-Gomes Jr CE, Barbosa ER, Nóbrega JP, Scaff M, Spina-França A. Primary amebic meningoencephalomyelitis. Report of a case. Arq Neuropsiquiatr. 1978; 36(2): 139-42.
Acanthamoeba infections, basically keratitis, represent the highest incidence of amoeba contaminations in Brazil. In this group, investigations dated after 2010 described molecular approaches (Table I-D), indicating this technology became more accessible in the laboratory routine.
The widely debated misdiagnosis of FLA infection6262. Lorenzo-Morales J, Khan NA, Walochnik J. An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite. 2015; 22(10): 1-20. has also been reported in the Brazilian literature, as discussed in a retrospective study of cases of amoebic keratitis, in which the herpes virus was the most frequent initial suspicion.115115. dos Santos DL, Kwitko S, Marinho DR, Araújo BS, Locatelli CI, Rott MB. Acanthamoeba keratitis in Porto Alegre (southern Brazil): 28 cases and risk factors. Parasitol Res. 2018; 117(3): 747-50. The same occurred for amoeba brain infections, in which a fatal case in Brazil was first hypothesised and treated for viral meningitis.116116. Silva RA, Araújo SA, Avellar IFDF, Pittella JEH, Oliveira JT, Christo PP. Granulomatous amoebic meningoencephalitis in an immunocompetent patient. Arch Neurol. 2010; 67(12): 1516-20. Despite that, the overall tendency to rapidly and accurately diagnose FLA proposed in Brazilian surveys may decrease the misdiagnosis. On the other hand, monitoring of intra-FLA resistant microorganisms is an issue of concern worldwide11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.,9797. Lorenzo-Morales J, Coronado-Álvarez N, Martínez-Carretero E, Maciver SK, Valladares B. Detection of four adenovirus serotypes within water-isolated strains of Acanthamoeba in the Canary Islands, Spain. Am J Trop Med Hyg. 2007; 77(4): 753-6.,117117. 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(3): 131-40. that is still absent in the clinical category of Brazilian papers.
Environmental reports and the assessment of FLA as a water quality marker in Brazil - Acanthamoeba, Naegleria, Vermamoeba, and Balamuthia were detected in Brazilian habitats, including university buildings, hospitals, swimming pools, tap and freshwater, dust, soil samples, and inside insects118118. da Silva MA, da Rosa JA. Isolation of potencially pathogenic free-living amoebas in hospital dust. Rev Saude Publica. 2003; 37(2): 242-6.
119. Pens CJ, Costa M, Fadanelli C, Caumo K, Rott MB. Acanthamoeba spp. and bacterial contamination in contact lens storage cases and the relationship to user profiles. Parasitol Res. 2008; 103(6): 1241-5.
120. Landeli MF, Salton J, Caumo K, Broetto L, Rott MB. Isolation and genotyping of free-living environmental isolates of Acanthamoeba spp. from bromeliads in Southern Brazil. Exp Parasitol. 2013; 134(3): 290-4.
121. Becker-Finco A, Costa AO, Silva SK, Ramada JS, Furst C, Stingher AE, et al. Physiological, morphological, and immunochemical parameters used for the characterization of clinical and environmental isolates of Acanthamoeba. Parasitology. 2013; 140(3): 396-405.
122. Maschio VJ, Chies F, Carlesso AM, Carvalho A, Rosa SP, Van Der Sand ST, et al. Acanthamoeba T4, T5 and T11 isolated from mineral water bottles in Southern Brazil. Curr Microbiol. 2014; 70(1): 6-9.
123. Fabres LF, Santos SPR, Benitez LB, Rott MB. Isolation and identification of Acanthamoeba spp. from thermal swimming pools and spas in Southern Brazil. Acta Parasitol. 2016; 61(2): 221-7.
124. Caumo K, Frasson AP, Pens CJ, Panatieri LF, Frazzon APG, Rott MB. Potentially pathogenic Acanthamoeba in swimming pools: a survey in the southern Brazilian city of Porto Alegre. Ann Trop Med Parasitol. 2009; 103(6): 477-85.
125. Carlesso AM, Artuso GL, Caumo K, Rott MB. Potentially pathogenic Acanthamoeba isolated from a hospital in Brazil. Curr Microbiol. 2010; 60(3): 185-90.
126. Costa AO, Castro EA, Ferreira GA, Furst C, Crozeta MA, Thomas-Soccol V. Characterization of Acanthamoeba isolates from dust of a public hospital in Curitiba, Paraná, Brazil. J Eukaryot Microbiol. 2010; 57(1): 70-5.
127. Winck MAT, Caumo K, Rott MB. Prevalence of Acanthamoeba from tap water in Rio Grande do Sul, Brazil. Curr Microbiol. 2011; 63(5): 464-9.
128. Alves DSMM, Moraes AS, Nitz N, Oliveira MGC, Hecht MM, Gurgel-Gonçalves R, et al. Occurrence and characterization of Acanthamoeba similar to genotypes T4, T5, and T2 / T6 isolated from environmental sources in Brasília, Federal District, Brazil. Exp Parasitol. 2012; 131(2): 239-44.
