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  • 1 National Public Health Center, Hungary
  • | 2 Szent István University, Hungary
Open access

The protista Acanthamoeba is a free-living amoeba existing in various environments. A number of species among protista are recognized as human pathogens, potentially causing Acanthamoeba keratitis (AK), granulomatous amoebic encephalitis (GAE), and chronic granulomatous lesions. In this study, 10 rhizosphere samples were collected from maize and alfalfa plants in experimental station at Institute of Genetics, Microbiology and Biotechnology, Szent István University. We detected Acanthamoeba based on the quantitative real-time PCR assay and sequence analysis of the 18S rRNA gene. All studied molecular biological methods are suitable for the detection of Acanthamoeba infection in humans. The quantitative real-time PCR-based methods are more sensitive, simple, and easy to perform; moreover, these are opening avenue to detect the effect of number of parasites on human disease. Acanthamoeba species were detected in five (5/10; 50%) samples. All Acanthamoeba strains belonged to T4 genotype, the main AK-related genotype worldwide. Our result confirmed Acanthamoeba strains in rhizosphere that should be considered as a potential health risk associated with human activities in the environment.

Abstract

The protista Acanthamoeba is a free-living amoeba existing in various environments. A number of species among protista are recognized as human pathogens, potentially causing Acanthamoeba keratitis (AK), granulomatous amoebic encephalitis (GAE), and chronic granulomatous lesions. In this study, 10 rhizosphere samples were collected from maize and alfalfa plants in experimental station at Institute of Genetics, Microbiology and Biotechnology, Szent István University. We detected Acanthamoeba based on the quantitative real-time PCR assay and sequence analysis of the 18S rRNA gene. All studied molecular biological methods are suitable for the detection of Acanthamoeba infection in humans. The quantitative real-time PCR-based methods are more sensitive, simple, and easy to perform; moreover, these are opening avenue to detect the effect of number of parasites on human disease. Acanthamoeba species were detected in five (5/10; 50%) samples. All Acanthamoeba strains belonged to T4 genotype, the main AK-related genotype worldwide. Our result confirmed Acanthamoeba strains in rhizosphere that should be considered as a potential health risk associated with human activities in the environment.

Introduction

Acanthamoeba is a genus of free-living amoebae widely distributed in various ecological environments [13]. The life cycle of Acanthamoeba species (sp.) consists of the active trophozoites and dormant cysts stages. Acanthamoeba trophozoites have a size between 20 and 40 μm, although this range can vary significantly among isolates of different species genotypes. Cysts are double-walled and range in size from 10 and 20 μm. This difference in size between the cyst and trophozoite involves a significant loss of cell volume mail due to cellular dehydrations. Acanthamoeba spp. are thermotolerant, which are resistant to extreme temperature, pH conditions, UV, as well as to chlorine and other disinfectant media.

Most of the environmental studies are focusing on pathogenic Acanthamoeba sp. taxonomic and pathogenic markers, geographic distribution, ecology, and transmission dynamic [46]. Unlike obligate parasites, pathogenic Acanthamoeba spp. can complete their life cycle, environmental performance without having to enter the human or animal host [7, 8]. The genus Acanthamoeba has been currently classified into 21 different genotypes, T1–T21, based on 18S rRNA nucleotide sequence [9, 10]. Some genera of Acanthamoeba cause different infections, which produce Acanthamoeba keratitis (AK), subacute or chronic granulomatous amoebic encephalitis, and skin infections. Human infections with these amoebae have been reported from all over the world [11]. The first cases that clearly established Acanthamoeba as causative agents of disease in humans have been reported in the early 1970s [12]. In many cases, AK infections occur after water exposure or a history of swimming in lakes, following contact with soil or plants, or while wearing contact lenses [13, 14].

In general, Acanthamoeba are metabolically active and use a wide variety of bacteria, fungi, and organic matter as a food source [15].

Therefore, in this study, high microbial activities showing rhizosphere soil used for isolation protozoan organisms to test their occurrences are not in human host. Moreover, the isolated strains morphologically characterized by electron microscopy molecularly characterized based on the 18S rRNA gene sequence and the robust phylogenetic analysis was also measured.

