Reported Incidence of Infections Caused by Pathogens Transmitted Commonly Through Food: Impact of Increased Use of Culture-Independent Diagnostic Tests — Foodborne Diseases Active Surveillance Network, 1996–2023
Weekly / July 4, 2024 / 73(26);584–593
Hazel J. Shah, MPH1; Rachel H. Jervis, MPH2; Katie Wymore, MPH3; Tamara Rissman, MPH4; Bethany LaClair, MPH5; Michelle M. Boyle, MPH6; Kirk Smith, DVM, PhD7; Sarah Lathrop, DVM, PhD8; Suzanne McGuire, MPH9; Rosalie Trevejo, DVM, PhD10; Marcy McMillian, MPH11; Stic Harris, DVM12; Joanna Zablotsky Kufel, PhD13; Kennedy Houck, MPH1; Carey E. Lau1; Carey J. Devine, MPH1; Dave Boxrud, MS1; Daniel L. Weller, PhD1 (View author affiliations)
View suggested citationSummary
What is already known about this topic?
Increased use of culture-independent diagnostic tests (CIDTs) affects observed trends in foodborne infection incidence.
What is added by this report?
During 2023, the incidence of eight domestically acquired infections transmitted commonly through food either increased or remained stable compared with 2016–2018, the baseline used to track progress toward disease reduction goals. Incidence of CIDT-diagnosed infection also increased during 2023.
What are the implications for public health practice?
CIDTs allow for diagnosis of infections that previously would have been undetected; recent increases in incidence appear to be driven by increased CIDT use. Continued surveillance is needed to monitor the impact of changing diagnostic practices on disease trends. Targeted prevention efforts are needed to reduce disease incidence.
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Abstract
Reducing foodborne disease incidence is a public health priority. This report summarizes preliminary 2023 Foodborne Diseases Active Surveillance Network (FoodNet) data and highlights efforts to increase the representativeness of FoodNet. During 2023, incidences of domestically acquired campylobacteriosis, Shiga toxin-producing Escherichia coli infection, yersiniosis, vibriosis, and cyclosporiasis increased, whereas those of listeriosis, salmonellosis, and shigellosis remained stable compared with incidences during 2016–2018, the baseline used for tracking progress towards federal disease reduction goals. During 2023, the incidence and percentage of infections diagnosed by culture-independent diagnostic tests (CIDTs) reported to FoodNet continued to increase, and the percentage of cases that yielded an isolate decreased, affecting observed trends in incidence. Because CIDTs allow for diagnosis of infections that previously would have gone undetected, lack of progress toward disease reduction goals might reflect changing diagnostic practices rather than an actual increase in incidence. Continued surveillance is needed to monitor the impact of changing diagnostic practices on disease trends, and targeted prevention efforts are needed to meet disease reduction goals. During 2023, FoodNet expanded its catchment area for the first time since 2004. This expansion improved the representativeness of the FoodNet catchment area, the ability of FoodNet to monitor trends in disease incidence, and the generalizability of FoodNet data.
Introduction
Reducing the incidence of foodborne and enteric diseases is a public health priority. The Healthy People 2030 (HP2030) initiative established disease reduction goals for Campylobacter, Listeria, Salmonella, and Shiga toxin-producing Escherichia coli (STEC) infections (1). To evaluate progress toward HP2030 goals, CDC’s Foodborne Diseases Active Surveillance Network (FoodNet) monitors infections caused by eight pathogens transmitted commonly through food. This report summarizes preliminary 2023 surveillance data and describes changes in incidence compared with average annual incidence during 2016–2018, the reference period used by HP2030 (1).