129. Otta DA, Rott MB, Carlesso AM, Santos O. Prevalence of Acanthamoeba spp. (Sarcomastigophora : Acanthamoebidae) in wild populations of Aedes aegypti (Diptera : Culicidae). Parasitol Res. 2012; 111: 2017-22.
130. Magliano ACM, Teixeira MMG, Alfieri SC. Revisiting the Acanthamoeba species that form star-shaped cysts (genotypes T7, T8, T9, and T17): characterization of seven new Brazilian environmental isolates and phylogenetic inferences. Parasitology. 2011; 139(1): 45-52.-131131. Zanella J, Costa SOP, Zacaria J, Echeverrigaray S. A rapid and reliable method for the clonal isolation of Acanthamoeba from environmental samples. Brazilian Arch Biol Technol. 2012; 55(1): 1-6. (Table II).
A summary of the environmental isolations of free-living amoeba (FLA) in Brazil, from 1986 to 2020
The first isolation in the environment is dated from 1986 and pointed out the presence of N. fowleri in an artificial lake in Rio de Janeiro city, state of Rio de Janeiro, the Southeast region.132132. Salazar HC, Moura H, Fernandez O, Peralta JM. Isolation of Naegleria fowleri from a lake in the city of Rio de Janeiro. Trans R Soc Trop Med Hyg. 1986; 80(2): 348-9. Dust samples from hospitals and university buildings yielded positive results for Naegleria spp, in the municipalities of Presidente Prudente and Santos, respectively, both in São Paulo state, the Southeast region.118118. da Silva MA, da Rosa JA. Isolation of potencially pathogenic free-living amoebas in hospital dust. Rev Saude Publica. 2003; 37(2): 242-6.,133133. Teixeira LH, Rocha S, Pinto RMF, Caseiro MM, Costa SOP. Prevalence of potentially pathogenic free-living amoebae from Acanthamoeba and Naegleria genera in non-hospital, public, internal environments from the city of Santos, Brazil. Brazilian J Infect Dis. 2009; 13(6): 395-7. Although based on morphological analysis, a study indicated the N. fowleri presence by its ability for supporting 43ºC and flagellating.11. Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004; 34(9): 1001-27.,133133. Teixeira LH, Rocha S, Pinto RMF, Caseiro MM, Costa SOP. Prevalence of potentially pathogenic free-living amoebae from Acanthamoeba and Naegleria genera in non-hospital, public, internal environments from the city of Santos, Brazil. Brazilian J Infect Dis. 2009; 13(6): 395-7.
Naegleria and Vermamoeba (Hartmanella) identifications were less frequent compared to Acanthamoeba,134134. Possamai CO, Loss AC, Costa AO, Falqueto A, Furst C. Acanthamoeba of three morphological groups and distinct genotypes exhibit variable and weakly inter-related physiological properties. Parasitolol Res. 2018; 117(5): 1389-400.,135135. Magliano ACM, da Silva FM, Teixeira MMG, Alfieri SC. Genotyping, physiological features and proteolytic activities of a potentially pathogenic Acanthamoeba sp. isolated from tap water in Brazil. Exp Parasitol. 2009; 123(3): 231-5. but they were found coexisting in the same habitats (Table II).136136. Soares SS, Souza TK, Berte FK, Cantarelli VV, Rott MB. Occurrence of infected free-living amoebae in cooling towers of southern Brazil. Curr Microbiol. 2017; 74(12): 1461-8.,137137. Bellini NK, da Fonseca ALM, Reyes-Batlle M, Lorenzo-Morales J, Rocha O, Thiemann OH. Isolation of Naegleria spp. from a Brazilian water source. Pathogens. 2020; 9(2): 90. Environmental findings of B. mandrillaris were reported to be associated with Acanthamoeba populations in air conditioning systems of hospitals.138138. Fonseca JDG, Gómez-Hernández C, Barbosa CG, Rezende-Oliveira K. Identification of T3 and T4 genotypes of Acanthamoeba sp. in dust samples isolated from air conditioning equipment of public hospital of Ituiutaba-MG. Curr Microbiol. 2020; 77(5): 890-5. Across the globe, FLAs have been sampled in natural habitats related to water and soil139139. Sousa-Ramos D, Reyes-Batlle M, Bellini NK, Rodríguez-Expósito RL, Piñero JE, Lorenzo-Morales J. Free-living amoebae in soil samples from Santiago Island, Cape Verde. Microorganisms. 