Materials and Methods

Samples collection

Rhizosphere samples were collected from experimental station at Institute of Genetics, Microbiology and Biotechnology, Szent István University (longitude: 19°21′39.85″, latitude: 47°35′37′63″) in June 27, 2018. Rhizosphere samples were taken from the depth of 0–20 cm. During the sampling period, altogether 10 samples from rhizosphere of maize and alfalfa plants samples were taken.

The sampling was performed, in which 10 samples were taken from rhizosphere of maize and alfalfa plants (notation: K1_1, K1_2, K1_3; K2_1, K2_2, K2_3; and L1_1, L1_2, L1_3, L2_1).

Culture-confirmed detection method

To concentrate Acanthamoeba spp., the samples were filtered, eluted, and centrifuged. Soil samples (1 g) collected from rhizosphere of maize and alfalfa plants were dissolved in 10 ml of sterile physiological saline solution (0.85%) buffer and 500 μl of each sample was inoculated onto PAGE agar 9-cm plates seeded with heat-killed Escherichia coli and incubated at 36 °C [16].

Microscopic detection

Samples were examined under a microscope for 72–96 h at 400× with an inverted ZEISS microscope (Figure 1).

Figure 1.
Figure 1.

Photomicrograph of Acanthamoeba trophozoites (A) and cysts (B) with 400× magnification. Photographer: Erika Orosz

Citation: Acta Microbiologica et Immunologica Hungarica AMicr 67, 3; 10.1556/030.66.2019.041

Molecular analysis

The Acanthamoeba species were isolated by dilution method. For this purpose, the samples of soil (1 g) were suspended in 10 ml of sterile physiological saline solution (0.85%). After preparation, the DNA extraction was treated with High Pure PCR Template Preparation Kit (Germany), according to the instructions of the manufacturer. If further processing was delayed, the isolates were stored at 4 °C for 24 h or at –20 °C for a longer period. The DNA amplification was performed using genus-specific primers and genus-specific fluorescence resonance energy transfer (FRET) hybridization probes, previously described by Orosz et al. [17]. Each experiment included one reaction mixture without DNA as a negative control; positive control and each specimen were run in duplicate for real-time PCR assay in parallel. We have used serial dilutions of Acanthamoeba (GenBank accession number: KC434439) strain to determine the calibration curve that the liquid chromatography device could determine the additional samples parasite number in copy numbers.

PCR products were purified with PCR Clean up-M Kit (Viogene, Sunville, CA). The sequence of each amplicon was determined by cycle sequencing with primers for the 5′-NTR region and with primers with BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, Germany), according to the manufacturer’s instruction. The electrophoresis was carried out on Applied Biosystems 3500 Genetic Analyzer (Applied Biosystems, Budapest, Hungary).

The 5′-NTR and VP1 gene sequences were subject to nucleotide–nucleotide BLAST analysis [18] using the online server at the National Center for Biotechnology Information (http://blast.ncbi.nlm.nih.gov/Blast).

The unknown sequences were aligned with known published sequences of the major genotypes using the alignment program MULTALIN (http://multalin.toulouse.inra.fr/multalin) [19]. The genotypes of samples were determined based on this comparison.

The phylogenetic tree was constructed by the neighbor-joining method of genetic distance calculated by the MEGA 6 (http://www.megasoftware.net) [20].

Genotype identification was carried out with a real-time FRET PCR assay based on sequence analysis of the 18S rRNA gene, and sensitivity and specificity were evaluated in comparison with traditional parasitological techniques.

Results

Microscopic detection

All investigated samples revealed Acanthamoeba were able to grow at 36 °C, the approximate temperature of the human organism. Microscopically 5 out of the 10 samples were declared as Acanthamoeba positive (Medicago sativa – L1_2, L1_3 and Zea mays – K1_2, K2_1, K2_3). Five rhizosphere samples (Medicago sativa – L1_1, L1_3 and Zea mays – K1_1, K1_3, K2_2) were microscopically negative. Further examination of the obtained results was conducted by FRET PCR.

Molecular analysis

This study reports successful PCR amplification for 5 (5/10; 50.0%) positive cases. The samples of five Acanthamoeba – positive samples, detected by PCR method, were sequenced to identify the species. Sequence analysis using a BLAST search indicated an identity of >98% with Acanthamoeba 18r rRNA gene reference sequences. It was found that all obtained sequences of amoebae isolates from the cases belong to the different T4 genotypes Acanthamoeba spp. Neighbor-joining analysis inferred relationships between the PCR products isolated from rhizosphere samples reference strains obtained from NCBI GenBank, shown in Figure 2, respectively.

