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                                                                              Consequences in Georgia of a Nationwide
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                                                                              Outbreak of Salmonella Infections:

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                                                             :.O;             What You Don't Know Might Hurt You
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                                                                              Barbara E. Mahon, MD, MPH, Laurence Slutsker, MD, MPH, Lor-i Hutwagner, MS,
                                                                              Cherie Drenzek, DVM, Kathleen Maloney, Kathleen Toomey, MD, MPH, and
                                                                              Patricia M. Griffin, MD

                                                                                   Widespread outbreaks of foodbome ill-        and Schwan's attempted to wam customers.
                                                                              ness are a growing threat to public health in     Schwan's mailed letters about the outbreak
                                                                              the United States. Increasingly, foods are        and recall of implicated products to cus-
                                                                              produced in enormous volumes in central           tomers. Schwan's home delivery drivers were
                                                                     VR.      locations and then distributed widely; conta-     instructed to collect these products from cus-
                                                                              mination   during production can cause large      tomers. The first press release about the out-
                                                                              outbreaks of foodbome illness.IA Such out-        break was issued on October 7, beginning
                                                                              breaks present many challenges, including         several weeks ofnationwide media coverage.
                                                                              informing the at-risk public about how to               Because Schwan's distributes directly to
                                                                              avoid illness and retrieving the contaminated     households, customer lists were available.
                                                                              food for safe disposal. Generally, the public     Thus, unlike the usual situation, the identity of
                                                                              is informed through the news media, and           consumers who may have had the contamin-
                                                                     ;11 jw   contaminated food is retrieved through prod-      ated products at home was known. This situ-
                                                                      tg      uct recalls. However, evaluating the effec-       ation was an opportunity to investigate when
                                                                     k        tiveness of these measures for products that      and how at-risk persons heard the waming
                                                                              have already been purchased is difficult          that the implicated ice cream should not be
                                                                              because the identity of consumers who have        eaten and whether they heeded the waming.
                                                                              the products at home is rarely known.             We describe an investigation in Georgia of
                                                                                    A recent nationwide outbreak of Salmo-      the impact of the waming on Schwan's cus-
                                                                              nella serotype Enteritidis infections caused      tomers, the magnitude of the outbreak, and
                                                                              by commercially produced ice cream5 exem-         the content and timing of news reports about
                                                                              plifies both the trend toward widespread out-     the outbreak. We use "the waming" to mean
                                                                              breaks and the challenge of preventing addi-      any information about the outbreak available
                                                                              tional illnesses after a vehicle has been         to at-risk customers and restrict "the out-
                                                                              identified. In early October 1994, the Min-       break" to the actual diarrheal illnesses con-
                                                                              nesota Department of Health determined that       stituting the outbreak.
                                                                              ice cream manufactured in Marshall, Minn,
                                                                              by Schwan's Sales, Inc, and distributed
                                                                              through a route driver system directly to         At the time of the study, Barbara E. Mahon, Laurence
                                                                              households in the continental United States       Slutsker, Cherie Drenzek, and Patricia Griffin were
                                                                              was responsible for an outbreak of Salmo-         with the Foodbome and Diarrheal Diseases Branch,
                                                                     gg       nella serotype Enteritidis infections. The        Centers for Disease Control and Prevention (CDC),
                                                                              source of contamination was probably tanker       Atlanta, Ga. Dr Mahon is now with the Department
                                                                                                                                of Pediatrics, University of Medicine and Dentistry
                                                                              trucks that delivered ice cream premix to the     of New Jersey-Robert Wood Johnson Medical
                                                                              factory for freezing; starting in July 1994,      School, New Brunswick, NJ. Lori Hutwagner and
                                                                              these trucks also routinely hauled liquid raw     Kathleen Maloney are with the Biostatistics and
                                                                              eggs, a common source of Salmonella               Information Management Branch, CDC, Atlanta, Ga.
                                                                              serotype Enteritidis.6                            Kathleen Toomey is with the Georgia Department of
                                                                                    This outbreak was the largest common-       Human Resources, Atlanta.
                                                                              vehicle Salmonella outbreak ever recognized             Requests for reprints should be sent to Lau-
                                                                                                                                rence Slutsker, MD, MPH, Foodborne and Diar-
                                                                              in the United States; 41 states reported out-     rheal Diseases Branch, Mailstop A-38, Centers for
                                                                     BWsZ.    break-related cases, and the total number of      Disease Control and Prevention, 1600 Clifton Rd,
                                                                              cases was estimated at 224 000.5 After the        Atlanta, GA 30333.
                                                                              vehicle was identified, public health officials         This paper was accepted June 18, 1998.

