https://orcid.org/0000-0001-8558-8779
Figures
Abstract
Background
While acute gastroenteritis (AGE) occurs year-round, norovirus has a winter seasonality in the United States.
Objective
We analyzed norovirus seasonality within a US integrated healthcare delivery system from 2016–2019.
Methods
Electronic medical records were collected for acute gastroenteritis (AGE) encounters with specific ICD-9/10 codes or clinical stool testing. Norovirus percent positivity was calculated as the 8-week centered rolling average. Temperature and absolute humidity data were measured via weather station. The relationship between these factors and weekly norovirus episodes were modeled via negative binomial models.
Results
From 2016–2019, there were 198,181 AGE episodes reported; among the 18,998 episodes tested, 892 (5%) were norovirus positive. Norovirus percent positivity peaked in epidemiologic week 7 at 9%. Two negative binomial models showed significant inverse relationships between weekly number of norovirus episodes and both temperature and absolute humidity.
Citation: Mattison CP, Calderwood LE, Cates JE, Donald J, Hall AJ, Schmidt MA, et al. (2025) Seasonality of medically attended norovirus gastroenteritis and its association with climatic factors within an US integrated healthcare system, 2016–2019. PLoS One 20(5): e0318077. https://doi.org/10.1371/journal.pone.0318077
Editor: Shinya Tsuzuki, National Center for Global Health and Medicine, JAPAN
Received: October 15, 2024; Accepted: January 9, 2025; Published: May 9, 2025
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Data Availability: This study used medical record data, which is personally identifiable and not publicly available due to these restrictions. Data required for this analysis include personally identifiable information including; medical encounter dates, chronic health conditions, age, gender, race, ethnicity, and other socio-economic variables. Datasets can be made available upon request via contacting the Viral Gastroenteritis branch at the centers of disease control and prevention at ncirddvdgast@cdc.gov.
Funding: This work was supported by the CDC Foundation (institutional research funding to the Kaiser Permanente Center for Health Research) and Takeda Vaccines, Inc. (investigator-initiated research grants IISR-2015-101015 and IISR-2017-101938 to the Kaiser Permanente Center for Health Research). Takeda had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The CDC received no funding from Takeda.
Competing interests: CPM, LEC, JEC, AJH, & SAM report no conflicts of interest. JD received an institutional research grant from Takeda Pharmaceuticals for this work. JD has also received grants from Moderna and HilleVax. MAS received grants from Takeda Pharmaceuticals, CDC Foundation, and the Centers for Disease Control and Prevention for this work. MAS has also received grants from Moderna, HilleVax, Pfizer, NIH, Janssen, and CDC. MAS has an unpaid role in the Wahkiakum Health and Human Services Community Advisory Board. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. This does not alter our adherence to PLOS ONE policies on sharing data and materials. There are no patents, products in development or marketed products associated with this research to declare.
Introduction
Viral acute gastroenteritis (AGE), defined as diarrhea or vomiting caused by viruses such as rotavirus and norovirus, has a substantial global disease burden [1]. While rotavirus is the leading cause of AGE among children <5 years old worldwide [2], in countries that have introduced rotavirus vaccine, such as the United States, norovirus is now the leading cause of AGE [3].
While viruses cause AGE year-round, viral AGE tends to have a winter seasonality [4–5]. Norovirus has been defined by its winter seasonality and was originally known as “winter vomiting disease” [6]. US-based surveillance systems of AGE outbreaks and sporadic disease also show a winter seasonality for norovirus, starting in November and peaking in December/January [7,8]. The US rotavirus season typically begins in January and peaks mid-spring; post-vaccine introduction, rotavirus has developed a biennial pattern with alternating high and low seasons [9].
