Skip to main content

Advertisement

SpringerLink
Log in

Occurrence of Staphylococcus spp. and investigation of fecal and animal viral contaminations in livestock, river water, and sewage from Tunisia and Romania

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The objective of this study was to determine the occurrence of Staphylococcus spp., Escherichia coli, somatic coliphages, F-specific RNA bacteriophages, hepatitis E virus (HEV), and bovine enterovirus (BEV) in fecal and water samples. The occurrence of Staphylococcus spp. was investigated in treated wastewater samples collected from slaughterhouse of Tunisia. Results showed that Staphylococcus spp. were detected in the totality of collected samples with an average mean of 5.44 Log10 (CFU/100 ml). Regarding fecal indicator bacteria, E. coli was detected in the totality of water samples and was more abundant in Tunisian samples than in samples collected from Romania (P < 0.05). Concerning somatic coliphages and F-specific RNA bacteriophages used as viral indicators, they were detected in all raw and treated wastewaters. Bovine enterovirus (BEV) was detected in 20.1% and 28% of bovine stool samples collected from Tunisia and Romania, respectively. BEV was also detected in 60% of porcine stool samples from Romania. BEV was absent in all treated sewage samples. HEV was detected in raw sewage and bovine fecal sample from Romania with low occurrence and none sample from Tunisia was positive. This study may give us an insight into the monitoring of water quality in Tunisia and Romania.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abebe, R., Hatiya, H., Abera, M., Megersa, B., & Asmare, K. (2016). Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at Hawassa milk shed, South Ethiopia. BMC Veterinary Research, 12(1), 270. https://doi.org/10.1186/s12917-016-0905-3.

    Article  Google Scholar 

  • Aziz, F., Rubio, J. P., Ouazani, N., Dary, M., Manany, H., Morgado, B. R., & Mandi, L. (2016). Sanitary impact evaluation of drinking water in storage reservoir in Morrocan rural area. Saudi Journal of Biological Sciences, 24(4), 767–777. https://doi.org/10.1016/j.sjbs.2016.01.034.

    Article  Google Scholar 

  • Béji-Hamza, A., Hassine-Zaafrane, M., Khelifi-Gharbi, H., Della Libera, S., Iaconelli, M., Muscillo, M., Petricca, S., Ciccaglione, A. R., Bruni, R., Taffon, S., Aouni, M., & La Rosa, G. (2015). Hepatitis E virus genotypes 1 and 3 in wastewater samples in Tunisia. Archives for Virology, 160(1), 183–189. https://doi.org/10.1007/s00705-014-2251-8.

    Article  CAS  Google Scholar 

  • Ben Said, M., Abbassi, M. S., Gómez, P., Ruiz-Ripa, L., Sghaier, S., Ibrahim, C., Torres, C., & Hassen, A. (2017). Staphylococcus aureus isolated from wastewater treatment plants in Tunisia: occurrence of human and animal associated lineages. Journal of Water and Health, 15(4), 638–643. https://doi.org/10.2166/wh.2017.258.

    Article  Google Scholar 

  • Brinkman, N. E., Fout, G. S., & Keely, S. P. (2017). Retrospective surveillance of wastewater to examine seasonal dynamics of enterovirus infections. mSphere. https://doi.org/10.1128/mSphere.00099-17.

  • Brion, G. M., Meschke, J. S., & Sobsey, M. D. (2002). F-specific RNA coliphages: occurrence, types, and survival in natural waters. Water Research, 36(9), 2419–2425. https://doi.org/10.1016/s0043-1354(01)00547-4.

    Article  CAS  Google Scholar 

  • Costan-Longares, A., Mocé-Livina, L., Avellon, A., Jofre, J., & Luecena, F. (2008). Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. Journal of Applied Microbioly, 105(6), 1945–1955. https://doi.org/10.1111/j.1365-2672.2008.03954.x.

    Article  CAS  Google Scholar 

  • Gentry-Shieds, J., Myers, K., Pisanic, N., Heaney, C., & Stewart, J. (2015). Hepatitis E virus and coliphages in waters proximal to swine concentrated animal feeding operations. Science of the Total Environment, 505(1), 487–493. https://doi.org/10.1016/j.scitotenv.2014.10.004.

    Article  CAS  Google Scholar 

  • Gómez, P., Lozano, C., Benito, D., Estepa, V., Tenorio, C., Zarazaga, M., & Torres, C. (2016). Characterization of staphylococci in urban wastewater treatment plants in Spain, with detection of methicillin resistant Staphylococcus aureus ST398. Environmental Pollution, 212, 71–76. https://doi.org/10.1016/j.envpol.2016.01.038.

