Literature DB >> 33882112

Investigation and public health response to a COVID-19 outbreak in a rural resort community-Blaine County, Idaho, 2020.

Eileen M Dunne1,2, Tanis Maxwell3, Christina Dawson-Skuza3, Matthew Burns1, Christopher Ball1, Kathryn Turner1, Christine G Hahn1, Melody Bowyer3, Kris K Carter1,4, Logan Hudson3.   

Abstract

Blaine County, Idaho, a rural area with a renowned resort, experienced a COVID-19 outbreak early in the pandemic. We undertook an epidemiologic investigation to describe the outbreak and guide public health action. Confirmed cases of COVID-19 were identified from reports of SARS-CoV-2-positive laboratory test results to South Central Public Health District. Information on symptoms, hospitalization, recent travel, healthcare worker status, and close contacts was obtained by medical record review and patient interviews. Viral sequence analysis was conducted on a subset of available specimens. During March 13-April 10, 2020, a total of 451 COVID-19 cases among Blaine County residents (1,959 cases per 100,000 population) were reported, with earliest illness onset March 1. The median patient age was 51 years (interquartile range [IQR]: 37-63), 52 (11.5%) were hospitalized, and 5 (1.1%) died. The median duration between specimen collection and a positive laboratory result was 9 days (IQR: 4-10). Forty-four (9.8%) patients reported recent travel and an additional 37 cases occurred in out-of-state residents. Healthcare workers comprised 56 (12.4%) cases; 33 of whom worked at the only hospital in the county, leading to a 15-day disruption of hospital services. Among 562 close contacts monitored by public health authorities, laboratory-confirmed COVID-19 or compatible symptoms were identified in 51 (9.1%). Sequencing results from 34 specimens supported epidemiologic findings indicating travel as a source of SARS-CoV-2, and identified multiple lineages among hospital workers. Community mitigation strategies included school and resort closure, stay-at-home orders, and restrictions on incoming travelers. COVID-19 outbreaks in rural communities can disrupt health services. Lack of local laboratory capacity led to long turnaround times for COVID-19 test results. Rural communities frequented by tourists face unique challenges during the COVID-19 pandemic. Implementing restrictions on incoming travelers and other mitigation strategies helped reduce COVID-19 transmission early in the pandemic.

Entities:  

Mesh:

Year:  2021        PMID: 33882112      PMCID: PMC8059800          DOI: 10.1371/journal.pone.0250322

Source DB:  PubMed          Journal:  PLoS One        ISSN: 1932-6203            Impact factor:   3.240


Introduction

Rural residents might be particularly vulnerable to the novel coronavirus disease (COVID-19) pandemic. Approximately 15% of Americans live in rural areas, and rural populations in the United States tend to be older, have higher rates of underlying conditions, and less access to health services [1, 2]. The health gap between rural and urban US was highlighted by a 2017 report identifying higher age-adjusted death rates for the five leading causes of death in nonmetropolitan areas [3]. Rural health departments face unique challenges related to serving the needs of populations that experience poorer health outcomes in large geographical areas with limited resources [2]. Survey data indicate that the COVID-19 pandemic has broad, negative impacts on the well-being of rural populations in the American West [4]. The state of Idaho, located in the northwest region of the United States, has an estimated population of approximately 1.79 million, of which 32.4% reside in rural areas [5]. Idaho is divided into 44 counties, 32 (73%) of which are classified as rural [6], and seven autonomous public health districts comprising 4 to 8 counties each. On March 13, 2020, a case of confirmed COVID-19 in a Blaine County resident was reported to South Central Public Health District (SCPHD); this was the second case identified in Idaho. Blaine County is a scenic, mountainous rural area with an estimated 23,021 residents, of whom 23.5% are Hispanic or Latino [7]. It is a popular weekend and vacation destination, with abundant outdoors and cultural activities, including the Sun Valley Resort, an internationally renowned ski area. An estimated 32% of housing units are occupied seasonally as second homes or short-term rentals [8]. The county is economically diverse, with a 2018 median household income of $51,968 and a poverty rate of 14% [9]. In this report, we present the epidemiology of the COVID-19 outbreak in Blaine County including patient characteristics, hospitalization rates, travel history, and healthcare worker status. Sequence analysis of available SARS-CoV-2 specimens supported epidemiological findings. We examine positive COVID-19 test turnaround times and describe the interruption of hospital services, and the public health response.

Methods

Case identification and investigation

A confirmed COVID-19 case was defined as detection of SARS-CoV-2 RNA in a clinical specimen (nasopharyngeal swab, nasal swab, or oropharyngeal swab) by using real-time reverse transcriptase polymerase chain reaction (RT-PCR). Confirmed COVID-19 cases were identified via reporting of SARS-CoV-2-positive laboratory tests to SCPHD. Case information, including electronic laboratory reports, was collected and stored using Idaho’s National Electronic Disease Surveillance System (NEDSS) Base System (NBS), a Centers for Disease Control and Prevention (CDC)-supported integrated disease surveillance system. Initial investigation determined the usual residence of the patient to confirm reporting jurisdiction, as cases in out-of-state residents are not included in official case counts per standard reporting procedures [10]. Data on symptom onset, hospitalization, recent travel, healthcare worker status, and close contacts were obtained by medical record review and interviews with patients or their proxies. Healthcare workers were defined as paid employees or volunteers who worked at a hospital or other healthcare facility, pharmacists, emergency medical service responders, and firefighters with emergency medical technician certification. Initially, close contacts were defined as household members and others who spent ten minutes or more within a six feet of a patient from 1 day prior to symptom onset in the patient with COVID-19; this time frame was expanded to 2 days prior to symptom onset following further evidence of presymptomatic transmission [11]. Close contacts were monitored through 14 days after exposure.

