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Journal of Food Protection, Vol. 85, No. 7, 2022, Pages 1000-1007
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https://doi.org/10.43 15/JFP-22-007
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Published 2022 by the International Association for Food Protection
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This is an open access article under the CC BY-NC-ND license (https://creativecommons.org/licenses/by-nc-nd/4.0/)
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Research Paper
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Foodborne Outbreak Rates Associated with Restaurant Inspection
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Grading and Posting at the Point of Service: Evaluation Using
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National Foodborne Outbreak Surveillance Data
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THUY N. KIM@htps:/orcid.org/0000-0001-6470-7046,'* LAURA WILDEY,? BRIGETTE GLEASON,* JULIA BLESER,*
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MELANIE J. FIRESTONE@ hiips://orcid.org/0000-0003-2244-3729,! GINA BARE,? JESSE BLISS,* DANIEL DEWEY-MATTIA,?
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HARLAN STUEVEN,° LAURA BROWN,° DAVID DYJACK,? AnD CRAIG W. HEDBERG!
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!University of Minnesota School of Public Health, Division of Environmental Health Sciences, 420 Delaware Street S.E., MMC 807, Minneapolis,
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Minnesota 55455; *National Environmental Health Association, 720 South Colorado Boulevard, 1000N, Denver, Colorado 80246; *National Center for
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Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, Georgia 30329; National Network
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of Public Health Institutes, 1300 Connecticut Avenue N.W., no. 150, Washington, DC 20036; *Dining Safety Alliance, 200 Union Boulevard, Suite 200,
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Lakewood, Colorado 80228; and °National Center for Environmental Health, Centers for Disease Control and Prevention, 4770 Buford Highway N.E.,
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MS F58, Atlanta, Georgia 30341, USA
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MS 22-007: Received 11 January 2022/Accepted 14 February 2022/Published Online 17 February 2022
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ABSTRACT
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A previously conducted national survey of restaurant inspection programs associated the practice of disclosing inspection
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results to consumers at the restaurant point of service (POS) with fewer foodborne outbreaks. We used data from the national
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Foodborne Disease Outbreak Surveillance System (FDOSS) to assess the reproducibility of the survey results. Programs that
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participated in the survey accounted for approximately 23% of the single-state foodborne illness outbreaks in restaurant settings
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reported to FDOSS during 2016 to 2018. Agencies that disclosed inspection results at the POS reported fewer outbreaks (mean =
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0.29 outbreaks per 1,000 establishments) than those that disclosed results online (0.7) or not at all (1.0). Having any grading
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method for inspections was associated with fewer reported outbreaks than having no grading method. Agencies that used letter
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grades had the lowest numbers of outbreaks per 1,000 establishments. There was a positive association (correlation coefficient,
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R* = 0.29) between the mean number of foodborne illness complaints per 1,000 establishments, per the survey, and the mean
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number of restaurant outbreaks reported to FDOSS (R? = 0.29). This association was stronger for bacterial toxin-mediated
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outbreaks (R* = 0.35) than for norovirus (R? = 0.10) or Salmonella (R* = 0.01) outbreaks. Our cross-sectional study findings are
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consistent with previous observations that linked the practice of posting graded inspection results at the POS with reduced
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occurrence of foodborne illnesses and outbreaks associated with restaurants. Support for foodborne illness surveillance
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programs and food regulatory activities at local health agencies is foundational for food safety systems coordinated at state and
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federal levels.
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HIGHLIGHTS
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¢ Jurisdictions with point-of-service disclosure reported fewer outbreaks.
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* Grading used in inspections was associated with fewer outbreaks than no grading.
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¢ Foodborne illness complaints may lead to increased outbreak detection and reporting.
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Key words: Foodborne illness; Foodborne outbreak; Inspection results; Public disclosure, Restaurant inspection; Restaurant
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inspection grading
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It is estimated that known foodborne pathogens are incident in which two or more people become ill from the
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responsible for 9.4 million illnesses annually in the United same contaminated food or drink (J); sporadic cases are
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States (2, 19). Depending on the pathogen, <1 to 10% of — jJInesses that have not been identified to be part of an
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cases are known to be associated with a recognized outbreak
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(3). Nevertheless, outbreak investigations provide key
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information on the food, pathogens, and settings associated
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with foodborne illness. An outbreak is defined by the
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Centers for Disease Control and Prevention (CDC) as an
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outbreak. Restaurants are an important setting for both
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outbreak-associated and sporadic (non—outbreak-associated)
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foodborne illness in the United States (2, 1/3). The
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percentage of foodborne illness outbreaks attributed to
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restaurant settings increased from a mean of 41% for the
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* Author for correspondence. Tel: 612-503-9277; E-mail: period 1967 to 1997 (/4) to a mean of 61% for the period
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kim00977@umn.edu. 2009 to 2015 (8).
