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Complex etiology and pathology of mycotoxic nephropathy in South African pigs

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Abstract

Spontaneous nephropathy in pigs seen in South Africa was found to have multi-mycotoxic etiology involving several mycotoxins such as ochratoxin A (OTA), penicillic acid (PA) and fumonisin B1 (FB1) in addition to a not yet identified mycotoxin. Contamination levels of OTA were comparatively low (67–75 μg/kg) in contrast to high contamination levels of FB1 (5,289–5,021 μg/kg) and PA (149–251 μg/kg). A heavy contamination with Gibberella fujikuroi var. moniliformis and Penicillium aurantiogriseum complex (mainly P. polonicum) was observed in the fed forages in contrast to the light contamination with Aspergillus ochraceus, P. verrucosum and P. citrinum. The pathomorphological picture of this nephropathy was found to differ from the classical description of mycotoxic porcine nephropathy as originally made in Scandinavia by the extensive vascular changes.

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Notes

  1. CEI - Chloroform-Ethyl Acetate-Propan-2-ol (90:5:5, v/v/v);

    TEF - Toluene-Ethyl Acetate-Formic Acid (6:3:1, v/v/v);

    CM - Chloroform-Methanol (95:5, v/v);

    CM2 - Chloroform-Methanol (3:2 ,v/v);

    BWA - Butanol-Water-Acetic acid (12:5:3, v/v/v);

    CtE - Carbon tetrachloride-Ethanol (98:2, v/v);

    ChE - Cyclohexane-Ether (3:1, v/v)

Abbreviations

AFs:

Aflatoxins

BEN:

Balkan endemic nephropathy

CIT:

Citrinin

CA:

Cyclopiazonic acid

DAS:

Diacetoxyscirpenol

DON:

Deoxynivalenol

ERY:

Erythroskyrin

FB1 :

Fumonisin B1

FB2 :

Fumonisin B2

GLI:

Gliotoxin

ISL:

Islanditoxin

KA:

Kojic acid

LUT:

Luteoskyirin

MPN:

Mycotoxic porcine nephropathy

MCN:

Mycotoxic chicken nephropathy

MON:

Moniliformin

MTT:

3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

OTA:

Ochratoxin A

OTC:

Ochratoxin C

OOS:

Oosporein (isoosporin)

PenA:

Penitrem A

PAT:

Patulin

PA:

Penicillic acid

ppb:

μg/kg

T-2:

T-2 toxin

UM:

Unknown metabolite

XA:

Xanthomegnin

ZEA:

Zearalenone.

References

  • Abado-Becognee K, Mobio TK, Ennamany R, Fleurat-Lessard F, Shier WT, Badria F, Creppy EE (1998) Cytotoxicity of fumonisin B1: implication of lipid peroxidation and inhibition of protein and DNA syntheses. Arch Toxicol 72:233–236

    Article  PubMed  CAS  Google Scholar 

  • Abdulkadar AHW, Al-Ali AA, Al-Kildi M, Al-Jedah JH (2004) Mycotoxins in food products available in Qatar. Food Control 15:543–548

    Article  CAS  Google Scholar 

  • Bennett GA, Richard JL (1994) Liquid chromatographic method for analysis of the naphthalene dicarboxaldehyde derivative of fumonisins. J AOAC Int 77(2):501–506

    CAS  Google Scholar 

  • Bernhoft A, Keblys M, Morrison E, Larsen HJS, Flåøyen A (2004) Combined effects of selected Penicillium mycotoxins on in vitro proliferation of porcine lymphocytes. Mycopathologia 158:441–450

    Article  PubMed  CAS  Google Scholar 

  • Bily AC, Reid LM, Savard ME, Reddy R, Blackwell BA, Campbell CM, Krantis A, Durst T, Philogene BJR, Arnason JT, Regnault-Roger C (2004) Analysis of Fusarium graminearum mycotoxins in different biological matrices by LC/MS. Mycopathologia 157:117–126

    Article  PubMed  CAS  Google Scholar 

  • Boudra H, Morgavi DP (2006) Development and validation of a HPLC method for the quantitation of ochratoxins in plasma and raw milk. J Chromatogr B 843:295–301