                                                                                                                                        American Journal of Public Health 31
Mahon et al.

Methods                                          multiplied by the estimated number of out-          respondents who had heard the warning, 124
                                                 break-related illnesses in Georgia.                 (76%) remembered when they had first heard
Survey of Customer Households                                                                        it; the median time was 5 days after the first
                                                 Examination ofMedia Reports                         press release (Figure 1). Television news was
      We conducted a survey of 250 ran-                                                              the first medium to reach most respondents,
domly selected Schwan's customers in Geor-             To obtain news reports on the outbreak,       although word of mouth from friends or fam-
gia, 1% of those in the state, to determine      we searched the NEXIS database (Reed Else-          ily members was also important (Table 1).
when and how customers heard the warning         vier, Inc, New York, NY), a news information        Although Schwan's reported mailing letters to
and the incidence and correlates of diarrheal    service including regional, national, and inter-    all customers and instructing all drivers to col-
illness. We telephoned customers between         national newspapers, news wires, and maga-          lect implicated products, only 21% and 50%
October 20 and 24, 13 to 17 days after the       zines, for reports mentioning "ice cream" and       of respondents said they had ever been con-
warning was first issued. Eligible customers     also "Salmonella" or "Schwan's" from Octo-          tacted by these means, respectively.
were households (businesses were excluded)       ber 7, the date of the first press release,               After first hearing the warning, 42
that had purchased any Schwan's products         through October 19, the day before our survey       (26%) of the 163 respondents thought the
since July 1, 1994, the beginning of the         began. We selected all reports distributed in       implicated products were "OK to eat," and 16
likely period of contamination. An eligible      Georgia, including national news wire ser-          (10%) were not sure; only 10 (17%) of these
respondent was the person on the customer        vices, summaries of national television and         58 respondents had since decided they were
list or another person aged 18 years or older    radio news programs and television news pro-        not "OK to eat." In 22 (31%) ofthe 72 house-
who lived in the household and who knew          grams from two Georgia stations, and articles       holds in which implicated products were pre-
which Schwan's products had been pur-            in nationally distributed newspapers and in         sent when the respondent first heard the
chased for the household.                        the Atlanta Journal/Constitution, which is dis-     warning, a household member subsequently
      Implicated products were defined as the    tributed statewide. The NEXIS database does         ate the product; 20 (9 1%) of these respon-
recalled ice cream, frozen yogurt, sherbet,      not include strictly local radio, television, and   dents said that the household member had not
and ice cream novelty products that were         newspapers. For each report, we determined          believed there was actually a problem with
manufactured in Schwan's Marshall, Minn,         whether it said that implicated Schwan's prod-      the ice cream. Among the 157 households
factory. We used a questionnaire to ask          ucts should not be eaten and what customers         that had bought implicated products, 38
which Schwan's products had been pur-            with these products should do with them.            (26%) of the 144 whose respondents had
chased for the household since July 1, and,                                                          heard the warning still had the product, com-
regarding the warning, whether the respon-       Statistical Analysis                                pared with 3 (23%) of the 13 whose respon-
dent had heard it ("Have you heard about a                                                           dents had not heard. Similarly, 9 (27%) of the
problem with Schwan's ice cream prod-                 We analyzed the data in Epi Info, ver-         33 households whose respondents reported
