Abstract
Foodborne illness is common in the United States with most, but not all, foodborne pathogens causing symptoms of acute gastroenteritis (AGI). Outpatient care is the most frequent type of medical care sought; however, more accurate estimates of outpatient costs are needed to inform food safety policy decision. Using the U.S. MarketScan Commercial Claims and Encounters database, we quantified the per-visit cost of outpatient visits with any AGI-related diagnosis (including pathogen-specific and nonspecific or symptom-based diagnoses) and for those with a pathogen-specific diagnosis for 1 of 29 pathogens commonly transmitted through food (including pathogens that cause AGI and some that do not). Our estimates included the per-case cost of office visits and associated laboratory tests and procedures as well as the conservative estimates of prescription cost. Most AGI outpatient visits were coded using nonspecific codes (e.g., infectious gastroenteritis), rather than pathogen-specific codes (e.g., Salmonella). From 2012 to 2015, we identified more than 3.4 million initial outpatient visits with any AGI diagnosis and 45,077 with a foodborne pathogen-specific diagnosis. As is typical of treatment cost data, severe cases of illness drove mean costs above median. The mean cost of an outpatient visit with any AGI was $696 compared with the median of $162. The mean costs of visits with pathogen-specific diagnoses ranged from $254 (median $131; interquartile range [IQR]: $98–184) for Streptococcus spp. Group A (n = 22,059) to $1761 (median $161; IQR: $104-$1101) for Clostridium perfringens (n = 30). Visits with two of the most common causes of foodborne illness, nontyphoidal Salmonella and norovirus, listed as a diagnosis, had mean costs of $841 and $509, respectively. Overall, the median per-case costs of outpatient visits increased with age, with some variation by pathogen. More empirically based estimates of outpatient costs for AGI and specific pathogens can enhance estimates of the economic cost of foodborne illness used to guide food policy and focus prevention efforts.
Introduction
The United States experiences an estimated 48 million foodborne illnesses each year (Scallan et al, 2011a; Scallan et al, 2011b). Many pathogens commonly transmitted through food (hereafter, foodborne pathogens) cause acute gastroenteritis (AGI; i.e., diarrhea and vomiting), including the two leading causes of foodborne illness in the United States—Salmonella and norovirus (CDC, 2019; Scallan et al, 2011b). Some foodborne pathogens do not usually manifest as AGI, including Listeria monocytogenes and Toxoplasma gondii. Roughly 20% of people with a foodborne illness have an outpatient visit (e.g., primary care physician or emergency room visit); <1% are hospitalized (Scallan et al, 2011b). While the cost of outpatient care is low compared with hospitalization, the high incidence of foodborne illnesses coupled with the relatively frequent use of outpatient care makes it important to build a stronger empirical basis for estimating the cost of foodborne illness outpatient care.
The U.S. cost of foodborne illness estimates contribute to policy analysis and public education about the impact of these illnesses. However, more detailed, information is needed to determine how best to estimate the cost of U.S. foodborne outpatient cases. Prior estimates of the cost of foodborne illnesses have assumed that all outpatient cases cost the same and based estimates on administrative payment schedules or studies of a single pathogen (Gastanaduy et al, 2013; Hoffmann et al, 2015; Ralston et al, 2011; Scharff, 2015; Scharff, 2012; Scharff et al, 2009; Weycker et al, 2009). In contrast, both medical and epidemiology analyses highlight substantial variation in the type and severity of illness by pathogen and serotype (Jones et al, 2008; Kennedy et al, 2004; Scallan et al, 2011b).
In this study, we quantified the per-visit cost of outpatient visits with any AGI diagnoses (including pathogen-specific and nonspecific or symptom-based diagnoses) and those with specific foodborne pathogens listed as a diagnosis using a large sample of commercial insurance claims from 2012 to 2015. We also explore variation in per-visit costs by age.
Materials and Methods
Data source
We used a commercial insurance claims database, MarketScan Commercial Claims and Encounters (Truven Health Analytics, Ann Arbor, MI). This database contains insurance billing data for outpatient visits (including office and emergency department visits), hospital stays, diagnostic tests and procedures, and prescription medications for >90 million persons in the United States covered by employer-sponsored health insurance (about half of the U.S. population is covered by employer-sponsored health insurance) (Hansen, 2018; Kaiser Family Foundation, 2019). This includes employees, retirees younger than 65, former employees, and spouses/partners and dependents of these individuals. These data are widely used in U.S. cost of medical treatment studies (Appendix A1). Due to changes in diagnostic codes, we limited this analysis to 2012–2015 to improve consistency. MarketScan contains deidentified, preexisting insurance billing records only. As a result, the analysis did not meet the definition of human subjects research (Appendix A1).