    Article  CAS  Google Scholar 

  • Bucci TJ, Howard PC, Tolleson WH, Laborde JB, Hansen DK (1998) Renal effects of fumonisin mycotoxins in animals. Toxicol Pathol 26:190–194

    Google Scholar 

  • Chan PK, Hayes AW (1981) Effect of penicillic acid on biliary excretion of indocyanine green in the mouse and rat. J Toxicol Environ Health 7:169–179

    Article  PubMed  CAS  Google Scholar 

  • Creppy EE, Röschenthaler R, Dirheimer G (1984) Inhibition of protein synthesis in mice by ochratoxin A and its prevention by phenylalanine. Food Chem Toxicol 22:883–886

    Article  PubMed  CAS  Google Scholar 

  • Creppy EE, Chiarappa P, Baudrimont I, Borracci P, Moukha S, Carratù MR (2004) Synergistic effects of fumonisin B1 and ochratoxin A: are in vitro cytotoxicity data predictive of in vivo acute toxicity. Toxicology 201:115–123

    Article  PubMed  CAS  Google Scholar 

  • Diaz CT, Sogbe E, Ascanio E, Hernandez M (2001) Ochratoxin A and fumonisin B1 natural interaction in pigs. Clinical and pathological studies. Rev Cient Fac Cien V:314–321

    Google Scholar 

  • Dickens F, Jones HE (1961) Carcinogenic activity of a series of reactive lactones and related substances. Br J Cancer 15:85–100

    PubMed  CAS  Google Scholar 

  • Domijan A, Peraica M, Jurjevic Z, Ivic D, Cvjetkovic B (2005) Fumonisin B1, fumonisin B2, zearalenone and ochratoxin A contamination of maize in Croatia. Food Addit Contam 22:677–680

    Article  PubMed  CAS  Google Scholar 

  • Domijan A, Zeljezic D, Kopjar N, Peraica M (2006) Standard and Fpg-modifed comet assay in kidney cells of ochratoxin A-and fumonisin B1-treated rats. Toxicology 222:53–59

    Article  PubMed  CAS  Google Scholar 

  • Doster RC, Sinnhuber RO (1972) Compаrative rates of hydrolysis of ochratoxin A and B in vitro. Food Cosmet Toxicol 10:389–394

    Article  PubMed  CAS  Google Scholar 

  • Dutton MF, Kinsey A (1995) Incidence of mycotoxins and fungi in feedstuffs in Natal in 1995. Mycopathologia 131:31–36

    Article  PubMed  CAS  Google Scholar 

  • Faucet V, Pfohl-Leszkowicz A, Dai J, Castegnaro M, Manderville RA (2004) Evidence for covalent DNA adduction by ochratoxin A following chronic exposure to rat and subacute exposure to pig. Chem Res Toxicol 17:1289–1296

    Article  PubMed  CAS  Google Scholar 

  • Geiser DM, Jimenez-Gasco M, Kang S, Makalowska I, Veerrarghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) Fusarium-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479

    Article  CAS  Google Scholar 

  • Gelderblom WCA, Marasas WFO, Farber E (1992) The cancer initiating potential of the fumonisin B mycotoxins. Carcinogenesis 13:433–437

    Article  PubMed  CAS  Google Scholar 

  • Hanna GD, Phillips TD, Kubena LF, Cysewski SJ, Ivie GW, Heidelbaugh ND, Witzel DA, Hayes AW (1981) High pressure liquid chromatographic determination of penicillic acid in chicken tissues. Poultry Sci 60:2246–2252

    CAS  Google Scholar 

  • Hinojo MJ, Medina A, Valle-Algarra FM, Gimeno-Adelantado JV, Jimenez M, Mateo R (2006) Fumonisin production in rice cultures of Fusarium verticillioides under different incubation conditions using an optimized analytical method. Food Microbiol 23:119–127