2021; 9(7): 1460.,140140. Reyes-Batlle M, Díaz FJ, Sifaoui I, Rodríguez-Expósito R, Rizo-Liendo A, Piñero JE, et al. Free living amoebae isolation in irrigation waters and soils of an insular arid agroecosystem. Sci Total Environ. 2021; 753: 141833.,141141. Mahmoudi MR, Zebardast N, Masangkay FR, Karanis P. Detection of potentially pathogenic free-living amoebae from the Caspian Sea and hospital ward dust of teaching hospitals in Guilan, Iran. J Water Health. 2021; 19(2): 278-87. besides extreme environments such as treatment water plants, chlorinated swimming pools, hot spring water, and ice samples.142142. Le Calvez T, Trouilhé MC, Humeau P, Moletta-Denat M, Frère J, Héchard Y. Detection of free-living amoebae by using multiplex quantitative PCR. Mol Cell Probes. 2012; 26(3): 116-20.,143143. Schroeder JM, Booton GC, Hay J, Niszl IA, Seal DV, Markus MB, et al. Use of subgenic 18S ribosomal DNA PCR and sequencing for genus and genotype identification of Acanthamoebae from humans with keratitis and from sewage sludge. J Clin Microbiol. 2001; 39(5): 1903-11.,144144. Reyes-Batlle M, Niyyati M, Martín-Navarro CM, López-Arencibia A, Valladares B, Martínez-Carretero E, et al. Unusual Vermamoeba vermiformis strain isolated from snow in upon observation of the snow samples cultured in. Mount Teide, Tenerife, Canary Islands, Spain.Nov Biomed. 2015; 3(4): 189-92. Global warming can favor the spreading of thermophilic pathogenic FLA145145. Nichols G, Lake I, Heaviside C. Climate change and water-related infectious diseases. Atmosphere (Basel). 2018; 9(10): 1-60.,146146. Xue J, Lamar FG, Zhang B, Lin S, Lamori JG, Sherchan SP. Quantitative assessment of Naegleria fowleri and fecal indicator bacteria in brackish water of lake Pontchartrain, Louisiana. Sci Total Environ. 2018; 622-623: 8-16. and intra-FLA pathogenic bacteria.147147. Marciano-Cabral F, Jamerson M, Kaneshiro ES. Free-living amoebae, Legionella and Mycobacterium in tap water supplied by a municipal drinking water utility in the USA. J Water Health. 2010; 8(1): 71-82. In Brazil, a tropical zone directly exposed to global warming effects,148148. Alves MTR, Machado KB, Ferreira ME, Vieira LCG, Nabout JC. A snapshot of the limnological features in tropical floodplain lakes: the relative influence of climate and land use. Acta Limnol Bras. 2019; 31(e10). the presence of potentially pathogenic FLA strains described in water-related samples (Table II) can pose a health concern. Although the country’s regulatory legislation of water quality does not address FLA risks for humans,149149. MMA - Ministério do Meio Ambiente/Conselho Nacional do Meio Ambiente. Resolução CONAMA n 357. Brasil; 2005. [Internet]. 23 June, 2021. [cited 2021 Nov 15]. Available from: http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=459.
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the need for research on tools to detect them is identified in the global literature.150150. Plutzer J, Karanis P. Neglected waterborne parasitic protozoa and their detection in water. Water Res. 2016; 101: 318-32.
Progression of FLA detection and characterisation tools in Brazil - With the expansion of studies on FLA in the country, methods for detection and characterisation of environmental and clinical samples have improved, with a tendency to adopt molecular approaches over time (Fig. 5).
progression of the methods used in Brazil to monitor FLA presence in clinical (A) and environmental (B) samples.
Microscopy-based methods for detection and characterisation were adopted in all studies (54/54) and in some, (17/54) it was the only option to identify the FLA. This approach predominates until 2005 (Fig. 5). Between 2010 and 2020, 23 out of 34 FLA environmental and clinical investigations included molecular-based tools for FLA detection, in contrast with five “morphological” and six “Morphological & Immunohistochemical” based analyses. Moreover, it is worth noting that DNA-based investigations were more prevalent on environmental (18/25) than clinical (9/29) references (Fig. 5).