ucts?") and, if so, when, how, and what the      sion 6.8 To control for household clustering        receiving a letter from Schwan's still had the
respondent understood the warning to mean        of diarrheal illness, the association between       product, compared with 28 (26%) of the 109
(whether he or she thought the implicated        reported diarrhea and potentially explanatory       households that did not receive a letter. How-
products were "OK to eat"). We also asked        variables-including whether the respondent          ever, only 10 (14%) of the 70 that had heard
the respondent about each household mem-         had heard the warning, whether the ill house-       the warning from a driver still had the prod-
ber's history, since July 1, of consumption of   hold member had eaten implicated ice                uct, compared with 27 (38%) of the 72 that
Schwan's ice cream products, diarrhea            cream, and household membership-was                 had not heard from a driver (relative
(defined as 3 or more loose or watery stools     analyzed in SAS,9 using the set of general-         risk= 0.38, P< .01).
in a 24-hour period), and other symptoms.        ized estimating equations (GEE) described                 Illness. Respondents reported diarrhea
      We estimated the number of potentially     by Liang and Zeger.'0 Interactions among            status for 615 (98%) of the 628 household
exposed Georgians-those who may have             explanatory variables were also examined.           members; 129 (21%; median age 32 years,
eaten implicated products-by multiplying                                                             range 7 months to 72 years) had reportedly
the number of Schwan's Georgia customers                                                             had diarrhea since July 1, with a 2-day
by the proportion of customers that repre-       Results                                             median duration. Other symptoms included
sented households that bought implicated                                                             abdominal cramps (65%), headache (50%),
products and then by the mean number of          Survey of Customer Households                       nausea (46%), fever (36%), vomiting (33%),
persons in those households who ever ate                                                             and bloody stool (3%). Only 9 of these
Schwan's ice cream. We estimated the                  Population. We contacted 211 (84%) of          household members (7%) had sought med-
impact of the outbreak in Georgia by multi-      the 250 selected customers and interviewed          ical attention, and none had been hospital-
plying the excess diarrhea rate among house-     respondents for 179 households (85%; 31             ized or had had a stool specimen cultured.
hold members who ate implicated products         customers were ineligible and 1 refused).                 Household members who had eaten
(compared with those who did not) by the         The 179 households had 628 household                implicated products were more likely to have
estimated total number of potentially            members, a mean of 3.5 (median 3, range             been reported with diarrhea than those who
exposed Georgians. We estimated the pro-         1-8) persons per household, and represented         had not eaten implicated products (121/463
portion of illness due to exposure after the     63 of Georgia's 159 counties. Of these 179           [26%] vs 8/152 [5%]; GEE odds ratio [con-
warning as the proportion of diarrheal ill-      households, 157 (88%) had purchased impli-           trolling for household clustering] = 3.8; 95%
nesses among household members who ate           cated products, and 473 (85%) of the 554             confidence interval = 2.0, 7.5). Reported diar-
 implicated products with onset after October    members of these households had eaten                rhea rates among members of households that
 10 (3 days after the first press release; the   implicated products.                                 had heard the warning (109 [27%] of 409
usual incubation period for Salmonella ill-            Warning. Respondents for 16 (9%) ofthe         exposed vs 7 [5%] of 138 unexposed) were
ness is 1 to 2 days7) and the number due to       179 households had not heard anything about         similar to rates among members of house-
 exposure after the warning as this proportion   the warning before our interview. Of the 163         holds that had not (12 [22%] of 54 exposed vs

