0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Original Contribution |

Multinational Outbreak of Salmonella enterica Serotype Newport Infections Due to Contaminated Alfalfa Sprouts FREE

Chris A. Van Beneden, MD, MPH; William E. Keene, PhD, MPH; Robert A. Strang, MD, MHSc, FRCPC; Denise H. Werker, MD, MHSc, FRCPC; Arlene S. King, MD, MHSc, FRCPC; Barbara Mahon, MD, MPH; Katrina Hedberg, MD, MPH; Alison Bell, MD, MHSc, FRCPC; Michael T. Kelly, MD, PhD, FRCPC; Vijay K. Balan, MS; William R. Mac Kenzie, MD; David Fleming, MD
[+] Author Affiliations

Author Affiliations: Oregon Health Division, Portland (Drs Van Beneden, Keene, Hedberg, and Fleming); Epidemic Intelligence Service, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, Ga (Dr Van Beneden); Department of Health Care and Epidemiology, University of British Columbia, Vancouver (Drs Strang, King, and Bell); British Columbia Centre for Disease Control, Epidemiology Services, Vancouver (Drs Werker, King, and Bell); Field Epidemiology Training Program, Laboratory Centre for Disease Control, Health Canada, Ottawa, Ontario (Dr Werker); Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta (Dr Mahon); British Columbia Centre for Disease Control, Provincial Laboratory, Vancouver (Dr Kelly); Oregon State Public Health Laboratory, Portland (Mr Balan); and Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta (Dr Mac Kenzie).


JAMA. 1999;281(2):158-162. doi:10.1001/jama.281.2.158.
Text Size: A A A
Published online

Context In December 1995, reported Salmonella enterica serotype Newport (SN) infections increased sharply in Oregon and British Columbia but not elsewhere in North America. Similar unexplained increases had been noted in 6 other states in the fall of 1995.

Objective To determine the source of the outbreak(s).

Design Case-control studies, environmental investigations, bacterial subtyping, and surveillance information review.

Settings Oregon and British Columbia communities (winter 1995-1996) and Georgia, Oklahoma, Pennsylvania, Vermont, Virginia, and West Virginia (fall 1995).

Participants Oregon and British Columbia residents with culture-confirmed SN infections and onset from December 1, 1995, through February 29, 1996, and healthy community controls.

Main Outcome Measures Odds ratio (OR) of illness associated with exposures; distribution patterns and culture of alfalfa seeds and sprouts; subtyping of SN isolates.

Results We identified 133 cases in Oregon and British Columbia; 124 (93%) occurred in patients older than 18 years; 87 (65%) were female. Case patients were more likely than community control subjects to report having eaten alfalfa sprouts in the 5 days preceding illness (41% [17/41] vs 4% [3/75]; OR, 17.0; 95% confidence interval, 4.3-96.0). Case isolates shared a distinctive pulsed-field gel electrophoresis (PFGE) pattern. The SN was grown from seeds and alfalfa sprouts. The distribution of 1 seed lot to multiple growers corresponded to the distribution of cases. Distribution of a second seed lot from the same European wholesaler corresponded to the location of the fall outbreak, which was characterized by a similar demographic profile. The PFGE pattern of fall outbreak isolates and confiscated sprouts and seeds was indistinguishable from the Oregon and British Columbia outbreak and differed from background isolates.

Conclusions The SN-contaminated alfalfa seeds were distributed to multiple growers across North America in 1995 and resulted in a protracted international outbreak scattered over many months. Current sprouting methods are inadequate to protect consumers from such events. Alfalfa sprouts may be an elusive but important vehicle for salmonellosis and other enteric infections.