Overall, the studies included microscopy-based investigations combined with hematoxylin-eosin (HE),151151. de Moura H, Salazar HC, Fernandes O, Lisboa DC, de Carvalho FG. Free-living amoebae in human intestine: Evidence of parasitism. Rev Inst Med Trop São Paulo. 1985; 27(3): 150-6.,152152. Chimelli L, Hahn MD, Scaravilli F, Wallace S, Visvesvara GS. Granulomatous amoebic encephalitis due to leptomyxid amoebae : report of the first Brazilian case. Trans R Soc Trop Med Hyg. 1992; 86(6): 635. calcofluor and Giemsa stains.153153. Ruthes ACC, Wahab S, Wahab N, Moreira H, Moreira L. Conjunctivitis presumably due to Acanthamoeba. Arq Bras Oftal. 2004; 67(6): 897-900. Anti-B. mandrillaris antisera has been used for immunofluorescence purposes.116116. Silva RA, Araújo SA, Avellar IFDF, Pittella JEH, Oliveira JT, Christo PP. Granulomatous amoebic meningoencephalitis in an immunocompetent patient. Arch Neurol. 2010; 67(12): 1516-20.,154154. Silva-Vergara ML, Colombo ERC, Vissotto EDF, Silva ACAL, Chica JEL, Etchebehere RM, et al. Disseminated Balamuthia mandrillaris amoeba infection in an AIDS patient from Brazil. Am J Trop Med Hyg. 2007; 77(6): 1096-8. Before performing microscope slides, environmental and clinical samples were often cultured in non-nutritive agar plates155155. Carvalho FRDS, Carrijo-Carvalho LC, Chudzinski-Tavassi AM, Foronda AS, de Freitas D. Serine-like proteolytic enzymes correlated with differential pathogenicity in patients with acute Acanthamoeba keratitis. Clin Microbiol Infect. 2010; 17(4): 603-9. with an additional supply of bacteria such as Escherichia coli,153153. Ruthes ACC, Wahab S, Wahab N, Moreira H, Moreira L. Conjunctivitis presumably due to Acanthamoeba. Arq Bras Oftal. 2004; 67(6): 897-900.Enterobacter,2222. Barros JN, Mascaro VLD, Lowen M, Martins MC, Foronda A. Diagnosis of Acanthamoeba corneal infection by impression cytology: case report. Arq Bras Oftal. 2007; 70(2): 343-6.,153153. Ruthes ACC, Wahab S, Wahab N, Moreira H, Moreira L. Conjunctivitis presumably due to Acanthamoeba. Arq Bras Oftal. 2004; 67(6): 897-900.Aerobacter aerogenes,151151. de Moura H, Salazar HC, Fernandes O, Lisboa DC, de Carvalho FG. Free-living amoebae in human intestine: Evidence of parasitism. Rev Inst Med Trop São Paulo. 1985; 27(3): 150-6.Micrococcus luteus and Pseudomonas aeruginosa.156156. Moraes J, Alfieri SC. Growth, encystment and survival of Acanthamoeba castellanii grazing on different bacteria. FEMS Microbiol Ecol. 2008; 66(2): 221-9. Osmotolerance and thermotolerance assays have been performed in NNA plates for checking pathogenicity.124124. Caumo K, Frasson AP, Pens CJ, Panatieri LF, Frazzon APG, Rott MB. Potentially pathogenic Acanthamoeba in swimming pools: a survey in the southern Brazilian city of Porto Alegre. Ann Trop Med Parasitol. 2009; 103(6): 477-85.,128128. Alves DSMM, Moraes AS, Nitz N, Oliveira MGC, Hecht MM, Gurgel-Gonçalves R, et al. Occurrence and characterization of Acanthamoeba similar to genotypes T4, T5, and T2 / T6 isolated from environmental sources in Brasília, Federal District, Brazil. Exp Parasitol. 2012; 131(2): 239-44.,157157. Wopereis DB, Bazzo ML, De Macedo JP, Casara F, Golfeto L, Venancio E, et al. Free-living amoebae and its relationship with air quality in hospital environments: isolation and characterization of Acanthamoeba spp. from air-conditioning system. Parasitology. 2020; 147(7): 789-90. Molecular-based approaches comprised PCR assays in which 18S rDNA regions5050. Corsaro D, Köhsler M, Venditti D, Rott MB, Walochnik J. Recovery of an Acanthamoeba strain with two group I introns in the nuclear 18S rRNA gene. Eur J Protistol. 2019; 68: 88-98.,158158. Caumo K, Rott MB. Acanthamoeba T3, T4 and T5 in swimming-pool waters from Southern Brazil. Acta Trop. 2011; 117(3): 233-5. or ITS regions159159. Bellini NK, Santos TM, da Silva MTA, Thiemann OH. The therapeutic strategies against Naegleria fowleri. Exp Parasitol. 2018; 187: 1-11. were used to genotyping FLA isolates, and the V3 region of 16S rDNA of bacteria was used to detect intra-FLA bacteria.9898. Maschio VJ, Corção G, Bücker F, Caumo K, Rott MB. Identification of Paenibacillus as a symbiont in Acanthamoeba. Curr Microbiol. 2015; 71(3): 415-20. Among the wet-bench category of papers, one study has employed a high-throughput sequencing (HTS) methodology to analyse mitochondrial gene sequences elucidative to investigate diversity in Amoebozoa.4040. Fuciková K, Lahr DJG. Uncovering cryptic diversity in two amoebozoan species using complete mitochondrial genome sequences. J Eukaryot Microbiol. 2016; 63(1): 112-22.