The exact factors that influence seasonality of viral AGE are unknown but may include human behaviors, virologic factors, and climatic factors, such as temperature, humidity, and rainfall. A review of studies looking at the relationship of various climatic factors and norovirus outbreaks found lower temperatures were correlated with periods of high norovirus transmission, while the relationship between norovirus and humidity was mixed [10]. Studies reviewed found both positive and negative correlations between relative humidity and norovirus transmission [10–12]. The relationship between rainfall and norovirus was also unclear; some studies found that norovirus was correlated with rainfall while others found a correlation with dry weather [10]. While the exact mechanism of how climate factors such as; temperature, humidity, and rainfall may interact to impact norovirus stability and transmission is unknown, it is possible these factors may both change human behavior and influence virus stability and allow for increased transmission. Additionally, temperature extremes may change human behavior, increasing time spent indoors in possibly crowded conditions resulting in increased contacts, and conditions for increased disease transmission. Understanding the relationship between climatic factors and AGE may help predict periods of increased disease transmission and future changes to disease transmission dynamics in the face of continued climate change.
While a winter seasonality for viral AGE pathogens is seen in other large US surveillance systems, few studies have had the ability to analyze the healthcare burden and seasonality of sporadic norovirus AGE across all ages. The goal of this analysis is to better understand the seasonal burden of all-cause and norovirus-associated AGE on the healthcare system and its relationship to climatic factors using electronic medical record data from the Kaiser Permanente Northwest (KPNW) healthcare system. Since KPNW data was collected from a distinct geographic area, we had the opportunity to dive more deeply into the data to understand what factors could be impacting the seasonality of viral AGE. We analyzed the seasonality of medically attended AGE in across all age groups and medical settings and modeled the relationship between norovirus-associated AGE and both temperature and absolute humidity.
Methods
Study site
Data were collected from the Kaiser Permanente Northwest (KPNW) healthcare system, which serves approximately 600,000 people centered in the Portland, Oregon metropolitan area, including areas of southern Washington state and northern and central Oregon [13]. Portland is in the Willamette Valley with a temperate seasonality and average monthly temperatures ranging between 40–70°F (4–21°C) throughout the year; extreme temperatures range from the single digits in December and January to over 100°F (38°C) in June, July, and August [14].
Dataset criteria
The dataset included all healthcare encounters for acute gastroenteritis (AGE) from January 1, 2016 to December 31, 2019. Data were accessed from the electronic health record for research purposes on September 7th, 2020. AGE encounters were identified via ICD-9/10 code (S1 Table) or a clinician ordered stool laboratory test (e.g., stool culture, Clostridium difficile test, parasitic test, or PCR panel) (S2 Table). A medically attended AGE episode was defined as all AGE encounters occurring within 30 days of each other. Episodes were classified based on the highest level of care received across included encounters; level of care was ranked as inpatient, emergency department, urgent care, outpatient, or remote (email or telephone) from highest to lowest, respectively. A single patient could have multiple AGE episodes during the study period. Data on clinical stool testing, as well as demographics, such as age, sex, and race, were collected from electronic health records. Age (in years) was defined at episode start date.
To reduce the likelihood of including chronic AGE patients, episodes >30 days were excluded. Additionally, patients classified as having a chronic AGE ICD-9/10 code and no ICD-9/10 code for vomiting at their encounter were excluded (S3 Table). Dialysis encounters were also excluded, regardless of ICD-9/10 codes or laboratory orders linked to those encounters.
Data classification
A clinical test was linked to an AGE episode if ordered or completed within 7 days of the start or end of an episode. On January 20, 2016, KPNW introduced PCR panel viral stool testing via the xTAG® Gastrointestinal Pathogen Panel (Luminex Molecular Diagnostics, Austin, TX, USA) and on September 23, 2019, switched to enteric bacterial, parasitic, and viral BD MAXTM PCR panels (BD Diagnostics, Baltimore, MD, USA). An AGE episode was classified as norovirus or rotavirus positive if a linked PCR panel test was positive for either pathogen.
AGE episodes were categorized into 52 epidemiological weeks (EW) per year by episode start date. All EW were defined to begin on a Sunday and EW 1 was assigned as the first week with at least four days within that calendar year [15]. Norovirus surveillance year was defined as EW 27 to EW 26 of the following calendar year [13]. Rotavirus surveillance year was defined by calendar year. Seasonal onset was defined as the EW where 10% of the cumulative seasonal cases for norovirus or rotavirus had occurred, and offset was defined as the EW where 90% of the cumulative seasonal cases had occurred [7]. Season length was defined as the number of EW between onset and offset. Weekly percent positivity was calculated as the number of norovirus or rotavirus associated episodes divided by the number of episodes with testing as an 8-week centered rolling average.