    Article  CAS  Google Scholar 

  • Hmaied, F., Keskes, S., Jebri, S., Amri, I., Yahya, M., Loisy-Hamon, F., Lebeau, B., & Hamdi, M. (2015). Removal of rotavirus and bacteriophages by membrane bioreactor technology from sewage. Current Microbiology, 71(5), 540–545. https://doi.org/10.1007/s00284-015-0882-y.

    Article  CAS  Google Scholar 

  • Inoue, J., Masaharu, T., Yasuyuki, Y., Tsud, F., & Okamoto, H. (2006). Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. Journal of Virological Methods, 137(2), 325–333. https://doi.org/10.1016/j.jviromet.2006.07.004.

    Article  CAS  Google Scholar 

  • ISO. (1995). ISO 10705–1: water quality - detection and enumeration of bacteriophages - part 1: Enumeration of FSpecific RNA bacteriophages. Geneva: International Organisation for Standardisation.

    Google Scholar 

  • ISO. (2000). ISO 10705–2: water quality - detection and enumeration of bacteriophages - part 2: enumeration of somatic coliphages. Geneva: International Organisation for Standardisation.

    Google Scholar 

  • Jebri, S., Hmaied, F., Jofre, J., Yahya, M., Mendez, J., Barkallah, I., & Hamdi, M. (2013). Effect of gamma irradiation on bacteriophages used as viral indicators. Water Research, 47(11), 3673–3678. https://doi.org/10.1016/j.watres.2013.04.036.

    Article  CAS  Google Scholar 

  • Jebri, S., Hmaied, F., Yahya, M., Ben Ammar, A., & Hamdi, M. (2016). Total coliphages removal by activated sludge process and their morphological diversity by transmission electron microscopy. Water Science and Technology, 74(2), 318–323. https://doi.org/10.2166/wst.2016.178.

    Article  CAS  Google Scholar 

  • Julian, R., & Schwab, K. (2012). Challenges in environmental detection of human viral pathogens. Current Opinion in Virology, 2(1), 78–83. https://doi.org/10.1016/j.coviro.2011.10.027.

    Article  CAS  Google Scholar 

  • Kirs, M., & Smith, C. (2006). Multiplex quantitative real-time reverse transcriptase PCR for F+-specific RNA coliphages: a method for use in microbial source tracking. Applied and Environmental Microbiology, 73(3), 808–814. https://doi.org/10.1128/AEM.00399-06.

    Article  CAS  Google Scholar 

  • Knowles, N. J., Hovi, T., Hyypia, T., Kuig, A. M. Q., Lindberg, A. M., Pallansch, M. A., Palmenberg, A. C., Simmonds, P., Skern, T., & Stanway, G. (2012). Picornaviridae. In A. M. Q. King, M. J. Adams, E. B. Carstens, & E. J. Lefkowitz (Eds.), Virus taxonomy: classification and nomenclature of viruses: ninth report (pp. 855–880). San Diego: Elsevier.

    Google Scholar 

  • Kumar, R., Yadav, B. R., & Singh, R. S. (2011). Antibiotic resistance and pathogenicity factors in Staphylococcus aureus isolated from mastitic Sahiwal cattle. Journal of Biosciences, 36(1), 175–188. https://doi.org/10.1007/s12038-011-9004-6.

    Article  CAS  Google Scholar 

  • Kuroda, K., Nakada, N., Hanamoto, S., Inaba, M., Katayama, H., Do, A. T., Nga, T. T., Oguma, K., Hayashi, T., & Takizawa, S. (2015). Pepper mild mottle virus as an indicator and a tracer of fecal pollution in water environments: comparative evaluation with wastewater-tracer pharmaceuticals in Hanoi, Vietnam. Science of the Total Environment, 15(506–507), 287–298. https://doi.org/10.1016/j.scitotenv.2014.11.021.

    Article  CAS  Google Scholar 

  • Ley, V., Higgins, J., & Fayer, R. (2002). Bovine enteroviruses as indicators of fecal contamination. Applied and Environmental Microbiology, 68(7), 3455–3461. https://doi.org/10.1128/aem.68.7.3455-3461.2002.

    Article  CAS  Google Scholar 

  • Li, M., Baker, C. A., Danyluk, M. D., Belanger, P., Boelaert, F., Cressey, P., Gheorghe, M., Polkinghorne, B., Toyofuku, H., & Havelaar, A. H. (2018). Identification of biological hazards in produce consumed in industrialized countries: a review. Journal of Food Protection, 81, 1171–1186. https://doi.org/10.4315/0362-028X.JFP-17-465.