Reviews and dry-bench studies in the core class - A group of literature reviews covered a diversity of FLA-related topics. The first literature review dates from 2000, and it is devoted to reporting predisposing factors commonly associated with amoebic keratitis, including clinical aspects, diagnosis strategies, and therapeutic options.160160. Alvarenga LS, de Freitas D, Hofling-Lima AL. Ceratite por Acanthamoeba. Arq Bras Oftal. 2000; 63(1): 155-9. Two comprehensive reviews addressed mechanisms developed by intra Acanthamoeba microorganisms to enhance their survival and multiplication chances.161161. Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RHS. Acanthamoeba spp. as a universal host for pathogenic microorganisms: one bridge from environment to host virulence. Microbiol Res. 2016; 193: 30-8.,162162. Silva LKDS, Boratto PVM, La Scola B, Bonjardim CA, Abrahão JS. Acanthamoeba and mimivirus interactions: the role of amoebal encystment and the expansion of the 'Cheshire Cat' theory. Curr Opin Microbiol. 2016; 31: 9-15. Since several ARMs are capable of proliferating in FLAs and in the human host, other reviews discussed the hypothesis that ARMs can use the amoeba cell to gain virulence before inhabiting humans.161161. Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RHS. Acanthamoeba spp. as a universal host for pathogenic microorganisms: one bridge from environment to host virulence. Microbiol Res. 2016; 193: 30-8. Subsequent work discussed clinical aspects of N. fowleri infection and debated therapeutic challenges when treating PAM patients.159159. Bellini NK, Santos TM, da Silva MTA, Thiemann OH. The therapeutic strategies against Naegleria fowleri. Exp Parasitol. 2018; 187: 1-11. The latest literature review was published in 2019, describing the role of extracellular vesicles of bacteria, fungi, and protozoans with a particular emphasis on A. castellanii.163163. Gonçalves DS, Ferreira MS, Guimarães AJ. Extracellular vesicles from the protozoa Acanthamoeba castellanii: their role in pathogenesis, environmental adaptation and potential applications. Bioengineering. 2019; 6(1): 12.
Finally, the dry-bench references gathered relevant information for ARM monitoring. For example, a study accessed genomic signatures shared by Acanthamoeba entoorganisms by using oligonucleotide relative frequencies (OnRF) and relative codon usage (RCU) approaches.164164. Serrano-Solís V, Soares PET, de Farías ST. Genomic signatures among Acanthamoeba polyphaga entoorganisms unveil evidence of coevolution. J Mol Evol. 2019; 87(1): 7-15. An additional publication described the tridimensional structure of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) of N. gruberi.165165. Machado ATP, Silva M, Iulek J. Structural studies of glyceraldehyde-3-phosphate dehydrogenase from Naegleria gruberi, the first one from phylum. Biochim Biophys Acta Proteins Proteom. 2018; 1866: 581-8.
Auxiliary category - The auxiliary class grouped 58 references on broad subjects that also embraced FLA topics. It includes virus replication,166166. Abrahão JS, Dornas FP, Silva LCF, Almeida GM, Boratto PVM, Colson P, et al. Acanthamoeba polyphaga mimivirus and other giant viruses: an open field to outstanding discoveries. Virol J. 2014; 11: 1-12.,167167. Boratto PVM, Dornas FP, Silva LCF, Rodrigues RAL, Oliveira GP, Cortines JR, et al. Analyses of the Kroon virus major capsid gene and its transcript highlight a distinct pattern of gene evolution and splicing among Mimiviruses. J Virol. 2018; 92(2): 1-11.,168168. Dornas FP, Assis FL, Aherfi S, Arantes T, Abrahão JS, Colson P, et al. A Brazilian Marseillevirus is the founding member of a lineage in family Marseilleviridae. Viruses. 2016; 8(76): 1-16.,169169. Dornas FP, Khalil JYB, Pagnier I, Raoult D, Abrahão J, La Scola B. Isolation of new Brazilian giant viruses from environmental samples using a panel of protozoa. Front Microbiol. 2015; 6: 1-9. microbial keratitis,170170. Moriyama AS, Hofling-Lima AL. Contact lens-associated microbial keratitis. Arq Bras Oftalmol. 2008; 71(7): 32-6.,171171. Müller RT, Abedi F, Cruzat A, Witkin D, Baniasadi N, Cavalcanti BM, et al. Degeneration and regeneration of subbasal corneal nerves after infectious keratitis: a longitudinal in vivo confocal microscopy study. Ophthalmology. 2015; 122(11): 2200-9. main aspects of central nervous disorders172172. Frade MTS, Ferreira JS, Nascimento MJR, Aquino VVF, Macêdo IL, Carneiro RS, et al. Central nervous system disorders diagnosed in dogs. Pesq Vet Bras. 2018; 38(5): 935-48.,173173. Gasparetto EL, Cabral RF, Hygino LC, Domingues RC. Diffusion imaging in brain infections. Neuroimaging Clin NA. 2011; 21(1): 89-113.,174174. Chimelli L. Co-infection of HIV and tropical infectious agents that affect the nervous system. Rev Neurol (Paris). 2012; 168(3): 270-82. and cutaneous infections,175175. Kollipara R, Peranteau AJ, Nawas ZY, Tong Y, Woc-colburn L, Yan AC, et al. Emerging infectious diseases with cutaneous manifestations: fungal, helminthic, protozoan and ectoparasitic infections. J Am Acad Dermatol. 2016; 75(1): 19-30. reaction of microorganisms against phototherapies,176176. Decarli MC, Carvalho MT, Corrêa TQ, Bagnato VS, Souza CWO. Different photoresponses of microorganisms: from bioinhibition to biostimulation. Curr Microbiol. 2016; 72(4): 473-81. among others.