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2202 Ainr 6} Uo Jasn UOqUaAaLd pUe JOUOD eseasiq 40) s1ajUBD Aq JPd'Q001-2-S8-2606-P76 L/6S78Z0E/000 L/Z/Se/yPd-a|on1e/dy[/Woo'ssasdualje"ueIpuaW/:dyY Woy papeojuMog
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J. Food Prot., Vol. 85, No. 7
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In recognition of the important role that restaurants
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play in prevention of foodborne illness and outbreaks,
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studies have identified model practices for agencies that
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inspect restaurants for compliance with food safety
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regulations. Study findings suggest that disclosing inspec-
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tion results at the point of service (POS) (1.e., at the
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establishment) using some form of grading (letter grade,
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color, numerical score, emoji, etc.) is associated with
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improved public health outcomes (5, 9, 20, 23). The
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evidence gathered by these efforts suggests that such
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disclosure yielded improved inspection scores (5), improved
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sanitary conditions (23), decreased incidence of Salmonella
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infection (9), and decreased hospitalizations due to
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foodborne illness (20). The results of these studies strongly
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suggest that the actions of restaurant inspection programs
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play an important role in reducing foodborne illness
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transmitted in restaurant settings.
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In 2021, a national survey of restaurant inspection
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programs found that disclosure at the POS was associated
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with fewer foodborne illness outbreaks reported per 1,000
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licensed food establishments. Survey methods were previ-
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ously described (/5). Briefly, the survey was disseminated to
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a total of 790 restaurant inspection agencies at two times: 7
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January 2020 and 3 March 2020 (/5). A third dissemination
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of the same survey occurred on 2 November 2020. Although
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not included in the original study results, these data were
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included in the analysis for this study. The net total number
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of agencies responding to the survey was 165. Of these, 140
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respondents represented local agencies, whereas the remain-
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der represented state or territorial agencies (/5).
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This survey captured various restaurant inspection
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agency characteristics across the United States, including
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estimates of complaints received and use of methods of
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grading, inspection results disclosure, and inspection
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violation schemes. It also captured counts of foodborne
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illness outbreaks, sporadic illness cases, and foodborne
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illness complaints. Survey recipients represented inspection
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agencies that disclosed inspection results online and those
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enrolled in the U.S. Food and Drug Administration (FDA)
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Voluntary National Retail Food Regulatory Program
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Standards program (Retail Program Standards). This
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program helps food regulatory programs meet the widely
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recognized Voluntary National Retail Food Regulatory
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Program Standards (2/). The FDA Food Code is a model
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set of science-based, comprehensive food safety guidelines
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that provides the technical and legal basis for local, state,
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tribal, and federal food codes that regulate retail food
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service in the United States (22).
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A limitation of the survey-reported data was the lack of
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important details on the etiologic agent (e.g., bacterial or
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viral pathogen) and setting of these outbreaks (/5). We
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sought to address these gaps by using data routinely
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reported by state public health agencies to the CDC through
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the Foodborne Disease Outbreak Surveillance System
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(FDOSS). FDOSS is a national, passive surveillance system
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that collects information on enteric and nonenteric food-
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borne outbreaks, including information on the number of
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cases, case outcomes, dates of illness onset, implicated
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foods, and locations of food preparation (1). The objective
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of our present study was to use FDOSS outbreak data to
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EVALUATION OF RESTAURANT GRADING SURVEY RESULTS 1001
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compare the number of outbreaks per 1,000 licensed
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restaurants by restaurant inspection grading and disclosure
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practices conducted by agencies responding to the initial
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survey (15).
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MATERIALS AND METHODS
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We used results from the previously conducted national
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survey of regulatory restaurant inspection agencies at state,
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county, city, district, and territorial levels as a baseline for this
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study (15). We limited analyses to local agencies representing city,
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county, or district jurisdictions (7 = 140), hereafter referred to as
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“agencies.” The decision to focus on local agencies is supported
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by the tendency of restaurant inspection programs to operate at the
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local government level (/5). The agencies were drawn from 34
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states representing all regions of the country (median = three
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agencies per state, range = | to 14). This current study used the
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following data from the original survey: jurisdiction of the survey
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respondents, number of licensed restaurants, number of com-
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plaints received from 2016 to 2018, method of inspection grading,
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and method of public disclosure of inspection results.
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As with inspection practices, inspection terminology can vary
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by agency. We defined public disclosure as the act of voluntarily
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and preemptively publicizing some or all inspection data to the
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public (e.g., posting at the restaurant or online). This study also
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defined grading method as the act of applying an ordinal ranking
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system to inspection results (e.g., numerical scores or letter
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grades). Disclosure at the POS is inclusive of any type of display
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of inspection results on the restaurant premises, regardless of font
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size or location. Complaints are reports to public health of possible
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foodborne illness from the public, including individuals or groups
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of individuals (7).
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We obtained foodborne outbreak data for our analysis from
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FDOSS; data also contained associated details about etiology and
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food preparation location. We applied the following inclusion
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criteria to the FDOSS data extracted on 18 November 2019: the
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primary mode of transmission was foodborne; the outbreak report
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was finalized; date of first illness was between | January 2016 and
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31 December 2018; the number of estimated primary illnesses was
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greater than one; the exposure location was within the jurisdiction
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of an agency that participated in our survey; and the location
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where food was prepared was a restaurant setting—including sit-
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down dining, buffet, fast food, or other or unknown restaurant
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type.
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We linked the FDOSS data to the survey data by jurisdiction,
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identified by the reporting agency. An outbreak was attributed to a
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regulatory agency if the agency’s jurisdiction was listed in FDOSS
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as the location in which the exposure occurred. Outbreaks in
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which exposure occurred in multiple counties were assigned to
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agencies based on the listed exposure locations. If a multicounty
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outbreak had exposure locations in jurisdictions for multiple
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agencies, each outbreak was counted once for each agency.