Methods
Data Source
FoodNet conducts active, population-based surveillance for laboratory-diagnosed Campylobacter, Cyclospora, Listeria, Salmonella, Shigella, STEC, Vibrio, and Yersinia infections and pediatric hemolytic uremic syndrome (HUS) at 10 U.S. sites;* HUS is monitored because it can be a complication of STEC infection. FoodNet’s catchment area expanded during 2023 to include all of Colorado, and now represents 16% of the U.S. population (53.6 million persons); in 2023, the historic catchment area represented 15% of the U.S. population (51.0 million persons). Compared with the historic catchment area, the expansion increased representation for specific populations, including Hispanic or Latino ([Hispanic]; 8% increase), American Indian or Alaska Native (AI/AN; 8% increase), and Native Hawaiian or Pacific Islander (NH/PI; 6% increase) persons (FoodNet collects race and ethnicity as separate variables) as well as persons living in rural counties (10% increase).
Laboratory Testing and Data Collection
Bacterial infections were diagnosed by culture or culture-independent diagnostic tests (CIDTs). Cyclosporiasis was diagnosed by polymerase chain reaction or microscopy. Pediatric HUS surveillance is conducted through a network of nephrologists and infection preventionists and by hospital discharge data review.† This report includes 2022 data on pediatric HUS cases, the most recent year for which data are available. This activity was reviewed by CDC, deemed not research, and conducted in accordance with applicable federal law and CDC policy.§
Statistical Methods
Bayesian negative binomial models were implemented to estimate changes in incidence in the historic catchment area during 2023 compared with average annual incidence during 2016–2018 (overall, and for domestically acquired infections), using R statistical software (version 2.14.0; R Foundation).¶,** Incidence in 2023 was considered substantially different†† from that during 2016–2018 if the 95% credible interval (CrI) for the incidence rate ratio (IRR) did not include 1.0. Cross-tabulations by demographic and other characteristics were also performed.§§
Results
Incidence in 2023 Compared with Average Annual Incidence During 2016–2018
During 2023, FoodNet identified 29,607 infections, 7,234 hospitalizations, and 177 deaths overall (including domestically acquired and travel-associated infections) in the historic catchment area (Table 1) (Table 2), compared with 31,492 infections, 7,588 hospitalizations, and 184 deaths in the expanded catchment area¶¶ (Supplementary Table; https://stacks.cdc.gov/view/cdc/157822). In both the historic and expanded catchment areas, 15% of cases were associated with international travel. Overall, and for domestically acquired infections only, incidence of campylobacteriosis was highest, followed by salmonellosis and STEC infection. In the historic catchment area during 2023, incidences of domestically acquired campylobacteriosis, cyclosporiasis, STEC infection, vibriosis, and yersiniosis increased compared with those during 2016–2018, whereas listeriosis, salmonellosis, and shigellosis incidences remained stable.
Generally, the overall percentage of infections attributable to specific Campylobacter, Shigella, Vibrio, and Yersinia species, Salmonella serotypes, and STEC serogroups was lower in 2023 than in all previous years (Table 3). The overall incidence of infections for which the pathogen was not speciated, serotyped, or serogrouped increased substantially compared with incidence during 2016–2018 (Table 2). During 2023, 78% of all bacterial infections were diagnosed by CIDTs in the historic catchment area, including 46% diagnosed using only CIDTs. The percentage of CIDT-diagnosed infections for which a reflex culture*** was attempted decreased from 71% during 2016–2018 to 68% during 2023. This decrease was largest for Yersinia, Vibrio, and STEC infections. For all illnesses except listeriosis, the percentage of reflex cultures that yielded an isolate (successful [or positive] reflex culture) was lower in 2023 than during previous years (Table 3). This decrease in isolate availability has been associated with a decrease in serotyped, serogrouped, and speciated infections. For example, from 2016–2018 to 2023, the overall incidence of unspeciated infections increased substantially for Campylobacter,††† Shigella,§§§ Yersinia,¶¶¶ and Vibrio****; the percentage of speciated infections declined from 33% to 26% for Campylobacter, from 65% to 41% for Shigella, from 49% to 23% for Yersinia, and from 61% to 34% for Vibrio. Although only culture-independent methods are used to diagnose cyclosporiasis, increases in CIDT-diagnosed cyclosporiasis and cyclosporiasis incidence mirror CIDT-driven increases in bacterial infection incidence.