Prospection surveys concerned with waterborne protozoans have shown Giardia and Acanthamoeba in saline water and oysters samples, highlighting both as a concern for human health.177177. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M, et al. Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res. 2018; 137: 273-80. Similarly, a foodborne parasite-based examination in salad samples of Brazilian restaurants showed Acanthamoeba presence ranking in the first position with 23.5% identifications.178178. Perim LV, Custódio NCC, Lima VCV, Igreja JASL, Alves DSMM, Storchilo HR, et al. Occurrence of parasites in salads in restaurants in Aparecida de Goiânia, Goiás, Brazil. J Trop Pathol Vol. 2020; 49(3): 207-14. Although this identification suggests the importance of food as a source of free-living amoeba, as far as we know, there is no evidence of infections elicited by ingesting FLA.
A study on keratitis has indicated the following groups as etiological agents of corneal infections: bacteria (Staphylococcus, Streptococcus, Enterobacter), fungi (Candida, Rhodatorula), and protozoan groups (Acanthamoeba) as possible etiological agents of corneal infections.179179. Marujo FI, Hirai FE, Yu MCZ, Hofling-Lima AL, de Freitas D, Sato EH. Distribution of infectious keratitis in a tertiary hospital in Brazil. Arq Bras Oftalmol. 2013; 76(6): 370-3. From 2007 to 2014, another study examined 242 patients from a specialised eye hospital whose results indicated bacteria as the first cause of keratitis infection, and the successive positions in the ranking were occupied by fungi and Acanthamoeba infections.180180. Farias R, Pinho L, Santos R. Epidemiological profile of infectious keratitis. Rev Bras Oftalm. 2017; 76(3): 116-20.
Concerned with treatments, the auxiliary literature has investigated UV light and natural compounds acting as photosensitisers for treat a diversity of parasitic and microbial infections, including Acanthamoeba keratitis.181181. Yin R, Dai T, Avci P, Jorge AES, Melo WCMA, Vecchio D, et al. Light based anti-infectives: ultraviolet C irradiation, photodynamic therapy, blue light, and beyond. Curr Opin Pharmacol. 2013; 13(5): 731-62. A related survey concerned with the ranges of visual acuity recovery has examined the efficacy of Boston keratoprothesis type I for Acanthamoeba keratitis.182182. Santos A, Silva LD, Sousa LB, de Freitas D, Oliveira LA. Results with the Boston Type I keratoprosthesis after Acanthamoeba keratitis. Am J Ophtalmol Case Rep. 2017; 6: 71-3. Other contributions are assays to investigate the effectivity of a biosurfactant on Candida and Acanthamoeba183183. da Silva A, Nobre Jr H, Sampaio L, Nascimento B, da Silva C, de Andrade Neto JB, et al. Antifungal and antiprotozoal green amino acid-based rhamnolipids: mode of action, antibiofilm efficiency and selective activity against resistant Candida spp. strains and Acanthamoeba castellanii. Colloids Surf B Biointerfaces. 2020; 193: 111148. and anti-amoebic action of metabolites from Penicillium.184184. Lopes FC, Tichota DM, Sauter IP, Meira SMM, Segalin J, Rott MB, et al. Active metabolites produced by Penicillium chrysogenum IFL1 growing on agro-industrial residues. Ann Microbiol. 2013; 63: 771-8.
Sixty-seven percent (39/58) of the auxiliary references describe investigations specific to ARMs. Fungi and FLA interactions addressed Trichophyton rubrum,9090. de Faria LV, do Carmo PHF, da Costa MC, Peres NTA, Chagas IAR, Furst C, et al. Acanthamoeba castellanii as an alternative interaction model for the dermatophyte Trichophyton rubrum. Mycoses. 2020; 63(12): 1331-40.Fusarium,8585. Nunes TET, Brazil NT, Fuentefria AM, Rott MB. Acanthamoeba and Fusarium interactions: a possible problem in keratitis. Acta Trop. 2016; 157: 102-7.Sporothrix,185185. Tavares PL, Ribeiro AC, Berte FK, Hellwig AHS, Pagani DM, Souza CCT, et al. The interaction between Sporothrix schenckii sensu stricto and Sporothrix brasiliensis with Acanthamoeba castellanii. Mycoses. 2020; 63(3): 302-7.Paracoccidioides spp.,186186. Albuquerque P, Nicola AM, Magnabosco DAG, Derengowski LS, Crisóstomo LS, Xavier LCG, et al. A hidden battle in the dirt: soil amoebae interactions with Paracoccidioides spp. PLoS Negl Trop Dis. 2019; 13(10): e0007742. and Cryptococcus species,183183. da Silva A, Nobre Jr H, Sampaio L, Nascimento B, da Silva C, de Andrade Neto JB, et al. Antifungal and antiprotozoal green amino acid-based rhamnolipids: mode of action, antibiofilm efficiency and selective activity against resistant Candida spp. strains and Acanthamoeba castellanii. Colloids Surf B Biointerfaces. 2020; 193: 111148.,187187. Derengowski LS, Paes HC, Albuquerque P, Tavares AHFP, Fernandes L, Silva-Pereira I, et al. The transcriptional response of Cryptococcus neoformans to ingestion by Acanthamoeba castellanii and macrophages provides insights into. Eukaryot Cell. 2013; 12(5): 761-74.,188188. Rizzo J, Albuquerque PC, Wolf JM, Nascimento R, Pereira MD, Nosanchuk JD, et al. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol. 2017; 121(6-7): 602-14. all associated with Acanthamoeba. Some of these reports highlight that fungi-FLA interactions in the environment mimic those found between fungi and host cells, possibly contributing to the development of virulence and immune escape strategies.187187. Derengowski LS, Paes HC, Albuquerque P, Tavares AHFP, Fernandes L, Silva-Pereira I, et al. The transcriptional response of Cryptococcus neoformans to ingestion by Acanthamoeba castellanii and macrophages provides insights into. Eukaryot Cell. 2013; 12(5): 761-74.,188188. Rizzo J, Albuquerque PC, Wolf JM, Nascimento R, Pereira MD, Nosanchuk JD, et al. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol. 2017; 121(6-7): 602-14.,189189. Ribeiro NS, Santos FM, Garcia AWA, Ferrareze PAG, Fabres LF, Schrank A, et al. Modulation of zinc homeostasis in Acanthamoeba castellanii as a possible antifungal strategy against Cryptococcus gattii. Front Microbiol. 2017; 8: 1-11.
