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Applied Biosafety: Journal of the American Biological Safety Association logoLink to Applied Biosafety: Journal of the American Biological Safety Association
. 2022 Sep 14;27(3):153–168. doi: 10.1089/apb.2022.0023

Undergraduate Teaching During COVID-19

Claudia Gentry-Weeks 1,*, Dell Rae Ciaravola 2, Marc Barker 3, Kelly Long 4, Lori Lynn 5, Heather Pidcoke 6, Kenneth Quintana 7, Benjamin Withers 8
PMCID: PMC9908288  PMID: 36779199

Abstract

Introduction:

Universities were challenged during the COVID-19 pandemic to continue providing quality education for their students while navigating the uncertainties of the SARS-CoV-2 virus.

Objectives:

The goal of this article is to describe strategies used by Colorado State University (CSU) to mitigate SARS-CoV-2 transmission among faculty, staff, and students and to describe procedures used in microbiology teaching laboratories.

Methods:

Information concerning CSU's pandemic response was gathered via email communications to the CSU community, town hall meetings, and interviews with leaders, researchers, and staff who spearheaded public health initiatives.

Results:

To date, there have been no known cases of transmission of SARS-CoV-2 in the classroom. Early strategies that contributed to this success included social norming of safe public health behaviors, development of low-cost, rapid screening and surveillance methods, an online COVID-19 reporting system, contact tracing and quarantine, rearranging classrooms to reduce the capacity by 50%, increasing air flow, enhanced cleaning and production of sanitizer, and flexible instructors who quickly changed their courses for remote delivery or launched extra risk management procedures for face-to-face delivery of laboratory, performance, or studio classes.

Conclusion:

Intense collaboration among the CSU community, open and frequent communication, coordination of efforts, flexible instructors, and the willingness to follow safe public health behaviors allowed CSU to continue face-to-face teaching in courses that required hands-on learning or demanded in-person instruction. It is the hope of the authors that this information can provide both a historical account and useful information for others dealing with the COVID-19 pandemic.

Keywords: quarantine, laboratories, pooled saliva, sanitizer, social norming, microbiology laboratories, wastewater, pooled saliva, BSL-2

Introduction

In early 2020, Colorado State University (CSU) President Joyce McConnell convened the Pandemic Preparedness Team (PPT) and the Teaching Continuity and Recovery Team (TCRT) in response to news that SARS-CoV-2 was quickly spreading internationally and causing significant morbidity and mortality. An intensive collective response from CSU leaders, public health officials, and CSU employees followed as they worked 7 days a week debating the best options for class delivery, consulting with infectious disease researchers, and implementing changes to reduce SARS-CoV-2 transmission.

This article describes university strategies used to ensure safe teaching continuity and those employed by the Department of Microbiology, Immunology, and Pathology to continue teaching in-person microbiology laboratories at CSU throughout the pandemic. For a comprehensive account, see the Report of the TCRT 2020–2022.1

Methods and Results

COVID-19 Initial Response, Timeline, and Requirements

On March 2, 2020, President McConnell announced that a Task Force (later designated the CSU PPT) of CSU leaders and CSU Health Network had been formed and was partnering with the local, county and state officials to prepare for a potential coronavirus outbreak2 (see Table 1 for timeline). The PPT met three times daily, and with the CSU President once daily, to develop plans for responding to the looming pandemic. On March 5, the first official cases of SARS-CoV-2 were announced in the state of Colorado.3 On March 10, Colorado Governor Jared Polis declared a state of emergency.4 CSU's spring break was approaching and there were no known cases of COVID-19 on the CSU campus at that time.

Table 1.

Timeline of key events, public health requirements, and responses at the CSU—Fort Collins campus