Figures in this Article

Foodborne illness is a worldwide problem. In the United States alone, at least 6.5 million cases of acute foodborne illness occur every year.1 In the past decade, new problems with food safety have been recognized, reflecting changes in the way food is produced, distributed, prepared, and consumed. Increasingly, epidemiologists are detecting outbreaks that cross regional and international boundaries, mirroring the widespread distribution of both raw agricultural commodities and processed foods.25

In January 1996, public health officials in Oregon and British Columbia independently noted marked increases in reported Salmonella enterica serotype Newport (SN) infections. Routine notification of surrounding states and provinces led to the recognition of this coincidence. The resulting coordinated epidemiologic investigation identified a common source outbreak.

Discussions with epidemiologists at the Centers for Disease Control and Prevention (CDC) led to the retrospective identification of a large and previously unexplained outbreak of SN infections affecting the central and eastern United States in the fall of 1995. Isolate subtyping and epidemiologic evidence suggest that both North American outbreaks were actually manifestations of a protracted outbreak caused by contaminated alfalfa seeds originally noted in Denmark in June 1995.6 These outbreaks heighten concern about the safety of a familiar food item and illustrate how contamination of a single, widely distributed product can lead to extensive, prolonged, and often difficult-to-recognize international outbreaks.

Oregon and British Columbia Outbreaks

Salmonellosis is reportable by law to public health agencies in Oregon and British Columbia. All Salmonella isolates are serotyped at central public health laboratories. In early January 1996, laboratorians in both areas noted an increase in isolations of SN.

Case Finding and Definitions. We defined an outbreak case patient as a resident of Oregon or British Columbia with onset of diarrhea between December 1, 1995, and February 29, 1996, from whom SN was cultured.

Case-Control Studies. We conducted hypothesis-generating telephone interviews with case patients who had illness onset in December 1995. For the case-control study, we compared case patients with onsets between January 1 and February 8, 1996, with 2 independent sets of control subjects. We excluded potential controls who reported having diarrhea within the preceding 30 days and those who were younger than 18 years, given the known age distribution of cases (only 7% of case patients were <18 years old). With use of a standard questionnaire, case patients and control subjects were asked about demographic characteristics and—for the 5 days before illness onset (cases) or interview (controls)—meals and snacks eaten away from home, travel, and consumption of an extensive list of specific food items.

Salmonellosis Controls. We surveyed currently healthy adults who had been previously diagnosed as having salmonellosis in 1995 as identified from provincial and state laboratories databases. We excluded those whose infections had been caused by serotype Newport or Stanley. (An outbreak of serotype Stanley infections elsewhere had been linked to sprout consumption in 1995.7)

Community Controls. We obtained a second set of controls by interviewing adults reached at randomly selected telephone numbers from the Portland, Ore, and Vancouver, British Columbia, residential directories.

Environmental Investigations and Tracebacks. We traced the distribution of sprouts eaten by case patients from retailers and restaurants back to local sprout growers and finally to alfalfa seed distributors. Public health inspectors reviewed food-handling practices at restaurants and sprouting facilities, collecting samples of seeds and sprouts when possible. We also interviewed staff at each restaurant identified by a case patient to determine if alfalfa sprouts were served on any menu items.

Multistate Outbreak, Fall 1995

Background. At the time of the Oregon–British Columbia outbreak, federal epidemiologists at the CDC and at the Laboratory Centre for Disease Control in Ottawa, Ontario, were unaware of any concurrent unusual SN activity. Six states, however, had reported marked increases in SN cases between August and October of 1995 (Laurence Slutsker, MD, CDC, oral communication, January 1996). A case-control study among Vermont college students with diarrhea, including 2 with SN infections, had implicated alfalfa sprouts as the probable source (Susan Schoenfeld, RN, MSPH, Vermont Department of Health, oral communication, January 1996). In the other 5 states, no specific sources had been identified, and the outbreaks had not been linked to each other. We hypothesized that contaminated alfalfa sprouts had caused these earlier outbreaks.