Inclusion criteria
We constructed a sample that comprised persons with at least one outpatient office visit diagnosed as any AGI or as caused by a specific foodborne pathogen, with the initial visit between January 2012 and December 2015 (Table 1). Any AGI was previously defined by the CDC (Scallan et al, 2011b) as International Classification of Disease (ICD) codes 001-008 (intestinal infections with pathogen-specific diagnoses), 009 (ill-defined intestinal infections), 558.9 (other and unspecified noninfectious diarrhea), or 787.91 (diarrhea, not otherwise specified). The CDC includes “other and unspecified diarrhea” (noninfectious cases) in its definition of AGI because in practice this code is often erroneously used to code infectious illness, including foodborne illnesses (Scallan et al, 2018; Scallan Walter et al, 2020). We refer to the International Classification of Diseases, Ninth Revision (ICD-9) codes 001-008 as pathogen-specific AGI and 009, 558.9, and 787.91 as nonspecific (symptom-based) AGI.
Defined Pathogens or Illness Groupings with Associated International Classification of Diseases, Ninth Revision, Clinical Modification Codes
The heading “Potentially foodborne pathogen-specific diagnoses” is used to refer to cases that have been diagnosed as having an infection with a pathogen that is frequently foodborne.
Excluding 008.45 (Clostridium difficile colitis) and 005.1 (botulism).
AGI, acute gastroenteritis; ICD-9, International Classification of Diseases, Ninth Revision; STEC,
Following CDC's AGI definition, we exclude cases diagnosed as Clostridium difficile colitis (008.45) or botulism food poisoning from any AGI. We also identified cases diagnosed with infections from 29 specific foodborne pathogens including Clostridium botulinum, an important foodborne pathogen (Table 1). Our goal was to include cases with diagnoses for all 31 foodborne pathogens for which the CDC has incidence estimates, but sapovirus and “Vibrio, other species” do not have specific ICD-9 diagnostic codes.
We include care in any outpatient setting (office, clinic, or emergency department). We exclude emergency department visits resulting in hospitalization. We only include claims for the first clinic visit with an AGI diagnosis code as most AGI patients have one visit per illness episode. We include only prescriptions filled on the day of this visit to limit costs to those most likely incurred for AGI care. We analyzed a subsample of cases and found a marked increase in the percentage of prescriptions used to treat non-AGI illnesses, particularly chronic health conditions, among those filled after the day of the outpatient visit. Persons covered by capitated insurance plans or plans without prescription drug coverage were also excluded (Appendix A1).
Analytical approach
For each outpatient visit, insurer and out-of-pocket payments for office visits, laboratory testing, and prescription drugs were totaled. We report claim frequencies, and mean, median, and interquartile ranges (IQRs) of per-case cost by diagnosis category and by age (0–4, 5–17, 18–64 years). Laboratory costs are included in office visit costs because it is not possible to separate laboratory from office visit costs for a large proportion of records (hereafter visit costs). A single visit may have several diagnoses. Thus, the sum of claim frequencies for AGI subgroups exceeds that of any AGI. Costs were standardized to July 2015 U.S. dollars. Data management and analyses were conducted using SAS software version 9.4 (SAS Institute, Cary, NC).
Results
Per-case total outpatient costs
From 2012 to 2015, we found more than 3.4 million initial outpatient visits with any AGI diagnosis code listed (Table 2) (visit codes henceforth referred to as diagnosis). Per-case total costs (visit plus prescription costs) were right-skewed, with means often exceeding the 75th percentile. The median cost of an outpatient visit with any AGI diagnosis code listed was $156 (mean: $678; IQR: $95–$520). The median cost of an outpatient visit diagnosed with nonspecific AGI ranged from $120 (IQR: $83–$196; mean: $322) for “ill-defined infections” (n = 264,363) to $201 (IQR: $110–$779; mean: $776) for “diarrhea, other gastrointestinal illness symptoms” (n = 1,741,599). Cases diagnosed as having “other and unspecified diarrhea from noninfectious causes” (n = 1,197,986) had a median cost of $150 (IQR: $91–$821; mean: $807). Only 1.2% of visits with any AGI diagnosis (n = 400,189) received a pathogen-specific diagnosis. The median cost of any pathogen-specific AGI outpatient visit was $117 (IQR: $82–$208; mean: $409).