Climate data
Daily weather data during the study period were obtained from the Portland International Airport weather station. Temperature data were accessed via the Global Historical Climatology Network [16]. Relative humidity data were accessed from the Integrated Surface Dataset [17]. Both datasets were compiled by the National Centers for Environmental Information, National Oceanic and Atmospheric Administration. Since relative humidity is a measure of the amount of water vapor in the air compared to the maximum amount possible and changes with air temperature, we converted relative humidity to absolute humidity to assess temperature and humidity separately. Absolute humidity (g/m3) was calculated using the following equation with maximum daily temperature (T) and maximum daily relative humidity (rh): [18]. Weekly climate measures were calculated by averaging daily values over the EW.
Statistics
Two negative binomial models were used to assess the relationship between the weekly number of norovirus positive episodes and climatic factors utilizing data from mid-2016 (EW 27) through the end of 2019. The first model used maximum temperature as a predictor and second used absolute humidity. A time lag between climate measurements and number of positive episodes from 0 to 4 weeks was analyzed. Interaction terms with both age (<18 years, > 18 years) and level of care (outpatient, more severe than outpatient) were also investigated. Model fit was determined by the Akaike information criterion (AIC). Due to the small number of rotavirus positive episodes in our sample (n = 204), the relationship between weekly rotavirus positive episodes and climatic factors could not be analyzed.
Ethics
This project was reviewed and approved by the Kaiser Permanente Northwest Institutional Review Board (FWA00002344). The institutional review board granted this study a waiver of informed consent for this data, as all data was collected from the electronic medical record. Our dataset did not include individuals who have opted their medical records out of Kaiser Permanente Research activities.
Results
From 2016 to 2019, 132,156 persons presented to Kaiser Permanente Northwest for 198,181 medically attended AGE episodes (Table 1). The majority (72%) of individuals with a medically attended AGE episode experienced only one episode during our study period. Annually, the number of AGE episodes ranged from 44,532 episodes in 2016–53,399 episodes in 2019, increasing over the 4-year period.
Almost half (44%) of episodes were classified as outpatient, while 7% were urgent care, 16% were emergency department, and 25% were inpatient (Table 1). Seven percent of episodes were classified as remote. The median age of an AGE patient was 52 years old (range: 0–106 years); 6% were under 5 years old, and a third were 65 years or older (Table 1). There was no difference in the number of AGE episodes that occurred from October to March (51%) versus from April to September (49%).
Of all AGE episodes, 10% (n = 18,998) had stool tested for AGE pathogens via PCR panel. This varied by setting; 18% of urgent care episodes had PCR panel testing, followed by 15% of outpatient episodes, 5% of emergency department episodes, and 3% of inpatient episodes (Table 1). Less than 1% of remote episodes had testing. Of episodes with testing, 12% were positive for at least one pathogen; 892 (5%) were norovirus positive and 204 (1%) were rotavirus positive. Patients under 5 years old had the highest percent positivity for norovirus (14%) and rotavirus (4%). Percent positivity decreased with each age group for norovirus and rotavirus; 5–17 year-olds had 5% and 3% of healthcare episodes positive while, 18–64 year-olds had 4% and 1% of episodes positive, respectively. Those over 65 years old had the lowest percent positivity (3% for norovirus; 1% for rotavirus) throughout the year (Fig 1). Percent positivity for any pathogen ranged from 10.5% in October to 15.3% in December. Other commonly detected pathogens included Campylobacter (3%), Salmonella (1%) and E. coli (1%).
Eight week rolling average of viral AGE percent positivity by epidemiologic week of episode*, Kaiser Permanente Northwest, Portland, OR, USA, 2016–2019; A) Norovirus positivity among all age groups, B) Rotavirus positivity among all age groups, C) Norovirus and rotavirus positivity among patients <5 years old, D) Norovirus and rotavirus positivity among patients 65 + years old. *All AGE encounters occurring within 30 days of each other were consolidated into a single AGE episode. A single patient may be represented by multiple episodes within the dataset.
