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New insight into genetic variation and haplotype diversity of Fasciola hepatica from Algeria

  • Genetics, Evolution, and Phylogeny - Original Paper
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Abstract

The liver fluke Fasciola hepatica is the main cause of fasciolosis in North Africa leading to significant economic losses and public health problems. In this study, the ribosomal internal transcribed spacer (ITS), cytochrome c oxidase I (COI), the mitochondrial region spanning the COI-trnT-rrnL, and the NADH dehydrogenase subunit I (NADI) markers were used to characterize Fasciola flukes from Algeria. Fasciola appeared widespread from the east to the west of Algeria. Among 1701 sampled cattle from 8 Algerian provinces, 5% were infected. Using morphological and morphometric analysis, one morphotype of Fasciola was observed. Nuclear ITS marker indicated that all collected flukes belong to F. hepatica. Multiple alignments of ITS dataset revealed two haplotypes, one described here for the first time. Analysis of molecular variance (AMOVA) of mitochondrial markers revealed weak population structure in Algeria. Mismatch distributions, neutrality tests, and median-joining network analysis all were compatible with a recent expansion of Algerian F. hepatica population. Fasciolosis appeared common in Algerian cattle, it seems that the absence of control strategy coupled to the favorable Mediterranean climate may lead to a reconstruction and dispersion of its populations. This study provides important results concerning the genetic characterization and variability of F. hepatica in Algeria as well as the significant role of cattle importation in shaping its dispersal route worldwide.

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References

  • Ai L, Weng YB, Elsheikha HM, Zhao GH, Alasaad S, Chen JX, Li J, Li HL, Wang CR, Chen MX, Lin RQ, Zhu XQ (2011) Genetic diversity and relatedness of Fasciola spp. isolates from different hosts and geographic regions revealed by analysis of mitochondrial DNA sequences. Vet Parasitol 181(2–4):329–334

    Article  CAS  PubMed  Google Scholar 

  • Ai L, Cai Y-C, Lu Y, Chen J-X, Chen S-H (2017) Human Cases of Fascioliasis in Fujian Province, China. Korean J Parasitol 55(1):55–60

    Article  PubMed  PubMed Central  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723

    Article  Google Scholar 

  • Alasaad S, Huang CQ, Li QY, Granados JE, Garcia-Romero C, Perez JM, Zhu XQ (2007) Characterization of Fasciola samples from different host species and geographical localities in Spain by sequences of internal transcribed spacers of rDNA. Parasitol Res 101(5):1245–1250

    Article  CAS  PubMed  Google Scholar 

  • Ali H, Ai L, Song HQ, Ali S, Lin RQ, Seyni B, Issa G, Zhu XQ (2008) Genetic characterisation of Fasciola samples from different host species and geographical localities revealed the existence of F. hepatica and F. gigantica in Niger. Parasitol Res 102(5):1021–1024

    Article  CAS  PubMed  Google Scholar 

  • Amer S, Dar Y, Ichikawa M, Fukuda Y, Tada C, Itagaki T, Nakai Y (2011) Identification of Fasciola species isolated from Egypt based on sequence analysis of genomic (ITS1 and ITS2) and mitochondrial (NDI and COI) gene markers. Parasitol Int 60(1):5–12

    Article  CAS  PubMed  Google Scholar 

  • Amer S, ElKhatam A, Zidan S, Feng Y, Xiao L (2016) Identity of Fasciola spp. in sheep in Egypt. Parasit Vectors 9(1):623

    Article  PubMed  PubMed Central  Google Scholar 

  • Amor N, Halajian A, Farjallah S, Merella P, Said K, Slimane BB (2011) Molecular characterization of Fasciola spp. from the endemic area of northern Iran based on nuclear ribosomal DNA sequences. Exp Parasitol 128:196–204

    Article  CAS  PubMed  Google Scholar 

  • Arafa WM, Hassan AI, Snousi SAM, El-Dakhly KM, Holman PJ, Craig TM, Aboelhadid SM (2018) Fasciola hepatica infections in cattle and the freshwater snail Galba truncatula from Dakhla Oasis, Egypt. J Helminthol 92:56–63

