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Volume 3, Number 4—December 1997
THEME ISSUE
Foodborne
Controlling Emerging Foodborne Microbial Hazards

Epidemiology and Detection as Options for Control of Viral and Parasitic Foodborne Disease

Lee-Ann JaykusComments to Author 
Author affiliation: North Carolina State University, Raleigh, North Carolina, USA

Main Article

Table 2

Emerging detection methods for human enteric viruses in foods

Field
Pathogen Sample Detection limit app. Ref.
Nucleic Acid Extraction/RT-PCR
HAV Clams 2000 particles/g
(10 PFU/g) No 44
Poliovirus Oysters 38 PFU/20 g
(2 PFU/g) No 42
HAV Clams/Oysters 100 PFU/1.5 g
(67 PFU/g) No 43
Norwalk Clams/Oysters 5-10 PCRU/1.5 g
(3-7 PCRU/g) No 43
Poliovirus Oysters/Mussels 10 PFU/5 g
(2 PFU/g) No 45
SRSV Oysters/Mussels Not specified Yes 46
Polivirus,
HAV Clams 100 PFU/50 g
(2 PFU/g) No 50
Norwalk Clams 1000 PCRU/50 g
(20 PCRU/g) No 50
Norwalk Various 20-200 PCRU/10 g
(2-20 PCRU/g) No 47
Antibody-Capture/RT-PCR
HAV Clams/Oysters Not specified No 48
HAV Oysters Not specified Yes 19
Virion Concentration
Poliovirus,
HAV Oysters 10 PFU/50 g
(0.02 PFU/g) Yes 49,
Norwalk Oysters 4500 PCRU/50 g
(90 PCRU/g) No 49,51
Poliovirus,
HAV Clams 1000 PFU/50 g
(20 PFU/g) No 50
Norwalk Clams 100 PCRU/50 g
(2 PCRU/g) No 50

HAV = hepatitis A virus; RT-PCR = reverse transcriptase polymerase chain reaction; PCRU = PCR-amplifiable units; SRSV = small round-structured gastrointestinal virus.