From mid-2016 (EW 27) to mid-2019 (EW 26), norovirus percent positivity on average peaked in EW 7 (mid-February) at 9% and was lowest in EW 34 (late-August) at 2%. On average, norovirus seasonal onset occurred in EW 34 (late-August) and the offset was by EW 19 (early-May). Across all surveillance years combined, norovirus seasonal peaks were higher for inpatient (9%), emergency department (23%), and urgent care (15%) episodes compared to outpatient episodes (5%) (Fig 2).
Eight week rolling average of viral AGE percent positivity by epidemiologic week of episode* and highest level of care sought†, Kaiser Permanente Northwest, Portland, OR, USA, 2016–2019. A) Norovirus positivity among all levels of care, B) Rotavirus positivity among all levels of care. *All AGE encounters occurring within 30 days of each other were consolidated into a single AGE episode. A single patient may be represented by multiple episodes within the dataset. †Encounters were classified into outpatient, urgent care, emergency department, or inpatient based on encounter type. Episodes were classified by highest level of care, with inpatient as highest level and outpatient and lowest.
Rotavirus percent positivity had different seasonal patterns in odd and even years. In 2017 and 2019, the rotavirus season had an onset in EW 5–6 and offset between EW 25–34 and peaked in EW 14 with a percent positivity of 4%. In 2016 and 2018, rotavirus had a later and less distinct season, with onset in EW 18–19 and offset in EW 49 and peaked in EW 39 at 2% (Fig 3).
Eight week rolling average of viral AGE percent positivity, plotted with temperature and absolute humidity, Kaiser Permanente Northwest, Portland, OR, USA, 2016–2019.
Temperature and absolute humidity peaked in the summer and were the lowest in the winter, displaying an opposite seasonal pattern to norovirus positivity (Fig 3). Using data from mid-2016 (EW 27) through the end of 2019 in a negative binomial model, we found temperature had a significant inverse relationship with the weekly count of norovirus positive AGE episodes (Table 2). A three-week time lag between temperature and norovirus positive episodes had the best model fit. For every 5-degree Celsius increase in the maximum weekly temperature, three weeks later weekly counts of norovirus positive AGE episodes decreased by 21% (95% CI: 16–25%). Absolute humidity also had a significant inverse relationship with the weekly count of norovirus positive AGE episodes (Table 3). For this model, a two-week time lag had the best model fit. For every 5 g/m3 increase in absolute humidity, two weeks later, weekly counts of norovirus positive AGE episodes decreased by 28% (95% CI: 22–33%) (Table 3). We found no significant interactions between these relationships by age group (<18 years old vs. > 18 years old) or encounter type (outpatient vs. more severe than outpatient).
Discussion
In this integrated healthcare system in Portland, Oregon, AGE was associated with nearly half a million medically-attended AGE encounters during 2016‒2019. Across all healthcare settings and ages, norovirus-associated AGE represented a significant burden and displayed a winter seasonality, peaking in January and February. Norovirus-associated AGE seasonal peaks were the highest in younger age groups, urgent cares, and emergency departments, demonstrating the increased burden norovirus-AGE has among these age groups and in these healthcare settings. Rotavirus-associated AGE showed a biennial seasonality and spring peak. Using two negative binomial models, both temperature and absolute humidity were inversely correlated with the weekly number of norovirus-positive healthcare episodes.
These results align with previous reports of the significant burden [5,19] and seasonal nature of norovirus and rotavirus in the US [7,20]. Consistent with patterns shown since US rotavirus vaccine introduction, rotavirus associated AGE displayed a biennial pattern, with more during odd years, and less during even years [9]. While individual rotavirus vaccine data was not available for this population, other studies have shown >75% coverage among age-eligible children within Kaiser Permanente Northwest [21]. Since rotavirus vaccine introduction, vaccine coverage and birth rate have been found to have an impact on US rotavirus seasonality, independent of climatic factors [22]. In alignment with other surveillance systems and publications on sporadic norovirus illness and outbreaks, norovirus had a winter seasonality in this system. [7 20]. We saw the highest norovirus percent positivity among those <5 years old, and norovirus percent positivity decreased with age. This finding aligns with the higher burden of norovirus among children <5 years shown in other large-scale datasets [19]. With norovirus vaccine candidates under development [23], norovirus seasonal patterns may also change after vaccine introduction, depending on the vaccine’s target population and uptake.