Viral sequence analysis

Following diagnostic testing at the Idaho Bureau of Laboratories, aliquots of viral transport media were preserved at -80°C until a subset was selected for sequencing. Selected samples were preserved in Zymo DNA/RNA Shield, a proprietary reagent which stabilizes nucleic acid samples at ambient temperatures, and sent to the University of New Mexico Center for Global Health for whole genome sequence analysis. Sequencing was conducted using the ARCTIC protocol, version 3 and assembly was performed by the Center for Global Health [12]. All finished sequences were uploaded with required metadata to the GISAID EpiCoV™ (S1 Table). All complete, high coverage, SARS-CoV-2 sequences from samples collected during March 1–March 12, 2020 in the USA were downloaded from the GISAID database (S2 Table) [13]. This period represents the 10 days prior to the first laboratory confirmed COVID-19 case in Idaho. Idaho sequences from Blaine County were BLASTed against this subset of sequences using the MEGABLAST tool within Bionumerics. The top two hits by sequence identity were selected for further analysis. The BLAST hits, Blaine County sequences, and sequences from other Idaho counties (collected March 1–April 1, 2020) were compared using Bionumerics Multiple Sequence Alignment Tool and clustered using a Minimum Spanning Tree.

Community mitigation measures

Information on school and business closures and governmental orders was obtained from press releases. Data on the estimated proportion of county residents staying at home were made publicly available by SafeGraph, Inc [14].

Data analysis

Data were analyzed using Stata version 14.2 and graphs created in Excel. Data were reported as percentages for categorical variables and median, interquartile range (IQR), and range for continuous variables. Multivariable logistic regression was used to evaluate variables associated with hospitalization, with robust standard error to account for possible lack of independence, and results reported as adjusted odds ratios (aOR) with 95% confidence intervals (95% CI). Methods for census block group analysis are described in S3 Table.

Research determination

COVID-19 is a reportable disease under Idaho Department of Health and Welfare Rules, IDAPA 16.02.10. Case investigation, data collection, and analysis were conducted for public health purposes. Data were fully anonymized prior to analysis. This project was reviewed by the Center for Surveillance, Epidemiology, and Laboratory Services Human Subjects Contact at the CDC. The project was determined to meet the requirements of public health surveillance covered by the U.S. Department of Health and Human Services Policy for the Protection of Human Research Subjects as defined in 45 CFR 46.102 (https://www.hhs.gov/ohrp/regulations-and-policy/regulations/45-cfr-46/index.html), and the decision was made that this project was nonresearch and did not require ethical review by the CDC Human Research Protection Office. Ethical approval was waived and informed consent was not required.

Results

Four weeks after the first case was identified, a total of 452 confirmed cases were reported among Blaine County residents. One case was excluded because the patient was temporarily residing in another state during the outbreak. An additional 37 cases were identified among out-of-state residents who were tested in Blaine County; these included 26 residents of areas where COVID-19 outbreaks were known to have been occurring (15 patients from King County, Washington and 11 patients from counties in California where community spread had occurred). Blaine County experienced one of the highest rates of COVID-19 cases per capita (1,959/100,000) in the US at the time of this investigation. Of the 451 patients, 239 (53.0%) were female. The median age at onset was 51 years (IQR: 38–63 years), with 5 (1.1%) patients aged <18 years, 169 (37.4%) aged 18–44 years, 172 (38.1%) aged 45–64 years, and 106 (23.5%) aged ≥65 years. Race and ethnicity data indicated that 332 (73.5%) patients were white (non-Hispanic or Latino), 9 (2.0%) other race, and 73 (16.2%) Hispanic or Latino, with data missing for 37 (8.2%) patients. Among 447 patients with symptom data available, 446 (99.8%) reported at least one symptom. Most commonly reported symptoms included cough (n = 299, 66.9%), fever (measured or subjective; n = 275, 61.5%), myalgia or body aches (n = 208, 46.5%), fatigue (n = 205, 45.9%), headache (n = 164, 36.7%), and shortness of breath (n = 137, 30.6%). Other reported symptoms included chills (n = 111, 24.8%), loss of taste or smell (n = 101, 22.6%), sore throat (n = 83, 18.6%), diarrhea (n = 83, 18.6%), congestion (n = 81, 18.1%), pain or tightness in chest (n = 55, 12.4%), nausea or vomiting (n = 54, 12.1%), loss of appetite (n = 39, 8.7%), and runny nose (n = 36, 8.1%). The median total number of symptoms reported per patient was 4 (IQR: 3–6, range = 0–11); 187 (41.8%) of patients reported having five or more symptoms. A total of 52 (11.5%) patients were hospitalized. The number and proportion of patients who were hospitalized increased with age, ranging from no (0%) patients aged <18 years, 5 (3.0%) patients aged 18–44 years, 14 (8.1%) aged 45–64 years, and 33 (31.4%) persons aged ≥65 years. Although information on underlying medical conditions was not available, multivariable regression analysis to examine factors associated with hospitalization found that age group 45–64 years (aOR 4.0, 95%CI 1.0–15.5), age group ≥65 years (aOR 23.0,95%CI 5.6–94.4), Hispanic or Latino ethnicity (aOR 3.6, 95%CI 1.2–10.5), and having five or more symptoms (aOR 3.1,1.5–6.4) were associated with increased odds of hospitalization (S4 Table). The median length of admission was 5 days (IQR: 2–11 days, range = 1–38 days). Of 50 hospitalized patients with available data, 21 (42%) were admitted to the intensive care unit. Overall, five (1.1%) patients died; all were aged >60 years and 4 (80%) were male. The median duration between symptom onset and specimen collection was 5 days (IQR: 2–8; range = 0–24). The median duration from specimen collection to reporting of a positive SARS-CoV-2 laboratory result was 9 days (IQR: 4–10 days; range = 1–22 days): 2 days (IQR: 1–3; range = 1–5) for high-priority specimens (e.g., from healthcare workers and hospitalized patients) tested by the Idaho Bureau of Laboratories (n = 41), and 9 days (IQR: 5–10; range = 1–22) for specimens tested at commercial laboratories (n = 410). In total, the median time between illness onset and reporting of a SARS-CoV-2 positive test was 13 days (IQR: 10–16; range = 2–34). Idaho Bureau of Laboratories began SARS-CoV-2 testing on March 2, and regional commercial laboratories began SARS-CoV-2 testing on March 5. Testing availability increased in Blaine County following the March 17 opening of a COVID-19 screening and testing center adjacent to the sole hospital in the county (Hospital A) and operated by their health system. At least 11 cases occurred in Blaine County residents who attended three events (a ski festival and two private events) held during February 27 to March 7 that attracted many out-of-state and international travelers. Data on recent travel history and healthcare worker status were available for 450/451 (99.8%) cases. Of these, 44 (9.8%) patients reported travel from another state or country during the 2 weeks prior to symptom onset. In total, 56 (12.4%) cases were among healthcare workers, 33 of whom worked at Hospital A, a critical access hospital (a designation given to eligible rural hospitals by the Centers for Medicare and Medicaid Services). Affected hospital staff held clinical and non-clinical roles throughout the hospital. Fig 1 illustrates the epidemiologic curve for COVID-19 illness onset among 447 patients with available data, including healthcare workers, and shows dates of the ski festival and two private events and community mitigation measures. The epidemic curve indicated a peak in illness onset in mid-March, consistent with exposures occurring during the two weeks prior. Hospital A suspended normal operations on March 20, one day after community spread in Blaine County was announced. Hospital A’s emergency department and COVID-19 screening and testing center remained open; however, non-emergent appointments and procedures were postponed, inpatient services discontinued, and affiliated community clinics closed. Patients requiring admission were transported by emergency medical services to the nearest regional hospital located 78 miles away. Hospital A resumed limited services on April 3. S1 Fig depicts hospitalizations over time by date of admission.
Fig 1