Case Finding; Case and Control Definitions. In the United States, state public health laboratories report all Salmonella isolates and serotypes to CDC through the Public Health Laboratory Information System. We reviewed summary data for 1995 SN infections. Information was available for 43 of 50 states. We defined outbreak states as those with a greater than 10-fold increase in reported SN incidence during the fall outbreak period (August-October 1995) relative to the rates from January through July 1995. We defined control states as those reporting a less than 4-fold increase, excluding states with 4- to 9-fold increases.

Case-Control Study. In 1995, more than 70% of alfalfa seed sold to sprout growers in the United States came from a single distributor. We reviewed shipping records from this distributor and compiled a list of seed lots shipped to sprout growers throughout the United States during the outbreak period. In a case-control analysis, we compared the distribution of specific seed lots with outbreak and control states, excluding states receiving no seeds from the national distributor during this period.

Laboratory Investigations. In Oregon, alfalfa sprouts and seeds were screened for Salmonella with use of a commercial enzyme-linked immunosorbent assay kit following broth enrichment, followed by standard culture methods.8,9 Canada's Health Protection Branch used preenrichment followed by selective enrichment and streaking onto selective agars.10 Confiscated seeds were also germinated in the laboratory and subsequently cultured.9,10

The SN isolates were characterized by pulsed-field gel electrophoresis (PFGE), cutting with XbaI,11 and bacteriophage typing12 as previously described.

Statistical Analysis

Data were analyzed using the χ2 test, the 2-tailed Fisher exact test, or stratified analysis as appropriate.13

Oregon and British Columbia Outbreak

Descriptive Epidemiology. We identified a total of 133 case patients, ranging in age from 1 day to 94 years (median, 36 years); 124 (93%) were aged 18 years or older. Eighty-seven (65%) were female. (In contrast, in 1995 only 62% of the 1213 reported salmonellosis cases in Oregon and British Columbia were aged ≥18 years; 50% were female.) All patients reported diarrhea. Ten percent of the outbreak case patients were hospitalized; there were no deaths.

Geographically, cases were scattered across western Oregon and southern British Columbia. Most case patients reported onsets of symptoms in December and January (Figure 1). Almost no cases were linked by exposure to shared meals at restaurants, other public gatherings, or within a household.

Figure. Epidemic Curve by Week of Onset, January 1995-June 1996
Graphic Jump Location
The curve shows confirmed cases of Salmonella enterica serotype Newport infection in Oregon and British Columbia (BC). Cases increased sharply in early December 1995 and then declined dramatically after recall of alfalfa seeds and sprouts.

Case-Control Studies. Although case patients were not more likely than either set of control subjects to have eaten at a particular restaurant, they were more likely to have eaten meals away from home in general (95% of case patients vs 74% of salmonellosis controls [odds ratio (OR), 6.7; 95% confidence interval (CI), 1.5-61.0] and 57% of community controls [OR, 14.5; 95% CI, 3.3-131.0]). Alfalfa sprouts were the only item from among a list of more than 70 foods and drinks that was statistically associated with illness compared with both sets of controls, although only a minority of case patients in the case-control study recalled sprout consumption in the 5 days before onset 17 (41%) of 41 case patients reported eating sprouts vs 10 (12%) of 86 salmonellosis controls (OR, 5.4; 95% CI, 2.0-15.0) and 3 (4%) of 75 community controls (OR, 17.0; 95% CI, 4.3-96.0). (Another 4 cases reported eating foods that, according to restaurant staff, always included alfalfa sprouts.) At least 26 case patients (63%) ate at a restaurant that served alfalfa sprouts, compared with 17 (20%) of 86 salmonellosis controls. Similar data were unavailable for community controls.

The incubation periods for the 16 case patients for whom a unique sprout consumption date could be determined ranged from 12 hours to 5 days (mean, 3.5 days; median, 4 days).