Data from other countries have found a relationship between temperature and norovirus [12,24,25]. Predictive models from South Korea and China found that cold temperature was the most important climatic predictor of norovirus outbreaks [26,27]. A Hong Kong based study found low temperature and humidity extremes were the best predictors of pediatric AGE hospital admissions [28] Experimental studies have found that norovirus persisted in water and on surfaces longer at lower temperatures, showing that virus survivability and transmissibility may be longer during in the winter season [29,30]. In agreement, our study found that as temperature decreased, norovirus-associated AGE increased; our model had the best fit with a three-week time lag, meaning that, temperature best predicted norovirus-associated AGE episodes three weeks later.
In this study, we analyzed the relationship between norovirus-associated AGE and absolute, as opposed to relative, humidity. Absolute humidity measures the amount of water vapor (moisture) in the air, regardless of temperature, whereas relative humidity is the percentage of the amount of water vapor present compared to amount needed for saturation at the air’s temperature. For this reason, to separate potential impacts on norovirus from temperature and humidity, we focused on absolute and not relative humidity. Indoor and outdoor absolute humidity are also highly correlated; therefore, fluctuations in outdoor absolute humidity may impact norovirus transmission in indoor settings where outbreaks commonly occur [31]. Laboratory studies have found that absolute humidity has a large impact on norovirus survivability and infectiousness and low absolute humidity improves the survival of human norovirus surrogates [32]. A Swedish study found that a drop in absolute humidity coincided with an increase in norovirus outbreaks [33]. This is consistent with our study findings, where the highest number of norovirus-associated healthcare episodes occurred when absolute humidity was the lowest. Other studies have found relationships between AGE and rainfall, hydrology, and land development use [10,11]. However, we did not analyze these factors in this study.
This study was unique in being able to analyze the impact of climatic factors on norovirus-associated AGE episodes, something few US based studies have been able to do. However, this study is subject to multiple limitations. The use of electronic healthcare record data allowed us to utilize four years of data and hundreds of thousands of medical encounters and clinical tests along with corresponding climatic data for the same years. However, data were selected based on ICD-9/10 codes and clinical testing and most patients did not have stool tests performed, limiting the data available and potentially introducing bias. Additionally, we know from other Kaiser Permanente studies that AGE patients seeking healthcare are more likely to have more severe disease and a longer duration of symptoms than those who not seeking healthcare [34]. Additionally, as an ecological study, we do not have data to analyze exposures or biases at the individual level. Our negative binomial models assume a linear relationship, which may not reflect the complexity of the interaction between climatic factors and disease. While we found a significant relationship for norovirus-associated episodes, sample sizes restricted our ability to run models for rotavirus-associated episodes or control for any confounders. We examined different interactions between age and encounter type, which were not significant. These models also do not give us the ability to assess causality, only correlation. With absolute humidity and temperature highly correlated with each other, it is unclear which factor may be influencing norovirus transmission. As well, it is not possible to tell how these factors are directly impacting viral survivability and transmissibility or are influencing may behavior and subsequently transmission.
Behavior, regardless of climatic factors, can have strong impact on AGE transmission. This was seen during the COVID-19 pandemic; AGE incidence and outbreaks decreased substantially when non-pharmaceutical interventions were put into place in 2020 and 2021, such as social distancing and enhanced cleaning measures [35–37]. However, we did not have data on seasonal behavior changes that may impact norovirus disease dynamics. The US school year typically begins in August or September and multiple holidays, including Thanksgiving (in late November), Christmas (in late December) and New Years (on January 1st), align with the winter season and provide opportunities for large gatherings to drive disease transmission. In Belgium, an influenza transmission study found that person-to-person contacts increased significantly on workdays compared to weekends and holidays, while temperature, rainfall, and humidity had a minor influence on the number of contacts [38]. Other studies have found that norovirus season in children often precedes that among older age groups, potentially indicating transmission in settings such as schools and childcares drives norovirus seasonality [39]. However, in this study, children had higher and sharper seasonal peaks but did not peak earlier than older age groups.
