Prototheca from bovine milk and associated minimal algaecide concentration of chlorhexidine and povidone-iodine in Taiwan

Abstract

Objective Protothecal mastitis has emerged and affected the dairy industries globally in last decades; however, little is known about the occurrence of Prototheca in Taiwan. The present study identified the Prototheca isolated from bovine milk and revealed the algaecide efficacy of 2 disinfectants.

Material and methods From 2011 to 2014, a total of 176 Prototheca isolates were obtained from 10 625 milk samples collected from dairy cows in 24 Taiwanese dairy farms. Of these, 149 isolates were identified by biochemical tests and genotype differentiation with a specific PCR protocol. Minimal algaecide concentration (MAC) of chlorhexidine and povidone-iodine were obtained from 16 isolates by microdilution method.

Results Almost all (n = 147) isolates were P. zopfii, and remaining 2 isolates were P. wickerhamii and unidentified, respectively. Based on molecular genotyping, all P. zopfii isolates belonged to genotype 2. The MAC of 2 commonly used disinfectants, chlorhexidine and povidone-iodine, against 16 P. zopfii isolates was 1.56–3.13 and 48.83–390.63 µg/ml, respectively.

Conclusion This report revealed for the first time the prevalence and the predominant P. zopfii genotype 2 of bovine protothecal infection in Taiwan. In vitro algaecide efficacy indicated that both tested disinfectants were effective against P. zopfii.

Zusammenfassung

Ziel Mastitiden des Rindes, die durch Prototheken verursacht werden, treten weltweit auf und haben die Branche in den letzten Jahrzehnten belastet. Über das Vorkommen von Prototheken in Taiwan ist jedoch wenig bekannt. In der Studie wurden Prototheken aus Kuhmilch isoliert und die algizide Wirkung von 2 Desinfektionsmitteln bestimmt.

Material und Methoden In den Jahren von 2011 bis 2014 wurden aus 10 625 Milchproben, die aus 24 Milchkuhbeständen in Taiwan stammten, 176 Protothekenisolate gewonnen. Insgesamt149 Isolate wurden letztendlich biochemisch identifiziert und weiterhin mit molekularbiologisch unterschiedlicher genotypspezifischer PCR-Systeme analysiert. Minimale Algizidkonzentrationen (MAC) von Chlorhexidin und Povidon-Jod wurden von 16 Isolaten durch Mikrodilution erhalten.

Ergebnisse Bei den 149 identifizierten Isolaten von Prototheca spp. handelte es sich um 147 Isolate von P. zopfii und 2 Isolate von P. wickerhamii. Basierend auf der molekularen Genotypisierung gehörten alle P. zopfii-Isolate zum Genotyp 2. Die MAC der beiden häufig verwendeten Desinfektionsmittel Chlorhexidin und Povidon-Iod für 16 P. zopfii-Isolate betrug 1,56–3,13 bzw. 48,83–390,63 µg/ml.

Schlussfolgerung Diese Studie beschreibt zum ersten Mal die Inzidenz und den vorherrschenden P. zopfii-Genotyp 2 der protothekalen Mastitis bei Rindern in Taiwan. Die Untersuchung der In-vitro-Algizidfähigkeit zeigte an, dass die beiden getesteten Desinfektionsmittel gegen P. zopfii wirksam waren.