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Multistate outbreaks were excluded from analysis. Some counties
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contain city agencies that conduct inspections independently of the
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county agency. These incidences were identified by comparing the
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survey-reported population served by the county agency with the
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U.S. Census Bureau estimates of population for the jurisdiction.
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Using this method, city-level exposure data were used to identify
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and assign outbreak counts to the appropriate agency for four
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outbreaks. Outbreaks for which multiple pathogens were identified
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were counted only once in the outbreak total but were counted for
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each pathogen for pathogen-specific analyses.
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We grouped FDOSS restaurant outbreaks by etiology.
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Outbreaks in FDOSS with the suspected etiology of “other-
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7202 Ainr 6} UO JasN UOHUBAaIq PUB [OJUOD aseasiq JO} s19}UB_ Aq Jpd'Q001-2-G8-2606-P 6 | /6S78Z0€/0001/2/S84Pd-a}oI12/dj[/Woo'ssaidualje"uelpiewu//:dy}Y Woy pepeo|umMoq
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1002 KIM ET AL.
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TABLE 1. Etiological distribution of outbreaks in restaurant
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settings reported to the FDOSS for agencies participating in the
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restaurant grading project survey compared with all other
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jurisdictions, 2016 to 2018°
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J. Food Prot., Vol. 85, No. 7
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TABLE 2. Number and mean annual rate of outbreaks in
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restaurant settings reported to the FDOSS by disclosure methods
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and grading methods for agencies participating in the restaurant
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grading project survey, 2016 to 2018"
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Restaurant outbreaks for Restaurant outbreaks in
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survey group agencies, all other jurisdictions,
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n (%) (n = 381) n (%) (n = 1,257)
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Bacterial toxin 36 (9) 109 (9)
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Bacillus 11 23
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Clostridium 10 44
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Staphylococcus 6 37
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Unspecified 9 5
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Campylobacter 10 (3) 30 (2)
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Ciguatoxin 0 (0) 3 (0.2)
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Cryptosporidium 1 (0.3) 2 (0.2)
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Cyclospora 4 (1) 23 (2)
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Escherichia 6 (2) 18 (1)
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Hepatitis 1 (0.3) 9 (0.7)
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Norovirus 177 (46)? 489 (39)
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Salmonella 48 (13) 125 (10)
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Sapovirus 2 (0.5) 5 (0.4)
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Scombroid toxin 4 (1) 27 (2)
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Shigella 0 (0) 5 (0.4)
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Vibrio 39 (10)? 18 (1)
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Multiple etiologies 6 (2) 22 (2)
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Unknown etiology 47 (12)? 372 (30)
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“ FDOSS, Foodborne Disease Outbreak Surveillance System.
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° Proportion of outbreaks significantly different between survey
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group and all other jurisdictions. Norovirus (RR = 1.14; 95% CI
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= 1.01, 1.29) and Vibrio (RR = 2.94; 95% CI = 1.99, 4.35) were
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more frequently reported by agencies in the survey group,
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whereas unknown etiologies (RR = 0.48; 95% CI = 0.36, 0.66)
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were less frequently reported.
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bacterium” were reviewed; most were attributed to an unspecified
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bacterial toxin based on details provided by the reporting agency.
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These counts were then combined with Bacillus cereus, Clostrid-
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ium perfringens, and Staphylococcus aureus and collectively
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referred to as “bacterial toxin—mediated.” The proportions of
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outbreaks by etiology were compared between agencies that
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participated in the restaurant grading project survey (survey
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group) and all other agencies reporting to FDOSS. This
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comparison between the two groups enumerated the contributions
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of the survey group in the context of the overall national outbreak
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surveillance data for the study period.
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We calculated mean and median values for rates to identify
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trends in outcomes based on each category of grading method,
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disclosure method, and inspection violation scheme. Mean rates
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for the survey group and all other agencies were compared using t¢
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tests, and P values were reported based on unequal variance
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assumptions. The level of significance was set at a = 0.05.
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Analysis was conducted using SAS 9.4 (SAS Institute, Cary, NC).
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Scatterplots and R* values were obtained using Microsoft Excel
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(Microsoft, Redmond, WA) to assess the relationship between the
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mean number of complaints reported and the mean number of
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outbreaks by etiology.
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RESULTS
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There were 2,608 single-state foodborne outbreaks
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reported to FDOSS during 2016 to 2018, with 1,638
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attributed to food prepared in a restaurant setting. Of these,
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Outbreaks per
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No. of 1,000 restaurants
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No. of | outbreaks in. }=——W—————_
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agencies restaurants Mean(SD) Median
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Disclosure methods
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Point of service 8 24 0.29 (0.2) 0.3
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Online 36 226 0.70 (0.7) 0.4
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None 11 72 1.0 (1.0) 0.5
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Grading methods
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Letter grade 42 310 0.57 (0.7) 0.3
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Numerical score 19 148 0.69 (0.7) 0.4
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None 12 89 0.96 (0.9) 0.7
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Other 16 138 0.76 (0.8) 0.4
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“ FDOSS, Foodborne Disease Outbreak Surveillance System.
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outbreaks in the survey group jurisdictions accounted for
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23% (n= 381), and all other jurisdictions accounted for the
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remaining 77% (n = 1,257).