Outpatient Costs per-Case, Acute Gastrointestinal Illness-Related Commercial Insurance Claims Aggregated by Diagnostic Code, 2012–2015, 2015 Dollars
Total cost includes the cost of in-patient visits, associated laboratory tests and procedures, and cost of prescriptions filled the day of the office visit. Visits due to an infection with a particular pathogen may be diagnosed with pathogen-specific and nonpathogen-specific diagnoses. For example, cases of salmonellosis may be diagnosed as Salmonella or as AGI.
The heading “Potentially foodborne pathogen-specific diagnoses” is used to refer to cases that have been diagnosed as having an infection with a pathogen that is frequently foodborne.
Outpatient and prescription drug costs aggregated on patient identification number and visit date, means and medians assessed for all ICD-9-CM codes with the diagnosis code examined.
Percent of total cost attributed to prescription drug costs calculated for each record, then averaged for all ICD-9-CM codes with diagnosis code examined.
ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification; IQR, interquartile range; RX, prescriptions; SD, standard deviation; STEC,
There were 45,077 outpatient visits diagnosed with one of the 29 foodborne pathogens included in this study. Their median per-case costs ranged from $113 (IQR: $80–$235; mean: $525) for cases diagnosed “Escherichia coli diarrheagenic, other” (n = 305) to $320 (IQR: $123–$1407; mean: $1323) for Cryptosporidium spp. (n = 334). Mean costs ranged from $254 (median $131; IQR: $98–184) for cases diagnosed with Streptococcus spp. Group A (n = 22,059) to $1761 (median $161; IQR: $104-$1101) for Clostridium perfringens (n = 30). Outpatient visits with nontyphoidal Salmonella (n = 2511) and norovirus (n = 1011) listed as diagnoses had median costs of $167 (IQR: $97–$455; mean: $841) and $132 (IQR: $90–$256; mean: $509), respectively.
We assessed the impact of including more than one outpatient visit on per-case cost by looking at six common diagnoses. Most (85%) people with any AGI diagnosis had only one visit in 30 days. Including all of a patient's outpatient visits with a foodborne-illness-related diagnosis within 30 days of their initial diagnosis increased the per-person cost for cases diagnosed as any AGI by ∼19%. Cost increases ranged from 10% for cases diagnosed as ill-defined intestinal infections to 35% for those with toxoplasmosis diagnoses (Appendix A1).
Per-case prescription costs
One-third (35%) of outpatient visits with any AGI diagnosis filled a prescription on their visit day; their prescription costs were 16% of mean total per-case visit costs (Table 2). For those diagnosed with nonspecific AGI, the percentage filling a prescription was 33% for “diarrhea, other AGI symptoms,” 36% for “other and unspecified diarrhea from noninfectious causes,” and 42% for “ill-defined infectious gastroenteritis” (representing 16%, 15%, and 16% of their mean total per-case costs, respectively).
Similarly, 34% of outpatient visits with a pathogen-specific AGI diagnosis filled prescriptions on the visit day (17% of the total costs). For visits with individual foodborne pathogens diagnoses, the percent filling same-day prescriptions ranged from 16% for toxoplasmosis (26% of total per-case visit cost) to 72% for Streptococcus spp. Group A claims (18% of cost). Almost one-third (32%) of outpatient visits with a nontyphoidal Salmonella diagnosis and 41% with a norovirus diagnosis filled a prescription on the same day as their visit, representing 16% and 17% of total visit costs, respectively.
Per-case total outpatient costs by age
Costs of visits with any-AGI diagnosis increased with age. Specifically, they were highest among those age 18–64 (n = 2,338,147; mean: $828; median: $193; IQR: $109–$874) compared with those age 5–17 years (n = 557,577; mean: $437; median: $119; IQR: $82–$238) and <5 (n = 523,035; mean: $262; median: $105; IQR: $78–$172) (Table 3). This held for cases with pathogen-specific or nonspecific AGI diagnoses. However, trends varied among cases with individual foodborne pathogen diagnoses. For example, the median per-case cost of an outpatient visit increased with age for those diagnosed with nontyphoidal Salmonella ($127, $157, and $182 for those <5, 5–17, and 18–64, respectively), but decreased with age for those diagnosed with rotavirus ($388, $227, and $137) or Campylobacter ($466, $380, and $304).
Total Outpatient Costs per-Case by Age Group, Acute Gastrointestinal Illness-Related Commercial Insurance Claims Aggregated by Diagnostic Code, 2012–2015, 2015 Dollars
Total cost includes the cost of in-patient visits, associated laboratory tests, and cost of prescriptions filled the day of the office visit. The heading “Potentially foodborne pathogen-specific diagnoses” is used to refer to cases that have been diagnosed as having an infection with a pathogen that is frequently foodborne.