Epidemic curve showing cases of COVID-19 in Blaine County, Idaho residents by date of illness onset (n = 447).

Cases in health care workers (HCW) are shown in orange and non-HCW in blue. Onset dates from cases reported from March 13–April 10, 2020 are included on the graph. Dates of events linked to 11 cases are indicated with gray boxes, and implementation dates for community mitigation measures are shown with arrows.

Epidemic curve showing cases of COVID-19 in Blaine County, Idaho residents by date of illness onset (n = 447).

Cases in health care workers (HCW) are shown in orange and non-HCW in blue. Onset dates from cases reported from March 13–April 10, 2020 are included on the graph. Dates of events linked to 11 cases are indicated with gray boxes, and implementation dates for community mitigation measures are shown with arrows. Analysis of SARS-CoV-2 sequences was conducted on a convenience sample of available specimens from Idaho patients diagnosed with COVID-19, including 23 from Blaine County residents and 11 from other counties in Idaho. Several genomes from Blaine County residents were closely related to sequences identified in other states including New York, Louisiana, Mississippi, and Rhode Island (Fig 2). Three genomes from patients who were residents of other Idaho counties but spent time in Blaine County prior to illness onset were closely related to genomes from Blaine County residents (Fig 2). Analysis of viral sequences from Hospital A staff members identified two SARS-CoV-2 lineages (B.1 and A.1), suggesting that the outbreak among Hospital A staff was not due to a single source.
Fig 2

Minimum spanning tree showing SARS-CoV-2 sequences from Blaine County residents who worked at Hospital A (n = 14, dark blue), Blaine County residents who did not work at Hospital A (n = 9, light blue), residents of other Idaho counties with no travel to Blaine County (n = 7, light green), residents of other Idaho counties who traveled in Blaine County prior to illness (n = 3, dark green), related sequences from other US states identified by BLAST (n = 19, white), and the reference sequence from Wuhan, China (black).

GSAID accession numbers are listed in S1 Table.

Minimum spanning tree showing SARS-CoV-2 sequences from Blaine County residents who worked at Hospital A (n = 14, dark blue), Blaine County residents who did not work at Hospital A (n = 9, light blue), residents of other Idaho counties with no travel to Blaine County (n = 7, light green), residents of other Idaho counties who traveled in Blaine County prior to illness (n = 3, dark green), related sequences from other US states identified by BLAST (n = 19, white), and the reference sequence from Wuhan, China (black).

GSAID accession numbers are listed in S1 Table. Census block group estimates were used to examine geographic distribution and community characteristics for 402 (89.1%) COVID-19 patients whose addresses were matched to a census block group, which can serve as a proxy for neighborhood. At least one case occurred in each of the 13 census block groups in Blaine County (S3 Table). Community characteristics varied substantially by census block group. Over half (n = 216, 53.7%) of cases occurred among residents of four census block groups. Within these four census block groups, the proportion of the population that are Hispanic or Latino ethnicity ranged from 4.6% to 47.1% and the proportion of persons in renter-occupied housing ranged from 11.1% to 49.2%. Public health authorities, the county government, and local stakeholders undertook several measures to contain the outbreak and limit community transmission. SCPHD conducted contact tracing and monitored 562 close contacts of Blaine County cases; 22 (3.9%) of these close contacts tested positive for SARS-CoV-2 and an additional 29 (5.2%) became symptomatic but were not tested. During March 9–April 10, SCDPH staff worked 4,074 hours on COVID-19 emergency response. This response supported all eight counties in the jurisdiction, however 452/495 (91.3%) cases occurred in Blaine County. Volunteers spent 158 hours conducting contact monitoring activities. Blaine County School District closed school buildings on March 14. Sun Valley Resort closed for the season on March 16. The Idaho Department of Health and Welfare (IDHW) issued an order of isolation for Blaine County residents on March 20. Central District Health, whose jurisdiction borders SCPHD and includes the state capital of Boise (less than three hours driving time from Sun Valley Resort) issued a statement on March 22 instructing anyone with recent travel to Blaine County to shelter in place following identification of four COVID-19 cases among residents who had recently been in Blaine County. On March 25, IDHW issued a statewide order to self-isolate. On March 27, Blaine County issued an order with additional restrictions including the prohibition of non-essential travel into or out of Blaine County and 14-day self-quarantine for residents or visitors coming from out of state. S2 Fig shows the timing of these measures along with cumulative case counts. Publicly accessible data from SafeGraph, Inc. reported county-level percentage of people staying home all day (based on GPS data from anonymous mobile devices) indicating that the proportion of people staying at home increased steadily from March 15 through early April (Fig 3).
Fig 3