Main Article

References
  1. Morse  SS. Factors in the emergence of infectious disease. Emerg Infect Dis. 1995;1:5–10. DOI
  2. Jaykus  LA, Hemard  MT, Sobsey  MD. Human enteric pathogenic viruses. In: Hackney CR, Peirson MD, editors. Environmental indicators and shellfish safety. New York: Chapman and Hall; 1994.
  3. DuPont  HL, Chappell  CL, Sterling  CR, Okhuysen  PC, Rose  JB, Jakubowski  W. The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med. 1995;332:855–9. DOIPubMed
  4. Haas  CN. Estimation of risk due to low doses of microorganisms: a comparison of alternative methodologies. Am J Epidemiol. 1983;118:573–82.PubMed
  5. Moe  CL. Waterborne transmission of infectious agents. In: Hurst CJ, Knudsen GR, McInerney MJ, Stenzenbach LD, Walter MV, editors. Manual of environmental microbiology. Washington (DC): American Society for Microbiology; 1996.
  6. Council for Agricultural Science and Technology. Foodborne pathogens: risks and consequences. Washington (DC): Library of Congress No. 122; 1994.
  7. Jenkins  S, Horman  JT, Isreal  E, Cukor  G, Blacklow  NR. An outbreak of Norwalk-related gastroenteritis in a boys' camp. Am J Dis Child. 1985;139:787–9.PubMed
  8. Hedberg  CW, Osterholm  MT. Outbreaks of foodborne and waterborne viral gastroenteritis. Clin Microbiol Rev. 1993;6:199–210.PubMed
  9. Bean  NH, Griffin  PM. Foodborne disease outbreaks in the United States, 1973-1987: pathogens, vehicles, and trends. J Food Prot. 1990;53:804–17.
  10. Kaplan  JE, Feldman  R, Campbell  DS, Lookabaugh  C, Gary  W. The frequency of a Norwalk-like pattern of illness in outbreaks of acute gastroenteritis. Am J Public Health. 1982;72:1329–32. DOIPubMed
  11. Kaplan  JE, Gary  GW, Baron  RC, Singh  N, Schonberger  LB, Feldman  R, Epidemiology of Norwalk gastroenteritis and the role of Norwalk virus in outbreaks of acute nonbacterial gastroenteritis. Ann Intern Med. 1982;96:756–76.PubMed
  12. Cliver  DO, Ellender  RD, Fout  GS, Shields  PA, Sobsey  MD. Foodborne viruses. In: Vanderzant C, Splittstoesser DF, editors. Compendium of methods for the microbiological examination of foods. Washington (DC): American Public Health Association; 1992.
  13. Centers for Disease Control. Foodborne and waterborne disease outbreaks annual summary 1976. Washington (DC): U.S. Department of Health, Education, and Welfare Publication No. CDC 78-8185; 1978.
  14. Gerba  CP, Goyal  SM. Detection and occurrence of enteric viruses in shellfish: a review. J Food Prot. 1978;41:743–54.
  15. Appleton  H. Small round viruses: classification and role in food-borne infections. In: Ciba Foundation Symposium. Novel Diarrhoea Viruses. Chinchester, England: Wiley Publishers; 1987.
  16. Heun  EM, Vogt  RL, Hudson  PJ, Parren  S, Gary  GW. Risk factors for secondary transmission in households after a common-source outbreak of Norwalk gastroenteritis. Am J Epidemiol. 1987;126:1181–6.PubMed
  17. White  KE, Osterholm  MT, Mariotti  JA, Korlath  JA, Lawrence  DH, Ristinen  TL, A foodborne outbreak of Norwalk virus gastroenteritis: evidence for post-recovery transmission. Am J Epidemiol. 1986;124:120–6.PubMed
  18. Xu  ZY, Li  ZH, Wang  JX, Xiao  ZP, Dong  DH. Ecology and prevention of a shellfish-associated hepatitis A epidemic in Shanghai, China. Vaccine. 1992;Suppl 1:S67–8. DOIPubMed
  19. Desenclos  JCA, Klontz  KC, Wilder  MH, Nainan  OV, Margolis  HS, Gunn  RA. A multistate outbreak of hepatitis A caused by the consumption of raw oysters. Am J Public Health. 1991;81:1268–72. DOIPubMed
  20. Centers for Disease Control and Prevention. Multistate outbreak of viral gastroenteritis associated with consumption of oysters-Apalachicola Bay, Florida, December 1995-January 1995. MMWR Morb Mort Wkly Rpt. 1995;44:37–9.