                                                                                                                        January 1999, Vol. 89, No. 1
32 American Journal of Public Health
                                                                                                                                   Salmonellosis in Georgia

1 [7%] of 14 unexposed). Similarly, in the
GEE model, eating implicated products was              30 Number of respondents
independently associated with reported diar-
rhea, whereas the respondent's having heard
the warning was not. Illness onset dates were          20
reported for 85 household members who had
eaten implicated products (Figure 2); 14 of            15
these illnesses (16%) began after October 10,
which was 3 days after the first press release.        10    First   press
      We estimate that about 51 000 Georgians
may have eaten implicated products (approxi-
mately 23 000 Schwan's customers x 85% that
were eligible households x 88% that bought              0

implicated products X 3.5 persons per house-           25    Number of media            reports

hold that bought implicated products x 85% of
members of those households who ate                    20
Schwan's ice cream) and that about 11 000
illnesses occurred as a result of this outbreak        15

(51 000 persons X 21% [26% diarrhea rate
among exposed persons minus 5% diarrhea                10
rate among unexposed persons]). About 1760
cases could have been due to exposure after the         5

waming (11000 cases x 16% with onset after
October 10) and therefore might have been                      7        8       9        10       11   12   13     14      15    16    17      18   19
prevented by a completely effective waming.
                                                                                                   October 1994
Examination ofMedia Reports
     From October 7 through October 19, a             FIGURE 1-Date respondents in Georgia first heard the warning about an
                                                                outbreak of Salmonella infections (n = 124) and dates of news
total of 64 news reports on the outbreak                        reports about the outbreak in the Georgia media that are
appeared in Georgia in sources listed in                        summarized in the NEXIS database (n = 64).
NEXIS. The median report date, October 13,
was 6 days after the warning was issued (Fig-
ure 1). Only 4 reports (6%) said that impli-      not to eat the food implicated in     a large               our respondents were still not aware of the
cated products should not be eaten. Thirty-one    nationwide outbreak of Salmonella infec-                    problem.
reports (48%) said something about what cus-      tions. We do not know of any other study of                      Many customers misunderstood or were
tomers who had implicated products at home        the effectiveness of a warning among an at-                 skeptical of the warning. After first hearing
should do with them, usually by referring to      risk population about a foodbome outbreak.                  the warming, 36% of the respondents did not
Schwan's product collection efforts.              In Georgia, although most respondents had                   understand that the implicated ice cream
                                                  heard about the outbreak, the waming was                    should not be eaten. Respondents who had
                                                  neither as timely nor as convincing as we                   heard the waming were no less likely than
Discussion                                        would have hoped. Customers first heard the                 others to still have implicated products at
                                                  warning a median of 5 days after it was                     home. Worse, in 31% of the households that
     This study documents serious problems        issued, and although we began interviewing                  had implicated products, a member of the
with the process of waming at-risk persons        customers 13 days after it was issued, 9% of                household had eaten the product after hearing

   TABLE 1-Media Through Which Respondents Heard About the Warning on Contaminated Ice Cream Products and Median
            Date of First Hearing: Georgia, October 20-24, 1994
                                        Respondents Who                                                                               Respondents Who
                                       First Heard Through           Median No. of Days After            No. of Respondents                 Ever Heard
                                              Medium                 October 7 Warning That            Who Remembered Date             Through Medium
          Medium                        No.            %             Respondent First Heard               They First Heard            No.                %
   Television news                      93           (57)                           4                            65                   130                (80)
   Friend/family member                 27           (17)                           4                            23                    60                (37)
   Local newspaper                      16           (10)                           5                            13                    50                (31)
   Schwan's route driver                15            (9)                           6                            15                    81                (50)
   Radio                                 9            (6)                           3                             5                    32                (20)
   Letter from Schwan's                  2            (1)                           8                             2                    34                (21)
   Doctor/health worker                  0            (0)                        ...                             ...                    1                 (1)
   Note. Of the 179 respondents interviewed, 163 had heard about the warning before the interview. The denominator used in calculating
     percentages was either 163 or 162 because of missing data.

January 1999, Vol. 89, No.   I                                                                                          American Journal of Public Health 33
Mahon et al.

                                                                                                             First press release
                         Number of persons

                     1       8    15
                                        22    29
                                                   I.   5   12

                                                                                  2      9
                                                                                                      23                      14
                                                            Onset date, 1994
   FIGURE 2-Dates of onset of diarrheal illness in Georgia consumers of implicated ice cream products, July-October 1994
                    (n = 85).