Figure 2.
Figure 2.

Phylogenetic relations of Acanthamoeba species PCR product sample L1_2, sample L1_3, sample K2_1, sample K2_1, sample K2_3, and reference strains from NCBI GenBank inferred by neighbor-joining analysis from pairwise comparisons (180-bp fragments)

Citation: Acta Microbiologica et Immunologica Hungarica AMicr 67, 3; 10.1556/030.66.2019.041

Discussion and Conclusions

Studies of Acanthamoeba have grown exponentially. To the best of our knowledge, this is the second study of occurrence of Acanthamoeba similar to T4 genotypes in rhizosphere samples from Hungary. These organisms have gained attention from the broad scientific community studying environmental biology, molecular biology, and biochemistry. Literature describes T4 genotype Acanthamoeba, as the most common in the environment. These results are consistent with previous findings indicating that T4 is worldwide predominant [2124].

However, the correct understanding of the factors influencing the occurrence of the different species appears of great concern, as these amoebae are free-living organisms, and their potential capabilities to cause severe infections of the central nervous system, ocular keratitis, and other disorders are now ascertained worldwide.

All the isolates in this study exhibited morphological features of the genus Acanthamoeba confirmed by means of quantitative real-time PCR. Quantitative real-time PCR with FRET hybridization probes method is the most sensitive with a short turnaround time. It is possible even to estimate the parasite number in the samples with method. Therefore, only molecular methods allow reliable differentiation of the Acanthamoeba species. Based on rRNA gene sequences, the genus Acanthamoeba is divided into 21 different genotypes to date (T1–T21). Each genotype exhibits 5% or more sequence divergence between different genotypes. Five isolates were characterized as similar to genotype T4 due to their strict correspondence to the reference sequences of this genotype (GenBank accession number: KJ786514, KU936114, KJ786526, and MF197424). Sequence date indicate that the vast majority of them causes human infections. Contrary to data on Acanthamoeba infections in humans, little is known about infections in rhizosphere. It has been concluded that the rhizosphere isolates are most closely related to strains commonly isolated from human infections, especially AK [2529].

In conclusion, our results confirm and support previous report on Acanthamoeba genotype free-living amoeba in rhizosphere soil. A homologous analysis of the 18S rRNA of five Acanthamoeba species isolated from rhizosphere of maize and alfalfa was identified into one genotype, namely T4. These genotypes were associated with AK or encephalitis; therefore, the presence of Acanthamoeba should be considered as potential health threat associated with human activity in soil.

Acknowledgements

This work was supported by Higher Education Institutional Excellence Program (NKFIH-1159-6/2019) awarded by the Ministry of Human Capacities within the framework of water-related researches of Szent István University.

Conflict of Interest:

There is no conflict of interest. The corresponding author assures that there are no links with a company whose product is mentioned in the article or a company that distributes a competing product. The presentation of the topic is independent and the presentation of the content is product-neutral.

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  • 1.

    Shatilovich, A., Shmakova, L., Gubin, S., Goodkov, A., Gilichinsky, D.: Viable protozoa in late Pleistocene and Holocene permafrost sediments. Dokl Biol Sci 401, 136138 (2005).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Siddiqui, R., Khan, N. A.: Biology and pathogenesis of Acanthamoeba. Parasit Vectors 10, 6 (2012).

  • 3.

    Reyes-Batlle, M., Zamora-Herrera, J., Vargas-Mesa, A., Valerón-Tejera, M. A., Wagner, C., Martín-Navarro, C. M., López-Arencibia, A., Sifaoui, I., Martínez-Carretero, E., Valladares, B., Piñero, J. E., Lorenzo-Morales, J.: Acanthamoeba genotypes T2, T4, and T11 in soil sources from El Hierro island, Canary Islands, Spain. Parasitol Res 115, 29532956 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Podlipaeva, J., Shmakova, L., Gilichinski, D., Goodkov, A.: Heat shock protein of hsp70 family revealed in some contemporary freshwater amoebae and in Acanthamoeba sp. from cysts isolated from permafrost samples. Tsitologiia 48, 691694 (2006).