Key words

Udder infection - algae - disinfection

Schlüsselwörter

Euterinfektion - Algen - Desinfektion

Publication History

Received: 25 March 2020

Accepted: 25 May 2020

Article published online:
04 December 2020

• References

• 1 Ahrholdt J, Murugauyan J, Straubinger RK. et al. Epidemiological analysis of worldwide bovine, canine and human clinical Prototheca isolates by PCR genotyping and MALDI-TOF mass spectrometry proteomic phenotyping. Med Mycol 2012; 50: 234-243 DOI: 10.3109/13693786.2011.597445.
• 2 Buzzini P, Turchetti B, Facelli R. et al. First large-scale isolation of Prototheca zopfii from milk produced by dairy herds in Italy. Mycopathologia 2004; 158: 427-430 DOI: 10.1007/s11046–004–1819–3.
• 3 Carfora V, Noris G, Caprioli A. et al. Evidence of a Prototheca zopfii genotype 2 disseminated infection in a dog with cutaneous lesions. Mycopathologia 2017; 182: 603-608 DOI: 10.1007/s11046–016-0108–2.
• 4 Chuang ST, Shyu CL, Chan JPW. et al. Isolation and identification of Prototheca zopfii from bovine mastitis in Taiwan. Taiwan Vet J 2002; 28: 94-98
• 5 Corbellini LG, Driemeier D, Cruz C. et al. Bovine mastitis due to Prototheca zopfii: clinical, epidemiological and pathological aspects in a Brazilian dairy herd. Trop Anim Health Prod 2001; 33: 463-470 DOI: 10.1023/A:1012724412085.
• 6 Endo S, Sekiguchi M, Kishimoto Y. et al. The first case of feline Prototheca wickerhamii infection in Japan. J Vet Med Sci 2010; 72: 1351-1353 DOI: 10.1292/jvms.09–0504.
• 7 Gao J, Zhang HQ, He JZ. et al. Characterization of Prototheca zopfii associated with outbreak of bovine clinical mastitis in herd of Beijing, China. Mycopathologia 2012; 173: 275-281 DOI: 10.1007/s11046–011–9510-y.
• 8 Guiry MD, Guiry GM. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway: http://www.algaebase.org searched on 24.04.2020
• 9 Ito T, Kano R, Sobukawa H. et al. Experimental infection of bovine mammary gland with Prototheca zopfii genotype 1. J Vet Med Sci 2011; 73: 117-119 DOI: 10.1292/jvms.10–0242.
• 10 Jagielski T, Bakuła Z, Gawor J. et al. The genus Prototheca (Trebouxiophyceae, Chlorophyta) revisited: implications from molecular taxonomic studies. Algal Res 2019; 43: 101639 DOI: doi:10.1016/j.algal.2019.101639.
• 11 Jagielski T, Lassa H, Ahrholdt J. et al. Genotyping of bovine Prototheca mastitis isolates from Poland. Vet Microbiol 2011; 149: 283-287 DOI: 10.1016/j.vetmic.2010.09.034.
• 12 Jagielski T, Roeske K, Bakuła Z. et al. A survey on the incidence of Prototheca mastitis in dairy herds in Lublin province, Poland. J Dairy Sci 2019; 102: 619-628 DOI: 10.3168/jds.2018–15495.
• 13 Jánosi S, Rátz F, Szigeti G. et al. Pathophysiology: review of the microbiological, pathological, and clinical aspects of bovine mastitis caused by the alga Prototheca zopfii. Vet Q 2001; 23: 58-61 DOI: 10.1080/01652176.2001.9695082.
• 14 Jánosi S, Szigeti G, Rátz F. et al. Epidemiology: Prototheca zopfii mastitis in dairy herds under continental climate conditions. Vet Q 2001; 23: 80-83 DOI: 10.1080/01652176.2001.9695087.
• 15 Krukowski H, Lisowski A, Nowakowicz-dębek B. et al. Susceptibility of Prototheca zopfii strains isolated from cows with mastitis to chlorhexidine and iodine. Turk J Vet Anim Sci 2013; 37: 106-108 DOI: 10.3906/vet-1110–43.
• 16 Kurumisawa T, Kano R, Nakamura Y. et al. Is bovine protothecal mastitis related to persistent infection in intestine?. J Vet Med Sci 2018; 80: 950-952 DOI: 10.1292/jvms.17–0710.
• 17 Marques S, Huss VAR, Pfisterer K. et al. Internal transcribed spacer sequence-based rapid molecular identification of Prototheca zopfii and Prototheca blaschkeae directly from milk of infected cows. J Dairy Sci 2015; 98: 3001-3009 DOI: 10.3168/jds.2014–9271.
• 18 Marques S, Silva E, Carvalheira J. et al. In vitro antimicrobial susceptibility of Prototheca wickerhamii and Prototheca zopfii isolated from bovine mastitis. J Dairy Sci 2006; 89: 4202-4204 DOI: 10.3168/jds.S0022–0302(06)72465–1.