Date Message via email, CSU source article, or town hall meetings
January 2020 PPT and TCRT formed.
March 5, 2020 First cases of COVID-19 reported in Colorado.
March 10, 2020 Colorado Governor declares state of emergency.
March 19, 2020 First COVID-19-infected person associated with CSU confirmed by Larimer County Health Department.
March 23, 2020 Remote work for CSU personnel, only those with essential in-person functions can work on CSU campus.
March 25, 2020 Governor institutes stay-at-home order statewide; 1000 cases; 19 deaths in CO.
March 25, 2020 Students continue with online courses from the spring break to end of semester.
April 2020 Wastewater surveillance for SARS-CoV-2 begins.
April 27, 2020 Colorado moves to safer-at-home; offices can reopen at 50% capacity; vulnerable populations stay home; medical, dental, and veterinary services resume.
April 29, 2020 CSU Recovery Plan Roadmap; four phases shared, announcement of formation of Recovery Decision Committee and Recovery Advisory Committee.
May 13, 2020 Plans for opening in-person classes in fall 2020 classes and modifications to class schedules/space/delivery are announced.
May 29, 2020 Classes to move online after fall break until end of semester.
June 5, 2020 Tuition freeze for 2020–2021.
July 2020 Daily online symptom checker announced.
July 31, 2020 Social norming begins with message to returning students.
August 11, 2020 CSU recognized as #4 of 10 research universities for COVID response: on vaccines, treatment, testing, contagion mapping, contact tracing, data analysis, and education. More than 125 investigators engaged in more than 170 COVID-related research projects.
August 18, 2020 Cameron Peak Fire interferes with air quality; CSU mountain campus evacuated. Building filtration changes occur weekly.
August 20, 2020 Messaging to incoming students: https://www.youtube.com/watch?v=1Gv2BaSaQdI “COVID-19: Public Health Requirements for Fall 2020 at Colorado State University” with link to informational website; https://covid.colostate.edu/public-health-precautions-during-the-semester; masks required on campus; reservations required for move-in to residence halls with limitations on persons per hall per hour. Quarantine spaces set aside. Virtual activities for students.
September 21, 2020 University update guidelines for potential classroom COVID exposure and notification process.
September 24, 2020 Quarantine of two residence halls based on wastewater surveillance results.
September 29, 2020 Quarantine of residence halls lifted.
November 3, 2020 Saliva screening encouraged but not required.
November 4, 2020 COVID-19 reporter replaces the daily symptom checker.
November 24, 2020 Larimer County shifts to level red restrictions.
December 17, 2020 Phased spring 2021 schedule announced.
January 14, 2021 Mandated COVID saliva screening for students, faculty, and staff with exceptions for religious or health reasons.
February 16, 2021 CSU announces plans to reopen campus in fall 2021.
March 21, 2021 200 Doses of Moderna COVID-19 vaccine on campus.
March 30, 2021 COVID reporter and saliva screening required through end of semester; masks and 6-foot distancing remain; vaccines encouraged but not required.
April 2, 2021 All adults in Colorado eligible for COVID vaccine.
May 4, 2021 Remote work requirement lifted for faculty and staff. Telework applications accepted; applications not required for campus activities.
May 13, 2021 CDC relaxes mask restrictions for those fully vaccinated, CSU requirements for masking continue.
June 28, 2021 Physical distancing requirements lifted. Masks required indoors at CSU. Weekly saliva screening unless vaccinated. Vaccines encouraged.
July 12, 2021 Masks not required on university grounds. Masks still required in Health and Medical Center, Veterinary Teaching Hospital, on public transportation. Saliva screening not required if vaccinated.
July 30, 2021 Governor Polis and the administration announce that unvaccinated state workers must begin serial testing and continue mask-wearing indoors in public spaces.
August 3, 2021 Delta variant identified.
August 11, 2021 >20,000 Students vaccinated. Online portal available for submitting vaccine status. Mandate for masks, vaccines, and screening due to increased spread of Delta variant. CSU Board of Governors has the authority to mandate vaccines while waiting for FDA approval, which is predicted to happen soon. CSU will recognize, and accept with proof, all 16 vaccines approved for use by the World Health Organization. Students and employees must submit their proof of vaccination or declare an exemption with the CSU Health Network through its student portal by Wednesday, August 18. Twice-weekly screening if unvaccinated. Masks are required indoors in all university buildings regardless of vaccine status. Individuals living in the university housing must wear masks unless they are in their own room or apartment. Faculty and staff must wear a mask unless they are alone in their office. Masks are also required when more than one person is in a university vehicle or conducting university travel in a private vehicle.
August 26, 2021 FDA approval of Pfizer vaccine.
October 19, 2021 Almost 90% of students, faculty, and staff vaccinated. Larimer County and Colorado vaccine rates are 66% and 61%, respectively. Ten isolation or quarantine spaces used per week for students in university housing. 2500 reports submitted to COVID reporter. Most required to saliva screen weekly are complying; nasal swab follow-up is 0.51%.
October 20, 2021 Larimer County requires masks for all public indoor spaces.
December 14, 2021 Omicron variant reported in the United States.
December 30, 2021 CSU System Chancellor approves COVID booster requirement for spring 2022 for those on campus.
January 3, 2022 Omicron variant reported in Larimer County. Vaccine and boosters required. Exemptions accepted. One-time mandatory saliva screening for all students, faculty, and staff returning to campus. Twice-weekly mandatory saliva screening for unvaccinated persons. Masks in all buildings unless in residence hall rooms (students) or alone in office (students, faculty, and staff). Use of COVID reporter still in effect. 3-ply surgical masks and N95 respirators recommended.
January 13, 2022 Report vaccine and booster status through online portal.
January 28, 2022 Saliva screening shows 5.18% COVID positivity rate. Boosters required when eligible.
February 12, 2022 Larimer County Public Health Department lifts mask requirement; CSU mask requirement still in effect.
February 10–11, 2022 CSU continues requiring masks in all indoor areas until Larimer County transmission rate falls within moderate community transmission. Moderate is 50–99.9 per 100,000 cases in the past 7 days. Directions given for proper use of N95 respirators.
February 21, 2022 CSU moves to voluntary antigen testing, saliva testing discontinued. Current positive rate is 1% with saliva test. Still must wear a mask and provide documentation for vaccination and booster or exemption.
February 25, 2022 Free N95 masks for CSU students, faculty, and staff.
March 3, 2022 Masks no longer required on CSU campus.
April 1, 2022 8,350 Employees; 89.2% full or partial vaccination; 7.1% employee exemptions.
61.1% Employees with boosters; on-campus student enrollment (taking in-person classes) 24,192, 91.6% students full or partial vaccination, 8.2% exemptions.
May 2, 2022 24,077 on campus.
STUDENTS: portal submissions (99.9%) of 24,105; 22,093 on-campus students fully or partially vaccinated (91.7%) of 24,105; 12,095 on-campus students with boosters (56.2%); 1984 students with exemptions (8.2%).
EMPLOYEES: 7890 portal submissions (95.7%) of 8341; 7390 fully or partially vaccinated (88.6%); 4531 with boosters (62.2%); employees with exemptions 590 (7.1%). Faculty and staff numbers include employees who work across the state and nation and may or may not visit a university campus.
May 13–15, 2022 In-person commencement ceremonies.
May 13, 2022 Voluntary antigen testing closing. Students, faculty, and staff continue to be required to be fully vaccinated (two doses of Moderna or Pfizer, or one dose of J&J) or to declare an exemption for medical or nonmedical reasons. Boosters are not required but are strongly encouraged.