    Article  PubMed  CAS  Google Scholar 

  • Howard PC, Warbritton A, Voss KA, Lorenzen RJ, Thurman JD, Kovach RM, Bucci TJ (2001) Compensatory regeneration as a mechanism for renal tubule carcinogenesis of fumonisin B1 in F344/N/Nctr BR rat. Environ Health Persp 109:309–314

    Article  CAS  Google Scholar 

  • Jurjevic Z, Solfrizzo M, Cvjetkovic B, Avantaggiato G, Visconti A (1999) Ochratoxin A and fumonisins (B1 and B2) in maize from Balkan nephropathy endemic and non endemic areas of Croatia. Mycotoxin Res 15:67–80

    Article  CAS  Google Scholar 

  • Jurjevic L, Solfrizzo M, Cvjetkovic B, De Girolamo A, Visconti A (2002) Occurrence of beauvericin in corn from Croatia. Food Technol Biotechnol 40:91–94

    CAS  Google Scholar 

  • Kanisawa M (1984) Synergistic effect of citrinin on hepatorenal carcinogenesis of ochratoxin A in mice. Dev Food Sci 7:245–254

    CAS  Google Scholar 

  • Klaric MS, Rumora L, Ljubanovic D, Pepeljnjak S (2007) Cytotoxicity and apoptosis induced by fumonisin B1, beauvericin and ochratoxin A in porcine kidney PK15 cells: effects of individual and combined treatment. Arch Toxicol 82:247–255

    Article  PubMed  CAS  Google Scholar 

  • Klich MA (2002) Introduction; economic and medical importance of Aspergillus. In: Identification of common Aspergillus species. Centraalbureau voor Schimmelculture, Utrecht, pp 1–16

    Google Scholar 

  • Klich MA, Pitt JI (1988) A laboratory guide to common Aspergillus species and their teleomorphs. CSIRO Division of Food Research, North Ryde NSW

    Google Scholar 

  • Kokkonen M, Jestoi M, Rizzo A (2005) The effect of substrate on mycotoxin production of selected Penicillium strains. Int J Food Microbiol 99:207–214

    Article  PubMed  CAS  Google Scholar 

  • Koshinsky HA, Khachatourians GG (1994) Mycotoxicoses: The effects of mycotoxin combinations. In: Hui YH, Gorham JR, Murrell KD, Cliver DO (eds) Foodborne disease handbook. Diseases caused by viruses, parasites, and fungi, vol. 2. University of Saskatchewan, Saskatoon, pp 463–520

    Google Scholar 

  • Krogh P (1976) Mycotoxic nephropathy. In: Advances in veterinary science and comparative medicine, vol. 20. Academic, New York, pp 147–170

    Google Scholar 

  • Krogh P, Axelsen NH, Elling F, Gyrd-Hansen N, Hald B, Hyldgaard-Jensen J, Larsen AE, Madsen A, Mortensen HP, Moller T, Peterson OK, Ravnskov U, Rostgaard M, Aalund O (1974) Experimental porcine nephropathy: changes of renal function and structure induced by ochratoxin A-contaminated feed. Acta Pathol Microb Scand Sect A Suppl 246:1–21

    CAS  Google Scholar 

  • Kubena LF, Edrington TS, Harvey RB, Phillips TD, Sarr AB, Rottinghaus GE (1997) Individual and combined effects of fumonisin B1 present in Fusarium moniliforme culture material and diacetoxyscirpenol or ochratoxin A in turkey poults. Poultry Sci 76:256–264

    CAS  Google Scholar 

  • Kyriakidis N, Waight ES, Day JB, Mantle PG (1981) Novel metabolites from Penicillium crustosum, including penitrem E, a tremorgenic mycotoxin. Appl Environ Microbiol 42:61–62

    PubMed  CAS  Google Scholar 

  • Lillehoj EB, Ciegler A (1975) Mycotoxin synergism. In: Schlessinger D (ed) Microbiology. American Society of Microbiology, Washington, pp 344–358

    Google Scholar 

  • Macgeorge KM, Mantle PG (1990) Nephrotoxicity of Penicillium aurantiogriseum and P. commune from an endemic nephropathy area of Yugoslavia. Mycopathologia 112:139–145