    • Search Google Scholar
    • Export Citation
  • 5.

    Nuprasert, W., Putaporntip, C., Pariyakanok, L., Jongwutiwes, S.: Identification of a novel t17 genotype of Acanthamoeba from environmental isolates and t10 genotype causing keratitis in Thailand. J Clin Microbial 48, 46364640 (2010).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Visvesvara, G. S., Hercules, M., Schuster, F. L.: Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri and Sappinia diploidea. FEMS Immunol Med Microbiol 50, 126 (2007).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Alves, D. S., Moraes, A. S., Nitz, N., de Oliveira, M. G., Hecht, M. M., Gurgel-Gonçalves, R., Cuba, C. A.: Occurrence and characterization of Acanthamoeba similar to genotypes T4, T5, and T2/T6 isolated from environmental sources in Brasília. Exp Parasitol 131, 239244 (2012).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Karakavuk, M., Aykur, M., Şahar, E. A., Karakuş, M., Aldemir, D., Döndüren, Ö., Özdemir, H. G., Can, H., Gürüz, A. Y., Dağcı, H., Döşkaya, M.: First time identification of Acanthamoeba genotypes in the cornea samples of wild birds; Is Acanthamoeba keratitis making the predatory birds a target? Exp Parasitol 183, 137142 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Montoya, A., Miró, G., Saugar, J. M., Fernández, B., Checa, R., Gálvez, R., Bailo, B., Marino, V., Piñero, J. E., Lorenzo-Morales, J., Fuentes, I.: Detection and molecular characterization of Acanthamoeba spp. in stray cats from Madrid, Spain. Exp Parasitol 188, 812 (2018).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Corsaro, D., Köhsler, M., Di Filippo, MM., Venditti, D., Monno, R., Di Cave, D., Berrilli, F., Walochnik, J.: Update on Acanthamoeba jacobsi genotype T15, including full-length 18S rDNA molecular phylogeny. Parasitol Res 116, 12731284 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Khan, N. A., Jarroll, E. L., Paget, T. A.: Molecular and physiological differentiation between pathogenic and nonpathogenic Acanthamoeba. Curr Microbiol 45, 197202 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Jones, D., Visvesvara, G., Robinson, N.: Acanthamoeba polyphaga keratitis and Acanthamoeba uveitis associated with fatal meningoencephalitis. Trans Ophthalmol Soc UK 95, 221231 (1975).

    • Search Google Scholar
    • Export Citation
  • 13.

    Schroeder, J. M., Booton, G. C., Hay, J., Niszl, I. A., Seal, D. V., Markus, M. B., Fuerst, P. A., Byers, T. J.: 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 Microbial 39, 19031911 (2001).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Walochnik, J., Scheikl, U., Haller-Schober, E. M.: Twenty years of Acanthamoeba diagnostics in Austria. J Eukaryot Microbiol 62, 311 (2015).

  • 15.

    Neelam, S., Niederkorn, J. Y.: Pathobiology and immunobiology of Acanthamoeba keratitis: Insights from animal models. Yale J Biol Med 90, 261268 (2017).

    • Search Google Scholar
    • Export Citation
  • 16.

    Page, F. C.: A New Key to Freshwater and Soil Gymnamoebae. Freshwater Biological Association, Ambleside, Cumbria, 1988, 122 p.

  • 17.

    Orosz, E., Farkas, Á., Ködöböcz, L., Becsák, P., Danka, J., Kucsera, I., Füleky, G.: Isolation of Acanthamoeba from the rhizosphere of maize and lucerne plants. Acta Microbiol Immunol Hung 60, 2939 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J.: Basic local alignment search tool. J Mol Biol 215, 403410 (1990).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Corpet, F.: Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16, 1088110890 (1988).