PPT, Pandemic Preparedness Team; TCRT, Teaching Continuity and Recovery Team.

To reduce the possibility that traveling students and employees would unknowingly bring COVID-19 to the campus, on March 11, spring break was extended by 2 days and teaching moved online from March 23 to April 10.5 Five days later, at the advice of public health officials, CSU decided that students would not return, and classes would be online for the remainder of the semester.6 Off-campus courses were suspended or resumed online. Some residence and dining halls and university apartments remained open to accommodate the 600 students who could not move out immediately.

On March 19, 2020, the first case of COVID-19 associated with CSU was confirmed by the Larimer County Public Health Department (Email; Public Safety Team, March 22, 2020).

On March 23, all CSU operations moved online.7 All employees began working remotely except for those with essential in-person functions. Travel was suspended, off-campus events were canceled, commencement ceremonies were postponed to December, and anyone with nonessential functions was told to stay home. Persons performing essential in-person services maintained 6-foot social distancing guidelines, disinfected equipment after use, applied alcohol-based sanitizer (80% ethanol, 1.45% glycerol, and 0.125% hydrogen peroxide) when entering and exiting buildings, and minimized their time at CSU. With 1000 positive COVID-19 tests and 19 deaths in Colorado, the Governor called for a stay-at-home order on March 25, 2020.8

CSU researchers (∼125) pivoted their research to address COVID-19, with projects including diagnostic tests and vaccine development, monitoring wastewater, and measurement of particles expelled while singing.9,10

The quickly evolving pandemic necessitated swift policy changes and prompt university communication as information became available. There was initially great uncertainty and fear surrounding the COVID-19 disease and transmission as international borders and public schools were closed, toilet paper disappeared from shelves, grocery bags were being disinfected, and respirators were in short supply. CSU leaders, the CSU community, and local, county, and state authorities worked together to ensure safe continuity of teaching and operations.