Environmental Investigations and Tracebacks. Alfalfa sprouts consumed by 8 of 11 Oregon case patients with a single identifiable source were traced back to 1 Portland grower. During the outbreak period, lot A was identified as the only source of seed for this grower. Approximately 90% (16,340 kg) of lot A was shipped from the distributor to growers in Oregon and British Columbia. The restriction of cases to Oregon and British Columbia was thus explained by the distribution and sales of alfalfa sprouts germinated from a single seed lot, lot A. No noteworthy irregularities were found on inspection of this or any other sprouting facility involved in this outbreak.

The national distributor purchased alfalfa seed from multiple sources in several countries. Lot A seed came from another distributor in the Netherlands. No obvious evidence of contamination or mishandling was found at either distributor's facility. It was impossible to identify the farm or even the continent from which lot A seed originated; adequate records were not available from the Dutch facility.

Control Measures. Through media releases on February 8, 1996, we notified the public about the outbreak and its association with alfalfa sprouts. Health officials elsewhere in Canada and the United States were also alerted. Unsold alfalfa sprouts and approximately 9100 kg of unsprouted lot A seed were recalled. Reported SN infections soon declined to preepidemic levels (Figure 1).

Laboratory Investigations.Culture of Alfalfa Seed and Sprouts. The SN was grown from 1 of 52 samples of sprouts (an opened package) and none of 31 samples of lot A seed taken from grocery stores, homes, restaurants, and sprout growers in Oregon and British Columbia. Salmonella Newport was also grown from unsprouted lot A seed confiscated from a grower in California (Gregory Inami, BA, Microbial Diseases Laboratory, California Department of Health Services, oral communication, June 1997).

Subtyping. We subtyped 80 SN isolates from Oregon and British Columbia by PFGE. Thirty-five (81%) of 43 isolates obtained during the outbreak period were indistinguishable (the "outbreak pattern"); 3 other isolates differed by a single band. In contrast, the outbreak pattern was not seen in any of 19 preoutbreak isolates tested and in only 4 of 18 postoutbreak isolates. Salmonella Newport isolates cultured from confiscated sprouts and lot A seed shared the outbreak pattern. Nonoutbreak pattern isolates were extremely heterogenous.

We phage typed 96 SN isolates from Oregon and British Columbia; 83 (93%) of 89 outbreak period isolates were type 2, compared with only 1 of 7 preoutbreak isolates (that one coming just 1 week earlier). All isolates with the outbreak PFGE pattern or its close variant tested were phage type 2. All other isolates were phage type 4, 5, 8, or 14 or were untypable.

Multistate Outbreak, Fall 1995

Case-Control Study. We identified 6 outbreak states (Vermont, Pennsylvania, Georgia, Oklahoma, Virginia, and West Virginia) and 13 control states. The same national distributor shipped alfalfa seeds from 29 uniquely numbered lots to growers in these 19 states during August and September 1995. The mean number of sprout growers in outbreak and control states was similar (2.3 and 2.5, respectively), as was the mean quantity of seed shipped to growers in those states (3235 kg and 2433 kg, respectively). The distribution of only 1 lot, lot Z, was strongly associated with outbreak occurrence. Lot Z was shipped to 5 (83%) of 6 outbreak states and 1 (8%) of 13 control states (OR, 60; 95% CI, 2.2-3056.0). (Most of the sprouts sold in West Virginia—the 1 state that did not get lot Z seed—came from a grower in neighboring Pennsylvania that did receive seed from lot Z.) Lot Z was purchased by the same national distributor from the same Dutch seed broker as lot A, and was similarly untraceable to the continent or farm of origin.

Laboratory Investigations.Subtyping. By PFGE, we subtyped 31 SN isolates obtained from residents of the fall outbreak states (provided by public health laboratorians of those states and CDC). None of 6 isolates that were collected before distribution of lot Z seed matched the outbreak pattern, whereas 22 (85%) of 25 isolates obtained during the fall outbreak period were indistinguishable from the outbreak pattern. No lot Z seeds were available for microbiological testing. A representative isolate from the June 1995 Danish outbreak also matched the Oregon–British Columbia outbreak pattern.

