Surrogate Selection for Foot-and-Mouth Disease Virus in Disinfectant Efficacy Tests by Simultaneous Comparison of Bacteriophage MS2 and Bovine Enterovirus Type 1

In South Korea, testing disinfectants against foot-and-mouth disease virus (FMDV) that are contagious in livestock or that require special attention with respect to public hygiene can be manipulated only in high-level containment laboratories, which are not easily available. This causes difficulties in the approval procedure for disinfectants, such as a prolonged testing period. Additionally, the required biosafety level (BSL) in the case of FMDV has hindered its extensive studies. However, this drawback can be circumvented by using a surrogate virus to improve the performance of the efficacy testing procedure for disinfectants. Therefore, we studied bacteriophage MS2 (MS2) and bovine enterovirus type 1 (ECBO) with respect to disinfectant susceptibility for selecting a surrogate for FMDV according to the Animal and Plant Quarantine Agency (APQA) guidelines for efficacy testing of veterinary disinfectants. Effective concentrations of the active substances in disinfectants (potassium peroxymonosulfate, sodium dichloroisocyanurate, malic acid, citric acid, glutaraldehyde, and benzalkonium chloride) against FMDV, MS2, and ECBO were compared and, efficacies of eight APQA-listed commercial disinfectants used against FMDV were examined. The infectivity of FMDV and ECBO were confirmed by examination of cytopathic effects, and MS2 by plaque assay. The results reveal that the disinfectants are effective against MS2 and ECBO at higher concentrations than in FMDV, confirming their applicability as potential surrogates for FMDV in efficacy testing of veterinary disinfectants.

[1]  V. Schmidt,et al.  Use of the European standardization framework established by CEN/TC 216 for effective disinfection strategies in human medicine, veterinary medicine, food hygiene, industry, and domestic and institutional use – a review , 2022, GMS hygiene and infection control.

[2]  M. Her,et al.  Virucidal efficacy of potassium peroxymonosulfate, sodium dichloroisocyanurate, glutaraldehyde, and quaternary ammonium compounds against Newcastle disease virus , 2022, Journal of the Preventive Veterinary Medicine.

[3]  M. Her,et al.  Modified Vaccinia Virus Ankara as a Potential Biosafety Level 2 Surrogate for African Swine Fever Virus in Disinfectant Efficacy Tests , 2022, Pathogens.

[4]  Siyun Wang,et al.  The efficacy of different sanitizers against MS2 bacteriophage introduced onto plastic or stainless steel surfaces , 2022, Current research in food science.

[5]  S. Blome,et al.  The Efficacy of Disinfection on Modified Vaccinia Ankara and African Swine Fever Virus in Various Forest Soil Types , 2021, Viruses.

[6]  Gabrielle M. String,et al.  Selection of a SARS-CoV-2 Surrogate for Use in Surface Disinfection Efficacy Studies with Chlorine and Antimicrobial Surfaces , 2021, Environmental science & technology letters.

[7]  Liuyu Huang,et al.  Resistance of Poliovirus 1 and Enterovirus A71 Against Alcohol and Other Disinfectants. , 2021, Journal of virological methods.

[8]  E. Chrobak,et al.  Novel betulin dicarboxylic acid ester derivatives as potent antiviral agents: Design, synthesis, biological evaluation, structure-activity relationship and in-silico study. , 2021, European journal of medicinal chemistry.

[9]  D. Yoo,et al.  Epidemiological Characteristics of Foot-and-Mouth Disease in the Republic of Korea, 2014-2019. , 2021, Preventive veterinary medicine.

[10]  M. Her,et al.  Virucidal efficacy of acidic electrolyzed water (AEW) against African swine fever virus and avian influenza virus , 2020, The Journal of veterinary medical science.

[11]  L. Passvogel,et al.  Virucidal efficacy of different formulations for hand and surface disinfection targeting SARS CoV-2 , 2020, bioRxiv.

[12]  M. Dharmasena,et al.  Efficacy of novel aqueous photo‐chlorine dioxide against a human norovirus surrogate, bacteriophage MS2 and Clostridium difficile endospores, in suspension, on stainless steel and under greenhouse conditions , 2020, Journal of applied microbiology.

[13]  Jason Y. C. Lim,et al.  Sanitizing agents for virus inactivation and disinfection , 2020, View.

[14]  G. Woźniakowski,et al.  Virucidal effect of chosen disinfectants against African swine fever virus (ASFV) - preliminary studies. , 2019, Polish journal of veterinary sciences.

[15]  R. Mickelsen,et al.  The use of bacteriophage MS2 for the development and application of a virucide decontamination test method for porous and heavily soiled surfaces , 2019, Journal of applied microbiology.