Daily estimates of the percent of people in Blaine County, Idaho staying at home all day during March 1–April 10, 2020.

Data were obtained from SafeGraph, Inc. and are based upon global positioning system data from mobile devices. Dates of isolation orders and travel restrictions are indicated on the graph.

Daily estimates of the percent of people in Blaine County, Idaho staying at home all day during March 1–April 10, 2020.

Data were obtained from SafeGraph, Inc. and are based upon global positioning system data from mobile devices. Dates of isolation orders and travel restrictions are indicated on the graph.

Discussion

The start of the outbreak in Blaine County was likely linked to travel to the ski resort, high rates of seasonal residence, and three events held during late February and early March 2020 that attracted numerous out-of-state attendees. COVID-19 outbreaks have been identified in mountain resort communities elsewhere in the US and in Europe [15, 16]. Several published reports demonstrate how travel and events contributed to COVID-19 outbreaks. In the district of Tirschenreuth, Germany, travel to ski resorts and attendance at traditional beer festivities were implicated as early drivers of transmission for a COVID-19 outbreak that began in mid-March 2020, which was controlled following implementation of a 14-day quarantine for returning travelers and cancellation of large events [17]. In Maine, a 55-person wedding in a rural town with several out-of-state attendees was linked to 177 COVID-19 cases as well as outbreaks at a long-term care facility and a correctional facility [18]. Several COVID-19 cases identified in Blaine County occurred in residents of King County, Washington and counties in California where community spread had occurred prior to detection of the first COVID-19 case in Idaho. Cases in out-of-state residents, although not included in official case counts, are indicative of frequent travel from the west coast and likely contributed to the level of transmission observed. Blaine County was the first county in Idaho to announce community spread of COVID-19 despite being the 17th most populous county. Second home ownership, common in resort communities such as Blaine County, has been linked to the spread of COVID-19 from urban to rural areas in several countries including the United States [19, 20]. Improving strategies to detect and monitor SARS-CoV-2 infections among temporary residents might help resort communities better understand their role in transmission and prepare for potential healthcare and public health impacts. Interstate spread has been implicated in SARS-CoV-2 importations in other regions of the United States. Sequence analysis of SARS-CoV-2 found that 7 of 9 viral genomes from early COVID-19 cases in Connecticut clustered with a clade dominated by viruses from cases in Washington state [21]. Sequence analysis of SARS-CoV-2 from Blaine County supported the epidemiological findings, as several genomes clustered with viruses from other states, suggestive of links to travel. Because certain states were likely overrepresented in the database of available sequences from early in the pandemic, and Idaho sequences indicate multiple introductions of SARS-CoV-2, the geographic source of the outbreak could not be identified. Limitations on the use of viral sequencing for this epidemiologic investigation include that only a subset of specimens tested and stored at the state public health laboratory were available for sequence analysis, as commercial laboratories typically do not store specimens. Rural counties have fewer healthcare workers and facilities compared with urban areas, making rural areas vulnerable to staff shortages and facility closures that could reduce access to health care. The high number of affected workers from Hospital A led to temporary cessation of inpatient services at the only hospital in Blaine County. Sequencing analysis of SARS-CoV-2 from Hospital A staff indicated multiple exposures rather than a point-source outbreak caused by a single viral strain, and it was not possible to determine whether staff were infected in the community or in the workplace. Work exclusion of Hospital A staff who were identified as close contacts of COVID-19 cases also contributed to the staffing shortage. As Hospital A is part of a larger and well-resourced health system, it was able to remain partially open and received support from partner hospitals. Hospital planning for community spread of COVID-19, vaccination of healthcare workers, and developing strategies for mitigating staffing shortages are critical for maintaining healthcare access in rural areas. In Thailand, a rural hospital closed following confirmed cases of COVID-19 in three medical personnel and quarantine of the remaining 21 medical personnel of the hospital [22]. A survey of COVID-19 preparedness among hospitals in Idaho identified inconsistent implementation of CDC guidelines for infection prevention, and only 8 of 21 (38%) critical access hospitals had a written respiratory protection program [23]. Limited isolation facilities pose a challenge, as only 2 (10%) critical access hospitals had an airborne infection isolation room. The CDC has developed relevant resources including hospital preparedness checklist for COVID-19 (https://www.cdc.gov/coronavirus/2019-ncov/hcp/hcp-hospital-checklist.html). Telehealth is another strategy that can be leveraged to help rural hospitals during the COVID-19 pandemic by expanding healthcare capacity, reducing potential exposures of healthcare workers, and linking with tertiary hospitals to provide additional staffing support and reduce unnecessary patient transfers [24]. Case identification and contact tracing efforts were hindered by long lag times between symptom onset and receipt of laboratory results. Many contacts were not notified of their potential exposure until the second week of the 14-day isolation period. Delays in testing turnaround times might be more prominent in predominantly rural states like Idaho, where commercial testing during the investigation time frame was only available at regional laboratories located in other states. Public health laboratory support enabled faster turnaround times for high-priority specimens. Expansion of diagnostic testing availability, including at hospital and commercial diagnostic laboratories and point-of-care rapid tests, has subsequently led to shorter turnaround times in Idaho. A commentary advocated for expanded testing in rural areas, as the authors’ analysis found that states with higher prevalence of COVID-19 risk factors (hypertension, diabetes, and lung cancer), which tend to be more common in rural populations, had lower overall testing rates, and medically vulnerable people in rural areas have greater potential for severe outcomes [25]. Contact tracing, a key component of the public health response to COVID-19, depends on the ability to detect COVID-19 cases in a timely manner. Part-time residents are typically not included in population estimates, limiting the accuracy of disease incidence estimates in areas where tourism and seasonal residence are common, such as Blaine County, where the ski season attracts tourists and seasonal workers. Cases of COVID-19 among visitors to Blaine County who were tested outside of Idaho were not captured in our analysis, therefore we were not able to assess how exposures at the ski resort and elsewhere in Blaine County might have contributed to the spread of COVID-19 in other states. Additional limitations include that testing during the time of this investigation was primarily conducted on symptomatic persons, and testing of children was relatively uncommon. The rapid rise in reported cases seen in late March and early April might reflect expanded testing availability as well as disease transmission. Data on underlying conditions were not available, and relationships between patients (other than cases in contacts under monitoring) were not systematically captured, although several household clusters were identified. Geocoding patient addresses and census block group data indicated that the outbreak was not limited to a specific geographical region of the county, and it affected communities of varying socio-economic characteristics. Of patients with available race and ethnicity information, 17.6% were Hispanic or Latino, compared with 23.5% of the overall Blaine County population. This slight underrepresentation might be because of several factors including disparities in access to health care and testing [26]. However, Hispanic or Latino ethnicity was associated with increased odds of hospitalization, consistent with reports highlighting the disproportionate impact of COVID-19 on the Hispanic or Latino population in the United States [27, 28]. Evidence from four US metropolitan areas indicated that community mobility declined following implementation of stay-at-home orders [29]. Consistent with these findings, the estimated percentage of people staying at home in Blaine County, obtained via anonymous cellular phone data, increased following orders of isolation. In our experience, after the implementation of community mitigation measures, most contacts identified were household members. The Blaine County outbreak attracted intense local and national media coverage that could have encouraged residents’ adherence to stay-at-home orders [30, 31]. It is challenging to directly assess the impact of community mitigation measures on disease transmission, because of the time lag between exposure, symptom onset, and case detection, and the multitude of unmeasured factors that might influence COVID-19 transmission and case detection. In Blaine County, mitigation strategies including closure of the ski resort and a county-wide isolation order began within a week of the first reported case. The increase in cumulative cases in Blaine County began to slow approximately two weeks following implementation of the county order of isolation. Social distancing and stay-at-home orders were valuable tools for reducing transmission early in the pandemic before COVID-19 treatments or vaccines were available.