Daily Symptom Checker, COVID-19 Reporter, and Contact Tracing

Early in the pandemic, an online, self-reported daily COVID-19 symptom checker was created.11–14 Before coming to campus, students, staff, and faculty logged into the system to report their status. The CSU Public Health Office followed up with persons with COVID-19 symptoms or exposure. The Larimer County Public Health Office and the CSU Public Health Office worked together to trace contacts of anyone with symptoms or a possible exposure and to issue isolation or quarantine orders for 10–14 days.14 Contact tracing procedures are explained in Figure 1.15 The online daily symptom checker transitioned to the COVID-19 reporter for individuals to report symptoms, exposures, and positive tests and to receive an individualized response on the next steps from the CSU Public Health Office.16 In January 2022, the COVID-19 reporter was modified to provide instructions for those with possible exposure and to allow the CSU Public Health Office the bandwidth to address positive cases.

Figure 1.

Figure 1.

Infographics to explain contact tracing at CSU.

Cleaning and Custodial Activities

Custodians increased cleaning schedules and disinfected daily all frequently touched surfaces in elevators, classrooms, conference rooms, lobbies, restrooms, and lounges.17 They followed public health guidance (physical distancing, masks, frequent handwashing), used EPA-approved disinfectants (Q.T. Plus; Hillyard, Inc., St. Joseph, MO) effective against SARS-CoV-2 virus, and used CDC-approved methods.18 In October 2020, PreventX 24/7 (JennsCo, Springfield, TN), a nonchemical disinfectant, was used as an additional method to enhance disinfection.19 Instructors and students cleaned desks, chairs, tables, keyboards, and benchtops in classrooms and laboratories with REScue disinfectant wipes (Virox Technologies, Inc., Oakville, Canada11). Stairwell sweeping and mopping and vacuuming private offices changed to monthly, and vacuuming in classrooms was reduced to weekly. Persons in private offices emptied their trashcans into a central trash bin.17

Since hand sanitizer was scarce, the CSU President, the Vice President for Research, University Operations, the Translational Medicine Institute, and CSU researchers collaborated to produce 40-L containers of sanitizer (80% ethanol, 1.45% glycerol, and 0.125% hydrogen peroxide; prepared according to the WHO guidelines).20–25 For larger volumes, CSU partnered with two former alumni operating local breweries (The Gilded Goat and Copper Muse Distillery, Fort Collins, CO) for ethanol production, component mixing, bottling, and quality control to produce thousands of gallons of hand sanitizer.22

The Central Receiving Department Director worked with local fabricators to build about 900 disinfectant/sanitizer stations and, with assistance from Emergency Management, strategically placed them across CSU campuses (Figure 2)26 such as at classroom/laboratory entries and exits. Each station contained a QR code to quickly notify Central Receiving to replace supplies. A personal protective equipment (PPE) online central supply store was developed, providing supplies to CSU departments at cost.27

Figure 2.

Figure 2.

One of ∼900 sanitizer stations for dispensing in-house-produced hand sanitizer. The QR code enhances rapid notification for refills.

Air Quality

The Facilities Management team and engineers improved building ventilation and increased filtration and indoor air exchange with outside air rates.28,29 They consulted with CSU's Environmental Health Services, ASHRAE, and the HVAC experts to determine air quality improvement best practices in ∼117 buildings housing classrooms, laboratories, and offices. During 2020, Facilities personnel reviewed and tested all CSU automated controlled HVAC systems. Computer programs for the system were modified to respond quickly to any needed HVAC changes. Outside air percentages were increased by 10–15% above normal levels, with some classrooms gaining a 20% increase. Filters were replaced as often as weekly instead of waiting the normal 6- to 8-month time.

In August, the Cameron Peak fire reduced air quality significantly and filters were replaced weekly. Minimum efficiency reporting values (MERV; designates ability of a filter to capture 0.3-10 micron particles; a larger value shows increased ability) filter ratings were increased from 6 to 8 and the normal 30-min air flush period was replaced by a 2-h air flush before the start of business and after the close of business. Air changes per hour (ACH) were increased from 34 ACH to 8 ACH. Since CSU maintained filter stocks, there was no supply chain issue for replacement filters. Filtration units were installed in older classroom buildings with only windows for ventilation.

Classroom Capacity Planning

The spring and summer of 2020 brought a flurry of activity as the university prepared for a “new normal.” Classroom capacity was reduced to 50% or less with 6-foot spacing between students, based on the CDC guidance for institutions of higher education that was followed by the Colorado Department of Higher Education.30,31 Student spacing had priority over classroom capacity and Facilities Management assessed each classroom floor plan and made site visits to ensure that 6-foot spacing occurred (Figure 3). Eighty-eight percent of courses were scheduled for in-person delivery in fall 2020.32 This meant that classroom space demand was almost double the normal requirement. To complicate matters further, students had already registered for their courses using prepandemic classroom capacity plans.