IQR, interquartile range; SD, standard deviation; STEC,
Discussion
The goal of this study was to improve the basis for estimating the cost of outpatient treatment of foodborne disease in the United States. Limited prior research affected the way all three recent U.S. cost of foodborne illness estimated outpatient costs. Scharff (2012) assumed uniform per-case costs based on “usual, customary, and reasonable rates” from fee schedules for physician office visits, emergency room visits, and laboratory charges (Practice Management Information Corporation, 2009; Scharff, 2012). Noting a lack of research on pharmaceutical costs for foodborne illnesses, he based per-case cost on prior studies of a salmonellosis outbreak and of
Hoffmann et al (2012) assumed illnesses other than STEC had the same per-case outpatient visit cost as Salmonella (based on Frenzen et al, 1999 using 1994–1996 MarketScan data ($496 2015$)). Neither Hoffmann et al (2012) nor Minor et al (2015) included pharmaceutical costs due to a lack of research and a finding in Frenzen (2005) that drug costs were <2% of STEC total cost of illness. Ours is the first study to use a large national administrative data set to examine how outpatient treatment and pharmaceutical costs vary by AGI and specific foodborne pathogen diagnoses and by age.
Most outpatient visits in our study had nonspecific, that is, symptom-based, AGI diagnoses. Only 12% of all AGI visits had any pathogen-specific AGI diagnosis; there were even fewer visits with one of the 29 foodborne pathogen-specific diagnoses. Pathogen-specific diagnoses were used infrequently in comparison with their annual incidence. Norovirus, Salmonella, C. perfringens, Campylobacter, and Staphylococcus aureus collectively cause roughly 18% of all the estimated U.S. foodborne illnesses (known or unspecified etiology), but the number of visits with these diagnoses was <1% of visits with any-AGI diagnoses in our sample (Scallan et al, 2011b).
Differing severity of illness could explain the low utilization of pathogen-specific diagnoses presumably reflecting low rates of stool tests. Research examining laboratory data and medical records found that fewer than half of hospitalized patients with culture-confirmed Salmonella, Campylobacter, or E. coli O157 infection received a corresponding pathogen-specific diagnosis in their billing records (Scallan et al, 2018; Scallan Walter et al, 2020). Physicians may be even less likely to order stool tests in an outpatient setting since most of the outpatient treatments do not require a pathogen-specific diagnosis (Mullaney et al, 2019). Having bloody diarrhea or any diarrhea for more than 3 d has been associated with a higher rate of stool sample orders for outpatients than less severe illness with nonbloody diarrhea or diarrhea for 3 d or less (Mullaney et al, 2019; Scallan et al, 2011a).
Previous research found that physicians submitted a stool sample for only 19% of people who sought health care for nonbloody diarrhea (Scallan et al, 2011b). In a survey of U.S. Armed Forces members who visited a physician for AGI, 13% were asked to submit a stool sample, of these 89% did (Mullaney et al, 2019).
AGI is treated with several types of drugs: rehydration therapies, antimotility, antinausea, antiemetic drugs, antacids, probiotics, and antibiotics (Shane et al, 2017). A German study found that 31% of AGI patients reported taking a prescription drug for their AGI and 10% of patients reported taking an antibiotic (Wilking et al, 2013). A recent U.S. study found that 13% of AGI visits were prescribed antibiotics (Collins et al, in press). We found that 35% of patients with “any-AGI” diagnosis filled prescriptions the day of their visit (mean cost $108). Based on assumptions regarding medicine usage and average drug costs, Frenzen et al (2005) estimated prescriptions for treating STEC cost $73 (2015$) compared with our estimate of $126 for cases diagnosed as STEC O157.
What do these results say about best estimates of the cost of outpatient treatment for foodborne infections? First, right-skewed distributions are typical of medical treatment cost data. Cost-of-illness studies use mean estimates because severe/costly cases, not just typical cases, need to be reflected in society's cost of treating illness. ERS currently assumes uniform cost for outpatient visits, $496, for all pathogens except STEC O157 (2015$) (Hoffmann et al, 2012; USDA ERS, 2021). We find a mean per-case visit cost for cases with “any AGI” diagnoses of $678 (2015$), $409 for pathogen-specific AGI, and $322 for ill-defined intestinal infections. The mean cost of outpatient visits diagnosed with a specific foodborne pathogen ranges from $254 for Streptococcus spp. to $1761 for C. perfringens. Given the low rate of stool samples ordered in outpatient cases, most cases will be diagnosed as nonspecific AGI.