Conclusions

Rural communities frequented by travelers and seasonal residents, like Blaine County, can be heavily impacted by COVID-19, leading to disruption in available health services. Rural hospitals should develop pandemic preparedness plans that include strategies for mitigating staffing shortages. Expanding COVID-19 testing availability and speed will help rural health departments and healthcare systems detect and respond to COVID-19 outbreaks. Closing tourist attractions and implementing restrictions on incoming travelers in addition to stay-at-home orders and other policies targeting local residents were effective strategies for limiting community spread in rural areas prior to widespread availability of COVID-19 vaccines.

SARS-CoV-2 sequences from Idaho and others included in Fig 2.

(PDF) Click here for additional data file.

SARS-CoV-2 sequences from GSAID used in analyses.

(PDF) Click here for additional data file.

Distribution of confirmed COVID-19 cases (n = 402) and census block group characteristics for Blaine County, Idaho.

(PDF) Click here for additional data file.

Univariable and multivariable analysis of patient characteristics associated with hospitalization.

(PDF) Click here for additional data file.

Hospitalization of Blaine County, Idaho residents for COVID-19 by date of admission (n = 52).

(PDF) Click here for additional data file.

Timeline of the COVID-9 outbreak in Blaine County showing cumulative COVID-19 case counts and implementation dates for community mitigation measures.