    Article  Google Scholar 

  • Mandilara, G. D., Smeti, E. M., Mavridou, A. T., Lambiri, M. P., Vatopoulos, A. C., & Rigas, F. O. (2006). Correlation between bacterial indicators and bacteriophages in sewage and sludge. FEMS Microbiology Letters, 263, 119–126. https://doi.org/10.1111/j.1574-6968.2006.00414.x.

    Article  CAS  Google Scholar 

  • Masclaux, F. G., Hotz, P., Friedli, D., Savova-Bianchi, D., & Oppliger, A. (2013). High occurrence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses. Water Research, 47, 5101–5109. https://doi.org/10.1016/j.watres.2013.05.050.

    Article  CAS  Google Scholar 

  • Mellado, V., Yanez, M. A., & Catalan, V. (2006). Evaluation of the MicroFoss system for the analysis of Escherichia coli in water. Microbiological Research, 161, 20–24. https://doi.org/10.1016/j.micres.2005.04.001.

    Article  CAS  Google Scholar 

  • Meng, X. J. (2011). From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Research, 161, 23–30. https://doi.org/10.1016/j.virusres.2011.01.016.

    Article  CAS  Google Scholar 

  • Meng, X. J., Anderson, D. A., & Arankalle, V. A. (2011). Hepeviridae. In A. M. Q. King, M. J. Adams, E. B. Carstens, & E. J. Lefkowitz (Eds.), Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses (pp. 1021–1028). San Diego: Elsevier.

    Google Scholar 

  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., Decastelli, L., Mioni, R., Scuota, S., Bolzoni, G., Di Giannatale, E., Salinetti, A. P., La Salandra, G., Bartoli, M., Zuccon, F., Pirino, T., Sias, S., Parisi, A., Quagliaa, N. C., & Celano, G. V. (2005). Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 98, 73–79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008.

    Article  CAS  Google Scholar 

  • Park, J., Friendship, R. M., Poljak, Z., Weese, J. S., & Dewey, C. E. (2013). An investigation of exudative epidermitis (greasy pig disease) and antimicrobial resistance patterns of Staphylococcus hyicus and Staphylococcus aureus isolated from clinical cases. Canadian Veterinary Journal, 54(2), 139–144.

    Google Scholar 

  • Peel, B. J., Bothwell, G. C., Simmons, & Frost, A. (1975). A study of the number and phage patterns of Staphylococcus aureus in an abattoir. Australian Veterinary Journal, 51(3), 126–130. https://doi.org/10.1111/j.1751-0813.1975.tb09433.x.

    Article  CAS  Google Scholar 

  • Purcell, R. H., & Emerson, S. U. (2008). Hepatitis E: an emerging awareness of 415 an old disease. Journal of Hepatology, 48(3), 494–503. https://doi.org/10.1016/j.jhep.2007.12.008.

    Article  CAS  Google Scholar 

  • Qadir, M., Wichelns, D., Raschid-Sally, L., McCornick, P. G., Drechsel, P., Bahri, A., & Minhas, P. S. (2010). The challenges of wastewater irrigation in developing countries. Agricultural Water Management, 97(4), 561–568.

    Article  Google Scholar 

  • Renault, F., Morin-Crini, N., Badot, P. M., & Crini, G. (2010). Non-conventional sorbents for dye removal. In G. Crini & P. M. Badot (Eds.), Sorption processes and pollution. Conventionnal and non-conventionnal sorbents for pollutant removal from wastewaters (pp. 187–205). Besançon: Presses Universitaires de Franche-Comté.

  • Rodrıguez-Lazaro, D., Cook, N., Ruggeri, F. M., Sellwood, J., Nasser, A., Nascimento, M. S. J., D’Agostino, M., & Santos, R. (2012). Virus hazards from food, water and other contaminated environments. FEMS Microbiology Reviews, 36(4), 786–814. https://doi.org/10.1111/j.1574-6976.2011.00306.x.

    Article  CAS  Google Scholar 

  • Savey, M., Martin, P., & Desenclos, J .(2010). De l’agent zoonotique aux zoonoses. Diversité et unicité d’un concept en pleine evolution. BHE hors série 3–5.

  • Schmidt, T., Kock, M. M., & Ehlers, M. M. (2015). Diversity and antimicrobial susceptibility profiling of staphylococci isolated from bovine mastitis cases and close human contacts. Journal of Dairy Science, 98(9), 1–14. https://doi.org/10.3168/jds.2015-9715.