Consumption of a single lot of contaminated alfalfa seeds caused a large outbreak of salmonellosis in Oregon and British Columbia. Illness was strongly associated with sprout consumption, SN with the outbreak PFGE pattern was isolated from almost all outbreak-associated cases and from leftover sprouts and seeds, and SN infections rapidly declined following recall of the implicated lot. Temporal and geographical clustering of cases in 2 jurisdictions clearly indicates that the source of contamination was the seed itself and not contamination that occurred during production or mishandling of the final product.

Further evidence indicates that contaminated seed from the same distributor caused the previously unexplained SN outbreaks in other states during the fall of 1995. First, distribution of a different seed lot was statistically associated with the occurrence of large SN outbreaks with a similar demographic profile. Second, the PFGE patterns of isolates from these outbreaks matched the Oregon–British Columbia pattern, whereas the PFGE patterns from SN isolates collected before lot Z was distributed were different.

The knowledge that early in 1995 Denmark had implicated alfalfa sprouts in an SN outbreak greatly facilitated the focus of our investigation. The demographic profile and PFGE fingerprints of the Danish outbreak matched those found in Oregon and British Columbia.6

Collectively, these observations indicate that alfalfa seeds, most likely contaminated from a single source, were distributed through multiple channels first to growers in Europe and then to North America, causing numerous localized manifestations of 1 large outbreak that extended over at least 9 months. Seeds grown on different farms are commonly mixed. Lot numbers only correspond to shipping units, not processing or harvesting units; seeds from the same source could be shipped as multiple lots.

Several epidemiologic features of this investigation are worth highlighting. First, although finding a preponderance of adults (and particularly women) is neither a necessary nor sufficient criterion of a sprout-associated outbreak, it has been noted repeatedly; presumably women have different eating habits than men. Second, the median incubation period for these cases exceeded the maximum cited in a standard communicable disease reference.14 Had we restricted food histories to 3 or fewer days, we would not have statistically implicated alfalfa sprouts in our case-control study (data not shown). This long incubation period and general lack of case clustering by household or defined social gatherings suggest that the attack rate for persons who ate these sprouts was low, presumably reflecting low levels of sprout contamination. Third, in contrast to most foodborne outbreaks, only a minority of cases (in this outbreak, 41%) recalled eating the implicated food. This is likely because of cross-contamination of salad and sandwich bars or sprouts' concealed presence in other foods.7

Sprout-associated outbreaks are being increasingly recognized. Alfalfa sprouts were initially implicated as a vehicle of unidentified foodborne illness in 1973.15 Although they were implicated repeatedly in unpublished investigations in Finland during the 1980s and early 1990s,16 most epidemiologists gave little thought to sprouts as a potential vehicle until 1995, when a brief account of a large Scandinavian epidemic was published.17 A large North American outbreak of alfalfa sprout–associated salmonellosis, caused by serotype Stanley and with many similarities to the SN outbreak, occurred shortly thereafter in 1995.7 In the SN outbreak described herein, we estimate that more than 20,000 persons contracted SN infections from eating these contaminated alfalfa sprouts in North America alone, as fewer than 5% of Salmonella infections are thought to be reported.18 Since the SN epidemic, outbreaks of salmonellosis caused by different serotypes have been traced to alfalfa sprouts at least 4 times in North America1921 (W.E.K., unpublished data, October 1997). In almost every instance, investigations were triggered because of an increase in reports of relatively uncommon serotypes. This not only underscores the value of routine serotyping but also suggests that similar outbreaks caused by more common serotypes would be easy to miss. Alfalfa sprouts have also been implicated in a recent outbreak of Escherichia coli O157:H7 infections.22

Alfalfa sprouts are a well-suited vehicle for salmonellosis. Seeds are often stored for months or years under cool, dry conditions in which salmonellae are stable.23 During the 3- to 5-day sprouting process, numbers of salmonellae may increase by 3 to 4 orders of magnitude, decreasing little if at all during subsequent refrigeration.24,25 Alfalfa sprouts are rarely washed or cooked before consumption, and consumers are left with little protection other than chance.