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|
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Outbreak numbers and etiology by group. The
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proportion of outbreaks in restaurant settings was signifi-
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cantly higher among agencies in the survey group compared
|
|||
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with all other agencies (relative risk [RR] = 1.10, 95%
|
|||
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confidence interval [CI] = 1.03, 1.17; Table 1). The most
|
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common etiologies reported to FDOSS in restaurant settings
|
|||
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from the survey group were norovirus (177 [46%]
|
|||
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outbreaks), Salmonella (48 [13%] outbreaks), Vibrio spp.
|
|||
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(39 [10%] outbreaks), and bacterial toxin—mediated (36
|
|||
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[9%] outbreaks) (Table 1). The etiology was unknown for
|
|||
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47 outbreaks (12%) (Table 1). The proportions of restaurant
|
|||
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setting outbreaks attributed to norovirus (RR = 1.14; 95%
|
|||
|
CI= 1.01, 1.29) and Vibrio spp. (RR = 2.94; 95% CI= 1.99,
|
|||
|
4.35) were significantly higher among the survey group,
|
|||
|
whereas the proportion of unknown outbreaks was signif-
|
|||
|
icantly lower (RR = 0.48; 95% CI = 0.36, 0.64) among the
|
|||
|
survey group compared with all other agencies.
|
|||
|
|
|||
|
|
|||
|
Outbreak rates by inspection disclosure and grad-
|
|||
|
ing methods. There was a pattern of lower mean annual
|
|||
|
number of outbreaks per 1,000 licensed restaurants for
|
|||
|
agencies in the survey group that disclosed inspection
|
|||
|
results at the POS compared with agencies that either
|
|||
|
disclosed online or did not disclose (means: 0.29 POS
|
|||
|
versus 0.70 online, 1.0 did not disclose) (Table 2). A similar
|
|||
|
pattern was also seen for inspection grading methods;
|
|||
|
agencies with any form of grading method had a lower
|
|||
|
mean annual number of outbreaks per 1,000 licensed
|
|||
|
restaurants than agencies with no grading method (means:
|
|||
|
0.57 letter grade, 0.69 numerical score versus 0.96 no
|
|||
|
grading method).
|
|||
|
|
|||
|
|
|||
|
Comparison of POS and online disclosure methods.
|
|||
|
Inspection disclosure methods varied across agencies within
|
|||
|
states. For example, in 10 states that had six or more
|
|||
|
|
|||
|
|
|||
|
7202 Ainr 6} UO Jasn UOHUBAaIq PUB [OUD aseasiq JO} Ss19}UB_ Aq Jpd'Q00}-2-G8-2606-P 6 | /6S78Z0€/0001/2/S84Pd-a}oy12/dj[/Woo'ssaidualje"uelpiewu//:dy}Y Woy pepeo|umMoq
|
|||
|
|
|||
|
|
|||
|
J. Food Prot., Vol. 85, No. 7
|
|||
|
|
|||
|
|
|||
|
TABLE 3. Mean annual rate of outbreaks in restaurant settings
|
|||
|
reported to the FDOSS by POS disclosure versus online without
|
|||
|
POS disclosure for agencies participating in the restaurant
|
|||
|
grading project survey, 2016 to 2018*
|
|||
|
|
|||
|
|
|||
|
Outbreaks per 1,000 restaurants (n = 202)
|
|||
|
|
|||
|
|
|||
|
Mean (SD) Median P value?
|
|||
|
Disclosure method 0.002
|
|||
|
POS 0.3 (0.2) 0.3
|
|||
|
Online without POS 0.8 (0.7) 0.5
|
|||
|
|
|||
|
|
|||
|
“FDOSS, Foodborne Disease Outbreak Surveillance System;
|
|||
|
POS, point of service.
|
|||
|
° P value for comparison of means.
|
|||
|
|
|||
|
|
|||
|
agencies included in the survey, in only two states did all of
|
|||
|
the agencies in the state use the same practices for
|
|||
|
disclosing inspection results. Of the 28 agencies that
|
|||
|
disclosed at the POS according to the survey, 24 (86%)
|
|||
|
also disclosed online. However, there were fewer outbreaks
|
|||
|
reported by agencies that disclosed at the POS, compared
|
|||
|
with agencies that disclosed online without POS disclosure
|
|||
|
(0.3 POS versus 0.8 online, P = 0.002) (Table 3).
|
|||
|
|
|||
|
|
|||
|
Complaint rates by restaurant outbreak etiologies
|
|||
|
reported to FDOSS. There was a positive association
|
|||
|
(correlation coefficient, R*? = 0.29) between the mean
|
|||
|
number of complaints per 1,000 licensed restaurants per
|
|||
|
year reported to FDOSS and the mean number of restaurant
|
|||
|
outbreaks per year reported to FDOSS (R? = 0.29; Fig. 1).
|
|||
|
When reported restaurant outbreaks were stratified by
|
|||
|
etiology, there was a positive association between the mean
|
|||
|
number of complaints and the mean number of norovirus
|
|||
|
outbreaks in restaurants reported to FDOSS (R? = 0.10; Fig.
|
|||
|
2), and a positive association for bacterial toxin—mediated
|
|||
|
restaurant outbreaks (R* = 0.35; F ig. 3). Conversely, there
|
|||
|
was no meaningful trend for Salmonella (R* = 0.01; Fig. 4),
|
|||
|
suggesting that Salmonella outbreaks are not associated
|
|||
|
with foodborne illness complaints.