    Article  PubMed  CAS  Google Scholar 

  • Mantle PG, McHugh KM (1993) Nephrotoxic fungi in foods from nephropathy households in Bulgaria. Mycol Res 97:205–212

    Article  Google Scholar 

  • Micco C, Miraglia M, Onori R, Libanori A, Brera C, Mantovani A, Macri C (1991) Effect of combined exposure to ochratoxin A and penicillic acid on residues and toxicity in broilers. Rev Soc Ital Sci Aliment 20:101–108

    CAS  Google Scholar 

  • Miljkovic A, Pfohl-Leszkowicz A, Dobrota M, Mantle PG (2003) Comparative responses to mode of oral administration and dose of ochratoxin A or nephrotoxic extract of Penicillium polonicum in rats. Exp Toxicol Pathol 54:305–312

    Article  PubMed  CAS  Google Scholar 

  • Nelson PE, Toussoun TA, Marasas WFO (1983) Fusarium species: an illustrated manual for identification. The Pennsylvania State University Press, Pennsylvania

    Google Scholar 

  • Njobeh PB, Dutton MF, Chuturgoon AA, Koch SH, Steenkamp PA, Stoev SD (2009) Identification of a novel metabolite and its cytotoxic effect on human lymphocyte cells in comparison to other mycotoxins. Int J Biol Chem Sci 3(3):524–531

    Google Scholar 

  • Obrecht-Pflumio S, Dirheimer G (2000) In vitro DNA and dGMP adducts formation caused by ochratoxin A. Chem Biol Interact 127:29–44

    Article  PubMed  CAS  Google Scholar 

  • Oswald IP, Desautels C, Laffitte J, Fournout S, Peres SY, Odin M, Le Bars P, Le Bars J, Fairbrother JM (2003) Mycotoxin fumonisin B-1 increases intestinal colonization by pathogenic Escherichia coli in pigs. Appl Environ Microbiol 69:5870–5874

    Article  PubMed  CAS  Google Scholar 

  • Oswald IP, Marin DE, Bouhet S, Pinton P, Taranu I, Accensi F (2005) Immunotoxicological risk of mycotoxins for domestic animals. Food Addit Contam 22:354–360

    Article  PubMed  CAS  Google Scholar 

  • Palmgren MS, Ciegler A (1983) Toxicity and carcinogenicity of fungal lactones: patulin and penicillic acid. In: Keeler RF, Tu AT (eds) Handbook of natural toxins, vol. 1. Plant and fungal toxins. Marcel Dekker, New York, pp 325–341

    Google Scholar 

  • Parker R, Phillips T, Russell KL, LH HND (1982) Inhibition of pancreatic carboxypeptidase A: a possible mechanism of interaction between penicillic acid and ochratoxin A. J Environ Sci Health B17:77–91

    Google Scholar 

  • Patterson DSP, Roberts BA (1979) Mycotoxins in animal feedstuffs: Sensitive thin layer chromatographic detection of aflatoxin, ochratoxin A, sterigmatocystin, zearalenone and T2 toxin. J Assoc Off Anal Chem 62:1265–1267

    PubMed  CAS  Google Scholar 

  • Petrik J, Zanic´-Grubišic T, Barišic K, Pepeljnjak S, Radic B, Fereničic Z, Cepelak I (2003) Apoptosis and oxidative stress induced by ochratoxin A in rat kidney. Arch Toxicol 77:685–693

    Article  PubMed  CAS  Google Scholar 

  • Pfohl-Leszkowicz A, Molinié A, Tozlovanu M, Manderville RA (2008) Combined toxic effects of ochratoxin A and citrinin, in vitro and in vivo. In: Siantar DP, Trucksess MW, Scott PM, Herman EM (eds) Food contaminants, mycotoxins and food allergen. ACS Symposium series 1001. Oxford University Press, Oxford, pp 56–80

    Chapter  Google Scholar 

  • Phillips RD, Hayes AW, Berndt WO (1980) High-performance liquid chromatographic analysis of the mycotoxin citrinin and its application to biological fluids. J Chromatogr A 190:419–427