One study identified Pseudomonas in Acanthamoeba isolates.8686. Maschio VJ, Corção G, Rott MB. Identification of Pseudomonas spp. as amoeba-resistant microorganisms in isolates of Acanthamoeba. Rev Inst Med Trop São Paulo. 2015; 57(1): 81-3. Another survey adopted a co-culture model between this FLA genus and methicillin-resistant Staphylococcus aureus, showing mutual effects on cell growth or differentiation.190190. Souza TK, Soares SS, Benitez LB, Rott MB. Interaction between methicillin-resistant Staphylococcus aureus (MRSA) and Acanthamoeba polyphaga. Curr Microbiol. 2017; 74(5): 541-9. A third report investigated the role of a K(+) transporter gene in the nutrient uptake and replication of Legionella pneumophila inside A. castellanii.191191. Hori JI, Pereira MSF, Roy CR, Nagai H, Zamboni DS, Celular B, et al. Identification and functional characterization of K(+) transporters encoded by Legionella pneumophila kup genes. Cell Microbiol. 2013; 15(12): 2006-19.
Several reports on ARMs (30/39) have comprised the giant viruses, placing this topic as a highlight in the auxiliary category. Relevant contributions included new virus species and lineages described after prospection in Brazilian environments.192192. Silva LKDS, Rodrigues RAL, Andrade ACDSP, Hikida H, Andreani J, Levasseur A, et al. Isolation and genomic characterization of a new mimivirus of lineage B from a Brazilian river. Arch Virol. 2020; 165(4): 853-63.
193. Boratto PVM, Arantes TS, Silva LCF, Assis FL, Kroon EG, La Scola B, et al. Niemeyer virus: a new mimivirus group A isolate harboring a set of duplicated aminoacyl-tRNA synthetase genes. Front Microbiol. 2015; 6: 1-11.
194. Boratto PVM, Oliveira GP, Machado TB, Andrade ACSP, Baudoin J-P, Klose T, et al. Yaravirus: a novel 80-nm virus infecting Acanthamoeba castellanii. Proc Natl Acad Sci. 2020; 117(28): 202001637.
195. Campos RK, Boratto PV, Assis FL, Aguiar ERGR, Silva LCF, Albarnaz JD, et al. Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon. Virol J. 2014; 11(1): 1-11.
196. Abrahão J, Silva L, Silva LS, Khalil JYB, Rodrigues R, Arantes T, et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun. 2018; 9(1): 749.
197. Mougari S, Bekliz M, Abrahao J, Di Pinto F, Levasseur A, La Scola B. Guarani Virophage, a new sputnik-like isolate from a Brazilian lake. Front Microbiol. 2019; 10: 1003.
198. Rolland C, Andreani J, Louazani AC, Aherfi S, Francis R, Rodrigues R, et al. Discovery and further studies on Giant Viruses at the IHU mediterranee infection that modified the perception of the virosphere. Viruses. 2019; 11(4): 312.-199199. Abrahão J, Silva L, Oliveira D, Almeida G. Lack of evidence of mimivirus replication in human PBMCs. Microbes Infect. 2018; 20(5): 281-3. Exploring variable aspects of interaction, a set of reports addressed the morphological description of viral attachment, replication, and release200200. Souza F, Rodrigues R, Reis E, Lima M, La Scola B, Abrahão J. In-depth analysis of the replication cycle of Orpheovirus. Virol J. 2019; 16(1): 1-11.
201. Silva LCF, Araújo R, Rodrigues L, Oliveira GP, Dornas FP, La Scola B, et al. Microscopic analysis of the Tupanvirus cycle in Vermamoeba vermiformis. 2019; 10: 1-9.
