Aqueous Extracts of Hibiscus sabdariffa Calyces to Control Aichi Virus
- 176 Downloads
- 2 Citations
Abstract
Aqueous Hibiscus sabdariffa extracts possess antimicrobial properties with limited information available on their antiviral effects. Aichi virus (AiV) is an emerging foodborne pathogen that causes gastroenteritis. Vaccines are currently unavailable to prevent their disease transmission. The objective of this study was to determine the antiviral effects of aqueous H. sabdariffa extracts against AiV. AiV at ~5 log PFU/ml was incubated with undiluted (200 mg/ml), 1:1 (100 mg/ml) or 1:5 (40 mg/ml) diluted aqueous hibiscus extract (pH 3.6), phosphate-buffered saline (pH 7.2 as control), or malic acid (pH 3.0, acid control) at 37 °C over 24 h. Treatments were stopped by serially diluting in cell-culture media containing fetal bovine serum and titers were determined using plaque assays on confluent Vero cells. Each treatment was replicated thrice and assayed in duplicate. AiV did not show any significant reduction with 1:1 (100 mg/ml) or 1:5 (40 mg/ml) diluted aqueous hibiscus extracts or malic acid after 0.5, 1, or 2 h at 37 °C. However, AiV titers were reduced to non-detectable levels after 24 h with all the three tested concentrations, while malic acid showed only 0.93 log PFU/ml reduction after 24 h. AiV was reduced by 0.5 and 0.9 log PFU/ml with undiluted extracts (200 mg/ml) after 2 and 6 h, respectively. AiV treated with 1:1 (100 mg/ml) and 1:5 (40 mg/ml) diluted extracts showed a minimal ~0.3 log PFU/ml reduction after 6 h. These extracts show promise to reduce AiV titers mainly through alteration of virus structure, though higher concentrations may have improved effects.
Keywords
Aichi virus Reduction Aqueous H. sabdariffa calycesNotes
Acknowledgments
The authors gratefully acknowledge the funding provided partly by the University of Tennessee-Institute of Agriculture (Multistate Project S1056). The authors also acknowledge Dr. Dunlap at UT-Advanced Microscopy Center for his assistance with the Transmission electron microscopy sample preparations and observations.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
This article does not contain any studies with human participants or animals that were performed by any of the authors.
Informed Consent
As this article does not contain any studies with human participants or animals performed by any of the authors, informed consent was not required.
References
- Ali, B. H., Al Wabel, N., & Blunden, G. (2005). Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: A review. [Review]. Phytotherapy Research, 19(5), 369–375. doi: 10.1002/ptr.1628.
- Blanton, L. H., Adams, S. M., Beard, R. S., Wei, G., Bulens, S. N., Widdowson, M. A., et al. (2006). Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000–2004. Journal of Infectious Diseases, 193(3), 413–421. doi: 10.1086/499315.CrossRefPubMedGoogle Scholar
- Borges, A., Ferreira, C., Saavedra, M. J., & Simoes, M. (2013). Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. [Research Support, Non-U.S. Gov’t]. Microbial Drug Resistance, 19(4), 256–265. doi: 10.1089/mdr.2012.0244.CrossRefPubMedGoogle Scholar
- Chao, C. Y., & Yin, M. C. (2009). Antibacterial effects of roselle calyx extracts and protocatechuic acid in ground beef and apple juice. Foodborne Pathogens and Disease, 6(2), 201–206. doi: 10.1089/fpd.2008.0187.CrossRefPubMedGoogle Scholar
- Chomnawang, M. T., Surassmo, S., Nukoolkarn, V. S., & Gritsanapan, W. (2005). Antimicrobial effects of Thai medicinal plants against acne-inducing bacteria. [Research Support, Non-U.S. Gov’t]. Journal of Ethnopharmacology, 101(1–3), 330–333. doi: 10.1016/j.jep.2005.04.038.CrossRefPubMedGoogle Scholar