Salmonella Infections
Of 8,454 total (i.e., both domestically acquired and travel-associated) Salmonella infections during 2023 in the historic catchment area, 83% yielded an isolate; 89% of isolates were fully serotyped. The incidence of nonserotyped infections increased substantially.†††† The incidences of the most frequently reported serotypes, S. Enteritidis and S. Newport, remained stable during 2023 compared with those during 2016–2018, whereas the incidences of the next-most frequently reported serotypes, S. Typhimurium, S. Javiana, and S. I 4,[5],12:i:- decreased substantially.
STEC Infections
Of 3,351 total STEC infections in the historic catchment area during 2023, 57% yielded an isolate; 87% of isolates were fully serogrouped. The incidence of nonserogrouped infections increased substantially in 2023 compared with that during 2016–2018.§§§§ During 2023, STEC O157 incidence decreased compared with incidence during 2016–2018, and non-O157 STEC incidence remained stable.
Hemolytic Uremic Syndrome
During 2022, FoodNet identified 61 cases of postdiarrheal HUS in persons aged <18 years, including 39 among children aged <5 years. The incidence of postdiarrheal HUS among persons aged <18 years (0.6 per 100,000 persons) and those aged <5 years (1.4 per 100,000) remained stable in 2022 compared with that during 2016–2018.¶¶¶¶
Discussion
The current findings and previous FoodNet reports (2,3) suggest a lack of progress toward foodborne disease reduction goals; however, this outcome might reflect changing diagnostic practices such as the increased use of CIDTs rather than an actual increase in disease incidence. Increased use of CIDTs facilitates prompt clinical diagnosis and treatment but also complicates the interpretation of surveillance data and trends because CIDT adoption has varied over time, among clinical labs, and by pathogen. In addition, although CIDTs are generally considered more sensitive than are culture-based methods, some have high false-positive rates for certain pathogens (e.g., Vibrio) (4–6). Previous studies have indicated that increased CIDT use has resulted in the diagnosis of infections that previously would have gone undetected; increased use of CIDTs has been associated with marked increases in reported incidence (4,7).
Increases in CIDT-diagnosed infections are also associated with decreased rates of reflex culture, thereby reducing the number of isolates available for subtyping, whole genome sequencing, and antimicrobial resistance characterization (8). The impact of this reduction differs by species, serotype, and serogroup. Because an isolate is required for speciation, serotyping, and serogrouping, reduced isolate availability might result in underdetection of illnesses attributable to specific Campylobacter, Shigella, Vibrio, and Yersinia species, Salmonella serotypes, and STEC serogroups. The substantial increase in the incidence of infections for which the pathogen was not speciated, serotyped, or serogrouped is likely an artifact of changing diagnostic practices (i.e., increased CIDT use), resulting in a reduced availability of isolates for speciation and typing. Continued reductions in isolate availability might hinder outbreak identification and response (e.g., whole genome sequencing–based cluster identification and source attribution), detection of emerging antimicrobial resistance, and tracking of trends in illnesses attributable to specific species, subtypes, serotypes, and resistant strains. Increasing successful reflex culture rates after a CIDT diagnosis is a public health priority, which requires focused efforts and resources at the federal, state, and local levels.
FoodNet data are used to track trends in enteric illness, monitor progress toward disease reduction goals, and guide food safety policy*****,††††† (1). Because FoodNet is a sentinel surveillance system representing 10 sites, national extrapolation relies on strong assumptions of representativeness. Although the sites included in the FoodNet catchment area were selected nonrandomly, past analyses suggest that FoodNet’s catchment area is broadly representative of the national population (9,10). Previously, the only notable difference between FoodNet’s historic catchment area and the national population identified by these studies was that Hispanic persons were underrepresented in the catchment area relative to national representation (9,10). Investigating enteric disease epidemiology for AI/AN and NH/PI persons using FoodNet data has also been complicated by the small size of these populations in the historic catchment area. By increasing representation for these specific populations in the FoodNet catchment area, FoodNet’s expansion has helped to partially alleviate these limitations and improve the generalizability of FoodNet data. Additional expansion might be needed as national and catchment area demographics change.