From farm to table, many opportunities exist for contamination of alfalfa seeds or sprouts. Crops can be easily contaminated with dirty water, runoff from adjacent farms, animal fertilizers used in previous growing seasons, or droppings from rodents or ruminants. Assurance of a clean seed would require intensive monitoring of farmlands and dedication of fields and harvest machinery to a crop of seeds destined for sprouting. As only a minority of alfalfa seed production is earmarked for sprouting and therefore human consumption, the above methods might prove too expensive for farmers. Furthermore, few regulations are currently consistently applied to all sprout growers. In fact, whether a grower is considered a food producer or a farmer varies from state to state.

Some sprout distributors and growers are currently testing seed samples prior to distribution or sprouting. As contamination may be intermittent and low level, this testing is probably ineffective. For example, lot A seed samples cultured by the national distributor tested negative for Salmonella. Although "downstream" preventive efforts have been studied more closely, the fundamental problem is that the sprouting process contains no "kill step" that would eliminate pathogens without compromising a seed's germination potential. Calcium hypochlorite, sodium hypochlorite, hydrogen peroxide, and ethanol have all been tested as methods of seed decontamination before sprouting. These treatments can significantly reduce populations of Salmonella inoculated onto alfalfa seeds without adversely affecting germination. However, viable salmonellae can still be detected after treatment, indicating the potential for multiplication during sprouting. Salmonella organisms likely reside in seed crevices and between the cotyledon and testa, areas not reached by chemical treatments.26,27 Irradiation is currently being evaluated as an adjunct seed decontamination method. Until barriers to a pathogen-free seed are resolved, however, we conclude that alfalfa sprouts are a high-risk food for salmonellosis. All consumers, particularly those at greatest risk for severe disease (immunocompromised, elderly, and very young people), should consider this danger when deciding whether to eat alfalfa sprouts.