Climate change is expected to influence infectious diseases patterns globally [40]. Better understanding the impact of climate on AGE seasonality is key to preparing prevention efforts and predicting future shifts in AGE burden and seasonality as the climate warms. This study provides data on the burden and seasonality of AGE in a healthcare system to improve understanding of medically-attended AGE and inform timing of prevention efforts, including promotion of proper disinfection techniques, hand hygiene, and isolation of ill individuals, as well as future vaccination campaigns. Understanding how AGE burden varies throughout the year can help healthcare systems plan resources and prepare for times of peak transmission. Moving forward, more studies looking at the relationship between climatic factors, particularly temperature and absolute humidity and norovirus are warranted.
Supporting information
S1 Table. International Classification of Disease – Clinical Modification version 9 (ICD-9) and version 10 (ICD-10) codes used to identify healthcare encounters associated with acute gastroenteritis, Kaiser Permanente Northwest, Portland, Oregon, USA, 2016–2019.
https://doi.org/10.1371/journal.pone.0318077.s001
(DOCX)
S2 Table. Clinical stool tests used to identify healthcare encounters associated with acute gastroenteritis, Kaiser Permanente Northwest, Portland, Oregon, USA, 2016–2019.
https://doi.org/10.1371/journal.pone.0318077.s002
(DOCX)
S3 Table. International Classification of Disease – Clinical Modification version 9 (ICD-9) and version 10 (ICD-10) codes used to identify patients with chronic acute gastroenteritis, Kaiser Permanente Northwest, Portland, Oregon, USA, 2016–2019.
https://doi.org/10.1371/journal.pone.0318077.s003
(DOCX)
Acknowledgments
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. Takeda had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The Centers for Disease Control and Prevention received no funding from Takeda.
References
- 1. GBD 2016 Diarrhoeal Disease Collaborators. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis. 2018;18:1211–28.
- 2. Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, et al. Rotavirus Vaccination and the Global Burden of Rotavirus Diarrhea Among Children Younger Than 5 Years. JAMA Pediatr. 2018;172:958–65.
- 3. Liao Y, Hong X, Wu A, Jiang Y, Liang Y, Gao J, et al. Global prevalence of norovirus in cases of acute gastroenteritis from 1997 to 2021: An updated systematic review and meta-analysis. Microb Pathog. 2021;161(Pt A):105259. pmid:34687838
- 4. Patel MM, Pitzer VE, Alonso WJ, Vera D, Lopman B, Tate J, et al. Global Seasonality of Rotavirus Disease. The Pediatric Infectious Disease Journal. 2013;32(4).
- 5. Payne DC, Vinjé J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, et al. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med. 2013;368:1121–30.
- 6. Adler JL, Zickl R. Winter vomiting disease. J Infect Dis. 1969;119(6):668–73. pmid:5795109
- 7. Kambhampati AK, Calderwood L, Wikswo ME, Barclay L, Mattison CP, Balachandran N, et al. Spatiotemporal Trends in Norovirus Outbreaks in the United States, 2009-2019. Clin Infect Dis. 2023;76:667–73.