- Cowan, M. M. (1999). Plant products as antimicrobial agents. [Review]. Clinical Microbiology Reviews, 12(4), 564–582.PubMedPubMedCentralGoogle Scholar
- Cromeans, T., Park, G. W., Costantini, V., Lee, D., Wang, Q., Farkas, T., et al. (2014). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environment Microbiology, 80(18), 5743–5751. doi: 10.1128/AEM.01532-14.CrossRefGoogle Scholar
- Da-Costa-Rocha, I., Bonnlaender, B., Sievers, H., Pischel, I., & Heinrich, M. (2014). Hibiscus sabdariffa L.—A phytochemical and pharmacological review. Food Chemistry, 165, 424–443. doi: 10.1016/j.foodchem.2014.05.002. Epub 2014 May 27.CrossRefPubMedGoogle Scholar
- Djeussi, D. E., Noumedem, J. A., Seukep, J. A., Fankam, A. G., Voukeng, I. K., Tankeo, S. B., et al. (2013). Antibacterial activities of selected edible plants extracts against multidrug-resistant Gram-negative bacteria. BMC Complementary and Alternative Medicine, 1013, 164. doi: 10.1186/1472-6882-13-164.CrossRefGoogle Scholar
- Fino, V. R., & Kniel, K. E. (2008). UV light inactivation of hepatitis A virus, Aichi virus, and feline calicivirus on strawberries, green onions, and lettuce. Journal of Food Protection, 71, 908–913.PubMedGoogle Scholar
- Fullerton, M., Khatiwada, J., Johnson, J. U., Davis, S., & Williams, L. L. (2011). Determination of antimicrobial activity of sorrel (Hibiscus sabdariffa) on Escherichia coli O157:H7 isolated from food, veterinary, and clinical samples. Journal of Medicinal Food, 14(9), 950–956. doi: 10.1089/jmf.2010.0200. Epub 2011 May 6.CrossRefPubMedPubMedCentralGoogle Scholar
- Goyer, M., Aho, L. S., Bour, J. B., Ambert-Balay, K., & Pothier, P. (2008). Seroprevalence distribution of Aichi virus among a French population in 2006–2007. Archives of Virology, 153, 1171–1174.CrossRefPubMedGoogle Scholar
- Hall, A. J., Wikswo, M. E., Pringle, K., Gould, L. H., Parashar, U. D., Division of Viral Diseases, N. C. f. I., et al. (2014). Vital signs: Foodborne norovirus outbreaks—United States, 2009–2012. MMWR. Morbidity and Mortality Weekly Report, 63(22), 491–495.PubMedGoogle Scholar
- Higginbotham, K. L., Burris, K. P., Zivanovic, S., Davidson, P. M., & Stewart, C. N, Jr. (2014a). Antimicrobial activity of Hibiscus sabdariffa aqueous extracts against Escherichia coli O157:H7 and Staphylococcus aureus in a microbiological medium and milk of various fat concentrations. [Research Support, Non-U.S. Gov’t]. Journal of Food Protection, 77(2), 262–268. doi: 10.4315/0362-028X.JFP-13-313.CrossRefPubMedGoogle Scholar
- Higginbotham, K. L., Burris, K. P., Zivanovic, S., Davidson, P. M., & Stewart, C. N, Jr. (2014b). Aqueous extracts of Hibiscus sabdariffa calyces as an antimicrobial rinse on hot dogs against Listeria monocytogenes and methicillin-resistant Staphylococcus aureus. Food Control, 40, 274–277. doi: 10.1016/j.foodcont.2013.12.011.CrossRefGoogle Scholar
- Joshi, S. S., Dice, L., & H D’Souza, D. (2015). Aqueous extracts of Hibiscus sabdariffa decrease hepatitis A virus and human norovirus titers. Food and Environmental Virology. E-pub ahead of print.Google Scholar
- Jung, E., Kim, Y., & Joo, N. (2013). Physicochemical properties and antimicrobial activity of Roselle (Hibiscus sabdariffa L.). Journal of the Science of Food and Agriculture, 293(15), 3769–3776. doi: 10.1002/jsfa.6256.CrossRefGoogle Scholar
- Kakkar, S., & Bais, S. (2014). A review on protocatechuic Acid and its pharmacological potential. [Review]. ISRN Pharmacology, 2014, 952943, doi: 10.1155/2014/952943.