202. Andrade ACDSP, Rodrigues RAL, Oliveira GP, Andrade KR, Bonjardim CA, La Scola B, et al. Filling gaps about mimivirus entry, uncoating and morphogenesis. J Virol. 2017; 22: e01355-17.
203. Schrad JR, Young EJ, Abrahão JS, Cortines JR, Parent KN. Microscopic characterization of the Brazilian giant samba virus. Viruses. 2017; 9(30): 1-16.
204. Borges I, Rodrigues RAL, Dornas FP, Almeida G, Aquino I, Bonjardim CA, et al. Trapping the enemy: Vermamoeba vermiformis circumvents Faustovirus mariensis dissemination by enclosing viral progeny inside cysts. J Virol. 2019; 93(14): 1-19.
205. Rodrigues RAL, Silva LKS, Dornas FP, Oliveira DB, Magalhães TFF, Santos DA, et al. Mimivirus fibrils are important for viral attachment to the microbial world by a diverse glycoside interaction repertoire. J Virol. 2015; 89(23): 11812-9.
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So far, no literature review was devoted to critically analysing the Brazilian publications on the FLA topic, although two1818. Rayamajhee B, Subedi D, Peguda HK, Willcox MD, Henriquez FL, Carnt N. A systematic review of intracellular microorganisms within Acanthamoeba to understand potential impact for infection. Pathogens. 2021; 10(2): 1-26.,223223. Saberi R, Seifi Z, Dodangeh S, Najafi A, Abdollah Hosseini S, Anvari D, et al. A systematic literature review and meta-analysis on the global prevalence of Naegleria spp. in water sources. Transbound Emerg Dis. 2020; 67: 2389-402. out of four literature reviews on Vermamoeba spp,224224. Delafont V, Rodier MH, Maisonneuve E, Cateau E. Vermamoeba vermiformis: a free-living amoeba of interest. Microbial Ecology. 2018; 76: 991-1001.Naegleria,1515. Gharpure R, Bliton J, Goodman A, Ali IKM, Yoder J, Cope JR. Epidemiology and clinical characteristics of primary amebic meningoencephalitis caused by Naegleria fowleri: a global review. Clin Infect Dis. 2020; 73(1): e19-27.,223223. Saberi R, Seifi Z, Dodangeh S, Najafi A, Abdollah Hosseini S, Anvari D, et al. A systematic literature review and meta-analysis on the global prevalence of Naegleria spp. in water sources. Transbound Emerg Dis. 2020; 67: 2389-402. and Acanthamoeba1818. Rayamajhee B, Subedi D, Peguda HK, Willcox MD, Henriquez FL, Carnt N. A systematic review of intracellular microorganisms within Acanthamoeba to understand potential impact for infection. Pathogens. 2021; 10(2): 1-26. mentioned the country, several Brazilian reports are missing in the latest literature reviews.
Conclusions and directions - The present work is the first literature review devoted to critically integrating and debating FLA data produced in Brazil. The data described here outlined the main scientific issues related to FLA research in Brazil since the first publication in 1974 and covering the last 46 years. Even though several FLA genera were reported during this study period, most papers were related to Acanthamoeba, and the wet-bench investigations predominated.
Regarding the clinical reports, we believe there are many under-reported cases of FLA infections in Brazil, including keratitis and encephalitis cases, as previously suggested by retrospective studies. In addition, the possibility of pathogenic intra-amoebic microorganisms isolated from clinical FLA strains increases the potential of FLA-ARM interaction to be harmful to human health. Due to that, it is urgent to narrow the relations between researchers and clinicians, universities, hospitals, and medical laboratories in the country, aiming to close monitoring cases of FLA diseases, or even bacterial, fungal, and viruses infections likely carried through amoebas.
The Brazilian epidemiologic surveys on FLA in water collections did not consider the limnologic data on the samples. It is advisable for policymakers and environmental regulatory departments to integrate the efforts towards improving the knowledge on amoeba distribution. In this direction, understanding the correlation between amoeba presence and environmental characteristics may contribute to better evaluating public health risk areas. Finally, national funding opportunities and distribution across Brazil are extremely important to boost the spread of FLA research in the country and contribute to public health awareness.
ACKNOWLEDGEMENTS
To Marina Elisa de Oliveira for the support provided during the establishment of the protocol in StArt tool.
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Financial support: OHT had financial support from Biota-Fapesp Program (Process # 2018/20693-4); JLM had support from Red de Investigación Cooperativa en Enfermedades Tropicales - RICET, Spain (project # RD16/0027/0001, Programe Redes Temáticas de Investigación Cooperativa, FIS); Consorcio Centro de Investigación Biomédica en Red - CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, Spain (Project # CB21/13/00100); Ministerio de Sanidad, Gobierno de España; and Cabildo de Tenerife, Tenerife innova, Marco Estratégico de Desarrollo Insular-MEDI, Fondo de Desarrollo de Canarias -FDCAN (Project # 21/0587).
Publication Dates
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Publication in this collection
01 July 2022 -
Date of issue
2022
History
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Received
22 Nov 2021 -
Accepted
28 Mar 2022