|
|||
|
|
|||
|
|
|||
|
DISCUSSION
|
|||
|
|
|||
|
|
|||
|
Relevance to practice. Our findings were consistent
|
|||
|
with previous survey (/5) results that showed that the
|
|||
|
disclosure of graded inspection results at the POS was
|
|||
|
associated with fewer outbreaks reported to FDOSS. These
|
|||
|
results provide further support for recommendations (/5) to
|
|||
|
post graded restaurant inspection results at the POS by
|
|||
|
demonstrating that agencies that used some grading system
|
|||
|
had lower mean numbers of FDOSS restaurant outbreaks
|
|||
|
per 1,000 establishments than did agencies that did not post
|
|||
|
graded inspection results. Agencies that used letter grades
|
|||
|
had the lowest mean and median numbers of FDOSS
|
|||
|
restaurant outbreaks per 1,000 licensed restaurants, al-
|
|||
|
though the study had limited power to distinguish among
|
|||
|
the grading methods.
|
|||
|
|
|||
|
Restaurant inspections are a measure of how well a
|
|||
|
restaurant adheres to food safety guidelines that prevent
|
|||
|
foodborne illness. The finding that posting graded inspec-
|
|||
|
|
|||
|
|
|||
|
EVALUATION OF RESTAURANT GRADING SURVEY RESULTS 1003
|
|||
|
|
|||
|
|
|||
|
tion results at the POS was associated with fewer outbreaks
|
|||
|
occurring in restaurants based on FDOSS data is consistent
|
|||
|
with hypotheses that consumers use this information to
|
|||
|
guide their dining decisions (10, //, 23). Because access to
|
|||
|
this information is important to consumers, a favorable
|
|||
|
score may attract more consumers, whereas a less favorable
|
|||
|
score may provide food operators with additional incentive
|
|||
|
to improve their food safety performance. Disclosure of
|
|||
|
inspection results at the POS allows this measure of food
|
|||
|
safety performance to be readily available and interpretable
|
|||
|
to consumers at a location where many dining decisions are
|
|||
|
made.
|
|||
|
|
|||
|
|
|||
|
Distribution of outbreaks. The higher proportion of
|
|||
|
outbreaks reported by the survey group suggests that these
|
|||
|
agencies were more likely to report restaurant-associated
|
|||
|
outbreaks and were more likely to report outbreaks due to
|
|||
|
norovirus but were less likely to report outbreaks of
|
|||
|
unknown etiology than all other agencies. This suggests
|
|||
|
that agencies in the survey group were better at determining
|
|||
|
the outbreak setting and etiology of the outbreaks they
|
|||
|
investigated. The relative effectiveness of agencies in the
|
|||
|
survey group to detect and investigate outbreaks adds
|
|||
|
further support for the credibility of findings within this
|
|||
|
group regarding differences in outbreak reporting based on
|
|||
|
inspection grading and disclosure practices.
|
|||
|
|
|||
|
|
|||
|
Usefulness of consumer complaints. In addition to
|
|||
|
our findings regarding inspection reporting, the results of
|
|||
|
this study support the importance of agencies having a
|
|||
|
mechanism to receive foodborne illness complaints. Our
|
|||
|
finding of a positive correlation between the number of
|
|||
|
complaints received per 1,000 licensed restaurants and the
|
|||
|
number of restaurant outbreaks reported to FDOSS means
|
|||
|
that the ability to receive and investigate foodborne illness
|
|||
|
complaints may be an important predictor of the ability of
|
|||
|
the agency to detect foodborne outbreaks. In particular,
|
|||
|
the positive associations between complaints and restau-
|
|||
|
rant outbreaks of bacterial toxin—mediated and norovirus
|
|||
|
outbreaks reflects the reliance on complaint-based sur-
|
|||
|
veillance to detect these outbreaks with short incubation
|
|||
|
periods. It is primarily through complaint-based surveil-
|
|||
|
lance systems that these types of outbreaks, and others
|
|||
|
with short incubation periods, are detected by public
|
|||
|
health agencies, thereby underscoring the need for
|
|||
|
continued complaint-based surveillance systems (7). In
|
|||
|
contrast, Salmonella-associated outbreaks are detected
|
|||
|
primarily through pathogen-specific surveillance; this
|
|||
|
supports the finding of no effect between the occurrence
|
|||
|
of complaints and outbreaks of Salmonella, which has a
|
|||
|
longer incubation period than toxin-mediated pathogens
|
|||
|
(4, 17).
|
|||
|
|
|||
|
Complaint-based surveillance is one of the two main
|
|||
|
methods of foodborne outbreak detection in the United
|
|||
|
States (7). Although this study does not assume that having
|
|||
|
the ability to receive complaints is indicative of the
|
|||
|
existence of a complaint system, it is notable that 81% of
|
|||
|
local health departments have a complaint-based surveil-
|
|||
|
lance system (/6) and approximately 75% of all foodborne
|
|||
|
|
|||
|
|
|||
|
7202 Ainr 6} UO JASN UOHUBAaIq PUB [OUD aseasiq JO} s19}UB_ Aq Jpd'Q001-2-G8-2606-P 6 | /6S78Z0€/0001/2/S84Pd-a}oy12/dj[/Woo'ssaidualje"uelpLew//:dy}Y Woy pepeo|umoq