Figure 3.

Figure 3.

Classroom spacing in fall semester of 2020 in a standard classroom.

This necessitated a herculean effort by the Registrar's Office to maintain each student's schedule and classes in place while finding additional class space before school began. This was no small feat; 34,300 students enrolled for fall 2020.27 This meant that 6000 course sections were arranged to fit into the 50% reduced capacity classroom space, changing 3582 and 3968 sections from face-to-face to hybrid and online, respectively. The Registrar's Office successfully found suitable classroom space and notified students of location changes before fall 2020.

Housing and Dining

Housing and Dining Services, which serve 15 residence halls and 4 apartment complexes, remained open, but significantly changed operations.33,34 In 2020, Housing and Dining Services ramped up cleaning level and frequency and disinfected frequently touched surfaces with CDC-recommended disinfectants. Electrostatic disinfectant applicators were purchased to enhance adherence of disinfectant to surfaces. Community and suite restrooms were cleaned twice daily and once monthly, respectively, and students received cleaning kits. Plexiglass shields protected customer service areas and hand wipes/sanitizer were placed in residence halls and dining areas.

In fall 2020, 5576 students moved into university halls and apartments.34 Only 15 people per hall per hour were allowed to move in at once via a reservation system. Face masks and 6-foot distancing were required indoors and outdoors except when eating or if alone in a room or apartment.35 Guests were only allowed in residence halls or apartment lobbies. Guests in rooms were limited to individuals living on the same residence hall floor. Students with COVID-19 were temporarily moved to designated quarantine/isolation spaces and were supplied medical care (as needed) and meals.36

Students who required quarantine/isolation were contacted and procedures were explained, with the term “quarantine used for exposure/close contact and isolation used for someone who tested positive and/or was symptomatic. Both indicate having no contact with other people.”36 Students packed belongings that they would need for 10–14 days and were transported in a van to a designated area of one residence hall that was secured and had its own ventilation system. Rooms were cleaned by environmental services and were left empty for 48–72 h between each resident. The transport van was modified by Housing and Dining Services with a plastic screen between the driver and the passenger and was disinfected between transfers.

Dining Services staff delivered a bag to the door of each student once a day in quarantine/isolation and waited to make sure that the supplies were received and refrigerated. Each bag contained three meals, snacks, and beverages and students could call a hotline and request a custom delivery. Dining services were receptive to students' needs, even going so far as to deliver Campbell's tomato soup to a student on request.

Four dining halls, two minimarkets, and three express food locations were available for order-ahead, pick-up meals. Three locations were available for picking up quick meals without preordering.34

By fall 2021, restrictions were lifted, and students enjoyed in-person dining. This plan remained in effect through spring 2022, except that food options increased based upon student feedback.37 On-campus student isolation and quarantining continued.

Social Norming Campaign

A vigorous social norming campaign was critical for CSU's successful navigation of the pandemic38–40 (Figure 4) and exemplified the phrase “It takes a village,” with an addition “and hard work.” The Social Norming Task Force, led by the Assistant Vice President for Student Affairs and Dean of Students and the Associate Director of Housing and Dining Services, implemented methods based on research from the College of Liberal Arts, the Department of Journalism and Media Communication, the Department of Human Development and Family Studies, the College of Business, and the Department of Communication Studies.39

Figure 4.

Figure 4.

Examples of two graphics (top and bottom) developed by the Social Norming Task Force that were posted throughout the CSU campus to encourage observance of public health guidelines.

The catch phrase “Rams Take Care, Rams Take Action” was used to remind the CSU community of their role in helping their neighbors and their personal responsibility to mitigate the pandemic. In early April 2020, CSU President Joyce McConnell asked everyone to make and wear a mask to prevent SARS-CoV-2 spread.40

A student survey revealed that 91% of students practiced public health recommendations.38 The CSU President encouraged students to receive an optional, free COVID-19 test when they returned to the campus and gave the clear message that “Your test may mean the difference between getting to remain on campus this Fall or going home.”41 A few days later, the President sent a “COVID-19 Call to Action” to remind students of public health requirements and possible noncompliance consequences.42,43 A video was released to all students (see https://www.youtube.com/watch?v=1Gv2BaSaQdI) “COVID-19: Public Health Requirements for Fall 2020 at Colorado State University” with a link to a CSU COVID-19 informational website.44 By communicating directly and frankly—and compassionately—with students, they responded positively by registering for COVID-19 testing and maintaining compliance.

