More Bad News: Even Orange Juice is a Risk for Salmonellosis!

abstract & commentary

Synopsis: An outbreak of Salmonella serotype hartford infections associated with unpasturized orange juice is reported.

Source: Cook KA, et al. Outbreak of Salmonella serotype Hartford infections associated with unpasteurized orange juice. JAMA 1998;280:1504-1509.

A review of the Salmonella serotype-based surveillance system by the New Jersey Department of Health in June 1995 identified a cluster of Salmonella hartford infections among seven unrelated New Jersey residents returning from a theme park in Orlando during May 1995. This initiated an investigation into the source and extent of the outbreak.

Cases were found in the CDC’s national Salmonella surveillance system from reports of Salmonella hartford since May 1995. Cases were designated as a confirmed (S. hartford infection) or probable (Salmonella serogroup C1) infection in residents of visitors to Orlando in May or June 1995.

A matched case-control study was conducted to identify risk factors. All cases were limited to visitors to the theme park’s hotel because most of the patients had stayed at one of the 13 hotels. There were about three controls per case (with no history of diarrhea or vomiting during or within 7 days of the visit) who were matched for age, group, hotel, check-in date, and number of days spent visiting the theme park.

A total of 62 patients from 21 states were identified. Of the 32 patients enrolled in the study, 31 (97%) ill persons drank orange juice compared with 43 (54%) of 80 matched controls (matched odds ratio, undefined; 95% confidence interval, 5.2 to undefined; P < 0.001). Even though eating waffles was also statistically significant by univariate analysis, a significant positive association between orange juice and illness remained after those persons eating waffles (16/30, 53%) were excluded from analysis.

The only specific event or meal associated with illness was "character breakfasts" served in the theme park, which had been attended by 29 of 32 (91%) of ill persons compared with 48 (58%) of 83 controls. No other activities or attractions in the Orlando area such as swimming in water parks and hotel pools or direct contact with animals were associated with illness.

Of all orange juice served at the theme park and all orange juice served at the character breakfast, 88% was purchased from a local juice processor and was unpasteurized. Site inspection of the processing plant that provided all of the orange juice to the theme park identified several deficiencies. The processing room was poorly sealed from the environment and rodent and bird droppings were present and there were reports of frogs being observed around the equipment. Several serotypes of Salmonella were isolated from in and around the plant and orange groves providing the majority of oranges, including S. hartford from a toad found just outside the juice processing plant.

The pH of orange juice samples ranged from 4.1-4.5 (mean 4.3), less acidic than the average pH of Florida oranges (3.7) but within the FDA accepted pH level (4.6). All juice samples contained coliforms and Salmonella gaminara was cultured from 10 (83%) of 12 juice containers representing four lots produced in May and July 1995.

All isolates tested (human, orange juice, and toad) were susceptible to all antimicrobials tested. Seven representative human isolates were indistinguishable by PFGE; however, the PFGE patterns of the orange juice, toad isolates, and nine reference isolates were different from the outbreak strain.

Comment by Joseph F. john, md & philip mathew, MD

Woe be to those of us who love freshly squeezed orange juice! Now we need to make sure it is pasteurized since, as shown by this crafty, case-controlled study, there are suppliers who do not pasteurize their products. Furthermore, there is apparently significant contamination with Salmonella in the animal environment of Florida orange groves, particularly with amphibian excreta. Although the tree frog feces contained strains of Salmonella whose PFGE did not perfectly match the PFGE type of the outbreak strain, there were a limited number of frog strains studied. Perhaps we will be treated to a follow-up paper on the variety of Salmonella strains in Florida orange grove frogs, looking carefully of course for S. hartford serotype. And when the frog study is complete, we will also have the pleasure of knowing the pathogenic flora of insects, birds, and mammals.

The contamination probably came from the ground of the grove whence the orange lited, or from the processing plant. The orange peel and rind are removed mechanically before the squeezing occurred, but residue from potentially contaminated peel and rind remained on the equipment. Production capacity is huge—40,000 liters per day. So, even though pasteurization at the final stage of juice production should remove the Salmonellae, there is a large volume of product that will require quality control. It would be interesting to know the potential daily volumes from the first orange-associated outbreak of salmonellosis, this one causing typhoid at a hotel in Cleveland in 1944 (Am J Pub Health 1946;36:34-36).

Orange juice incriminated in this outbreak came from at least four growers not related by common water sources or picking crews. The groves were up to 60 miles apart. The product was distributed beyond the theme park but just how broadly distributed we do not know.

On our most recently purchased gallon of orange juice (back here in New Jersey), I noticed the inscription clearly printed on the pull off tab: PASTEURIZED. (Dr. Mathew is Senior Fellow, Robert Wood Johnson Medical School, New Brunswick, NJ.)