    Article  CAS  Google Scholar 

  • Pitt JI, Hocking AD (1997) Primary keys and miscellaneous fungi. In: Fungi and food spoilage, 2nd edn. Blackie, London, pp 59-171

  • Rahimtula AD, Bereziat JC, Bussachini-Griot V, Bartsch H (1988) Lipid peroxidation as possible cause of ochratoxin A toxicity. Biochem Pharmacol 37:4469–4477

    Article  PubMed  CAS  Google Scholar 

  • Samson RA, Seifert KA, Kuijpers AFA, Houbraken JAP, Frisvad JC (2004) Phylogentic analysis of Penicillium subgenus Penicillium using partial β-tubulin sequences. Stud Mycol 49:175–200

    Google Scholar 

  • Sansing GA, Lillehoj EB, Detroy RW, Müller MA (1976) Synergistic toxic effects of citrinin, ochratoxin A and penicillic acid in mice. Toxicon 14:213–220

    Article  PubMed  CAS  Google Scholar 

  • Shepherd EC, Phillips TD, Joiner GN, Kubena LF, Heidelbaugh ND (1981) Ochratoxin A and penicillic acid interaction in mice. J Environ Sci Health B 16:557–573

    Article  PubMed  CAS  Google Scholar 

  • Singh K, Frisvad JC, Thrane U, Mathur SB (1991) An illustrated manual on identification of some seed-borne Aspergilli, Fusaria, Penicillia and their mycotoxins. Institute of Seed Pathology for Developing Countries, Hellerup, Denmark, pp 8–12

  • Smedsgaard J (1997) Terverticillate penicillia studied by direct electrospray mass spectrometric profiling of crude extracts. II. Database and identification. Biochem Syst Ecol 25:65–71

    Article  CAS  Google Scholar 

  • Smedsgaard J, Frisvad JC (1996) Using direct electrospray mass spectrometry in taxonomy and secondary metabolite profiling of crude fungal extracts. J Microbiol Methods 25:5–17

    Article  CAS  Google Scholar 

  • Smedsgaard J, Nielsen J (2005) Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. J Exp Bot 56:273–286

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD (1998) The role of ochratoxin A as a possible cause of Balkan Endemic Nephropathy and its risk evaluation. Vet Hum Toxicol 40:352–360

    PubMed  CAS  Google Scholar 

  • Stoev SD (2008a) Mycotoxic nephropathies in farm animals-diagnostics, risk assessment and prevеntive measures. In: Oswald I, Taranu I, Pandalai SG (eds) Effect of mycotoxins in farm animals, chapter 8. Transworld Research Network 37/661 (2), Fort PO, Trivandrum-695 023, Kerala, India, pp 155-195

  • Stoev SD (2008b) Complex etiology, prophylaxis and hygiene control in mycotoxic nephropathies in farm animals and humans. Int J Mol Sci 9:578–605

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD, Hald B, Mantle P (1998a) Porcine nephropathy in Bulgaria: a progressive syndrome of complex of uncertain (mycotoxin) etiology. Vet Rec 142:190–194

    PubMed  CAS  Google Scholar 

  • Stoev SD, Stoeva J, Anguelov G, Hald B, Creppy EE, Radic B (1998b) Haematological, biochemical and toxicological investigations in spontaneous cases with different frequency of porcine nephropathy in Bulgaria. J Vet Med Ser A 45:229–236

    Article  CAS  Google Scholar 

  • Stoev SD, Anguelov G, Pavlov D, Pirovski L (1999) Some antidotes and paraclinical investigations in experimental intoxication with ochratoxin A and penicillic acid in chicks. Vet Arh 69:179–189

    CAS  Google Scholar 

  • Stoev SD, Anguelov G, Ivanov I, Pavlov D (2000a) Influence of ochratoxin A and an extract of artichoke on the vaccinal immunity and health in broiler chicks. Exp Toxicol Pathol 52:43–55

    PubMed  CAS  Google Scholar 

  • Stoev SD, Goundasheva D, Mirtcheva T, Mantle P (2000b) Susceptibility to secondary bacterial infections in growing pigs as an early response in ochratoxicosis. Exp Toxicol Pathol 52:287–296