(PDF) Click here for additional data file. 1 Mar 2021 PONE-D-21-03832 Investigation and public health response to a COVID-19 outbreak in a rural resort community — Blaine County, Idaho, 2020 PLOS ONE Dear Dr. Dunne, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Apr 15 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Shinya Tsuzuki, MD, MSc Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. Please confirm that your IRB board waived the need for ethical approval. Moreover, in ethics statement in the manuscript and in the online submission form, please provide additional information about the patient records used in your retrospective study. Specifically, please ensure that you have discussed whether all data were fully anonymized before you accessed them and/or whether the IRB or ethics committee waived the requirement for informed consent. 3.We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. Please see http://www.bmj.com/content/340/bmj.c181.long for guidelines on how to de-identify and prepare clinical data for publication. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. Additional Editor Comments: Both reviewers gave insightful suggestions then please revise your manuscript accordingly. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ********** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No Reviewer #2: Yes ********** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: No Reviewer #2: Yes ********** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ********** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Summary This report summarizes an outbreak investigation of COVID-19 in a rural county in Idaho with a popular resort community early in the course of pandemic-related events in the US. This report highlights some of the challenges faced early in the pandemic response, when testing was limited and public health action delayed due to the lack of widespread availability of rapid tests. This report is well written, and represents a thorough investigation, including case interview/medical record review, contact tracing, sequencing, etc. This report does not add much insight into COVID-19 epidemiology; however, it does provide insight into the issues challenging the response early in the pandemic and in rural areas. Major Issues This report is very well written and covers many important aspects of a COVID-19 outbreak investigation despite the limitations of being early in the pandemic when less was known about risk factors, asymptomatic spread, etc. I have very few suggestions to improve it, other than the few provided below. The report uses only descriptive statistics to describe the outbreak. However, there is a place for analytic epidemiology in this report. The authors should consider conducting multivariable logistic regression to examine risk factors for hospitalization and report ORs with 95% CIs instead of just frequency of age ranges for those hospitalized. Minor Issues Suggest reporting frequency/percent of individuals reporting one and multiple symptoms (e.g., 1, 2-4, 5+) or something similar. Were there any set of symptoms that most commonly occurred together? Reviewer #2: The authors have reported on an investigation of COVID-19 in a rural resort community. The report is comprehensive of many aspects of the outbreak and response. However, it lacks the focus that would make it a useful scientific paper. For example, it is noted that the outbreak occurred after a ski event at the local ski resort. However, there is no real assessment of how that event contributed to spread across the county. The rural nature of the county is emphasized, as is the resort nature of the community. These raise separate, important issues with regard to transmission risk and control, and neither is fully addressed. The abstract describes the occurrence of 452 cases during March 13-April 10. However, the epicurve (figure 1) identifies more than 60-70 cases with onset of symptoms before March 13. The epi-curve and the descriptions of the outbreak are difficult to reconcile. I think that it would be useful to focus on the impact of the ski resort in the initiation of the outbreak. It would also be useful to highlight the interactions of the control measures on the epi-curve (fig. 1). If the epi-curve could be labeled with all of the key time line events, (ski festival, school closure, resort closure, county isolation order, state isolation order, travel restriction) it would provide a clear visual guide to the progression of the outbreak. This would be a better way to relate control measures to case incidence than is achieved in figure 3. The use of cumulative frequency data make it difficult to track the rate of new case onsets. It would be an even bigger bonus if the cases identified by sequence cluster could also be indicated on the epi-curve. I recognize that may not be feasible. It seems that approximately 1/3 of the population of the county at any given time may be made up by visitors from out of state. It would be useful to try to estimate the rate of illness in this ephemeral group, or at least try to better estimate the impact of visitors on transmission dynamics. It is critical for similar resort communities to try to plan for potential disease introductions from tourists, and to have plans for surveillance and control of spread related to these temporary residents. It may be true that such cases are not typically counted as cases in the temporary community, but that does not diminish the importance of being able to track and account for them. There are descriptions of definitions of close contacts on p.4, and changes in the definition. There does not seem to be any use of this data in the paper. If it is not being used for analytical purposes, is it needed in the methods? Similarly, there is substantial description of census blocks in the methods. The results do not present more than a cursory analysis of the census block data, that could be omitted. How do the census blocks relate to housing for guests of the resort? The introductions and discussions are very broad. Given the vast literature that is being published on the pandemic, a narrower focus on the impact of the ski resort on the community would enhance the interest and usefulness of this paper. ********** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. 17 Mar 2021 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf Authors’ response: We have formatted our manuscript in accordance with PLOS ONE’s style requirements. 2. Please confirm that your IRB board waived the need for ethical approval. Moreover, in ethics statement in the manuscript and in the online submission form, please provide additional information about the patient records used in your retrospective study. Specifically, please ensure that you have discussed whether all data were fully anonymized before you accessed them and/or whether the IRB or ethics committee waived the requirement for informed consent. Authors’ response: We have provided additional information on research determination including the waiver of ethical approval and informed consent in the online submission form and in the ethics section of the manuscript. Please see the revised text below: COVID-19 is a reportable disease under Idaho Department of Health and Welfare Rules, IDAPA 16.02.10. Case investigation, data collection, and analysis were conducted for public health purposes. Data were fully anonymized prior to analysis. This project was reviewed by the Center for Surveillance, Epidemiology, and Laboratory Services Human Subjects Contact at the CDC. The project was determined to meet the requirements of public health surveillance covered by the U.S. Department of Health and Human Services Policy for the Protection of Human Research Subjects as defined in 45 CFR 46.102 (https://www.hhs.gov/ohrp/regulations-and-policy/regulations/45-cfr-46/index.html), and the decision was made that this project was nonresearch and did not require ethical review by the CDC Human Research Protection Office. Ethical approval was waived and informed consent was not required. 3.We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. Please see http://www.bmj.com/content/340/bmj.c181.long for guidelines on how to de-identify and prepare clinical data for publication. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. Authors’ response: Information on ethical and legal restrictions to sharing de-identified data has been provided in the revised cover letter as instructed. Additional Editor Comments: Both reviewers gave insightful suggestions then please revise your manuscript accordingly. Authors’ response: The manuscript has been revised in response to reviewer suggestions, with point-by-point responses to reviewer comments provided below. We thank the reviewers for their prompt and thorough review and appreciate their comments and feedback. Reviewers' comments: Reviewer #1: Summary This report summarizes an outbreak investigation of COVID-19 in a rural county in Idaho with a popular resort community early in the course of pandemic-related events in the US. This report highlights some of the challenges faced early in the pandemic response, when testing was limited and public health action delayed due to the lack of widespread availability of rapid tests. This report is well written, and represents a thorough investigation, including case interview/medical record review, contact tracing, sequencing, etc. This report does not add much insight into COVID-19 epidemiology; however, it does provide insight into the issues challenging the response early in the pandemic and in rural areas. Major Issues This report is very well written and covers many important aspects of a COVID-19 outbreak investigation despite the limitations of being early in the pandemic when less was known about risk factors, asymptomatic spread, etc. I have very few suggestions to improve it, other than the few provided below. The report uses only descriptive statistics to describe the outbreak. However, there is a place for analytic epidemiology in this report. The authors should consider conducting multivariable logistic regression to examine risk factors for hospitalization and report ORs with 95% CIs instead of just frequency of age ranges for those hospitalized. Authors’ response: Unfortunately, we did not collect data on underlying medical conditions, many of which have been associated with increased risk of severe illness from COVID-19 including hospitalization. Therefore, we were not able to conduct a thorough assessment of risk factors for hospitalization. However, we did conduct a multivariable analysis as suggested including age group, sex, race/ethnicity, healthcare worker status, and number of symptoms, with results summarized in the text (lines 156-160) and shown in S4 Table. Minor Issues Suggest reporting frequency/percent of individuals reporting one and multiple symptoms (e.g., 1, 2-4, 5+) or something similar. Were there any set of symptoms that most commonly occurred together? Authors’ response: We have added data on the number of symptoms reported to lines 151-152. Aside from the fact that commonly reported symptoms were often reported together, we did not observe any particular patterns regarding symptoms. Reviewer #2: The authors have reported on an investigation of COVID-19 in a rural resort community. The report is comprehensive of many aspects of the outbreak and response. However, it lacks the focus that would make it a useful scientific paper. For example, it is noted that the outbreak occurred after a ski event at the local ski resort. However, there is no real assessment of how that event contributed to spread across the county. The rural nature of the county is emphasized, as is the resort nature of the community. These raise separate, important issues with regard to transmission risk and control, and neither is fully addressed. Authors’ response: We have made several revisions based on reviewer #2’s feedback, including refining the focus and adding additional context and discussion regarding events and the impact of COVID-19 on rural communities. As our investigation was limited to cases reported South Central Public Health District in Idaho, we were not able to assess how exposures at the ski event might have contributed to national spread of COVID-19. However, we have noted this limitation in the discussion (lines 322-325). We have added some examples from the literature on how events (including travel to ski resorts and beer festivals in Germany and a wedding in rural Maine) and second homes contributed to COVID-19 spread in rural areas (lines 252-270). The abstract describes the occurrence of 452 cases during March 13-April 10. However, the epicurve (figure 1) identifies more than 60-70 cases with onset of symptoms before March 13. The epi-curve and the descriptions of the outbreak are difficult to reconcile. Authors’ response: March 13 to April 10th refer to the time frame during which COVID-19 cases were reported to South Central Public Health District, whereas the epi curve displays cases by date of symptom onset. In our study population, the median lag time between the date of symptom onset and the report date for a positive SARS-CoV-2 test was 13 days. This result has been added to lines 169-171. We have edited the abstract to indicate that March 13-April 10 refers to report dates, whereas illness onset began March 1. I think that it would be useful to focus on the impact of the ski resort in the initiation of the outbreak. It would also be useful to highlight the interactions of the control measures on the epi-curve (fig. 1). If the epi-curve could be labeled with all of the key time line events, (ski festival, school closure, resort closure, county isolation order, state isolation order, travel restriction) it would provide a clear visual guide to the progression of the outbreak. This would be a better way to relate control measures to case incidence than is achieved in figure 3. The use of cumulative frequency data make it difficult to track the rate of new case onsets. It would be an even bigger bonus if the cases identified by sequence cluster could also be indicated on the epi-curve. I recognize that may not be feasible. Authors’ response: As suggested, we have added the key time line events to the epi-curve (Figure 1). However, we did not include sequence information on this Figure as it would make the figure overly complicated and difficult to interpret. We have moved the figure showing cumulative case counts (previously Figure 3) to the supplementary information. It seems that approximately 1/3 of the population of the county at any given time may be made up by visitors from out of state. It would be useful to try to estimate the rate of illness in this ephemeral group, or at least try to better estimate the impact of visitors on transmission dynamics. It is critical for similar resort communities to try to plan for potential disease introductions from tourists, and to have plans for surveillance and control of spread related to these temporary residents. It may be true that such cases are not typically counted as cases in the temporary community, but that does not diminish the importance of being able to track and account for them. Authors’ response: We agree that understanding the role of visitors in disease transmission is important in resort communities. Surveillance of visitors and temporary residents would be difficult to implement using existing reportable disease systems, which are based on primary residence, and we were not able to conduct these type of estimates retrospectively for Blaine County. We have added some additional text to the discussion highlighting issues relating to temporary residents and recommend improving strategies to detect and monitor SARS-CoV-2 infections among temporary residents (lines 267-270). There are descriptions of definitions of close contacts on p.4, and changes in the definition. There does not seem to be any use of this data in the paper. If it is not being used for analytical purposes, is it needed in the methods? Authors’ response: Although we did not use contact tracing data for analytical purposes, we do report results on the number of close contacts monitored, what proportion of close contacts developed COVID-19 or COVID-19-compatible symptoms, and hours spent by volunteers conducting contact monitoring. For these reasons, we think defining close contacts in the methods section will be helpful to readers. Similarly, there is substantial description of census blocks in the methods. The results do not present more than a cursory analysis of the census block data, that could be omitted. How do the census blocks relate to housing for guests of the resort? Authors’ response: We have moved the description of census block analysis to the supplementary information. The aim of conducting the census block analysis was to determine if cases among Blaine County residents were limited to a particular geographic region or certain socio-economic groups within the county; results indicated that this was not the case. We did not relate census blocks to guests of the resort or other temporary residents; this might be difficult to conduct as visitor accommodation includes multiple hotels as well as Air BnB and other informal rental properties located throughout the county. The introductions and discussions are very broad. Given the vast literature that is being published on the pandemic, a narrower focus on the impact of the ski resort on the community would enhance the interest and usefulness of this paper. Authors’ response: We have modified the introduction and discussion and removed some of the more broad content and references. We agree that the impact of the ski resort is an important component of this paper. We also want to highlight two other key findings relevant to rural settings, namely that the high number of affected health care workers led to the temporary, partial closure of the only hospital in the county, and the long turnaround times for COVID-19 test results. Together, these findings demonstrate challenges faced by rural areas during the early stages of the COVID-19 pandemic. Submitted filename: Response to reviewers.docx Click here for additional data file. 6 Apr 2021 Investigation and public health response to a COVID-19 outbreak in a rural resort community — Blaine County, Idaho, 2020 PONE-D-21-03832R1 Dear Dr. Dunne, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Shinya Tsuzuki, MD, MSc Academic Editor PLOS ONE Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed ********** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ********** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ********** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ********** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ********** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Thank you for addressing my comments and the other reviewer's comments. This paper is much stronger now. Reviewer #2: The authors have addressed reviewer's comments. The figure with the control measures imposed on the epi-curve is very nice. ********** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: No 12 Apr 2021 PONE-D-21-03832R1 Investigation and public health response to a COVID-19 outbreak in a rural resort community — Blaine County, Idaho, 2020 Dear Dr. Dunne: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Shinya Tsuzuki Academic Editor PLOS ONE
  17 in total