Limitations
The findings in this report are subject to at least three limitations. First, underreporting might affect case counts because ill persons must seek care and be tested for their illness to be recorded as a case. Second, although ill persons might meet the FoodNet criteria for hospitalization or death, the underlying reason for hospitalization or death might be unknown. Deaths that occurred >1 week after specimen collection among nonhospitalized persons or after discharge for hospitalized persons might not be recorded. Finally, domestically acquired cases might be overestimated because of the inclusion of persons with unknown travel status.
Implications for Public Health Practice
FoodNet’s surveillance efforts are critical for tracking foodborne and enteric illnesses in the United States. During 2023, FoodNet expanded its catchment area for the first time since 2004, and it now includes all of Colorado. This expansion improved the representativeness of the FoodNet catchment area, and the ability of FoodNet to monitor trends in disease incidence, including the impact of changing diagnostic practices and the generalizability of FoodNet data. Continued surveillance is needed to monitor the impact of changing diagnostic practices on disease trends and evaluate the efficacy of prevention efforts in reducing incidence.
Acknowledgments
Workgroup members, Foodborne Diseases Active Surveillance Network (FoodNet), Emerging Infections Program, CDC.
Corresponding author: Daniel L. Weller, qok9@cdc.gov.
1Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 2Colorado Department of Public Health and Environment; 3California Emerging Infections Program, Oakland, California; 4Connecticut Emerging Infections Program, Yale School of Public Health, New Haven, Connecticut; 5Georgia Department of Public Health; 6Maryland Department of Health; 7Minnesota Department of Health; 8University of New Mexico, Albuquerque, New Mexico; 9New York State Department of Health; 10Oregon Health Authority; 11Tennessee Department of Health; 12Center for Food Safety and Applied Nutrition, Food and Drug Administration, College Park, Maryland; 13Food Safety and Inspection Service, U.S. Department of Agriculture, Washington, DC.
All authors have completed and submitted the International Committee of Medical Journal Editors form for disclosure of potential conflicts of interest. Tamara Rissman reports that she is an adjunct professor in the Public Health Department at Southern Connecticut State University. No other potential conflicts of interest were disclosed.
* FoodNet is a collaboration among CDC, 10 state health departments, the U.S. Department of Agriculture’s Food Safety and Inspection Service, and the Food and Drug Administration. The historic catchment area includes sites under surveillance since 2004, including Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, and Tennessee, and counties in California (three), Colorado (seven), and New York (34). The expanded catchment area includes these sites and 57 Colorado counties not in the historic catchment area (i.e., the rest of Colorado).
† FoodNet reviews hospital discharge data for pediatric HUS cases to validate surveillance reports and identify additional cases using International Classification of Diseases, Tenth Revision and International Classification of Diseases, Eleventh Revision codes.
§ 45 C.F.R. part 46.102(l)(2), 21 C.F.R. part 56; 42 U.S.C. Sect. 241(d); 5 U.S.C. Sect. 552a; 44 U.S.C. Sect. 3501 et seq.
¶ Incidence (cases per 100,000 persons) was calculated by dividing number of infections during 2023 by 2022 U.S. Census Bureau population estimates. Changes in incidence for the historic catchment area were quantified as described previously (https://www.medrxiv.org/content/10.1101/2022.09.14.22279742v1). Because only 1 year of expanded catchment area data are available, incidence changes could not be quantified for the expanded catchment area.
** If the ill person did not report international travel or had an unknown travel history, the illness was considered to have been domestically acquired. A history of international travel was defined as travel ≤30 days before listeriosis and S. Typhi and S. Paratyphi infections onset, ≤14 days before cyclosporiasis onset, and ≤7 days before onset for other infections.