    Article  CAS  Google Scholar 

  • Steyer, A., Naglič, T., Močilnik, T., Poljšak-Prijatelj, M., & Poljak, M. (2011). Hepatitis E virus in domestic pigs and surface waters in Slovenia: prevalence and molecular characterization of a novel genotype 3 lineage. Infection, Genetics and Evolution, 11(7), 1732–1737. https://doi.org/10.1016/j.meegid.2011.07.007.

    Article  CAS  Google Scholar 

  • Tran, N. H., Gin, K. Y., & Ngo, H. H. (2015). Fecal pollution source tracking toolbox for identification, evaluation and characterization of fecal contamination in receiving urban surface waters and groundwater. Science of the Total Environment, 538, 38–57. https://doi.org/10.1016/j.scitotenv.2015.07.155.

    Article  CAS  Google Scholar 

  • Troillet, N. (2014). Infections transmises par les chats et les chiens. Revue Médicale Suisse, 10, 1859–1863.

    CAS  Google Scholar 

  • Tymensen, L., Calvin, W. B., Sherry, J. H., Shaun, R. C., Rahat, Z., Ron, R., & Mc Allister, A. (2017). Environmental growth of enterococci and Escherichia coli in feedlot catch basins and a constructed wetland in the absence of fecal input. Environmental Science and Technology, 51(10), 5386–5395. https://doi.org/10.1021/acs.est.6b06274.

    Article  CAS  Google Scholar 

  • USEPA (2015) Review of coliphages as possible indicators of fecal contamination for ambient water quality EPA office of water (820-R-15-098).

  • Yahya, M., Hmaied, F., Jebri, S., Jofre, J., & Hamdi, M. (2015). Bacteriophages as indicators of human and animal faecal contamination in raw and treated wastewaters from Tunisia. Journal of Applied Microbiology, 118(5), 1217–1225. https://doi.org/10.1111/jam.12774.

    Article  CAS  Google Scholar 

  • Zhang, H., Liu, H., Bao, J., Guo, Y., Peng, T., Zhou, P., Zhang, W., Ma, B., Wang, J., & Gao, M. (2014). Characterization of an Enterovirus species E isolated from naturally infected bovine in China. Virus Research, 191, 101–107. https://doi.org/10.1016/j.virusres.2014.07.032.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We really appreciate George Nadăş and Roba Dana for their help and collaboration. This work was performed in the framework of international project between Tunisia and Romania.

Funding

This research was supported by the National Center of Nuclear Sciences and Technology as well as by Faculty of Veterinary Medicine of Cluj-Napoca, Romania. Faten RAHMANI received a travel fellowship from the “Eugen Ionescu” program granted by the Central and Eastern Europe Office of the University Agency of Francophonie.

Author information

Authors and Affiliations

  1. Laboratoire Biotechnologies et Technologie Nucléaire, CNSTN, Pôle Technologique Sidi Thabet, 2020, Sidi Thabet, Tunisia

    Faten Rahmani, Fatma Hmaied, Mariem Yahya & Sihem Jebri

  2. Department of Microbiology, Faculty of Veterinary Medecine, University Agricultural Sciences and Veterinary Medecine, 3-5 Mănăştur Street, 400372, Cluj-Napoca, Romania

    Ioana Matei, Flore Chirila & Nicodim Fit

  3. Laboratoire de Parasitologie, Univ. Manouba, École Nationale de Médecine Vétérinaire de Sidi Thabet, 2020, Sidi Thabet, Tunisia

    Safa Amairia

  4. Laboratoire d’Ecologie et de Technologie Microbienne, Institut National Sciences Appliquées de Tunis, Université de Carthage, BP 676, 1080, Tunis, Tunisia

    Moktar Hamdi

  5. Faculté des Sciences de Tunis, Université El Manar, Tunis, Tunisia

    Faten Rahmani

Authors
  1. Faten Rahmani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatma Hmaied
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ioana Matei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Flore Chirila
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicodim Fit
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mariem Yahya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sihem Jebri
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Safa Amairia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Moktar Hamdi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatma Hmaied.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahmani, F., Hmaied, F., Matei, I. et al. Occurrence of Staphylococcus spp. and investigation of fecal and animal viral contaminations in livestock, river water, and sewage from Tunisia and Romania. Environ Monit Assess 192, 206 (2020). https://doi.org/10.1007/s10661-020-8172-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-020-8172-y

Keywords

Search

Navigation