This successful social norming campaign was integrated in welcoming messages, town hall meetings, and placed on billboards and signs. A survey conducted from September to November 2020 showed that 93.9% of persons on or near the CSU campus were wearing face masks, with 95% wearing them correctly (covering the nose).45

Wastewater Surveillance

In April 2020, CSU researchers joined forces with GT Molecular (Fort Collins, CO) to take samples from 17 automatic samplers at CSU and 4 local wastewater collection sites 2–3 times weekly and test them for SARS-CoV-2 virus using digital droplet polymerase chain reaction (ddPCR; 24-h turnaround) (Figure 5).46–49 Results revealed infection trends since SARS-CoV-2 is shed at high levels in feces in infected persons and high levels could indicate a high infection rate.50 Variability occurred between different samples and sites depending on length of retention of sewage at the site. There was not a direct correlation between the number of infected persons and the level of virus detected; however, it provided valuable information about the infection trends and compliance with COVID-19 testing requirements. These data were submitted to CDC's National Wastewater Surveillance System,51 which tracked SARS-CoV-2 from 800 sites in the United States.

Figure 5.

Figure 5.

Sampling wastewater for SARS-CoV-2 surveillance.

The wastewater surveillance project was approved by the IBC, and BSL-2 practices, including a certified, Class II biosafety cabinet, were used for processing wastewater samples. The biosafety cabinet was cleaned with 70% ethanol, and spills inside the BSC were treated with 10% bleach, followed by 70% ethanol. PPE for collecting sewage from wastewater sampling sites included hard hats, eye protection, disposable surgical face masks, face shields, gloves, full Tyvek suits, and steel toed boots. PPE for processing samples in the laboratory included gloves, standard laboratory coats, face shield, and a disposable surgical face mask. After working with noninactivated wastewater samples in the biosafety cabinet, laboratory coats were removed, placed in a specific laundry bin, and cleaned weekly by a commercial service. Masks and gloves were disposed of in a biohazard waste container and autoclaved. Face shields were disinfected by wiping with 70% ethanol.

Sewage was treated with 10% bleach for 30 min to 24 h before disposal down the drain, all other biohazard wastes were autoclaved, and surfaces were cleaned with 70% ethanol. Researchers were required to be enrolled in the Occupational Health Services program and have hepatitis vaccinations. When SARS-CoV-2 vaccines were available, they were required for personnel. Testing/screening requirements for SARS-CoV-2 were the same as required by others on the CSU campus.

In late September 2020, high positive wastewater testing rates for two residence halls resulted in an immediate, mandatory, quarantine of these 900 students.52,53 These students were tested for COVID-19, provided medical care and meals, and connected to CSU physical and mental resources. The modified quarantine was implemented based on the CDC quarantine definition and was not dependent on close contact (i.e., “being within 6 feet of an infected person for at least 15 min starting from 2 days before illness onset”54). Fourteen students were COVID-19 positive. Those who tested negative returned to classes.55

Testing/Screening

The CSU Veterinary Diagnostic Laboratory, with assistance from the CSU's Health Network's Specialty Services Medical Director, received Clinical Laboratory Improvement Amendment approval in late March 2020.56–58 Approximately 2500 nasopharyngeal swabs were processed from community sites in the first month, however, due to anticipation of enormous testing numbers, an alternative plan was needed to test the entire CSU community.

Sample collection sites were established at the three CSU campuses. Students and employees self-administered nasal swab tests beginning in August 2020, using an FDA EUA-approved COVID-19 ddPCR diagnostic test (Biodesix, Inc., Boulder, CO; 27). Students in university housing and faculty and staff with high student contact were tested. As students returned for fall classes, they were offered free, optional COVID-19 tests.

In mid-October 2020, CSU switched to a pooled saliva screen test (for images of the saliva collection facility see https://www.youtube.com/watch?v=3NWkU5y7Rng).59–63 Saliva collection required persons to drool in a tube until it contained 1–2 mL of saliva. Initially there were concerns that the SARS-CoV-2 virus would be transmitted during collection. Researchers with expertise in aerosol movement and infectious disease calculated the spacing needed between persons in the saliva collection facility by using a modeling approach that takes into consideration the volume of air exhaled by one person and rebreathed by another (effective rebreathed volume), the size of the particles, and the role of proximity and confinement in transmission (for a detailed description of the modeling used, see Bond et al64). By calculating air distribution volume, overhead space, and number of persons present in the space at one time, the available space determined for each person was equivalent to 5-foot spacing outdoors.