†† In contrast to frequentist statistics, which use significance testing, in a Bayesian model, true significance testing is not done, and differences are described as substantial.
§§ Unknown responses were included in proportion denominators.
¶¶ Incidence was similar in the historic and expanded catchment areas during 2023 with the exception of a higher cyclosporiasis incidence and a higher percentage of outbreak-associated cases in the expanded catchment area because of a cyclosporiasis outbreak that affected the newly enrolled Colorado counties. https://cdphe.colorado.gov/press-release/cdphe-investigating-cyclospora-outbreak-on-western-slope
*** CIDTs do not require culturing for diagnosis; however, reflex culture might be attempted after CIDT-based diagnosis. Reflex culture refers to attempting to grow and isolate the detected pathogen in a laboratory culture medium after a positive CIDT test result. Reflex culture practices vary by diagnostic laboratory, state, and pathogen.
††† The most frequently reported Campylobacter species in the historic catchment area during 2023 were C. jejuni (2,672), C. coli (316), C. upsaliensis (79), C ureolyticus (19), and C. lari (13). Compared with 2016–2018, incidence of unspeciated campylobacteriosis increased substantially in 2023 (IRR = 1.31; 95% CrI = 1.19–1.45).
§§§ The most frequently reported Shigella species in the historic catchment area during 2023 were S. flexneri (926), S. sonnei (364), S. boydii (14), and S. dysenteriae (three). Incidence of unspeciated shigellosis increased substantially in 2023 compared with 2016–2018 (IRR = 2.33; 95% CrI = 1.79, 3.12).
¶¶¶ The most frequently reported Yersinia species in the historic catchment area during 2023 were Y. enterocolitica (294), Y. frederiksenii (28), Y. kristensenii (19), Y. intermedia (eight), and Y. massilkensis (four). Compared with 2016–2018, incidence of unspeciated yersinosis increased substantially in 2023 (IRR = 7.19; 95% CrI = 4.78–11.97).
**** The most frequently reported Vibrio species in the historic catchment area during 2023 were V. parahaemolytics (105), V. alginolytics (30), V. fluvialis (25), V. cholerae (20), and V. vulnificus (13). Compared with 2016–2018, incidence of unspeciated vibriosis increased substantially in 2023 (IRR = 4.29; 95% CrI = 3.00–6.59).
†††† Overall, the most frequently reported Salmonella serotypes in the historic catchment area during 2023 were not serotyped infections (2,297), S. Enteritidis (1,597), S. Newport (566), S. Typhimurium (541), S. Javiana (324), and S. I 4,[5],12:i:- (279). The IRR for nonserotyped, domestically acquired infections in the historic catchment area was 1.67 (95% CrI = 1.38–2.01).
§§§§ STEC isolates were considered fully serogrouped if the O antigen was determined. Overall, infections in which the isolate was not serogrouped (1,941) were more frequent than infections with fully serogrouped isolates (1,410); among all fully serogrouped isolates, serogroup O157 (298) was most frequently reported in the historic catchment area during 2023, followed by O103 (188), O26 (173), and O111 (160). The IRR for nonserogrouped, domestically acquired infections during 2023 compared with 2016–2018 was 1.79 (95% CrI = 1.36–2.48).
¶¶¶¶ The IRRs for pediatric HUS cases during 2022 compared with 2016–2018 for persons aged <18 years and <5 years were 1.0 (95% CrI = 0.8–1.2) and 1.0 (95% CrI = 0.8–1.3), respectively.
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Suggested citation for this article: Shah HJ, Jervis RH, Wymore K, et al. Reported Incidence of Infections Caused by Pathogens Transmitted Commonly Through Food: Impact of Increased Use of Culture-Independent Diagnostic Tests — Foodborne Diseases Active Surveillance Network, 1996–2023. MMWR Morb Mortal Wkly Rep 2024;73:584–593. DOI: http://dx.doi.org/10.15585/mmwr.mm7326a1.
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