- Kingsley, D. H., Chen, H., & Hoover, D. G. (2004). Inactivation of selected picornaviruses by high hydrostatic pressure. Virus Research, 102, 221–224.CrossRefPubMedGoogle Scholar
- Le Guyader, F. S., Le Saux, J. C., Ambert-Balay, K., Krol, J., Serais, O., Parnaudeau, S., et al. (2008). Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. Journal of Clinical Microbiology, 46(12), 4011–4017. doi: 10.1128/JCM.01044-08.CrossRefPubMedPubMedCentralGoogle Scholar
- Lin, H. H., Huang, H. P., Huang, C. C., Chen, J. H., & Wang, C. J. (2005). Hibiscus polyphenol-rich extract induces apoptosis in human gastric carcinoma cells via p53 phosphorylation and p38 MAPK/FasL cascade pathway. Molecular Carcinogenesis, 43(2), 86–99. doi: 10.1002/mc.20103.CrossRefPubMedGoogle Scholar
- Liu, K. S., Tsao, S. M., & Yin, M. C. (2005). In vitro antibacterial activity of roselle calyx and protocatechuic acid. Phytotherapy Research, 19(11), 942–945. doi: 10.1002/ptr.1760.CrossRefPubMedGoogle Scholar
- Lodder, W. J., Rutjes, S. A., Takumi, K., & de Roda Husman, A. M. (2013). Aichi virus in sewage and surface water, the Netherlands. Emerging Infectious Diseases, 19, 1222–1230.CrossRefPubMedPubMedCentralGoogle Scholar
- McKay, D. L., Chen, C. Y., Saltzman, E., & Blumberg, J. B. (2010). Hibiscus sabdariffa L. tea (tisane) lowers blood pressure in prehypertensive and mildly hypertensive adults. [Randomized Controlled TrialResearch Support, Non-U.S. Gov’tResearch Support, U.S. Gov’t, Non-P.H.S.]. Journal of Nutrition, 140(2), 298–303. doi: 10.3945/jn.109.115097.CrossRefPubMedGoogle Scholar
- Morton, J. (1987). Roselle. In Fruits of warm climates (pp. 281–286). Miami, FL.Google Scholar
- Oh, E.-G., Kim, K.-L., Shin, S., Son, K.-T., Lee, H.-J., Kim, T., et al. (2013). Antiviral activity of green tea catechins against feline calicivirus as a surrogate for norovirus. Food Science and Biotechnology, 22(2), 593–598. doi: 10.1007/s10068-013-0119-4.CrossRefGoogle Scholar
- Olaleye, M. (2007). Cytotoxicity and antibacterial activity of methanolic extract of Hibiscus sabdariffa. Journal of Medicinal Plants Research, 1, 9–13.Google Scholar
- Ravishankar, S., Jaroni, D., Zhu, L., Olsen, C., McHugh, T., & Friedman, M. (2012). Inactivation of Listeria monocytogenes on ham and bologna using pectin-based apple, carrot, and hibiscus edible films containing carvacrol and cinnamaldehyde. [Research Support, Non-U.S. Gov’tResearch Support, U.S. Gov’t, Non-P.H.S.]. Journal of Food Science, 77(7), M377–M382. doi: 10.1111/j.1750-3841.2012.02751.x.CrossRefPubMedGoogle Scholar
- Reuter, G., Boldizsar, A., Papp, G., & Pankovics, P. (2009). Detection of Aichi virus shedding in a child with enteric and extraintestinal symptoms in Hungary. Archives of Virology, 154, 1529–1532.CrossRefPubMedGoogle Scholar
- Reynolds, K. (2013). On tap: Aichi virus: Possible agent of unexplained cases of waterborne diarrhea. On Tap 55, 1, January 2013.Google Scholar
- Ribes, J. M., Montava, R., Tellez-Castillo, C. J., Fernandez-Jimenez, M., & Buesa, J. (2010). Seroprevalence of Aichi virus in a Spanish population from 2007 to 2008. Clinical and Vaccine Immunology, 17, 545–549.CrossRefPubMedPubMedCentralGoogle Scholar
- Saini, P., Gayen, P., Nayak, A., Kumar, D., Mukherjee, N., Pal, B. C., et al. (2012). Effect of ferulic acid from Hibiscus mutabilis on filarial parasite Setaria cervi: Molecular and biochemical approaches. [Research Support, Non-U.S. Gov’t]. Parasitology International, 61(4), 520–531. doi: 10.1016/j.parint.2012.04.002.CrossRefPubMedGoogle Scholar
- Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States—Major pathogens. Emerging Infectious Diseases, 17(1), 7–15. doi: 10.3201/eid1701.091101p1.CrossRefPubMedPubMedCentralGoogle Scholar
- Su, X., & D’Souza, D. H. (2011). Grape seed extract for control of human enteric viruses. Applied and Environment Microbiology, 77(12), 3982–3987. doi: 10.1128/AEM.00193-11.CrossRefGoogle Scholar