More severe cases, for example, those with bloody diarrhea, are more likely to have a stool sample ordered and therefore should be more costly. Some nonspecific AGI cases were more costly, likely because this category included noninfectious cases such as chronic gut disorders, but cannot be separated based on ICD codes. Ideally, one might calculate a weighted mean of the foodborne-pathogen-specific and nonspecific AGI per-case costs, but we are aware of no source of data to construct such a weighting for inpatient cases.
The mean per-case costs of cases with a foodborne pathogen-specific diagnosis, including pathogens not causing AGI symptoms, fall within one standard deviation of the mean cost of any AGI. The differences between mean any-AGI per-case outpatient cost and that of each foodborne pathogen diagnosis averages to $23. Together, this suggests that the practice of using a uniform per-case cost for outpatient cases is defensible even based on more detailed data than prior studies examined. In general, disease severity among cases treated in only an outpatient setting does not vary enough to create substantial differences in per-case medical treatment and prescription costs. The one exception is Streptococcus, which does not cause AGI. Cases with a Streptococcus diagnosis have a mean per-case cost, $254, that is less than half that of cases diagnosed as any AGI.
It is unclear to us why outpatient cases among adults younger than 65 would be more costly in general than those in children, particularly children younger than 5 years. It is possible that physicians are more likely to admit children <5 to the hospital than an adult with the same symptoms. There are foodborne pathogen-specific diagnoses for which those younger than 5 have higher mean per-case costs than adults, but with the exception of rotavirus, the number of observations is quite small.
These are several limitations to this analysis. First, although MarketScan provides a large sample of insured patients, it is not nationally representative (differences in patient characteristics, as well as plan and benefit type between these data and that of all privately insured individuals, may affect the results). Medical care seeking behavior may differ by insurance plan, which could impact the aggregate results. Most importantly, it does not include those 65 years and older. Analyses specific to Medicare would be needed to explore age effects more comprehensively. Second, as with all medical claims data, physicians use diagnostic codes inconsistently, affecting estimates. For instance, specific clinical features may influence a physician's decision to order laboratory diagnostics, such that those cases with a pathogen-specific diagnosis may differ from those with more generic, symptom-based coding.
Third, we examined costs resulting from the first outpatient visit for each person during the study time period. As most episodes of foodborne illness are self-limiting, most people have only one outpatient visit. All prior costs of foodborne illness estimates assume one outpatient visit. Our sensitivity analysis shows these results in conservative outpatient visit cost estimates. Similarly, our prescription costs include only prescriptions filled the day of the office visit resulting in conservative estimates of prescription costs, but less likely to pick up non-foodborne illness-related prescriptions, and in line with prior estimates. Fourth, some foodborne pathogens do not present with classic AGI symptoms (e.g., C. botulinum, Brucella, Listeria, and T. gondii). With the exception of Streptococcus, mean estimates of per-case costs of cases with these non-AGI diagnoses do not differ substantially from mean per-case cost of cases with “any-AGI” diagnosis.
Conclusion
Cost-of-illness estimates, along with incidence and burden estimates, help guide decisions about where to best focus scarce prevention resources. Although outpatient costs for many pathogens were comparable, some variation was observed. When conducting pathogen-specific economic analyses, researchers may consider these results to determine if general AGI or pathogen-specific costs are needed to most accurately reflect economic burden. Age effects were present both among aggregate AGI diagnosis groups and among cases with pathogen-specific diagnoses. These effects should be considered in cost or decision analytic studies specific to age subgroups and to inform weighting of cost estimates across diverse samples or populations.
Footnotes
Acknowledgments
We thank Megan Gerdes for providing analytic assistance, Scott Grosse for advice on methods, Lauren Sandell for preparing the article for publication, and the many subject matter experts within the CDC Division of Foodborne, Waterborne, and Environmental Diseases who provided pathogen-specific expertise in interpreting the results.
Authors' Contributions
All authors have taken part in writing the article, reviewing it, and revising its intellectual and technical content. All authors assume responsibility and accountability for the results.
Disclaimer
The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention or the U.S. Department of Agriculture and should not be construed to represent any official U.S. Government determination or policy.
Disclosure Statement
No competing financial interests exist.
Funding Information
Funding for MarketScan and government staff was provided by the Centers for Disease Control and Prevention and the Department of Agriculture, Economic Research Service.