the warning, usually not believing that it was      regardless, the result was ineffective delivery   health message. Word of mouth from friends
unsafe. Although some at-risk persons may           of the warning.                                   and family members can effectively commu-
always be hard to reach or convince, the high             This study also shows that what             nicate a risk warning. Individual contacts
failure rate of this warning raises concern         Schwan's Georgia customers didn't know            through visits, letters, or telephone calls are
about the delivery of urgent public health          did hurt them-a large outbreak appears to         slow but may reach persons who would not
messages.                                           have occurred in this population. Reported        be reached by other means. It is often appro-
     We tried to identify aspects of the deliv-     diarrhea peaked in early October 1994, as in      priate for a company to take responsibility for
ery of this warning that might indicate how         Minnesota and other states5; the decline in       certain communications to its customers;
communication could be improved.                    mid-October argues against recall bias as the     public health workers should help ensure the
Although the news media, especially televi-         reason for the peak. Persons who ate impli-       thoroughness of those communications and
sion, reached most people first, only 6% of         cated products had a significantly increased      of the retrieval of contaminated products.
Georgia news reports in NEXIS stated that           incidence of reported diarrhea, independent            Our investigation also highlights the
the implicated products should not be eaten.        of whether the respondent had heard the           need for further research on methods for
Most reports focused on ill persons and on          warning. A fully effective warning might          delivering effective warnings. We are aware
the ongoing investigation of the source of          have prevented much of this illness; eating       of only 4 other investigations on warnings
contamination. This focus on stories with           implicated products after the warning was         during acute outbreaks; all showed that com-
"news value" rather than on risk education is       first issued could have been responsible for      munication to the target population was late,
characteristic of reporting on outbreaks and        16% of the reported diarrhea.                     incomplete, or inaccurate,1-"18 and none were
other hazards,"'3 but it is not ideal for deliv-          Routine surveillance in Georgia             able to study possible ways to improve com-
ery of a public health warning. We do not           detected only one Salmonella serotype             munication. The potential for outbreaks
know whether public health officials may            Enteritidis infection during the outbreak, per-   affecting large numbers of persons continues
have missed opportunities in press inter-           haps in part because most of the illnesses        to increase; the need to rapidly and effectively
views to emphasize that customers should            were mild. Similarly, the Centers for Disease     wam consumers of an acute health threat is a
not eat the implicated products or whether          Control and Prevention received no reports        challenge we are likely to face again. K]
greater emphasis could have led to greater          of deaths associated with this outbreak.
coverage.                                           However, these data also point out the insen-
      Schwan's delivery of the warning was          sitivity of Salmonella surveillance systems       Contributors
also suboptimal. Although Schwan's                  even in large outbreaks. Schwan's would not       Dr Mahon organized the study, supervised data col-
reported mailing letters to all customers,          release national product distribution data;       lection, did the preliminary analyses, and was the
only 21% reported receiving a letter, and           however, 2% of wholesale distributors who         primary writer of the paper. Dr Slutsker and Dr
those who had received a letter were no less        received recalled ice cream had Georgia           Griffin closely supervised the entire project, directed
                                                                                                      the focus of the investigation, and contributed sub-
likely than others to still have implicated         addresses. If Georgia received 2% of the          stantially to writing the paper. Dr Drenzek partici-
products in the home. Similarly, only 50% of        contaminated products, the number of cases        pated in study design and data collection and analy-
respondents reported being contacted by a           nationwide could be roughly estimated at          sis; she also participated in writing and reviewing the
driver; drivers evidently implemented the           about 550 000 (11 000 cases/2%)-in the            manuscript. Dr Toomey collaborated with the CDC
recall inconsistently, since 14% of house-          same range as the more precise estimate of        authors in designing the study, assisted with organiz-
holds that reported hearing the warning from        224 000 cases calculated by Hennessy et al.5      ing the data collection, and participated in writing
                                                                                                      and reviewing the manuscript. Ms Hutwagner and
a driver still had implicated products. Anec-       The corresponding reporting rate of less than     Ms Maloney reviewed the primary data and the uni-
dotally, although some respondents told us           1% (593/550 000) is consistent with the          variate analyses, conducted the generalized estimat-
that their driver had made special efforts to       0.3% estimated by Hennessy et al.; both are       ing equations analysis, wrote the statistical portions
deliver the warning quickly, others said their      even lower than the 1% to 5% rate for Sal-        of the manuscript, and reviewed the entire paper.
driver never mentioned it. The discrepancies        monella infections estimated previously.'4
between Schwan's statements and cus-                      The lessons learned during this investi-
tomers' reports could be explained by slow          gation may be helpful in future outbreaks.           Acknowledgments
or incomplete implementation by the com-            The media, especially television, get the word       We thank Ms Onnalee Henneberry of the CDC for
pany or by customers' forgetting contacts;          out quickly but may not focus on the public          conducting the NEXIS search and Drs Luis

                                                                                                                            January 1999, Vol. 89, No. 1
34 American Journal of Public Health
                                                                                                                                          Salmonellosis in Georgia

Castellanos, Laurie Elam-Evans, Clarice Green, and               infections from ice cream. N Engl J Med.                ease, Disasters, and Other Hazards. New York,
Judith Moore of the CDC and Ms Barbara Car-                      1996;334: 1281-1286.                                    NY: Russell Sage Foundation; 1993.
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the US Food and Drug Administration for conducting               emergence of grade A eggs as a major source             tive characteristics of the 1994 British media
customer interviews.                                             of Salmonella enteritidis infections. New               outbreak. JInfect. 1995;30:63-65.
                                                                 implications for the control of salmonellosis.    13.   Glanz K, Yang H. Communicating about risk of
                                                                 JAMA. 1988;259:2103-2107.                               infectious diseases. JAMA. 1996;275:253-256.
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                   a for Community-Oriented Health Systems
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January 1999, Vol. 89, No. 1                                                                                                 American Journal of Public Health 35