[16]  D. Lantagne,et al.  Selection of a Biosafety Level 1 (BSL-1) surrogate to evaluate surface disinfection efficacy in Ebola outbreaks: Comparison of four bacteriophages , 2017, PloS one.

[17]  R. Davies,et al.  Efficacy of disinfectants and detergents intended for a pig farm environment where Salmonella is present. , 2017, Veterinary microbiology.

[18]  D. Patnayak,et al.  Efficacy of three disinfectants against Senecavirus A on five surfaces and at two temperatures , 2017, Journal of Swine Health and Production.

[19]  M. Ramakrishnan Determination of 50% endpoint titer using a simple formula. , 2016, World journal of virology.

[20]  Ocspp,et al.  Guidance to Registrants: Process for Making Claims Against Emerging Viral Pathogens not on EPA-Registered Disinfectant Labels , 2015 .

[21]  S. Lamaudière,et al.  Comparison of the virucidal efficacy of peracetic acid, potassium monopersulphate and sodium hypochlorite on bacteriophages P001 and MS2 , 2015, Journal of applied microbiology.

[22]  T. Morin,et al.  Prevalence of Human Noroviruses in Frozen Marketed Shellfish, Red Fruits and Fresh Vegetables , 2014, Food and Environmental Virology.

[23]  T. Morin,et al.  Prevalence of Human Noroviruses in Frozen Marketed Shellfish, Red Fruits and Fresh Vegetables , 2014, Food and Environmental Virology.

[24]  M. Janes,et al.  A double layer plaque assay using spread plate technique for enumeration of bacteriophage MS2. , 2014, Journal of virological methods.

[25]  S. Lamaudière,et al.  Comparison of the virucidal efficiency of peracetic acid, potassium monopersulfate and sodium hypochlorite on hepatitis A and enteric cytopathogenic bovine orphan virus , 2013, Journal of applied microbiology.

[26]  C. Gantzer,et al.  Removal of MS2, Qβ and GA bacteriophages during drinking water treatment at pilot scale. , 2012, Water research.

[27]  Luis L. Rodriguez,et al.  Disinfection of foot-and-mouth disease and African swine fever viruses with citric acid and sodium hypochlorite on birch wood carriers. , 2012, Veterinary microbiology.

[28]  Luis L. Rodriguez,et al.  Chemical disinfection of high-consequence transboundary animal disease viruses on nonporous surfaces. , 2011, Biologicals : journal of the International Association of Biological Standardization.

[29]  D. D'Souza,et al.  Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. , 2010, Foodborne pathogens and disease.

[30]  R H Davies,et al.  A comparison of the efficacy of different disinfection methods in eliminating Salmonella contamination from turkey houses , 2009, Journal of applied microbiology.

[31]  V. Thomas,et al.  Disinfection efficacy against parvoviruses compared with reference viruses. , 2009, The Journal of hospital infection.

[32]  M. Le Potier,et al.  Virucidal efficacy of nine commercial disinfectants against porcine circovirus type 2. , 2008, Veterinary journal.

[33]  S. Sattar Hierarchy of susceptibility of viruses to environmental surface disinfectants: a predictor of activity against new and emerging viral pathogens. , 2007, Journal of AOAC International.

[34]  M. S. Beato,et al.  Inactivation of Avian Influenza Viruses by Chemical Agents and Physical Conditions: A Review , 2007, Zoonoses and public health.

[35]  J. Steinmann Surrogate viruses for testing virucidal efficacy of chemical disinfectants , 2004, Journal of Hospital Infection.

[36]  E. Kaleta,et al.  Evaluation of virucidal activity of three commercial disinfectants and formic acid using bovine enterovirus type 1 (ECBO virus), mammalian orthoreovirus type 1 and bovine adenovirus type 1. , 2003, Veterinary journal.

[37]  E. Domingo,et al.  Foot-and-mouth disease virus. , 2002, Comparative immunology, microbiology and infectious diseases.

[38]  P. Maris Modes of action of disinfectants. , 1995, Revue scientifique et technique.

[39]  C. Dolea,et al.  World Health Organization , 1949, International Organization.

[40]  M. Her,et al.  Method development for efficacy testing of veterinary disinfectants using bacteriophage MS2 , 2021 .

[41]  T. Carpenter,et al.  Financial Impact of Foot-and-mouth disease outbreaks on pig farms in the Republic of Korea, 2014/2015. , 2018, Preventive veterinary medicine.

[42]  P. Lekcharoensuk,et al.  Inactivation of Foot-and-Mouth Disease Virus by Commercially Available Disinfectants and Cleaners. , 2015, Biocontrol science.

[43]  M. Penrith,et al.  Manual on procedures for disease eradication by stamping out , 2001 .