Bennett JV, Holmberg SD, Rogers MF, Solomon SL. Infectious and parasitic diseases. In: Amler RW, Dull HB, eds. Closing the Gap: The Burden of Unnecessary Illness. New York, NY: Oxford University Press; 1987.
Hedberg CW, MacDonald KL, Osterholm MT. Changing epidemiology of food-borne disease: a Minnesota perspective.  Clin Infect Dis.1994;18:671-682.
Herwaldt BL, Ackers ML.and the Cyclospora Working Group.  An outbreak in 1996 of cyclosporiasis associated with imported raspberries.  N Engl J Med.1997;336:1548-1556.
Lehmacher A, Bockemuhl J, Aleksic S. Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips.  Epidemiol Infect.1995;115:501-511.
Tauxe R, Kruse H, Hedberg C, Potter M, Madden J, Wachsmuth K. Microbial hazards and emerging issues associated with produce.  J Food Protection.1997;60:1400-1408.
Wegener HC, Baggesen DL, Neimann J, Nielsen SV. An outbreak of human salmonellosis in Denmark caused by alfalfa sprouts. In: Proceedings and abstracts of the International Symposium on Salmonella and Salmonellosis; Ploufragan, France; May 20-22, 1997:587-589.
Mahon BE, Ponka A, Hall WN.  et al.  An outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds.  J Infect Dis.1997;175:876-882.
AOAC International.  Salmonella in foods. In: Official Methods of Analysis of AOAC International. 16th ed. Arlington, Va: Association of Official Analytical Chemists International; 1995:chap 17.
Food and Drug Administration.  Bacteriological Analytical Manual. 7th ed. Arlington,Va: Association of Official Analytical Chemists International; 1992:chap 5.
Health Protection Branch.  Methods for the isolation and identification of salmonella from foods. In: Compendium of Analytical Methods.Vol. 2. Montreal, Quebec: Polyscience Publications Inc; 1978.
Taylor DE, Eaton M, Yan W, Chang N. Genome maps of Campylobacter jejuni and Campylobacter coli J Bacteriol.1992;174:2332-2337.
Anderson ES, Williams RE. Bacteriophage typing of enteric pathogens and staphylococci and its use in epidemiology.  J Clin Pathol.1956;9:94-114.
 Epi Info [computer program]. Version 6.04b. Atlanta, Ga: Centers for Disease Control and Prevention; 1995.
Benenson AS. Control of Communicable Diseases Manual. 16th ed. Washington, DC: American Public Health Association; 1995:412.
Centers for Disease Control.  Foodborne and Waterborne Disease Outbreaks Annual Summary—1973. Atlanta, Ga: Centers for Disease Control; 1974:23.
Puohiniemi R, Heiskanen T, Siitonen A. Molecular epidemiology of two international sprout-borne Salmonella outbreaks.  J Clin Microbiol.1997;35:2487-2491.
Pönkä A, Andersson Y, Siitonen A.  et al.  Salmonella in alfalfa sprouts.  Lancet.1995;345:462-463.
Chalker RB, Blaser MJ. A review of human salmonellosis, III: magnitude of Salmonella infection in the United States.  Rev Infect Dis.1988;9:111-124.
Mouzin E, Werner SB, Bryant RG.  et al.  When a health food becomes a hazard: a large outbreak of salmonellosis associated with alfalfa sprouts—California. In: Proceedings and abstracts of the 46th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 14-18, 1997.
Glynn MK, Patrick S, Wuhib T.  et al.  When health food isn't so healthy—an outbreak of Salmonella serotypes Anatum and Infantis associated with eating contaminated sprouts, Kansas and Missouri, 1997. In: Proceedings and abstracts of the 47th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 13-17, 1998.
Buck P, Grimsrud K, Waters J.  et al.  Would you like a little Salmonella with your sandwich? In: Proceedings and abstracts of the 47th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 13-17, 1998.
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;46:741-744.
Bryan FL. What the sanitarian should know about staphylococci and salmonellae in non-dairy products, II: salmonellae.  J Milk Food Technol.1968;31:131-140.
Andrews WH, Mislivec PB, Wilson CR.  et al.  Microbial hazards associated with bean sprouting.  J Assoc Off Analytical Chem.1982;65:241-248.
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;62:2212-2215.
Beuchat LR. Comparison of chemical treatments to kill Salmonella on alfalfa sprouts destined for sprout production.  Int J Food Microbiol.1997;34:329-333.
Itoh Y, Sugita-Konishi Y, Kasuga F.  et al.  Enterohemorrhagic Escherichia coli O157:H7 present in radish sprouts.  Appl Environ Microbiol.1998;64:1532-1535.

Figures

Figure. Epidemic Curve by Week of Onset, January 1995-June 1996
Graphic Jump Location
The curve shows confirmed cases of Salmonella enterica serotype Newport infection in Oregon and British Columbia (BC). Cases increased sharply in early December 1995 and then declined dramatically after recall of alfalfa seeds and sprouts.

