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Volume 5, Number 5—October 1999

Infections Associated with Eating Seed Sprouts: An International Concern

Peter J. Taormina*Comments to Author , Larry R. Beuchat*, and Laurence Slutsker†
Author affiliations: *University of Georgia, Griffin, Georgia, USA; and †Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Main Article

Table 2

Control of microorganisms in seed sprouts, by type of treatment and treatment results

Organism, origin Treatment Results of treatment Ref.
Aerobic bacteria, rice seeds 1,000 ppm NaOCl or 10,000 ppm H2O2 102 to 103 reductions in aerobic plate counts; germination inhibited 32
Enterobacteriaceae, pseudomonads, commercial sprouts Washing in water Ineffective in removing bacteria 33
Aerobic bacteria, mung bean sprouts 100 ppm chlorine or 5,000 ppm chlorine Reduced microflora by <1 log and 2 logs, respectively 35
Salmonella Stanley, alfalfa seeds Chlorine and hot water No reduction at low levels; reduction of S. Stanley achieved with 2,040 ppm chlorine 27
Salmonella, alfalfa seeds 1,800 ppm Ca(OCl)2 or 2,000 ppm NaOCl or 6% H2O2 or 80% ethanol Salmonella populations reduced by >3 logs, but pathogen not eliminated 37
E. coli O157:H7, alfalfa seeds 500, 1,000, or >2,000 ppm Ca(OCl)2; 500 ppm acidified ClO2; >100 ppm and 500 ppm acidified ClO2; 30% or 70% ethanol; >1% H2O2; 8% H2O2 for 10 min; dry storage Populations reduced but not eliminated; germination decreased; pathogen unaffected by dry storage at 5ºC 38
E. coli O157:H7, alfalfa seeds at various stages of sprouting 2,000 ppm NaOCl; 200 and 2,000 ppm Ca(OCl)2; 500 ppm acidified ClO2 Populations substantially reduced but not eliminated 30
 S. Stanley, alfalfa seeds Heat, 54 to 71ºC 54ºC for 5 min reduced population from 260 to 6-9 cfu/g; treatment for 10 min reduced viability of seed 27
E. coli O157:H7, alfalfa seeds and sprouts Irradiation at >1.0 kiloGray Pathogen controlled without affecting germination 39

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  1. Tauxe  R, Kruse  H, Hedberg  C, Potter  M, Madden  J, Wachsmuth  K. Microbial hazards and emerging issues associated with produce: a preliminary report to the national advisory committee on microbiologic criteria for foods. J Food Prot. 1997;60:14008.
  2. Centers for Disease Control and Prevention. FoodNet population survey atlas of exposures, 7/96–6/97, Atlanta: 1997.
  3. Portnoy  BL, Goepfert  JM, Harmon  SM. An outbreak of Bacillus cereus food poisoning resulting from contaminated vegetable sprouts. Am J Epidemiol. 1976;103:58994.PubMedGoogle Scholar
  4. Harmon  SM, Kautter  DA, Soloman  HM. Bacillus cereus contamination of seeds and vegetable sprouts grown in a home sprouting kit. J Food Prot. 1987;50:625.
  5. O'Mahony  M, Cowden  J, Smyth  B, Lynch  D, Hall  M, Rowe  B, An outbreak of Salmonella Saint-Paul infection associated with bean sprouts. Epidemiol Infect. 1989;104:22935. DOIGoogle Scholar
  6. Jerngklinchan  J, Saitanu  K. The occurrence of salmonellae in bean sprouts in Thailand. Southeast Asian J Trop Med Public Health. 1993;24:1148.PubMedGoogle Scholar
  7. Joce  R, O'Sullivan  DG, Strong  C, Rowe  B, Hall  MLM, Threlfall  EJ. A national outbreak of Salmonella Gold-Coast. Commun Dis Rep CDR Rev. 1990;4:34.
  8. Puohiniemi  R, Heiskanen  T, Siitonen  A. Molecular epidemiology of two international sprout-borne Salmonella outbreaks. J Clin Microbiol. 1997;35:248791.PubMedGoogle Scholar
  9. Ponka  A, Anderson  Y, Sitonen  A, deJong  B, Jahkola  M, Haikala  O, Salmonella in alfalfa sprouts. Lancet. 1995;345:4623. DOIPubMedGoogle Scholar
  10. Mahon  BE, Ponka  A, Hall  WN, Komatsu  K, Dietrich  SE, Sittonen  A, An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J Infect Dis. 1997;175:87682. DOIPubMedGoogle Scholar
  11. Van Beneden  CA, Keene  WE, Stang  RA, Werker  DH, King  AS, Mahon  B, Multinational outbreak of Salmonella enterica serotype Newport infections due to contaminated alfalfa sprouts. JAMA. 1999;281:15862. DOIPubMedGoogle Scholar
  12. Aabo  S, Baggesen  DL. Growth of Salmonella Newport in naturally contaminated alfalfa sprouts and estimation of infectious dose in a Danish Salmonella Newport outbreak due to alfalfa sprouts. In: Program and abstracts of Salmonella and Salmonellosis `97; Nice, France; 1997;425-6.
  13. Mouzin  E, Werner  SB, Bryant  RG, Abbott  S, Farrar  J, Angulo  F, When a health food becomes a hazard: a large outbreak of salmonellosis associated with alfalfa sprouts. In: Program and abstracts of the 46th Annual Epidemic Intelligence Service Conference. Atlanta, GA:1997:15.
  14. Glynn  MK, Patrick  S, Wuhib  T, Neimann  J, Flahert  R, Boxrud  D, When health food isn't so healthy—an outbreak of Salmonella serotypes Anatum and Infantis infections associated with eating contaminated sprouts, Kansas and Missouri, 1997. In: Programs and abstracts of the 47th Annual Epidemic Intelligence Service Conference. Atlanta, GA:1998;16.
  15. Buck  P, Grimsrud  K, Waters  J, Cardinal  R, Talbot  J, Anand  C, Would you like a little Salmonella with your sandwich? In: Program and abstracts of the 47th Annual Epidemic Intelligence Service Conference, International Night. Atlanta, GA:1998.
  16. Ministry of Health and Welfare of Japan. National Institute of Infectious Diseases and Infectious Disease Control Division. Verocytotoxin-producing Escherichia coli (enterohemorrhagic E. coli) infection, Japan, 1996–June 1997. Infectious Agents Surveillance Report. 1997;18:1534.
  17. Gutierrez  E. Japan prepares as O157 strikes again. Lancet. 1997;349:1156. DOIGoogle Scholar
  18. Centers for Disease Control and Prevention. Outbreaks of Escherichia coli O157:H7 infection associated with eating alfalfa sprouts—Michigan and Virginia, June-July 1997. MMWR Morb Mortal Wkly Rep. 1997;46:7414.
  19. Beuchat  LR. Pathogenic microorganisms associated with fresh produce. J Food Prot. 1996;59:20416.
  20. Beuchat  LR, Ryu  JH. Produce handling and processing practices. Emerg Infect Dis. 1997;3:45965. DOIPubMedGoogle Scholar
  21. Andrews  WH, Mislivec  PB, Wilson  CR, Bruce  VR, Poelma  PL, Gibson  R, Microbial hazards associated with bean sprouting. J Assoc Off Anal Chem. 1982;65:2418.PubMedGoogle Scholar
  22. Prokopowich  D, Blank  G. Microbiological evaluation of vegetable sprouts and seeds. J Food Prot. 1990;54:5602.
  23. Piernas  V, Guirand  JP. Microbial hazards related to rice sprouting. Int J Food Sci Technol. 1997;32:339. DOIGoogle Scholar
  24. Potter  AP, Ehrenfeld  EE. Microbial loads of bean sprouts: coliform, E. coli and Salmonella [poster Q-243]. In the 98th General Meeting of the American Society for Microbiology; 1998 May 17-21; Atlanta, Georgia.
  25. Patterson  JE, Woodburn  MJ. Klebsiella and other bacteria on alfalfa and bean sprouts at the retail level. J Food Sci. 1980;45:4925. DOIGoogle Scholar
  26. Sly  T, Ross  E. Chinese foods: relationship between hygiene and bacterial flora. J Food Prot. 1982;45:1158.
  27. Jaquette  CB, Beuchat  LR, Mahon  BE. Efficacy of chlorine and heat treatment in killing Salmonella stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl Environ Microbiol. 1996;62:22125.PubMedGoogle Scholar
  28. Itoh  Y, Sugita-Konishi  Y, Kusuga  F, Iwaki  M, Hara-Kudo  Y, Saito  N, Enterohemorrhagic Escherichia coli O157:H7 present in radish sprouts. Appl Environ Microbiol. 1998;4:15325.
  29. Hara-Kudo  Y, Konuma  H, Iwaki  M, Kasuga  F, Sugita-Konishi  Y, Ito  Y, Potential hazard of radish sprouts as a vehicle of Escherichia coli O157:H7. J Food Prot. 1997;60:11257.
  30. Taormina  PJ, Beuchat  LR. Behavior of enterohemorrhagic Escherichia coli O157:H7 on alfalfa sprouts during the sprouting process as influenced by treatment with various chemicals. J Food Prot. 1999;62:8506.PubMedGoogle Scholar
  31. Ingram  DT, Kantor  MA, Meng  J. Survival of E. coli O157:H7 during sprouting of inoculated alfalfa seeds. Int Assoc Milk Food Environ Sanit Ann Mtg, Prog and Abst Book, August 16-19, 1998, Nashville, TN. p. 36.
  32. Piernas  V, Guiraud  JP. Disinfection of rice seeds to sprouting. J Food Sci. 1997;62:6115. DOIGoogle Scholar
  33. Becker  B, Holzapfel  WH. Mikrobiologisches risiko von fertgverpackten keimlingen und maßnahmen zur reduzierung ihrer mikrobiellen belastung. Arch Lebensmittelhyg. 1997;48:7396.
  34. Naito  S, Shiga  I. Studies on utilization of ozone in food preservation. IX. Effect of ozone treatment on elongation of hypocotyl and microbial counts of bean sprouts. Journal of the Japanese Society of Food Science and Technology. 1989;36:1818.
  35. Splittstoesser  DF, Queale  DT, Andaloro  BW. The microbiology of vegetable sprouts during commercial production. J Food Saf. 1983;5:7986. DOIGoogle Scholar
  36. Moline  HE, Kulik  MM. Contamination and deterioration of alfalfa sprouts caused by a seedborne isolate of Erwinia herbicola. J Food Qual. 1997;20:5360. DOIGoogle Scholar
  37. Beuchat  LR. Comparison of chemical treatments to kill Salmonella on alfalfa seeds intended for sprout production. Int J Food Microbiol. 1996;34:32933. DOIGoogle Scholar
  38. Taormina  PJ, Beuchat  LR. Comparison of chemical treatments to eliminate enterohemorrhagic Escherichia coli O157:H7 on alfalfa seeds. J Food Prot. 1999;62:31824.PubMedGoogle Scholar
  39. Gordenker  A. Better detection methods needed for pathogens on fresh sprouts. Inside Lab Management. Association of Official Analytical Chemists International. 1999;3:213.
  40. Public meeting on sprout safety. U.S. Food and Drug Administration, Center for Food Safety and Applied Nutrition, Fresh Produce Subcommittee of the National Advisory Committee of Microbiological Criteria for Foods; 1998 Sep 28-29; Washington, D.C.
  41. Pargas  N. Sprout research to target 5-log reductions for E. coli O157:H7, Salmonella. Food Chemical News 1998; October 19:17.
  42. Interim advisory on alfalfa sprouts. FDA. Washington, DC: August 31, 1998.
  43. Tauxe  RV. Emerging foodborne diseases: an evolving public health challenge. Emerg Infect Dis. 1997;3:42534. DOIPubMedGoogle Scholar
  44. Tauxe  RV. New approaches to surveillance and control of emerging foodborne infectious diseases. Emerg Infect Dis. 1998;4:4556. DOIPubMedGoogle Scholar
  45. Hutwagner  LC, Maloney  EK, Bean  NH, Slutsker  L, Martin  SM. Using laboratory-based surveillance data for prevention: an algorithm for detecting Salmonella outbreaks. Emerg Infect Dis. 1997;3:395400. DOIPubMedGoogle Scholar
  46. Tauxe  RV, Hughes  JM. International investigation of outbreaks of foodborne disease. BMJ. 1996;313:10934.PubMedGoogle Scholar
  47. Killalea  D, Ward  LR, Roberts  D, de Louvois  J, Sufi  S, Stuart  JM, International epidemiological and microbiological study of outbreak of Salmonella agona infection from a ready to eat savoury snack–I: England, Wales, and the United States. BMJ. 1996;313:11057.PubMedGoogle Scholar

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