|
|||
|
|
|||
|
|
|||
|
1004 KIM ET AL.
|
|||
|
|
|||
|
|
|||
|
35
|
|||
|
_—_
|
|||
|
3)
|
|||
|
Qa
|
|||
|
n 3
|
|||
|
bol)
|
|||
|
.—
|
|||
|
£
|
|||
|
g
|
|||
|
w 2.5
|
|||
|
|
|||
|
@
|
|||
|
|
|||
|
o © 2
|
|||
|
ae ®
|
|||
|
-“
|
|||
|
cw
|
|||
|
£¢ -
|
|||
|
x 8 is > oo Vero
|
|||
|
ve @ ave 9**
|
|||
|
2" o | wc
|
|||
|
3 1 | ®e ———_--_ a 8
|
|||
|
6 = ae
|
|||
|
= jj x ggeast
|
|||
|
SC ioe Letts
|
|||
|
© 0.5 2 % e
|
|||
|
= 2 @e* e e
|
|||
|
|
|||
|
0 &e ”
|
|||
|
|
|||
|
0 50 100
|
|||
|
|
|||
|
|
|||
|
J. Food Prot., Vol. 85, No. 7
|
|||
|
|
|||
|
|
|||
|
150 200 250
|
|||
|
|
|||
|
|
|||
|
Mean no. complaints per 1,000 restaurants
|
|||
|
|
|||
|
|
|||
|
FIGURE 1. Mean annual number of outbreaks in restaurant settings per 1,000 restaurants reported to the Foodborne Disease Outbreak
|
|||
|
Surveillance System (FDOSS) and the mean number of survey-reported complaints per 1,000 restaurants per year for agencies (@)
|
|||
|
|
|||
|
|
|||
|
participating in the restaurant grading project survey, 2016 to 2018.
|
|||
|
|
|||
|
|
|||
|
outbreaks are detected through complaint systems (6). The
|
|||
|
usefulness of complaints to detect outbreaks has been
|
|||
|
demonstrated by multiple studies (/2, /6-/8, 25). A
|
|||
|
survey of local health departments identified a positive
|
|||
|
correlation between outbreak and complaint rates per
|
|||
|
population served; agencies that received more complaints
|
|||
|
detected more outbreaks (/6). An analysis of the Florida
|
|||
|
|
|||
|
|
|||
|
2.5
|
|||
|
|
|||
|
|
|||
|
1:5
|
|||
|
|
|||
|
|
|||
|
Mean no. norovirus outbreaks in restuarant
|
|||
|
settings per 1,000 restaurants
|
|||
|
|
|||
|
|
|||
|
0 50 100
|
|||
|
|
|||
|
|
|||
|
Department of Health’s complaint and outbreak reporting
|
|||
|
system found that 56% of foodborne outbreaks were
|
|||
|
identified through complaints (/8). Likewise, complaints
|
|||
|
led to detection of 80% of foodborne outbreaks in Rhode
|
|||
|
Island (25) and 79% of confirmed foodborne outbreaks in
|
|||
|
Minnesota (/7). Not only can complaints be used to detect
|
|||
|
outbreaks, but they can also help identify specific
|
|||
|
|
|||
|
|
|||
|
R? = 0.1033
|
|||
|
|
|||
|
|
|||
|
vooure*
|
|||
|
|
|||
|
|
|||
|
150 200 250
|
|||
|
|
|||
|
|
|||
|
Mean no. complaints per 1,000 restaurants
|
|||
|
|
|||
|
|
|||
|
FIGURE 2. Mean annual number of norovirus outbreaks in restaurant settings per 1,000 restaurants reported to the Foodborne Disease
|
|||
|
Outbreak Surveillance System (FDOSS) and the mean number of survey-reported complaints per 1,000 restaurants per year for agencies
|
|||
|
(®) participating in the restaurant grading project survey, 2016 to 2018.
|
|||
|
|
|||
|
|
|||
|
7202 Ainr 6} UO JasN UOHUBASIq PUB [OUD aseasiq JO} S19}UB_ Aq Jpd'Q001-2-G8-2606-P 6 | /6S78Z0€/0001/2/S84Pd-a}oy12/dj[/Woo'ssaidualje"ueIpewu//:dy}Y Woy pepeojumMoq
|
|||
|
|
|||
|
|
|||
|
J. Food Prot., Vol. 85, No. 7
|
|||
|
|
|||
|
|
|||
|
0.9
|
|||
|
©
|
|||
|
2
|
|||
|
|
|||
|
408
|
|||
|
|
|||
|
2 = e
|
|||
|
28
|
|||
|
ap
|
|||
|
BE og
|
|||
|
se”
|
|||
|
oo
|
|||
|
vor
|
|||
|
|
|||
|
0.5
|
|||
|
Es
|
|||
|
€a
|
|||
|
8 % 04 AAA
|
|||
|
coe ee er
|
|||
|
£3 = @ oe
|
|||
|
§ 8 03 wa
|
|||
|
0 5 eo oo
|
|||
|
2] 5 02 eee
|
|||
|
Om | eer*
|
|||
|
c+ :
|
|||
|
£201
|
|||
|
|
|||
|
)
|
|||
|
|
|||
|
) 50 100
|
|||
|
|
|||
|
|
|||
|
EVALUATION OF RESTAURANT GRADING SURVEY RESULTS 1005
|
|||
|
|
|||
|
|
|||
|
ry deg
|
|||
|
|
|||
|
|
|||
|
150 200 250
|
|||
|
|
|||
|
|
|||
|
Mean no. complaints per 1,000 restaurants
|
|||
|
|
|||
|
|
|||
|
FIGURE 3. Mean annual number of bacterial toxin—mediated outbreaks in restaurant settings per 1,000 restaurants reported to the
|
|||
|
Foodborne Disease Outbreak Surveillance System (FDOSS) and the mean number of survey-reported complaints per 1,000 restaurants
|
|||
|
per year for agencies (@) participating in the restaurant grading project survey, 2016 to 2018.