    Article  CAS  PubMed  Google Scholar 

  • Aryaeipour M, Bozorgomid A, Kazemi B, Behnia M, Azizi H, Rokni MB (2017) Molecular and morphometrical characterization of Fasciola species isolated from domestic ruminants in Ardabil Province, northwestern Iran. Iran J Public Health 46(3):318–325

    PubMed  PubMed Central  Google Scholar 

  • Asadian S, Mohebali M, Mahmoudi M, Kia EB, Heidari Z, Asgari M, Aryaeipour M, Moradi S, Rokni MB (2013) Seroprevalence of human fascioliasis in Meshkin-Shahr district, Ardabil Province, northwestern Iran in 2012. Iran J Parasitol 8(4):516–521

    PubMed  PubMed Central  Google Scholar 

  • Ashrafi K, Valero MA, Panova M, Periago MV, Massoud J, Mas-Coma S (2006) Phenotypic analysis of adults of Fasciola hepatica, Fasciola gigantica and intermediate forms from the endemic region of Gilan Iran. Parasitol Int 55:249–260

    Article  CAS  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bargues MD, Gayo V, Sanchis J, Artigas P, Khoubbane M, Birriel S, Mas-Coma S (2017) DNA multigene characterization of Fasciola hepatica and Lymnaea neotropica and its fascioliasis transmission capacity in Uruguay, with historical correlation, human report review and infection risk analysis. PLoS Negl Trop Dis 11(2):e0005352. https://doi.org/10.1371/journal.pntd.0005352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beesley NJ, Williams DJL, Paterson S, Hodgkinson JE (2017) Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow, possible implications for drug resistance. Int J Parasitol 47:11–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173

    Article  CAS  PubMed  Google Scholar 

  • Carnevale S, Malandrini JB, Pantano ML, Soria CC, Rodrigues-Silva R, Machado-Silva JR, Velasquez JN, Kamenetzky L (2017) First genetic characterization of Fasciola hepatica in Argentina by nuclear and mitochondrial gene markers. Vet Parasitol 245:34–38

    Article  CAS  PubMed  Google Scholar 

  • Coghlan A, Tyagi R, Cotton JA, Holroyd N, Rosa BA, Tsai IJ, Laetsch DR, Beech RN, Day TA, Hallsworth-Pepin K, et al (2019) Comparative genomics of the major parasitic worms. Nat Genet 51(1):163–174

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dosay-Akbuluta M, Trudgettb A, Stanhope M (2005) Understanding genetic diversity of the liver fluke Fasciola hepatica. Z Naturforsch 60:774–778

    Article  Google Scholar 

  • El-Rahimy HH, Mahgoub AM, El-Gebaly NSM, Mousa WM, Antably AS (2012) Molecular, biochemical, and morphometric characterization of Fasciola species potentially causing zoonotic disease in Egypt. Parasitol Res 111(3):1103–1111

    Article  PubMed  Google Scholar 

  • ElTahawy AS, Bazh EK, Khalafalla RE (2017) Epidemiology of bovine fascioliasis in the Nile Delta region of Egypt: Its prevalence, evaluation of risk factors, and its economic significance. Vet World 10(10):1241–1249

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinforma 1:47–50

    Article  CAS  Google Scholar 

  • Farjallah S, Sanna D, Amor N, Ben Mehel B, Piras MC, Merella P, Casu M, Curini-Galletti M, Said K, Garippa G (2009) Genetic characterization of Fasciola hepatica from Tunisia and Algeria based on mitochondrial and nuclear DNA sequences. Parasitol Res 105:1617–1621

    Article  PubMed  Google Scholar 

  • Farjallah S, Ben Slimane B, Piras CM, Amor N, Garippa G, Merella P (2013) Molecular characterization of Fasciola hepatica from Sardinia based on sequence analysis of genomic and mitochondrial gene markers. Exp Parasitol 135:471–478

    Article  CAS  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gabli A, Agabou A, Gabli Z (2015) Brucellosis in nomadic pastoralists and their goats in two provinces of the eastern Algerian high plateaus. Trop Anim Health Prod 47(6):1043–1048