• 19 Marques S, Silva E, Carvalheira J. et al. In vitro susceptibility of Prototheca to pH and salt concentration. Mycopathologia 2010; 169: 297-302 DOI: 10.1007/s11046–009–9254–0.
• 20 Melville PA, Benites NR, Sinhorini IL. et al. Susceptibility and features of the ultrastructure of Prototheca zopfii following exposure to copper sulphate, silver nitrate and chlorhexidine. Mycopathologia 2002; 156: 1-7 DOI: 10.1023/A:1021313118632.
• 21 Milanov D, Petrović T, Polaček V. et al. Mastitis associated with Prototheca zopfii – an emerging health and economic problem on dairy farms. J Vet Res 2016; 60: 373-378 DOI: 10.1515/jvetres-2016–0054.
• 22 Möller A, Truyen U, Roesler U. Prototheca zopfii genotype 2 –The causative agent of bovine protothecal mastitis?. Vet Microbiol 2007; 120: 370-374 DOI: 10.1016/j.vetmic.2006.10.039.
• 23 Moroni P, Nydam DV, Ospina PA. et al. Diseases of the teats and udder. In: Peek SF, Divers TJ. eds. Rebhun’s Diseases of Dairy Cattle. 3rd ed.. Missouri: Elsevier; 2018: 389-465
• 24 National Mastitis Council. Sample collection and handling. In: Middleton JR, Fox LK, Pighetti G. et al. eds. Laboratory Handbook on Bovine Mastitis. Minnesota: National Mastitis Council; 2017: 7-12
• 25 Nguyen QGL, Rosen T. Cutaneous protothecosis in a patient with chronic lymphocytic leukemia: a case report and literature review. J Fungi (Basel) 2015; 1: 4-12 DOI: 10.3390/jof1010004.
• 26 Osumi T, Kishimoto Y, Kano R. et al. Prototheca zopfii genotypes isolated from cow barns and bovine mastitis. Vet Microbiol 2008; 131: 419-423 DOI: 10.1016/j.vetmic.2008.04.012.
• 27 Pal M, Abraha A, Rahman MT. et al. Protothecosis: an emerging algal disease of humans and animals. Int J Life Sci Biotechnol Pharma Res 2014; 3: 1-13
• 28 Park HS, Moon DC, Hyun BH. et al. Occurrence and persistence of Prototheca zopfii in dairy herds of Korea. J Dairy Sci 2019; 102: 2539-2543 DOI: 10.3168/jds.2018–14979.
• 29 Pieper L, Godkin A, Roesler U. et al. Herd characteristics and cow-level factors associated with Prototheca mastitis on dairy farms in Ontario, Canada. J Dairy Sci 2012; 95: 5635-5644 DOI: 10.3168/jds.2011–5106.
• 30 Ricchi M, de Cicco C, Buzzini P. et al. First outbreak of bovine mastitis caused by Prototheca blaschkeae. Vet Microbiol 2013; 162: 997-999 DOI: 10.1016/j.vetmic.2012.11.003.
• 31 Roesler U, Hensel A. Longitudinal analysis of Prototheca zopfii-specific immune responses: correlation with disease progression and carriage in dairy cows. J Clin Microbiol 2003; 41: 1181-1186 DOI: 10.1128/JCM.41.3.1181–1186.2003.
• 32 Roesler U, Möller A, Hensel A. et al. Diversity within the current algal species Prototheca zopfii: a proposal for two Prototheca zopfii genotypes and description of a novel species, Prototheca blaschkeae sp. nov. Int J Syst Evol Microbiol 2006; 56: 1419-1425 DOI: 10.1099/ijs.0.63892–0.
• 33 Salerno T, Ribeiro MG, Langoni H. et al. In vitro algaecide effect of sodium hypochlorite and iodine based antiseptics on Prototheca zopfii strains isolated from bovine milk. Res Vet Sci 2010; 88: 211-213 DOI: 10.1016/j.rvsc.2009.08.001.
• 34 Shahid M, Ali T, Zhang L. et al. Characterization of Prototheca zopfii genotypes isolated from cases of bovine mastitis and cow barns in China. Mycopathologia 2016; 181: 185-195 DOI: 10.1007/s11046–015–9951–9.
• 35 Sobukawa H, Watanabe M, Kano R. et al. In vitro algaecide effect of disinfectants on Prototheca zopfii genotypes 1 and 2. J Vet Med Sci 2011; 73: 1527-1529 DOI: 10.1292/jvms.11–0256.
• 36 Thompson G, Silva E, Marques S. et al. Algaemia in a dairy cow by Prototheca blaschkeae. Med Mycol 2009; 47: 527-531 DOI: 10.1080/13693780802566341.
• 37 Vince AR, Pinard C, Ogilvie AT. et al. Protothecosis in a dog. Can Vet J 2014; 55: 950-954