- Su, X., & D’Souza, D. H. (2013). Grape seed extract for foodborne virus reduction on produce. Food Microbiology, 34(1), 1–6. doi: 10.1016/j.fm.2012.10.006.CrossRefPubMedGoogle Scholar
- Su, X., Howell, A. B., & D’Souza, D. H. (2010a). Antiviral effects of cranberry juice and cranberry proanthocyanidins on foodborne viral surrogates—A time dependence study in vitro. Food Microbiology, 27(8), 985–991. doi: 10.1016/j.fm.2010.05.027.CrossRefPubMedGoogle Scholar
- Su, X., Howell, A. B., & D’Souza, D. H. (2010b). The effect of cranberry juice and cranberry proanthocyanidins on the infectivity of human enteric viral surrogates. Food Microbiology, 27(4), 535–540. doi: 10.1016/j.fm.2010.01.001.CrossRefPubMedGoogle Scholar
- Su, X., Sangster, M. Y., & D’Souza, D. H. (2011). Time-dependent effects of pomegranate juice and pomegranate polyphenols on foodborne viral reduction. Foodborne Pathogens and Disease, 8(11), 1177–1183. doi: 10.1089/fpd.2011.0873. Epub 2011 Jul 21.CrossRefPubMedGoogle Scholar
- Sunday, O. A., Munir, A. B., Akeeb, O., Bolanle, A., & Badaru, S. O. (2010). Antiviral effect of Hibiscus sabdariffa and Celosia argen tea on measles virus. African Journal of Microbiology Research, 4(4), 293–296.Google Scholar
- Švraka-Latifovic, Sanela. (2011). Thesis on: A systematic approach to elucidate causes of gastroenteritis outbreaks of suspected viral etiology. Tergooiziekenhuizen: RIVM, Erasmus University Rotterdam.Google Scholar
- Tsai, P.-J., McIntosh, J., Pearce, P., Camden, B., & Jordan, B. R. (2002). Anthocyanin and antioxidant capacity in Roselle (Hibiscus sabdariffa L.) extract. Food Research International, 35(4), 351–356. doi: 10.1016/S0963-9969(01)00129-6.CrossRefGoogle Scholar
- Yamashita, T., Adachi, H., Hirose, E., Nakamura, N., Ito, M., Yasui, Y., et al. (2014). Molecular detection and nucleotide sequence analysis of a new Aichi virus closely related to canine kobuvirus in sewage samples. Journal of Medical Microbiology, 63(5), 715–720. doi: 10.1099/jmm.0.070987-0.CrossRefPubMedGoogle Scholar
- Yamashita, T., Ito, M., Tsuzuki, H., & Sakae, K. (2001). Identification of Aichi virus infection by measurement of immunoglobulin responses in an enzyme-linked immunosorbent assay. Journal of Clinical Microbiology, 39, 4178–4180.CrossRefPubMedPubMedCentralGoogle Scholar
- Yamashita, T., Kobayashi, S., Sakae, K., Nakata, S., Chiba, S., Ishihara, Y., & Isomura, S. (1991). Isolation of cytopathic small round viruses with BS-C-1 cells from patients with gastroenteritis. Journal of Infectious Diseases, 164, 954–957.CrossRefPubMedGoogle Scholar
- Yamashita, T., Sakae, K., Kobayashi, S., Ishihara, Y., Miyake, T., Mubina, A., & Isomura, S. (1995). Isolation of cytopathic small round virus (Aichi virus) from Pakistani children and Japanese travelers from Southeast Asia. Microbiology and Immunology, 9(6), 433–435.CrossRefGoogle Scholar
- Yamashita, T., Sakae, K., Tsuzuki, H., Suzuki, Y., Ishikawa, N., Takeda, N., et al. (1998). Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. Journal of Virology, 72, 8408–8412.PubMedPubMedCentralGoogle Scholar
- Yang, Y. S., Wang, C. J., Huang, C. N., Chen, M. L., Chen, M. J., & Peng, C. H. (2013). Polyphenols of Hibiscus sabdariffa improved diabetic nephropathy via attenuating renal epithelial mesenchymal transition. [Research Support, Non-U.S. Gov’t]. Journal of Agriculture and Food Chemistry, 61(31), 7545–7551. doi: 10.1021/jf4020735.CrossRefGoogle Scholar
- Yin, M. C., & Chao, C. Y. (2008). Anti-Campylobacter, anti-aerobic, and anti-oxidative effects of roselle calyx extract and protocatechuic acid in ground beef. International Journal of Food Microbiology, 127(1–2), 73–77. doi: 10.1016/j.ijfoodmicro.2008.06.002.CrossRefPubMedGoogle Scholar