  • 20.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S.: MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30, 27252729 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Montalbano Di Filippo, M., Santoro, M., Lovreglio, P., Monno, R., Capolongo, C., Calia, C., Fumarola, L., D’Alfonso, R., Berrilli, F., Di Cave, D.: Isolation and molecular characterization of free-living amoebae from different water sources in Italy. Int J Environ Res Public Health 12, 34173427 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Üstüntürk-Onan, M., Walochnik, J.: Identification of free-living amoebae isolated from tap water in Istanbul, Turkey. Exp Parasitol 195, 3437 (2018).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Reyes-Batlle, M., Hernández-Piñero, I., Rizo-Liendo, A., López-Arencibia, A., Sifaoui, I., Bethencourt-Estrella, C. J., Chiboub, O., Valladares, B., Piñero, J. E., Lorenzo-Morales, J.: Isolation and molecular identification of free-living amoebae from dishcloths in Tenerife, Canary Islands, Spain. Parasitol Res 118, 927933 (2019).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Orosz, E., Farkas, Á., Kucsera, I.: Laboratory diagnosis of Acanthamoeba keratitis in Hungary. Acta Microbiol Immunol Hung 63, 293299 (2016).

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  • 25.

    Khan, N. A.: Acanthamoeba: Biology and increasing importance in human health. FEMS Microbiol Rev 30, 564595 (2006).

  • 26.

    Corsaro, D., Walochnik, J., Köhsler, M., Rott, M. B.: Acanthamoeba misidentification and multiple labels: Redefining genotypes T16, T19, and T20 and proposal for Acanthamoeba micheli sp. nov. (genotype T19). Parasitol Res 114, 24812490 (2015).

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  • 27.

    Orosz, E., Szentmáry, N., Kiss, H. J., Farkas, Á., Kucsera, I., Nagy, Z. Z.: First report of Acanthamoeba genotype T8 human keratitis. Acta Microbiol Immunol Hung 65, 7379 (2018).

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  • 28.

    Gyenes, A., Orosz, E., Sándor, G. L., Fries, F. N., Seitz, B., Nagy, Z. Z., Szentmáry, N.: Early diagnosis and successful medical treatment of Acanthamoeba keratitis. Klin Monbl Augenheilkd 235, 14071410 (2018).

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  • 29.

    Orosz, E., Kriskó, D., Shi, L., Sándor, G., Kiss, H. J., Seitz, B., Nagy, Z. Z., Szentmáry, N.: Clinical course of Acanthamoeba keratitis isolates T4 and T8 in Hungary. Acta Microbiol Immunol Hung 66, 289300 (2019).

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Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Zsuzsanna SCHAFF (2nd Department of Pathology, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary

Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu

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  • Science Citation Index Expanded
2020  
Total Cites 662
WoS
Journal
Impact Factor
2,048
Rank by Immunology 145/162(Q4)
Impact Factor Microbiology 118/137 (Q4)
Impact Factor 1,904
without
Journal Self Cites
5 Year 0,671
Impact Factor
Journal  0,38
Citation Indicator  
Rank by Journal  Immunology 146/174 (Q4)
Citation Indicator  Microbiology 120/142 (Q4)
Citable 42
Items
Total 40
Articles
Total 2
Reviews
Scimago 28
H-index
Scimago 0,439
Journal Rank
Scimago Immunology and Microbiology (miscellaneous) Q4
Quartile Score Medicine (miscellaneous) Q3
Scopus 438/167=2,6
Scite Score  
Scopus General Immunology and Microbiology 31/45 (Q3)
Scite Score Rank  
Scopus 0,760
SNIP
Days from  225
sumbission
to acceptance
Days from  118
acceptance
to publication
Acceptance 19%
Rate

2019  
Total Cites
WoS
485
Impact Factor 1,086
Impact Factor
without
Journal Self Cites
0,864
5 Year
Impact Factor
1,233
Immediacy
Index
0,286
Citable
Items
42
Total
Articles
40
Total
Reviews
2
Cited
Half-Life
5,8
Citing
Half-Life
7,7
Eigenfactor
Score
0,00059
Article Influence
Score
0,246
% Articles
in
Citable Items
95,24
Normalized
Eigenfactor
0,07317
Average
IF
Percentile
7,690
Scimago
H-index
27
Scimago
Journal Rank
0,352
Scopus
Scite Score
320/161=2
Scopus
Scite Score Rank
General Immunology and Microbiology 35/45 (Q4)
Scopus
SNIP
0,492
Acceptance
Rate
16%

 

Acta Microbiologica et Immunologica Hungarica
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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation
1954
Publication
Programme
2021 Volume 68
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

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