Tables

References

Bennett JV, Holmberg SD, Rogers MF, Solomon SL. Infectious and parasitic diseases. In: Amler RW, Dull HB, eds. Closing the Gap: The Burden of Unnecessary Illness. New York, NY: Oxford University Press; 1987.
Hedberg CW, MacDonald KL, Osterholm MT. Changing epidemiology of food-borne disease: a Minnesota perspective.  Clin Infect Dis.1994;18:671-682.
Herwaldt BL, Ackers ML.and the Cyclospora Working Group.  An outbreak in 1996 of cyclosporiasis associated with imported raspberries.  N Engl J Med.1997;336:1548-1556.
Lehmacher A, Bockemuhl J, Aleksic S. Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips.  Epidemiol Infect.1995;115:501-511.
Tauxe R, Kruse H, Hedberg C, Potter M, Madden J, Wachsmuth K. Microbial hazards and emerging issues associated with produce.  J Food Protection.1997;60:1400-1408.
Wegener HC, Baggesen DL, Neimann J, Nielsen SV. An outbreak of human salmonellosis in Denmark caused by alfalfa sprouts. In: Proceedings and abstracts of the International Symposium on Salmonella and Salmonellosis; Ploufragan, France; May 20-22, 1997:587-589.
Mahon BE, Ponka A, Hall WN.  et al.  An outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds.  J Infect Dis.1997;175:876-882.
AOAC International.  Salmonella in foods. In: Official Methods of Analysis of AOAC International. 16th ed. Arlington, Va: Association of Official Analytical Chemists International; 1995:chap 17.
Food and Drug Administration.  Bacteriological Analytical Manual. 7th ed. Arlington,Va: Association of Official Analytical Chemists International; 1992:chap 5.
Health Protection Branch.  Methods for the isolation and identification of salmonella from foods. In: Compendium of Analytical Methods.Vol. 2. Montreal, Quebec: Polyscience Publications Inc; 1978.
Taylor DE, Eaton M, Yan W, Chang N. Genome maps of Campylobacter jejuni and Campylobacter coli J Bacteriol.1992;174:2332-2337.
Anderson ES, Williams RE. Bacteriophage typing of enteric pathogens and staphylococci and its use in epidemiology.  J Clin Pathol.1956;9:94-114.
 Epi Info [computer program]. Version 6.04b. Atlanta, Ga: Centers for Disease Control and Prevention; 1995.
Benenson AS. Control of Communicable Diseases Manual. 16th ed. Washington, DC: American Public Health Association; 1995:412.
Centers for Disease Control.  Foodborne and Waterborne Disease Outbreaks Annual Summary—1973. Atlanta, Ga: Centers for Disease Control; 1974:23.
Puohiniemi R, Heiskanen T, Siitonen A. Molecular epidemiology of two international sprout-borne Salmonella outbreaks.  J Clin Microbiol.1997;35:2487-2491.
Pönkä A, Andersson Y, Siitonen A.  et al.  Salmonella in alfalfa sprouts.  Lancet.1995;345:462-463.
Chalker RB, Blaser MJ. A review of human salmonellosis, III: magnitude of Salmonella infection in the United States.  Rev Infect Dis.1988;9:111-124.
Mouzin E, Werner SB, Bryant RG.  et al.  When a health food becomes a hazard: a large outbreak of salmonellosis associated with alfalfa sprouts—California. In: Proceedings and abstracts of the 46th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 14-18, 1997.
Glynn MK, Patrick S, Wuhib T.  et al.  When health food isn't so healthy—an outbreak of Salmonella serotypes Anatum and Infantis associated with eating contaminated sprouts, Kansas and Missouri, 1997. In: Proceedings and abstracts of the 47th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 13-17, 1998.
Buck P, Grimsrud K, Waters J.  et al.  Would you like a little Salmonella with your sandwich? In: Proceedings and abstracts of the 47th Annual Epidemic Intelligence Service Conference; Atlanta, Ga; April 13-17, 1998.
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;46:741-744.
Bryan FL. What the sanitarian should know about staphylococci and salmonellae in non-dairy products, II: salmonellae.  J Milk Food Technol.1968;31:131-140.
Andrews WH, Mislivec PB, Wilson CR.  et al.  Microbial hazards associated with bean sprouting.  J Assoc Off Analytical Chem.1982;65:241-248.
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;62:2212-2215.
Beuchat LR. Comparison of chemical treatments to kill Salmonella on alfalfa sprouts destined for sprout production.  Int J Food Microbiol.1997;34:329-333.
Itoh Y, Sugita-Konishi Y, Kasuga F.  et al.  Enterohemorrhagic Escherichia coli O157:H7 present in radish sprouts.  Appl Environ Microbiol.1998;64:1532-1535.

Letters

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 99

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles