Fresh fruit juice: how a healthy habit can lead to a nationwide outbreak of gastroenteritis by Salmonella Panama

Posted: September 24th, 2010 - 7:28am
Source: Infectious Diseases Bulletin Volume 21 Number 7

Summary: In the spring of 2008 within 2 weeks by several laboratories 15 patients with Salmonella infection reported in Panama, 2 times more than in all of 2007. To find out the cause and subsequent infection with S. Panama to avoid was epidemiological and microbiological research source used. From a case-control study with 23 patients and 24 control subjects showed that the outbreak was caused by consumption of unpasteurized fruit juices from a producer (odds ratio: 7.4, 95% CI: 1.5 to 37.2). An increasing number of consumers seek healthy food, but consequently exposed to the infection risk of fresh foods such as unpasteurized fruit juices, ready-to-eat salads and fruit salads. Therefore, consumers using the product should be informed about the possibility of microbial contamination. Strict enforcement of food safety procedures and a higher frequency of microbiological control during production, the risk of infection can limit.
Salmonella is a common cause of food poisoning which 2400 models are described. Salmonella enterica subspecies enterica serotype Panama is a member of serogroup D1 and in the past has been isolated from many foods from animals and water. (1) Infection with Salmonella (S.) Panama usually causes gastroenteritis, but may be somewhat more likely than other serotypes, including invasive disease may result. (2, 3) have reported patients with complications such as bacteremia and meningitis. (3, 4)
In the 80s and 90s was S. Panama regularly found in pigs and humans in the Netherlands (5% and 3% of all isolates between 1984 and 2001). (5) From the beginning of 2000, S. Panama has become a rare serotype reported fewer than 10 patients per year.
Through the nationwide network of the former regional laboratories received the RIVM Salmonella isolates for serotyping and phage typing. This surveillance will cover approximately 64% of the Dutch population. Each year, approximately 1500 isolates of laboratory-confirmed patients and investigated approximately 2500 isolates from food, animals and environmental samples.
Between January and May 2008 showed the early warning system for Salmonella a sharp increase in the number of laboratory-confirmed patients with S. Panama, throughout the Netherlands. Alone in week 16 and 17 of 2008, 15 patients reported 2 times as many as in 2007. In response, a study was launched in collaboration with the Food and Safety Authority (VWA) for the outbreak to identify and investigate sources with the ultimate goal to further infections with S. Panama to avoid.
For the study, patients were defined as persons with laboratory-confirmed infection with S. Panama and the first day of illness from January 1, 2008, in the seven days preceding the first day of illness stayed in the Netherlands. Gastroenteritis was defined as diarrhea (at least 3-times loose stools in 24 hours) or at least two of the following symptoms: vomiting, nausea, blood in stool, or abdominal pain. The laboratory provided information on the patients, including age, gender, address and date of diagnosis. The required details of the patients were delivered by the relevant health authorities by the sending physician. To generate hypotheses, was among the seven most recent patient survey conducted by telephone about possible exposures in the 8 days preceding the first day of illness. It was asked to purchase and consumption of certain foods, other possible sources of infection such as contact with animals or with another person with diarrhea, and recent travels. From these interviews showed that all patients beef or pork products had eaten, and that 5 of the 7 patients (71%) had been drinking fresh fruit juice.
Following July 1 questionnaires was a case-control study was conducted to test the hypothesis that patients often had been drinking fresh fruit juice than control subjects. Each patient was paired with two control subjects according to their place of residence and age (+ / - 5 years). This was the patient asked to contact three potential control subjects from their friends and acquaintances. A control person could not have had gastroenteritis in the 2 weeks prior to the first illness linked to the patient. On May 19 was an invitation by e-mail sent to the patients and control subjects, asking for a questionnaire to complete on the Internet about the symptoms of gastro-enteritis, possible sources of infection and travel behavior. This specifically inquired about buying, shopping and consumption, among other beef and pork products and fresh juices. Patients were asked that information about the three days preceding the first day of illness and the control subjects were asked about three typical days in April 2008.
The data from the questionnaires were statistically analyzed in STATA ® 10.0, with a two-tailed Fisher exact test was used for comparison of frequencies. Odd ratios were calculated by conditional logistic regression. For the analysis of case-control study was first looked at the association between gastroenteritis and each food product. Were then grouped into food preparation and composition, eg grouping of several types of pork sausage, pork and pork sandwiches. Variables were in the multivariate conditional logistic regression analysis included, when a p-value of an odds ratio lower than 0.25 in the univariate analysis, or when more than half of the patients had consumed a food product.
The historical database is searched and Salmonella isolates from food animals, corresponding to the S. Panama tribe of the outbreak. S. Panama recent isolates from patients and food animals were microbiologically compared with pulsed field gel electrophoresis (PFGE). (6) These data are analyzed in BioNumerics V.4.00, which PFGE patterns were regarded as different if they differed at least one band. The isolates were also tested for sensitivity to 12 commonly used antibiotics. (7) Following the results of microbiological tests and questionnaires did the VWA investigation into possible sources of infection.
Because during the growing source of research evidence that fresh fruit was the most likely source of infection for the outbreak, we have further examined the survival of S. Panama outbreak strain in fruit juices. This fruit was infected with S. Panama and refrigerated at 5 ° C. At 1, 2, 3 and 6 days after infection, the number of colony forming units (CFU) counted and compared with the number of CFU of S. Panama in a control medium that was kept under the same conditions. The acid tolerance was tested by counting the number of CFU before and after passage through (an imitation of) the human stomach. This outbreak strain was kept for 1 hour at pH 2.5 and a temperature of 37 ° C. For comparison, this was also done with two other strains of Salmonella, which are known to be acid resistant (and ST7945 ST060801). Salmonella may develop by staying in an acidic environment such as fruit juice better acid resistance and thus better survival against the bactericidal acidity in the human stomach. Therefore, the acid resistance both before and after exposure to fruit juices tested. Further details of the methods are described elsewhere. (8)
A total of 33 patients identified with laboratory-confirmed infection with S. Panama between April and June 2008, spread over 14 different health center. (Figure 1) between the first illness of the patient and characterization of the isolate sent to the RIVM sat an average of 16 days (range 8-48 days). The median age of patients was 18 years (range 0-66 years) and women were better represented than men (sex ratio F / M = 2.5). Ten patients had been hospitalized in a hospital. S. Panama was in 7 patients isolated from blood samples and in 1 patient from pus from a perianal abscess.
The questionnaire of the case-control study was completed by 23 patients and 24 control subjects. The day of onset of three-quarters (78%) of patients fell between 1915 and April 24. The most commonly reported symptoms were diarrhea (91%), abdominal pain (83%) and fever (68%). The most frequently consumed foods were fresh fruit juice (17/23), fried pork (15/23), ham and pork sandwiches (14/23) and pork (14/23). All patients reported that they had been shopping at supermarket X, compared to 19/24 controls (p = 0.01). Of the 17 patients who reported consumption of fresh fruit, 11 could still remember the kind of juice they had purchased, ie 500 ml bottles of brand Y. Juices were called by different composition, all of which contain orange juice or in combination with other fruits. Compared with controls, patients reported more frequent consumption of fresh fruit juice (odd ratio: 10.2. 95% CI: 1.3 to 81.5). Consumption of fruit juice brand Y was also significantly associated with disease (odd ratio: 5.4. 95% CI: 1.1 to 25.7). In the multivariate analysis, only consumption of fruit juice are significantly associated with disease (odd ratio: 7.4. 95% CI: 1.5 to 37.2). (Table 1)
Of the 33 S. Panama isolates from patients were collected between April and May 2008, 32 isolates had the same PFGE pattern and an isolate with a different band. (Figure 2) The patient with the different isolates had not participated in the case-control study. S. Panama isolates from the patients showed no resistance to 12 commonly used antibiotics. Salmonella in the historical database were 4 S. Panama isolates found in animals and feed, three different PFGE patterns. This seemed not related to the S. Panama -
strain of the outbreak.
The pH of the fresh juice from supermarket X, who had been drunk by the patients ranged between 3.4 and 3.6. Ensure the survival of S. Panama to investigate these juices were infected with S. Panama Tribe of the outbreak after the first juices tested were negative (CFU <100) in the presence of Salmonella. Seven days after infection of the fruit, decreased the number of CFU of S. Panama from a high 2.8 ° 107 CFU on day one to 2.0 ° 106 CFU (Figure 4). Based on the analysis estimates that the minimum pH for growth in the juice is 3.4 for this strain. The outbreak strain also survived the imitation of a passage through the human stomach. After 1 hour exposure to a pH of 2.5 and a temperature of 37 ° C, the number of CFU decreased from 5.4 to 2.3 ° × 105 103. Extent of survival was similar to the decrease in the number of CFU that was seen in two other strains of Salmonella, which are known to be acid resistant (ST7945 decreased from 5.0 × 105 to 7.8 · 103. ST060801 decreased from 3.7 × 105 to 2.1 ° 103).
In July 2008, concerning the outcome of the case-control study, contacted the supermarket X. The VWA put an inspection by the manufacturer of the suspect fresh fruit juices. During the inspection, no samples were taken from the production of microbiological research, because at that time for several weeks, no new patients were found. In the production were all rotten fruit rinsed with water and fruits were manually removed from it. Fresh orange juice was used as the basis for all types of fruit were produced. The juices were not pasteurized, so after production is the shelf life limited to seven days in the refrigerator. The VWA saw production rise to no concern regarding the disinfection and hygiene procedures were performed according to HACCP (Hazard Analysis and Critical Control Point) procedures. (9) It was the VWA inspectors, however, that the frequency of microbiological controls in the production was rather low in proportion to the amount of juice per day was produced.
Source Research has shown that nationwide outbreak of gastroenteritis S. Panama in the spring of 2008 was caused by a single point source, unpasteurized fruit juices from a producer and distributed throughout the country. The assortment of unpasteurized fruit juices brand of supermarket X Y contains not only fresh orange juice, but also a variety of mixed unpasteurised fruit juices of different fruits. All variants contain the assortment of fresh orange juice, however, so it is possible that contaminated juice was the common source of infection for all the juices of different composition. The
HACCP procedures of the producer were not sufficient for large scale production of unpasteurized fruit juices, making a cross-contamination could remain undetected. Based on the first day of illness of patients and the seven-day shelf life of fresh fruit juices of brand X, the most probable time of infection with the producer about the last two weeks of April 2008.
The most recent outbreak of S. Panama in Europe took place in the summer of 2007 in Germany. This outbreak was caused by another strain of S. Panama and source study showed that salami sausages had been the source of infection. (10) Our nationwide outbreak was 24% of patients reported invasive disease (bacteremia in 7 patients and a perianal abscess in 1 patient), which corresponds to the literature on the severity of disease caused by S. Panama. (3)
We expect the association between illness and consumption of fresh fruit juice from supermarket X is still underestimated, because not all patients could remember which fruits were contained in the fresh fruit they had been drinking. But all patients have remembered that the fresh juice from brand Y was. At the time the producer was visited by inspectors from the VWA, none of the accused parties more juice available for microbiological testing. This is due to the rapid production turnover appropriate to the short shelf life of only 7 days, from the unpasteurized fruit juices. During the mission, no samples were taken from the production line, because at that time for several weeks, no new patients were found. Because no suspect consignment of fruit juice could be identified, it also failed to determine which party fruits were infected, or how the fruit became infected. This is a problem often seen in outbreaks of gastroenteritis by fresh products with short shelf life.
The last outbreak in Europe described by Salmonella in combination with pasteurized juice is from 1922. (11) In contrast to Europe, reported the Centers for Disease Control and Prevention (CDC) in the United States between 1995 and 2005 alone, six outbreaks of Salmonella infections were associated with fruit juices, although as a decrease in fruit juice-related outbreaks was seen since the introduction of HACCP in 2001. (12, 13) In the United States and
Canada are also serious juice-related outbreaks of gastroenteritis caused by set
E. Coli O157: H7. (14-16) The food in Western Europe to similar standards and hygiene
HACCP standards in the United States. It is not clear why in Europe, fewer outbreaks of gastroenteritis by pasteurized juice would take place. There may be a relative under-reporting, allowing the extent and severity of gastroenteritis in Europe unpasteurized fruit juices are difficult to assess. Increasing the daily consumption of fruit and vegetables is an important goal of promoting public health (National Cancer Program 2007). The consumption of fruit juices is a good choice so as to achieve the recommended daily amount of fruit to pick. In the current outbreak, patients were predominantly young adult women, who, as evidenced by the results of the Dutch food consumption survey of 750 between 19 and 30 years in 2003, probably a preference for foods with a healthy image, such as freshly squeezed juices. The survey showed that the consumption of fruit juices, fortified with vitamins and minerals was higher among women (26%) than men (18%). (17) also shows that a large part of the Dutch population is exposed to the infection risks of pasteurized juice. It is therefore extremely important that these products are safe.
Strict compliance with HACCP procedures and a higher frequency of microbiological monitoring of juices should be sufficient to reduce the risk of infection from rural distributed fresh foods such as unpasteurized fruit juices, ready-to-eat salads and fruit salads. Producers should also be encouraged to innovate with new techniques to micro-organisms in fresh foods to kill. Fresh fruit should be subjected to further processing by the application of cold pasteurization methods such as Pulsed Electric Field (PEF) or High Pressure and Processing (HPP). Both methods can be extended shelf life and a 5-log reduction of micro-organisms are obtained (18), while the taste and nutritional value of fresh fruit juice preserved. (19)
Through the product of fresh fruit, consumers must be informed about the risks of unpasteurised foods and the possibility of microbial contamination, as happens in the United States since 1998. (13) In Europe, manufacturers of these risk foods should be encouraged on a voluntary basis with their regular product microbiological testing. The test results would be centralized, and a rapid identification of sources of infection possible.
1. Cordano AM, Virgilio R. Evolution of drug resistance in Salmonella panama isolates in Chile. Antimicrob Agents Other Chem. February 1996, 40 (2) :336-41.
2. Stanley J, N Baquar, Burnens A. Molecular subtypes of scheme for Salmonella panama. J Clin Microbiol. 1995 May; 33 (5) :1206-1911.
3. Yang YJ, Huang MC, Wang SM, Wu JJ, Cheng CP, Liu CC. Analysis of risk factors for bacteremia in children with Salmonella gastroenteritis nontyphoidal. Eur J Clin Microbiol Infect Dis. April 2002, 21 (4) :290-3.
4. Chen TL, Thien PF, Liaw SC, Fung CP, Siu LK. First report of Salmonella enterica serotype panama meningitis associated with consumption of contaminated breast milk by a neonate. J Clin Microbiol. 2005 Oct; 43 (10) :5400-2.
5. Duijker of E, remember when WJ, Houwers DJ, van Pelt W. Serotype and phage type distribution of salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. J Clin Microbiol. November 2002, 40 (11) :3980-5.
6. Bender JB, Hedberg CW, Boxrud DJ, Besser JM, Wicklund JH, Smith KE, et al Use of molecular subtypes within Salmonella enterica serotype Typhimurium for surveillance. N Engl J Med. 2001 Jan 18; 344 (3) :189-95.
7. Mevius D Pellican C, van Pelt W. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2004. The Netherlands: VANTURES, the Veterinary Antibiotic Usage and Resistance Surveillance Working Group, 2005.
8. Noel H, Hofhuis A, De Jonge R, Heuvelink AE, De Jong A, Heck ME, et al or Fresh Fruit Juice Consumption: How a Healthy Food Practices Caused a National Outbreak of Salmonella gastroenteritis Panama. Food Borne Dis pathogen. 2009 in November 1912.
9. U.S. Food and Drug Administration 2001, . Retrieved on July 20, 2010
10. Burckhardt F, Frank C. Salmonella Panama-Erkrankungen: Zu einem regionalen über, bei Kindern durch Ausbruch Mini-Salami Sticks. Epidemiologisches Bulletin. 2008, 2008 (5) :37-8.
11. Paquet PE. Fièvre typhoid epidemic: déterminée par la consommation the petit cidre. Revue d'Hygiene 1923, 45:165-9.
12. Daum LT, Barnes WJ, McAvin JC, Neidert MS, Cooper LA, Huff WB, et al Real-time PCR detection of salmonella in suspect foods from a gastroenteritis outbreak in Kerr County, Texas. J Clin Microbiol. August 2002, 40 (8) :3050-2.
13. Vojdani JD, LR Beuchat, RV Taux. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot. February 2008, 71 (2) :356-64.
14. Cody SH, Glynn MK, Farrar JA, Cairns KL, Griffin PM, Kobayashi J, et al An outbreak of Escherichia coli O157: H7 infection from unpasteurized commercial apple juice. Ann Intern Med. 1999 February 2, 130 (3) :202-9.
15. Besser RE, Lett SM, Weber JT, Doyle MP, Barrett TJ, Wells JG, et al An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157: H7 in fresh-pressed apple cider. Jama. 1993 May 5, 269 (1917) :2217-1920.
16. Woodward DL, Clark CG, Caldeira RA, Ahmed R, Rodgers FG. Verotoxigenic Escherichia coli (VTEC): A major public health threat in Canada. Can J Infect Dis. September 2002, 13 (5) :321-30.
17. Hulshof K, Ocke M, van Rossum C, Rethans Buurma-E, Brants H, Floaters J, et al [Results of the national food consumption survey 2003] Food Consumption Survey 2003, young adults. Bilthoven - the Netherlands: RIVM, 2004. Report No..: RIVM report 350030002/2004.
18. Tribst AA, Sant'Ana Ade S, Massaguer PR. Review: Microbiological Quality and Safety or fruit juices - Past, Present and future perspectives. Crit Rev Microbiol. 2009, 35 (4) :310-39.
19. Sanchez-Moreno C, Ancos B, Plaza L, Elez-Martinez P, Cano MP. Nutritional approaches and health-related properties of plant foods processed by high pressure and pulsed electric fields. Crit Rev Food Sci Nutr. June 2009, 49 (6) :552-76.

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Infectious Diseases Bulletin Volume 21 Number 7
A. Court house, H. Noël R. de Jonge, AE Heuvelink, A. de Jong, MEOC Heck, CM de Jager and W. van Pelt
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Infectious Diseases Bulletin Volume 21 Number 7
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