    Article  PubMed  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SeaView and Phylowin, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    CAS  PubMed  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights for sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Hamed N, Ayadi A, Hammami H (2014) Epidemiological studies on fasciolosis in northern Tunisia. Revue Méd Vét 165(1–2):49–56

    Google Scholar 

  • Hayashi K, Ichikawa-Seki M, Mohanta UK, Singh TS, Shoriki T, Sugiyama H, Itagaki T (2015) Molecular phylogenetic analysis of Fasciola flukes from eastern India. Parasitol Int 64:334–338

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Mohanta UK, Neeraja T, Itagaki T (2016) Molecular characterization of Fasciola gigantica in Delhi, India and its phylogenetic relation to the species from South Asian countries. J Vet Med Sci 78(9):1529–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa-Seki M, Ortiz P, Cabrera M, Hobán C, Itagaki T (2016) Molecular characterization and phylogenetic analysis of Fasciola hepatica from Peru. Parasitol Int 65(3):171–174

    Article  CAS  PubMed  Google Scholar 

  • Ichikawa-Seki M, Peng M, Hayashi K, Shoriki T, Mohanta UK, Shibahara T, Itagaki T (2017) Nuclear and mitochondrial DNA analysis reveals that hybridization between Fasciola hepatica and Fasciola gigantica occurred in China. Parasitology 144:206–213

    Article  CAS  PubMed  Google Scholar 

  • Itagaki T, Kikawa M, Sakaguchi K, Shimo J, Terasaki K, Shibahara T, Fukuda K (2005) Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131(05):679–685

    Article  CAS  PubMed  Google Scholar 

  • Januszkiewicz K, Norbury LJ, P Wilkowski, Zawistowska-Deniziak A, Wesołowska A, Wedrychowicz H (2015) Variations in cercarial production and the level of in vitro activation of metacercariae of two different isolates of Fasciola hepatica. Acta Parasitologica 60(3):509–514. https://doi.org/10.1515/ap-2015-0072

  • Kardjadj M (2018) History of Foot-and-mouth disease in North African countries. Vet Ital 54(1):1–12. https://doi.org/10.12834/VetIt.928.4711.2.

    Article  PubMed  Google Scholar 

  • Labruna MB, Costa F, Port-Carvalho M, Oliveira A, Souza S, Castro M (2018) Lethal fascioliasis in capybaras (Hydrochoerus hydrochaeris) in Brazil. J Parasitol 104(2):173–176

    Article  CAS  PubMed  Google Scholar 

  • Le TH, Blair D, Agatsuma T, Humair PF, Campbell NJ, Iwagami M, Littlewood DT, Peacock B, Johnston DA, Bartley J, Rollinson D, Herniou EA, Zarlenga DS, McManus DP (2000) Phylogenies inferred from mitochondrial gene orders-a cautionary tale from the parasitic flatworms. Mol Biol Evol 17(7):1123–1125

    Article  CAS  PubMed  Google Scholar 

  • Le TH, Nguyen KT, Nguyen NT, Doan HT, Le XT, Hoang CT, De NV (2012) Development and evaluation of a single-step duplex PCR for simultaneous detection of Fasciola hepatica and Fasciola gigantica (family Fasciolidae, class Trematoda, phylum Platyhelminthes). J Clin Microbiol 50:2720–2726

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5. A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu GH, Gasser RB, Young ND, Song HQ, Ai L, Zhu XQ (2014) Complete mitochondrial genomes of the ‘intermediate form’ of Fasciola and Fasciola gigantica, and their comparison with F. hepatica. Parasit Vectors 7(1):150

    Article  PubMed  PubMed Central  Google Scholar 

  • Lotfy WM, Brant SV, DeJong RJ, Le TH, Demiaszkiewicz A, Rajapakse RP, Perera VB, Laursen JR, Loker ES (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). Am J Trop Med Hyg 79(2):248–255

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Valladares M, Rojo-Vázquez FA (2014) Intraspecific mitochondrial DNA variation of Fasciola hepatica eggs from sheep with different level of anthelmintic resistance. Parasitol Res 113(7):2733–2741

    Article  PubMed  Google Scholar 

  • Mas-Coma S, Bargues MD (1997) Human liver flukes: a review. Res Rev Parasitol 57:145–218

    Google Scholar 

  • Mas-Coma S, Valero MA, Bargues MD (2008) Effects of climate change on animal and zoonotic helminthiases. Rev Sci Tech 27(2):443–457

    Article  CAS  PubMed  Google Scholar 

  • Mas-Coma S, Valero MA, Bargues MD (2009) Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69:41–146

    Article  PubMed  Google Scholar 

  • Mehmood K, Zhang H, Sabir AJ, Abbas RZ, Ijaz M, Durrani AZ, Saleem MH, Rehman MU, Iqbal MK, Wang Y, Ahmad HI, Abbas T, Hussain R, Ghori MT, Ali S, Khan AU, Li J (2017) A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microb Pathog 109:253–262

    Article  PubMed  Google Scholar 

  • Meissonnier E, Mage C (2007) Methods of detection of Fasciola hepatica in cattle in France. Bull Acad Vét France 160:395–406

    Article  Google Scholar 

  • Mekroud A, Benakhla A, Vignoles P, Rondeleaud D (2004) Preliminary studies on the prevalences of natural fasciolosis in cattle, sheep, and the host snail Galba truncatula in north-eastern Algeria. Parasitol Res 92:502–505

    Article  CAS  PubMed  Google Scholar 

  • Moazeni M, Sharifiyazdi H, Izadpanah A (2012) Characterization of Fasciola hepatica genotypes from cattle and sheep in Iran using cytochrome C oxidase gene (CO1). Parasitol Res 110:2379–2384

    Article  PubMed  Google Scholar 

  • Mucheka VT, Lamb JM, Pfukenyi DM, Mukaratirwa S (2015) DNA sequence analyses reveal co-occurrence of novel genotypes of Fasciola gigantica (Fasciolidae; Echinostomida; Trematoda) with F. hepatica in South Africa and Zimbabwe. Vet Parasitol 214(1–2):144–151

    Article  PubMed  Google Scholar 

  • Nyindo M, Lukambagire AH (2015) Fascioliasis: an ongoing zoonotic trematode infection. Biomed Res Int 2015:1–8. https://doi.org/10.1155/2015/786195

    Article  Google Scholar 

  • Ohari Y, Hayashi K, Mohanta UK, Kuwahara Y, Itagaki T (2017) First report of Fasciola larva infection in Galba truncatula (Muller, 1774) (Gastropoda, Lymnaeidae) occurring in the natural environment in Hokkaido, Japan. J Vet Med Sci 79(8):1381–1383

    Article  PubMed  PubMed Central  Google Scholar 

  • Omar MA, Metwally AM, Sultan K (2013) Molecular and phylogenetic status of Fasciola sp., of cattle in Qena, Upper Egypt Pak. J Biol Sci 16(15):726–730

    Google Scholar 

  • Ouchene-Khelifi NA, Ouchene N, Dahmani H, Dahmani A, Sadi M, Douifi M (2018) Fasciolosis due to Fasciola hepatica in ruminants in abattoirs and its economic impact in two regions in Algeria. Trop Biomed 35(1):181–187

    PubMed  Google Scholar 

  • Peng M, Ichinomiya M, Ohtori M, Ichikawa M, Shibahara T, Itagaki T (2009) Molecular characterization of Fasciola hepatica, Fasciola gigantica, and aspermic Fasciola sp. in China based on nuclear and mitochondrial DNA. Parasitol Res 105(3):809–815

    Article  PubMed  Google Scholar 

  • Righi S, Benakhla A, Mekroud A, Ouchene N, Sedraoui S (2016) Prevalence of Fasciola hepatica in Galba truncatula detected by multiplex PCR in the province of El Tarf (Algeria). Trop Biomed 33:149–158

    PubMed  Google Scholar 

  • Rokni M, Mirhendi H, Behnia M, Jalalizand N (2010) Molecular characterization of Fasciola hepatica isolates by RAPD-PCR and ribosomal ITS1 sequencing. Iran Red Crescent Med J 2010(1):27–32

    Google Scholar 

  • Rouhani S, Raeghi S, Spotin A (2017) Spermatogenic and phylo-molecular characterizations of isolated Fasciola Spp. from Cattle, North West Iran. Pak J Biol Sci 20(4):204–209

    Article  CAS  PubMed  Google Scholar 

  • Samuel AR, Knowles NJ, MacKay DKJ (1999) Genetic analysis of type O viruses responsible for epidemics of foot-and-mouth disease in North Africa. Epidemiol Infect 122:529–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkari B, Parhoode M, Abdolahi Khabisi S, Shafiei R, Mohammadi-Ghalehbin B (2017) Genetic diversity of Fasciola spp. isolates from northern part of Iran: comparison with southwestern isolates. J Parasit Dis 41(3):768–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shafiei R, Sarkari B, Sadjjadi SM, MowlaviGh R, Moshfe A (2014) Molecular and Morphological Characterization of Fasciola spp. isolated from different host species in a newly emerging focus of human fascioliasis in Iran. Vet Med Int 2014:1–10. https://doi.org/10.1155/2014/405740

    Article  CAS  Google Scholar 

  • Simsek S, Utuk AE, Balkaya I (2011) Molecular differentiation of Fasciola hepatica and Fasciola gigantica by PCR-RFLP and DNA sequence analysis. Helmintologia 48(1):3–7

    Article  Google Scholar 

  • Srairi MT, Benyoucef MT, Kraiem K (2013) The dairy chains in North Africa (Algeria, Morocco and Tunisia): from self-sufficiency options to food dependency? Springer Plus 162(2):1–13

    Google Scholar 

  • Stamatakis A (2006) Raxml-vi-hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) A Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Valero MA, Bargues MD, Calderon L, Artigas P, Mas-Coma S (2018) First phenotypic and genotypic description of Fasciola hepatica infecting highland cattle in the state of Mexico, Mexico Infect. Genet Evol 64:231–240

    Article  Google Scholar 

  • Vilas R, Vázquez-Prieto S, Paniagua E (2012) Contrasting patterns of population genetic structure of Fasciola hepatica from cattle and sheep: implications for the evolution of anthelmintic resistance. Infect Genet Evol 12:45–52

    Article  PubMed  Google Scholar 

  • Wannasan A, Khositharattanakool P, Chaiwong P, Piangjai S, Uparanukraw P, Morakote N (2014) Identification of Fasciola species based on mitochondrial and nuclear DNA reveals the co-existence of intermediate Fasciola sp. and Fasciola gigantica in Thailand. Exp Parasitol 146:64–70

    Article  CAS  PubMed  Google Scholar 

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Funding

The project was financially supported by the Vice Deanship of Research Chairs, Deanship of Scientific Research of the King Saud University

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Authors and Affiliations

  1. Animal Health and Productions Laboratory, High National Veterinary School-Algiers, B.P. 228, Oued Samar, Algiers, Algeria

    Linda Chougar, Khaled Harhoura & Miriem Aissi

  2. KSU Mammals Research Chair, Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Nabil Amor & Abdulaziz N. Alagaili

  3. Research Unit of Integrative Biology and Evolutionary and Functional Ecology of Aquatic Systems, Faculty of Science of Tunis, University of Tunis El Manar, Tunis, Tunisia

    Nabil Amor & Sarra Farjallah

  4. Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, Via Vienna 2, 07100, Sassari, Italy

    Paolo Merella

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  1. Linda Chougar
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Correspondence to Nabil Amor.

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Figure 1.

Consensus trees constructed with NJ method showing phylogenetic relationships among F. hepatica and F. gigantica. Phylogenies inferred from COI (a) NADI (b) and COI-trnT-rrnL (c) sequences. Numbers shown at nodes of branches are bootstrap values. Fascioloides magna (COI, NADI and COI-trnT-rrnL) was used as outgroup. (PNG 194 kb)

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Chougar, L., Amor, N., Farjallah, S. et al. New insight into genetic variation and haplotype diversity of Fasciola hepatica from Algeria. Parasitol Res 118, 1179–1192 (2019). https://doi.org/10.1007/s00436-019-06270-5

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