    PubMed  CAS  Google Scholar 

  • Stoev SD, Vitanov S, Anguelov G, Petkova-Bocharova T, Creppy EE (2001) Experimental mycotoxic nephropathy in pigs provoked by a mouldy diet containing ochratoxin A and penicillic acid. Vet Res Commun 25:205–223

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD, Daskalov H, Radic B, Domijan A, Peraica M (2002a) Spontaneous mycotoxic nephropathy in Bulgarian chickens with unclarified mycotoxin aetiology. Vet Res 33:83–94

    Article  PubMed  Google Scholar 

  • Stoev SD, Paskalev M, MacDonald S, Mantle PG (2002b) Experimental one year ochratoxin A toxicosis in pigs. Exp Toxicol Pathol 53:481–487

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD, Djuvinov D, Mirtcheva T, Pavlov D, Mantle P (2002c) Studies on some feed additives giving partial protection against ochratoxin A toxicity in chicks. Toxicol Lett 135:33–50

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD, Stefanov M, Denev S, Radic B, Domijan A, Peraica M (2004) Experimental mycotoxicosis in chickens induced by ochratoxin A and penicillic acid and intervention by natural plant extracts. Vet Res Commun 28:727–746

    Article  PubMed  CAS  Google Scholar 

  • Stoev SD, Dutton MF, Nkosi B (2009a) Cytotoxic effect of mycotoxins ochratoxin A, citrinin, penicillic acid, fumonisin B1 and their combinations on human peripheral blood mononuclear cells as measured by MTT assay. Open Toxinol J 2:1–8

    Article  CAS  Google Scholar 

  • Stoev SD, Dutton MF, Njobeh PB, Mosonik JS, Steenkamp PA (2009b) Mycotoxic nephropathy in Bulgarian pigs and chickens: complex etiology and similarity to Balkan Endemic Nephropathy, Food Addit Contam (in press)

  • Suzuki S, Satoh T, Yamazaki M (1977) The pharmacokinetics of ochratoxin A in rats. Jpn J Pharmacol 27:735–744

    Article  PubMed  CAS  Google Scholar 

  • Taranu I, Marin DE, Bouhet S, Oswald IP (2008) Effect of fumonisin on the pig. In: Oswald I, Taranu I, Pandalai SG (eds) Mycotoxins in farm animals. Chapter 5. Transworld Research Network 37/661 (2), Fort PO Trivandrum-695 023, Kerala, India, pp 91-111

  • Umeda M, Yamamoto T, Saito M (1972) DNA-strand breakage of HeLa cells induced by several mycotoxins. Jpn J Exp Med 42:527–539

    PubMed  CAS  Google Scholar 

  • Voss KA, Riley RT, Norred WP, Bacon CW, Meredith FI, Howard PC (2001) An overview of rodent toxicities: liver and kidney effects of fumonisins and Fusarium moniliforme. Environ Health Perspect 109:259–266

    Article  PubMed  CAS  Google Scholar 

  • Voss KA, Smith GW, Haschek WM (2007) Fumonisins: Toxicokinetics, mechanism of action and toxicity. Anim Feed Sci Technol 137:299–325

    Article  CAS  Google Scholar 

  • Yeulet SE, Mantle PG, Rudge MS, Greig JB (1988) Nephrotoxicity of Penicillium aurantiogriseum, a possible factor in the aetiology of Balkan Endemic Nephropathy. Mycopathologia 102:21–30

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research has been financially supported in part by Marie Curie Outgoing International Fellowship within the 6th European Community Framework Programme, Department of Science and Technology in South Africa, UK Royal Society Joint Project with Central and Eastern Europe, NATO grant and Foundation of Ministry of Science and Education of Bulgaria via five research projects.

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Stoev, S.D., Denev, S., Dutton, M.F. et al. Complex etiology and pathology of mycotoxic nephropathy in South African pigs. Mycotox Res 26, 31–46 (2010). https://doi.org/10.1007/s12550-009-0038-7

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