  21. Centers for Disease Control and Prevention. Viral gastroenteritis associated with consumption of raw oysters-Florida, 1993. MMWR Morb Mort Wkly Rpt. 1994;43:446–9.
  22. Centers for Disease Control and Prevention. State outbreak of viral gastroenteritis related to consumption of oysters-Louisiana, Maryland, Mississippi, and North Carolina, 1993. MMWR Morb Mort Wkly Rpt. 1993;42:945–8.
  23. Cannon  RO, Poliner  RJ, Hirshhorn  RB, Rodeheaver  DC, Silverman  PR, Brown  EA, A multistate outbreak of Norwalk virus gastroenteritis associated with consumption of commercial ice. J Infect Dis. 1991;164:860–4.PubMed
  24. Warner  RD, Carr  RW, McClesky  FK, Johnson  PC, Goldy Elmer  LM, Davison  VE. A large nontypical outbreak of Norwalk virus: gastroenteritis associated with exposing celery to nonpotable water and with Citrobacter freundii. Arch Intern Med. 1991;151:2419–24. DOIPubMed
  25. Centers for Disease Control and Prevention. Surveillance for waterborne disease outbreaks-United States, 1991-1992. MMWR Morb Mort Wkly Rpt. 1993;42:1–22.
  26. LeChevallier  MW, Norton  WD, Lee  RG. Giardia and Cryptosporidium spp. in filtered drinking water supples. Appl Environ Microbiol. 1991;57:2617–21.PubMed
  27. Rose  JB, Gerba  CP, Jakubowski  W. Survey of potable water supplies for Cryptosporidium and Giardia. Environ Sci Technol. 1991;25:1393–400. DOI
  28. Bean  NH, Griffin  PM, Goulding  JS, Ivey  CB. Foodborne disease outbreaks, 5-year summary, 1983-1987. MMWR Morb Mort Wkly Rpt. 1990;39(SS-1):15–57.
  29. Bean  NH, Goulding  JS, Lao  C, Angulo  FJ. Surveillance for foodborne disease outbreaks-United States, 1988-1992. MMWR Morb Mort Wkly Rpt. 1996;45(SS-5):1–66.
  30. Ortega  YR, Sterling  CR, Gilman  RH, Cama  VA, Diaz  F. Cyclospora speciesA new protozoan pathogen of humans. N Engl J Med. 1993;328:1308–12. DOIPubMed
  31. Hayes  EB, Matte  TD, O'Brien  TR, McKinley  TW, Logsdon  GS, Rose  JB, Large community outbreak of cryptosporidiosis due to contamination of a filtered public water supply. N Engl J Med. 1989;320:1372–6.PubMed
  32. MacKenzie  WR, Hoxie  NJ, Proctor  ME, Gradus  MS, Blair  KA, Peterson  DE, A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N Engl J Med. 1994;331:161–7. DOIPubMed
  33. Kapikian  AJ, Estes  MK, Chanock  RM. Norwalk group of viruses. In: Fields BN, Knipe DM, Howley PM, editors. Fields Virology. Philadelphia: Lippencott-Raven Publishers, Inc.; 1996.
  34. Current  WL, Garcia  LS. Cryptosporidiosis. Clin Microbiol Rev. 1991;4:324–58.
  35. Campbell  PN, Current  WL. Demonstration of serum antibodies to Cryptosporidium sp. in normal and immunodeficient humans with confirmed infections. J Clin Microbiol. 1983;18:165–9.PubMed
  36. Ungar  BLP, Soave  R, Fayer  R, Nash  TE. Enzyme immunoassay detection of immunoglobulin M and G antibodies to Cryptosporidium in immunocompetent and immunocompromised persons. J Infect Dis. 1986;153:570–8.PubMed
  37. DeLeon  R, Jaykus  L. Detection of bacteria and viruses in shellfish. In: Hurst CJ, Knudsen GR, McInerney MJ, Stenzenbach LD, Walter MV, editors. Manual of environmental microbiology. Washington (DC): American Society for Microbiology; 1996.
  38. Sobsey  MD, Carrick  RJ, Jensen  HR. Improved methods for detecting enteric viruses in oysters. Appl Environ Microbiol. 1978;36:121–8.PubMed
  39. Cole  MT, Kilgen  MB, Reily  LR, Hackney  CR. Detection of enteroviruses, bacterial indicators, and pathogens in Louisiana oysters and their overlying waters. J Food Prot. 1986;49:596–601.
  40. Jiang  X, Graham  DY, Wang  K, Estes  MK. Norwalk virus genome cloning and characterization. Science. 1990;250:1580–3. DOIPubMed
  41. Lambden  PR, Caul  EO, Ashley  CR, Clarke  IN. Sequence and genome organization of a human small round-structured (Norwalk-like) virus. Science. 1993;259:516–9. DOIPubMed
  42. Atmar  RL, Metcalf  TG, Neill  HF, Estes  MK. Detection of enteric viruses in oysters by using the polymerase chain reaction. Appl Environ Microbiol. 1993;59:631–5.PubMed
  43. Atmar  RL, Neill  HF, Romalde  JL, LeGuyader  F, Woodley  CM, Metcalf  TG, Detection of Norwalk virus and hepatitis A virus in shellfish tissues with the PCR. Appl Environ Microbiol. 1995;61:3014–8.PubMed
  44. Goswami  BB, Koch  WH, Cebula  TA. Detection of hepatitis A in Mercenaria mercenaria by coupled reverse transcription and polymerase chain reaction. Appl Environ Microbiol. 1993;59:2765–70.PubMed
  45. Lees  DN, Henshilwood  K, Dore  WJ. Development of a method for detection of enteroviruses in shellfish by PCR with poliovirus as a model. Appl Environ Microbiol. 1994;60:2999–3005.PubMed
  46. Lees  DN, Henshilwood  K, Green  J, Gallimore  CI, Brown  DWG. Detection of small round structured viruses in shellfish by reverse transcription-PCR. Appl Environ Microbiol. 1995;61:4418–24.PubMed
  47. Gouvea  V, Santos  N, Carmo Timenetsky  M, Estes  MK. Identification of Norwalk virus in artificially seeded shellfish and selected foods. J Virol Methods. 1994;48:177–87. DOIPubMed
  48. Deng  MY, Day  SP, Cliver  DO. Detection of hepatitis A virus in environmental samples by antigen-capture PCR. Appl Environ Microbiol. 1994;60:1927–33.PubMed
  49. Jaykus  L, DeLeon  R, Sobsey  MD. A virion concentration method for detection of human enteric viruses in oysters by PCR and oligoprobe hybridization. Appl Environ Microbiol. 1996;62:2074–80.PubMed
  50. Dix  A. Development of methods to extract human enteric viruses from hard-shelled clams for detection by reverse transcriptase-polymerase chain reaction (RT-PCR) and oligoprobe hybridization (OP) [thesis]. Raleigh (NC): North Carolina State University; 1997.
  51. Chung  H, Jaykus  L, Sobsey  MD. Improved detection of human enteric viruses in field oyster specimens by in vivo and in vitro amplification of nucleic acids. Appl Environ Microbiol. 1996;62:3772–8.PubMed
  52. Schaefer  FW III. Detection of protozoan parasites in source and finished drinking waters. In: Hurst CJ, Knudsen GR, McInerney MJ, Stenzenbach LD, Walter MV, editors. Manual of Environmental Microbiology. Washington (DC): American Society for Microbiology; 1996.
  53. LeChevallier  MW, Norton  WD, Siegel  JE, Abbaszadegan  M. Evaluation of the immunofluorescence procedure for detection of Giardia cysts and Cryptosporidium oocyts in water. Appl Environ Microbiol. 1995;61:690–7.PubMed
  54. Nieminski  EC, Schaefer  FW III, Ongerth  JE. Comparison of two methods for the detection of Giardia cysts and Cryptosporidium oocytes in water. Appl Environ Microbiol. 1995;61:1714–9.PubMed
  55. Versey  G, Slade  JS, Byrne  M, Shepard  K, Fricker  CR. A new method for the concentration of Cryptosporidium oocysts from water. J Appl Bacteriol. 1993;75:82–6.PubMed
  56. Rodgers  MR, Flanigan  DJ, Jakubowski  W. Identification of algae which interfere with the detection of Giardia cysts and Cryptosporidium oocysts and a method for alleviating this interference. Appl Environ Microbiol. 1995;61:3759–63.PubMed
  57. Campbell  AT, Robertson  LJ, Smith  HV. Viability of Cryptosporidium parvum oocytes: correlation of in vitro excystation with inclusion/exclusion of fluorogenic vital dyes. Appl Environ Microbiol. 1992;58:3488–93.PubMed
  58. Campbell  AT, Robertson  LJ, Smith  HV. Novel methodology in the detection of Cryptosporidium parvum: a comparison of cooled charge coupled device (CCD) and flow cytometry. Water Sci Technol. 1993;27:89–92.
  59. Campbell  AT, Haggart  R, Robertson  LJ, Smith  HV. Fluorescent imaging of Cryptosporidium using a cooled charge couple device (CCD). J Microbiol Methods. 1992;16:169–74. DOI
  60. Abbaszadegan  M, Gerba  CP, Rose  JB. Detection of Giardia cysts with a cDNA probe and applications to water samples. Appl Environ Microbiol. 1991;57:927–31.PubMed
  61. Erlandsen  SL, VanKeulen  H, Gurien  A, Jakubowski  W, Schafer  FW III, Wallis  P, Molecular approach to speciation and detection of Giardia: fluorochrome rDNA probes for identification of Giardia lamblia, Giardia muris, and Giardia ardeae in laboratory and environmental samples by in situ hybridization. In: Thompson RCA, Reynoldson JA, Lymbery AJ, editors. Giardia: from molecules to disease. Oxford: CAB International; 1994.
  62. Mahbubani  MH, Bej  AK, Perlin  M, Schaefer  FW III, Jakubowski  W, Atlas  RM. Detection of Giardia cysts by using polymerase chain reaction and distinguishing live from dead cysts. Appl Environ Microbiol. 1991;57:3456–61.PubMed
  63. Mahbubani  MH, Bej  AK, Perlin  M, Schaefer  FW III, Jakubowski  W, Atlas  RM. Differentiation of Giardia duodenalis and other Giardia spp. by using polymerase chain reaction and gene probes. J Clin Microbiol. 1992;30:74–8.PubMed
  64. Webster  KA, Pow  JDE, Giles  M, Catchpole  J, Woodward  MJ. Detection of Cryptosporidium parvum using a specific polymerase chain reaction. Vet Parasitol. 1993;50:35–44. DOIPubMed
  65. de la Cruz  AA, Sivaganesan  M. Detection of Giardia and Cryptosporidium spp. in source water samples by commercial enzyme-immunosorbant assay. In: Proceedings 1994 Water Technology Conference; 1994 Nov 6-10; San Francisco, California. Denver (CO): American Water Works Association, 1995.
  66. Sauch  JF, Flanigan  D, Galvin  ML, Berman  D, Jakubowski  W. Propidium iodide as an indicator of Giardia cyst viability. Appl Environ Microbiol. 1991;57:3243–7.PubMed
  67. Schupp  DG, Erlandsen  SL. A new method to determine Giardia cyst viability: correlation of florescein diacetate and propidium iodide staining with animal infectivity. Appl Environ Microbiol. 1987;53:704–7.PubMed
  68. Moe  CL, Gentsch  J, Ando  T, Grohmann  G, Monroe  SS, Jiang  X, Application of PCR to detect Norwalk virus in fecal specimens from outbreaks of gastroenteritis. J Clin Microbiol. 1994;32:642–8.PubMed
  69. Green  J, Norcott  JP, Lewis  D, Arnold  C, Brown  DWG. Norwalk-like viruses: demonstration of genomic diversity by polymerase chain reaction. J Clin Microbiol. 1993;31:3007–12.PubMed
  70. Wang  J, Jiang  X, Madore  HP, Gray  J, Desselberge  U, Ando  T, Sequence diversity of small, round-structured viruses in the Norwalk virus group. J Virol. 1994;68:5982–90.PubMed
  71. Ando  T, Monroe  SS, Gentsch  JR, Jin  Q, Lewis  DC, Glass  RL. Detection and differentiation of antigenically distinct small round-structured viruses (Norwalk-like viruses) by reverse transcription-PCR and southern hybridization. J Clin Microbiol. 1995;33:64–71.PubMed
  72. Centers for Disease Control and Prevention. Addressing emerging infectious disease threats: a prevention strategy for the United States. Atlanta (GA): U.S. Department of Health and Human Services, U.S. Public Health Service; 1996.

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The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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