|
|||
|
|
|||
|
|
|||
|
indicators of risk. For example, a study of consumer
|
|||
|
complaints in Washington, DC, found that complaints were
|
|||
|
significantly correlated with cited inspection violations of
|
|||
|
improper holding temperatures and contaminated equip-
|
|||
|
ment (/2). These studies highlight the usefulness of
|
|||
|
consumer complaints and underscore the need for
|
|||
|
|
|||
|
|
|||
|
0.9
|
|||
|
w
|
|||
|
pore)
|
|||
|
£
|
|||
|
5 08
|
|||
|
wu
|
|||
|
uw
|
|||
|
eS
|
|||
|
Ss 0.7
|
|||
|
I
|
|||
|
.
|
|||
|
8 2 06
|
|||
|
£f
|
|||
|
|
|||
|
=
|
|||
|
2805
|
|||
|
5S } =
|
|||
|
|
|||
|
Oo
|
|||
|
3 =) 0.4 ®
|
|||
|
sa :
|
|||
|
— —
|
|||
|
2 203
|
|||
|
S ®
|
|||
|
& e ° ° e
|
|||
|
A 02 |-
|
|||
|
ee a ee
|
|||
|
‘aa ee a ae
|
|||
|
: ©
|
|||
|
Ss 01 ° eo @
|
|||
|
> ° °°
|
|||
|
|
|||
|
0
|
|||
|
; - 100
|
|||
|
|
|||
|
|
|||
|
complaint-based surveillance in foodborne outbreak de-
|
|||
|
tection for pathogens with short incubation periods.
|
|||
|
|
|||
|
|
|||
|
Strengths and limitations. Strengths of this study
|
|||
|
|
|||
|
|
|||
|
include the use of national data (FDOSS) through a well-
|
|||
|
established outbreak surveillance system to validate out-
|
|||
|
|
|||
|
|
|||
|
150 200 250
|
|||
|
|
|||
|
|
|||
|
Mean no. complaints per 1,000 restaurants
|
|||
|
|
|||
|
|
|||
|
FIGURE 4. Mean annual number of Salmonella outbreaks in restaurant settings per 1,000 restaurants reported to the Foodborne Disease
|
|||
|
Outbreak Surveillance System (FDOSS) and the mean number of survey-reported complaints per 1,000 restaurants per year for agencies
|
|||
|
(®@) participating in the restaurant grading project survey, 2016 to 2018.
|
|||
|
|
|||
|
|
|||
|
7202 Ainr 6} UO JasN UOHUBAaIq PUB [OUD aseasiq JO) S19]UB_ Aq Jpd'Q00}-2-G8-2606- P76 | /6S78Z0€/0001/2/S84Pd-a}oI12/dj[/Woo'ssaidualje"uelpiew//:dyY Woy pepeo|umMoq
|
|||
|
|
|||
|
|
|||
|
1006 KIM ET AL.
|
|||
|
|
|||
|
|
|||
|
break counts reported via survey. The surveyed agencies
|
|||
|
accounted for nearly one-quarter of restaurant setting
|
|||
|
outbreaks reported to FDOSS. This study did not adjust
|
|||
|
for potential confounders such as jurisdiction size, geo-
|
|||
|
graphic region, state-level food program inspection and
|
|||
|
reporting requirements, funding, and staffing of the
|
|||
|
inspection agency. These factors may have affected an
|
|||
|
agency’s ability to investigate consumer complaints, detect
|
|||
|
outbreaks, and subsequently report them to FDOSS.
|
|||
|
However, there did not appear to be an association between
|
|||
|
jurisdiction size and reported outbreak rate (R? < 0.01). In
|
|||
|
most states there was considerable variation among
|
|||
|
agencies with respect to restaurant grading and disclosure
|
|||
|
practices. As noted above, the higher proportion of
|
|||
|
outbreaks attributable to norovirus and lower proportion
|
|||
|
of outbreaks with unknown etiology among the surveyed
|
|||
|
agencies may reflect that they had a better capacity to
|
|||
|
investigate foodborne illness outbreaks than did agencies
|
|||
|
that did not respond to the survey.
|
|||
|
|
|||
|
There are inherent limitations to the use of FDOSS
|
|||
|
data. First, because the FDOSS database is dynamic,
|
|||
|
agencies are permitted to submit, update, or delete reports
|
|||
|
at any time. Data used in the analysis for this study were
|
|||
|
pulled at one point in time; therefore, previous and future
|
|||
|
analyses using FDOSS data extracted in a similar fashion
|
|||
|
may produce slightly different results. Second, outbreak
|
|||
|
counts are reflective of those that were able to be detected.
|
|||
|
Not all outbreaks are identified by public health agencies,
|
|||
|
and as noted previously, the majority of foodborne illnesses
|
|||
|
are not a part of recognized outbreaks. It is unknown how
|
|||
|
well the etiologies and locations implicated in outbreaks
|
|||
|
reflect those of sporadic foodborne illnesses, i.e., illnesses
|
|||
|
not associated with outbreaks.