- 8. NREVSS, CDC. National Center for Immunization and Respiratory Diseases (NCIRD) CaORVD. Norovirus National Trends. [cited 2024 February 13, 2024]. https://www.cdc.gov/surveillance/nrevss/norovirus/natl-trend.html
- 9. Hallowell BD, Parashar UD, Curns A, DeGroote NP, Tate JE. Trends in the Laboratory Detection of Rotavirus Before and After Implementation of Routine Rotavirus Vaccination - United States, 2000-2018. MMWR Morb Mortal Wkly Rep. 2019;68(24):539–43. pmid:31220058
- 10. Shamkhali Chenar S, Deng Z. Environmental indicators for human norovirus outbreaks. Int J Environ Health Res. 2017;27(1):40–51. pmid:27876423
- 11. Kim JH, Lee DH, Joo Y, Zoh KD, Ko G, Kang J-H. Identification of environmental determinants for spatio-temporal patterns of norovirus outbreaks in Korea using a geographic information system and binary response models. Sci Total Environ. 2016;569–570:291–9. pmid:27343948
- 12. Lopman B, Armstrong B, Atchison C, Gray JJ. Host, weather and virological factors drive norovirus epidemiology: time-series analysis of laboratory surveillance data in England and Wales. PLoS One. 2009;4(8):e6671. pmid:19701458
- 13. Burke RM, Mattison CP, Marsh Z, Shioda K, Donald J, Salas SB, et al. Norovirus and Other Viral Causes of Medically Attended Acute Gastroenteritis Across the Age Spectrum: Results from the Medically Attended Acute Gastroenteritis Study in the United States. Clin Infect Dis. 2021;73(4):e913–20. pmid:34398953
- 14. Administration TNOA. NOWData - NOAA Online Weather Data. [cited 2023 December 29, 2023]. https://www.weather.gov/wrh/climate?wfo=pqr
- 15. NNDSS. Event Codes & Other Surveillance Resources. [cited 2024 February 13, 2024]. https://ndc.services.cdc.gov/event-codes-other-surveillance-resources/
- 16.
Menne MJ, Durre I, Korzeniewski B, McNeill S, Thomas K, Yin X, et al. Global Historical Climatology Network - Daily (GHCN-Daily). Version 3.31 ed. NOAA National Climatic Data Center; 2012.
- 17. NOAA National Centers for Environmental Information. Global Hourly – Integrated Surface Database (ISD). 2001. https://www.ncei.noaa.gov/products/land-based-station/integrated-surface-database
- 18. Wagner W, Pruß A. The IAPWS Formulation 1995 for the Thermodynamic Properties of Ordinary Water Substance for General and Scientific Use. Journal of Physical and Chemical Reference Data. 2002;31(2):387–535.
- 19. Burke RM, Mattison CP, Pindyck T, Dahl RM, Rudd J, Bi D, et al. Burden of Norovirus in the United States, as Estimated Based on Administrative Data: Updates for Medically Attended Illness and Mortality, 2001-2015. Clin Infect Dis. 2021;73:e1–e8.
- 20. Kambhampati AK, Wikswo ME, Barclay L, Vinjé J, Mirza SA, NoroSTAT Network. Notes from the Field: Norovirus Outbreaks Reported Through NoroSTAT - 12 States, August 2012-July 2022. MMWR Morb Mortal Wkly Rep. 2022;71(38):1222–4. pmid:36136940
- 21. Burke RM, Groom HC, Naleway AL, Katz EM, Salas B, Mattison CP, et al. Rotavirus Vaccine Is Effective Against Rotavirus Gastroenteritis Resulting in Outpatient Care: Results From the Medically Attended Acute Gastroenteritis (MAAGE) Study. Clin Infect Dis. 2021;72(11):2000–5. pmid:32322882
- 22. Burnett E, Parashar UD, Winn A, Curns AT, Tate JE. Major Changes in Spatiotemporal Trends of US Rotavirus Laboratory Detections After Rotavirus Vaccine Introduction-2009-2021. Pediatr Infect Dis J. 2022;41:759–63.