Persons waited outdoors at the saliva collection site to reduce the risk of exposure. Pooled saliva was screened and saliva samples in positive pools were tested individually using the Biodesix, Inc. test.61 Pooled screening saved time and money since multiple samples could be screened simultaneously and the COVID-19 positivity rate was relatively low (<5%).62,63 Testing costs during the first 3 months were $2.2 million using Biodesix, Inc., and $700,000 over the next 3 months for both pooled saliva screening and follow-up tests of positive screens. The overall COVID-19 positivity rate (confirmed by an FDA EUA-approved test) was between 3% and 4% in fall 2020.65

In spring 2021, as the Delta variant began to rise in the population, all faculty and staff or students participating in face-to-face classes or laboratories were required to screen weekly, as were students living in university housing or Greek houses.66 COVID-19-positive persons were not required to screen for 90 days to avoid false positive results. By February 12, at least 26,000 CSU students, faculty, and staff had been screened, reflecting a 25% increase from peak screening weeks in fall 2020.65 The COVID-19 positivity rate at that time was 0.5%.

EUA-approved SARS-CoV-2 vaccines became available during December 2020 (Pfizer and Moderna) and February 2021 (Johnson & Johnson) and everyone was required to show vaccination proof or an exemption in fall 2021.67,68 Mandatory twice-weekly screenings were required for all unvaccinated persons (∼3500) and of these, only 0.51% required follow-up COVID-19 tests (Email; PPT, October 19, 2021).

In January 2022, the Omicron variant prompted a one-time mandatory saliva screening for all persons returning to campuses (Email; PPT, January 3, 202269). Twice-weekly screening continued for all unvaccinated persons. About 24,000 persons were screened and the positivity rate was 5.18%. In March 2022, because CSU's positive COVID-19 rate was 1% and more faculty, staff, and students were getting vaccinated, mandatory saliva screening switched to voluntary antigen testing regardless of vaccination status.70

Vaccines

Two hundred doses of Moderna COVID-19 vaccine arrived at CSU on March 21, 2021, and were provided to priority groups through a tiered approach, based on an individual's risk as defined by Colorado.71,72 Hospital personnel were priority, followed by CSU's Health Network staff and persons with exposure to COVID-19 patients, CSU police, COVID-19 sample collection site staff, and COVID-19 researchers. The next group to be vaccinated was employees 70 years or older (∼200 persons) and then those between 65 and 69 years of age (∼350 persons). Instructors teaching face-to-face were in the fourth group (1B).72 By April 2, 2021, all adults in Colorado were eligible for a vaccine and vaccination clinics were hosted by the Larimer County Public Health Department on campus.73

In fall 2021, CSU mandated that all students, faculty, and staff be vaccinated or declare an exemption based on medical or nonmedical reasons (personal or religious beliefs).67,68 An online portal collected proof of vaccination, which included entering dates of vaccination, type of vaccine received, and providing a digital copy of the COVID-19 vaccination record card to the Office of Human Resources. Those requesting an exemption were directed to the Office of Equal Opportunity for accommodations.74 On August 20, 2021, 82% of CSU employees had submitted this information, 20,500 students were fully vaccinated, and 1500 had received their first vaccine (Email; President Joyce McConnell, August 20, 2021). By October 19, 2021, almost 90% of the CSU community were vaccinated, compared with 66% Larimer County residents and 61% of Coloradoans (Email; PPT, October 19, 2021).

In spring 2022, the vaccination mandate continued and on January 13, CSU encouraged persons eligible for the COVID-19 boosters to obtain one.74–76

Course Delivery and Public Health Protocols

The Facilities Management team removed excess seating from classrooms and study areas to encourage physical distancing, marked seating for 6-foot distancing, prepared and placed sanitizer/disinfection stations, modified air flow, and cleaned and disinfected spaces.

When classes abruptly moved online after spring break 2020, instructors had only 1 week to pivot from face-to-face to online teaching (Table 1).6 Amid chaos and uncertainty, instructors responded by working above and beyond expectations. In summer 2020, CSU, the Colorado Department of Higher Education, the TCRT, and instructors planned for delivering online courses or face-to-face for courses that required hands-on learning (laboratories, performances, studios, etc.), with the awareness that classes could change to online delivery if COVID-19 cases spiked.13,77

Instructors worked diligently over the summer to develop online courses that enhanced learning and contained engaging content.77 A “Keep Teaching” website78 was launched to assist instructors with designing effective online and hybrid courses. Throughout the pandemic, workshops addressing online teaching, building community online, and open educational resources for virtual laboratories, and best practices in teaching were available through The Institute for Learning and Teaching (TILT) and Academic Computer Network Services.79–82 The “Keep Teaching” website provided valuable information for teaching continuity and strategies for teaching during the pandemic. Where possible, technology improvements, microphones, and recording capabilities were implemented in classrooms.