|
|||
|
|
|||
|
Limitations related to using the survey methods
|
|||
|
described include the use of a convenience sample of
|
|||
|
agencies that were enrolled in the Retail Program Standards
|
|||
|
program, which limited the representativeness of these
|
|||
|
results to enrollees. Agencies that enroll in this voluntary
|
|||
|
program may differ from those that choose not to enroll;
|
|||
|
however, because most (98%) of the agencies participating
|
|||
|
in the study were participants in the Retail Program
|
|||
|
Standards program, participation in the Retail Program
|
|||
|
Standards program is unlikely to bias the findings with
|
|||
|
respect to the main effect measures. Due to the inquiry of
|
|||
|
data from multiple time points (survey results during 2019
|
|||
|
to 2020 and outbreak data during 2016 to 2018), survey
|
|||
|
responses may not be truly reflective of practices during the
|
|||
|
time the outbreaks occurred.
|
|||
|
|
|||
|
A consumer’s propensity to file a foodborne illness
|
|||
|
complaint involving a restaurant is influenced by a variety
|
|||
|
of factors, including poverty status. Unpublished work
|
|||
|
studying the association of foodborne illness and inspection
|
|||
|
report data in Hennepin County, MN, found that census
|
|||
|
blocks with high poverty levels were associated with fewer
|
|||
|
foodborne illness complaints (OR = 0.31; 95% CI: 0.13 to
|
|||
|
0.73) (24). Nevertheless, underlying poverty status in the
|
|||
|
survey group was not deemed an important confounder in
|
|||
|
our analysis. Because the ability to detect outbreaks in
|
|||
|
restaurants heavily relies on complaint-based surveillance,
|
|||
|
|
|||
|
|
|||
|
J. Food Prot., Vol. 85, No. 7
|
|||
|
|
|||
|
|
|||
|
any biasing effect that poverty status may have on consumer
|
|||
|
propensity to file a complaint would also be reflected in the
|
|||
|
number of outbreaks. There are also different kinds of
|
|||
|
complaints that can be received about a restaurant: those
|
|||
|
that relate specifically to foodborne illness and those that
|
|||
|
relate to specific good retail practice violations. Although
|
|||
|
our study did not differentiate between the two types, it is
|
|||
|
plausible that the occurrence of violations may be an
|
|||
|
indicator of food safety practices that could lead to
|
|||
|
foodborne illness in the future.
|
|||
|
|
|||
|
Although this was a cross-sectional study that cannot
|
|||
|
control for the effects of policy changes within inspection
|
|||
|
programs, our associations are consistent with studies in
|
|||
|
Los Angeles County (20) and New York City (9) that
|
|||
|
demonstrated reductions in the occurrence of foodborne
|
|||
|
illnesses after implementation of posting of inspection
|
|||
|
grades at the POS. This study assessed the impact of the
|
|||
|
presence of disclosure at the POS, rather than the specific
|
|||
|
manners (e.g., location, font size) by which it occurred. If
|
|||
|
additional evidence were needed to encourage local food
|
|||
|
regulatory agencies to adopt a practice of grading and
|
|||
|
posting inspection results at the POS, then a randomized
|
|||
|
community-control trial could be considered as a next step.
|
|||
|
|
|||
|
|
|||
|
Policy implications. Surveys of public health agencies
|
|||
|
that are validated by national surveillance data can be
|
|||
|
powerful tools to identify model practices that contribute to
|
|||
|
prevention of foodborne outbreaks and illnesses. Particu-
|
|||
|
larly, our cross-sectional study findings are consistent with
|
|||
|
previous observations that linked the practice of posting
|
|||
|
graded inspection results at the POS with reduced
|
|||
|
occurrence of foodborne illnesses and outbreaks associated
|
|||
|
with restaurants. Other food regulatory practices, such as
|
|||
|
maintaining a robust foodborne illness complaint system,
|
|||
|
may improve foodborne illness surveillance, outbreak
|
|||
|
detection, and response. Improving foodborne illness and
|
|||
|
outbreak surveillance is a prerequisite for improving and
|
|||
|
measuring the effectiveness of our food safety systems.
|
|||
|
Support for foodborne illness surveillance programs and
|
|||
|
food regulatory activities at local health agencies is
|
|||
|
foundational for food safety systems coordinated at state
|
|||
|
and federal levels.
|
|||
|
|
|||
|
|
|||
|
ACKNOWLEDGMENTS
|
|||
|
|
|||
|
|
|||
|
This study was funded through cooperative agreement
|
|||
|
6NU380T000300 between the Centers for Disease Control and Prevention
|
|||
|
(CDC) and the National Environmental Health Association (NEHA). The
|
|||
|
findings and conclusions are solely the responsibility of the authors and do
|
|||
|
not necessarily represent the official views of CDC and NEHA. Additional
|
|||
|
support was provided by the Global Food Ventures MnDRIVE Fellowship
|
|||
|
at the University of Minnesota.
|
|||
|
|
|||
|
|
|||
|
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|
|||
|
|
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|
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|||
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|||
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7202 Ainr 6} UO JasN UOHUBAaIq PUB [OUOD aseasiq JO) S19}UB_ Aq Jpd'Q00-2-G8-2606-P 6 | /6S78Z0€/0001/2/S84Pd-a}oy12/dj[/Woo'ssaidualje"uelpHewu//:dy}Y Woy pepeo|umMoq
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|||
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|