- 23. Armah G, Lopman BA, Vinjé J, O’Ryan M, Lanata CF, Groome M, et al. Vaccine value profile for norovirus. Vaccine. 2023;41 Suppl 2(Suppl 2):S134–52. pmid:37951692
- 24. Gao Y, Chen Y, Shi P, Zhang Q, Qian C, Xiao Y, et al. The Effect of Ambient Temperature on Infectious Diarrhea and Diarrhea-like Illness in Wuxi, China. Disaster Med Public Health Prep. 2022;16(2):583–9. pmid:33213594
- 25. Wang P, Goggins WB, Chan EYY. A time-series study of the association of rainfall, relative humidity and ambient temperature with hospitalizations for rotavirus and norovirus infection among children in Hong Kong. Sci Total Environ. 2018;643:414–22. pmid:29940452
- 26. Lee S, Cho E, Jang G, Kim S, Cho G. Early detection of norovirus outbreak using machine learning methods in South Korea. PLoS One. 2022;17(11):e0277671. pmid:36383630
- 27. Wang J, Ran L, Zhai M, Jiang C, Xu C. Prediction of Foodborne Norovirus Outbreaks in Coastal Areas in China in 2008-2018. Foodborne Pathog Dis. 2024;21(3):203–9. pmid:38150264
- 28. Chong KC, Chan EYY, Lee TC, Kwok KL, Lau SYF, Wang P, et al. A 21-year retrospective analysis of environmental impacts on paediatric acute gastroenteritis in an affluent setting. Sci Total Environ. 2021;764:142845. pmid:33183801
- 29. Liu P, Jaykus L-A, Wong E, Moe C. Persistence of Norwalk virus, male-specific coliphage, and Escherichia coli on stainless steel coupons and in phosphate-buffered saline. J Food Prot. 2012;75(12):2151–7. pmid:23212011
- 30. Tiwari A, Kauppinen A, Räsänen P, Salonen J, Wessels L, Juntunen J, et al. Effects of temperature and light exposure on the decay characteristics of fecal indicators, norovirus, and Legionella in mesocosms simulating subarctic river water. Sci Total Environ. 2023;859(Pt 2):160340. pmid:36423850
- 31. Nguyen JL, Schwartz J, Dockery DW. The relationship between indoor and outdoor temperature, apparent temperature, relative humidity, and absolute humidity. Indoor Air. 2014;24(1):103–12. pmid:23710826
- 32. Colas dela NA, Estienney M, Aho S, Perrier-Cornet JM, de Rougemont A, Pothier P, et al. Absolute Humidity Influences the Seasonal Persistence and Infectivity of Human Norovirus. Appl Environ Microbiol. 2014;80:7196–205.
- 33. Beck-Friis T, Sundell N, Gustavsson L, Lindh M, Westin J, Andersson L-M. Outdoor Absolute Humidity Predicts the Start of Norovirus GII Epidemics. Microbiol Spectr. 2023;11(2):e0243322. pmid:36786608
- 34. Hallowell BD, Burke RM, Salas SB, Groom H, Donald JL, Mattison CP, et al. Correlates of healthcare-seeking behavior for acute gastroenteritis-United States, October 1, 2016 -September 30, 2017. PLoS One. 2023;18:e0293739.
- 35. Kraay ANM, Han P, Kambhampati AK, Wikswo ME, Mirza SA, Lopman BA. Impact of Nonpharmaceutical Interventions for Severe Acute Respiratory Syndrome Coronavirus 2 on Norovirus Outbreaks: An Analysis of Outbreaks Reported By 9 US States. J Infect Dis. 2021;224(1):9–13. pmid:33606027
- 36. Lappe BL, Wikswo ME, Kambhampati AK, Mirza SA, Tate JE, Kraay ANM, et al. Predicting norovirus and rotavirus resurgence in the United States following the COVID-19 pandemic: a mathematical modelling study. BMC Infect Dis. 2023;23(1):254. pmid:37081456
- 37. Love NK, Douglas A, Gharbia S, Hughes H, Morbey R, Oliver I, et al. Understanding the impact of the COVID-19 pandemic response on GI infection surveillance trends in England, January 2020-April 2022. Epidemiol Infect. 2023;151:e147. pmid:37622322
- 38. Willem L, Van Kerckhove K, Chao DL, Hens N, Beutels P. A nice day for an infection? Weather conditions and social contact patterns relevant to influenza transmission. PLoS One. 2012;7(11):e48695. pmid:23155399
- 39. Donaldson AL, Harris JP, Vivancos R, O’Brien SJ. Can cases and outbreaks of norovirus in children provide an early warning of seasonal norovirus infection: an analysis of nine seasons of surveillance data in England UK. BMC Public Health. 2022;22(1):1393. pmid:35858892
- 40. Phillips MC, LaRocque RC, 3rd Thompson GR. Infectious Diseases in a Changing Climate. JAMA. 2024;331(15):1318–9. pmid:38506835