1.  Impacts of the COVID-19 pandemic on rural America.

Authors:  J Tom Mueller; Kathryn McConnell; Paul Berne Burow; Katie Pofahl; Alexis A Merdjanoff; Justin Farrell
Journal:  Proc Natl Acad Sci U S A       Date:  2021-01-05       Impact factor: 11.205

2.  The State of Rural Public Health: Enduring Needs in a New Decade.

Authors:  Jonathon P Leider; Michael Meit; J Mac McCullough; Beth Resnick; Debra Dekker; Y Natalia Alfonso; David Bishai
Journal:  Am J Public Health       Date:  2020-07-16       Impact factor: 9.308

3.  Data, disease and diplomacy: GISAID's innovative contribution to global health.

Authors:  Stefan Elbe; Gemma Buckland-Merrett
Journal:  Glob Chall       Date:  2017-01-10

4.  Presymptomatic Transmission of SARS-CoV-2 - Singapore, January 23-March 16, 2020.

Authors:  Wycliffe E Wei; Zongbin Li; Calvin J Chiew; Sarah E Yong; Matthias P Toh; Vernon J Lee
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2020-04-10       Impact factor: 17.586

5.  Coast-to-Coast Spread of SARS-CoV-2 during the Early Epidemic in the United States.

Authors:  Joseph R Fauver; Mary E Petrone; Emma B Hodcroft; Kayoko Shioda; Hanna Y Ehrlich; Alexander G Watts; Chantal B F Vogels; Anderson F Brito; Tara Alpert; Anthony Muyombwe; Jafar Razeq; Randy Downing; Nagarjuna R Cheemarla; Anne L Wyllie; Chaney C Kalinich; Isabel M Ott; Joshua Quick; Nicholas J Loman; Karla M Neugebauer; Alexander L Greninger; Keith R Jerome; Pavitra Roychoudhury; Hong Xie; Lasata Shrestha; Meei-Li Huang; Virginia E Pitzer; Akiko Iwasaki; Saad B Omer; Kamran Khan; Isaac I Bogoch; Richard A Martinello; Ellen F Foxman; Marie L Landry; Richard A Neher; Albert I Ko; Nathan D Grubaugh
Journal:  Cell       Date:  2020-05-07       Impact factor: 41.582

6.  Multiple COVID-19 Outbreaks Linked to a Wedding Reception in Rural Maine - August 7-September 14, 2020.

Authors:  Parag Mahale; Craig Rothfuss; Sarah Bly; Megan Kelley; Siiri Bennett; Sara L Huston; Sara Robinson
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2020-11-13       Impact factor: 17.586

7.  Unequal Distribution of COVID-19 Risk Among Rural Residents by Race and Ethnicity.

Authors:  Carrie Henning-Smith; Mariana Tuttle; Katy B Kozhimannil
Journal:  J Rural Health       Date:  2020-06-25       Impact factor: 5.667

8.  A Pandemic in Times of Global Tourism: Superspreading and Exportation of COVID-19 Cases from a Ski Area in Austria.

Authors:  Carlos L Correa-Martínez; Stefanie Kampmeier; Philipp Kümpers; Vera Schwierzeck; Marc Hennies; Wali Hafezi; Joachim Kühn; Hermann Pavenstädt; Stephan Ludwig; Alexander Mellmann
Journal:  J Clin Microbiol       Date:  2020-05-26       Impact factor: 5.948

9.  Mass gathering events and undetected transmission of SARS-CoV-2 in vulnerable populations leading to an outbreak with high case fatality ratio in the district of Tirschenreuth, Germany.

Authors:  M Brandl; R Selb; S Seidl-Pillmeier; D Marosevic; U Buchholz; S Rehmet
Journal:  Epidemiol Infect       Date:  2020-10-13       Impact factor: 2.451

10.  Timing of Community Mitigation and Changes in Reported COVID-19 and Community Mobility - Four U.S. Metropolitan Areas, February 26-April 1, 2020.

Authors:  Arielle Lasry; Daniel Kidder; Marisa Hast; Jason Poovey; Gregory Sunshine; Kathryn Winglee; Nicole Zviedrite; Faruque Ahmed; Kathleen A Ethier
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2020-04-17       Impact factor: 17.586

View more
  2 in total

1.  Evaluation of the Abbott BinaxNOW COVID-19 Test Ag Card for rapid detection of SARS-CoV-2 infection by a local public health district with a rural population.

Authors:  Rachel E Pollreis; Clay Roscoe; Rachel J Phinney; Surabhi S Malesha; Matthew C Burns; Aimee Ceniseros; Charles H Washington; Andrew J Nutting; Christopher L Ball
Journal:  PLoS One       Date:  2021-12-02       Impact factor: 3.240

2.  Missing science: A scoping study of COVID-19 epidemiological data in the United States.

Authors:  Rajiv Bhatia; Isabella Sledge; Stefan Baral
Journal:  PLoS One       Date:  2022-10-12       Impact factor: 3.752

  2 in total

北京卡尤迪生物科技股份有限公司 © 2022-2023.