In fall 2020, 34,300 students were enrolled, and two-thirds of courses had an in-person component.27,83 Classes with more than 99 students were delivered online and instructors were encouraged to provide online teaching if their course lacked a laboratory, studio, or rehearsal component. As reports of severe SARS-CoV-2 infections increased, instructors expressed concerns for their students, themselves, and their family's health while teaching face-to-face. Since public schools and daycare facilities closed, those with school-age children had to plan for work and teaching while remaining at home to care for their children or other family members.13,84,85 The Families First Coronavirus Response Act allowed employees to take a leave of absence and CSU supported those with dependents or were vulnerable (medical condition or older than 65 years) to apply for a temporary work adjustment.27

Students and instructors attending or teaching in-person classes were required to wear a mask, physically distance (6 feet), avoid gatherings, report COVID-19 symptoms, positive test results, and exposures through the online reporter. All persons were instructed to disinfect workspaces and wash their hands or use hand sanitizer when entering and leaving classrooms. Seating charts assisted contract tracing and CSU provided online tools to faculty for making seating charts and providing them to contact tracing teams.86 Students who were symptomatic, tested positive, or were exposed to an infected individual were required to report to CSU and to follow CSU's Public Health Office quarantine or isolate orders. Students who tested positive for COVID-19 or faced other challenges joined classes remotely.

Instructors were advised to be flexible and allow late assignments and make up opportunities for classwork and examinations.13 COVID-19 made teaching somewhat challenging due to the “revolving door” of student absenteeism, however, instructors remained flexible. Instructors were not required to provide multiple learning modalities, but most instructors posted minilectures or recordings in the CSU learning management system for students who could not attend class in-person or online. Students requesting remote learning worked with their academic advisor to identify options. Due to the massive interruption in routines, online teaching, and increased stress, students were given the choice of Satisfactory/Unsatisfactory grading from spring 2020 through summer 2021.87 Multiple resources were provided to address student medical issues, physical health, mental health, engagement and learning, food insecurity, and personal and family crises.88–90 Eligible students were aided through CSU Federal CARES Act Emergency Aid funding.

Approximately 32% of classes were face-to-face, 34% were hybrid, and 34% were fully online in spring 2021.71 Upon moving into university residence halls, students were tested immediately for SARS-CoV-2 and isolated pending the test results. This allowed infected students to be identified before attending classes. After the first week, laboratories or classes with an in-person component switched to in-person classes. Classes that had been remote returned to a hybrid format (both online and in-person instruction) based on Larimer County Public Health guidelines.

Previous CSU public health requirements (masking, distancing, reporting, etc.) continued. All students with face-to-face or hybrid instruction, who lived on campus or in Greek housing, and faculty and staff who had in-person contact with students or teaching face-to-face or hybrid classes were required to saliva screen weekly in spring 2021.66 Spring break was delayed by 1 month and all classes moved online following the break.91 Course withdrawal was extended to the last day of class to accommodate students who became ill during the semester.

CSU offered in-person, hybrid, and online courses in summer 2021.71 Forty percent of courses were in-person or hybrid and 60% were online.

The CSU main campus hosts summer camps and special academic programs.92 Many summer activities were canceled, but 1733 campers attended 17 summer activities.93 Special academic programs and athletic camps had to apply to the PPT to ensure participants and activities would follow public health guidelines.

By mid-May 2021, COVID-19 cases decreased, and public health requirements were modified.94 Classrooms, laboratories, and research spaces operated at 100% capacity, up from 50%, required distancing was 3 feet (vs. 6 feet), with masks required only indoors. Remote employees began returning to campus.95 Mandatory twice-weekly saliva screening (unless fully vaccinated), reporting of COVID-19 symptoms, positive tests, exposures, and contact tracing continued. On July 12, 2021, the mask requirement was lifted except within the Health and Medical Center, the Veterinary Teaching Hospital, and in public transportation.

In fall 2021, about 2545 students moved into residence halls and more than 20,000 CSU students were fully vaccinated.35,67 With the spread of the Delta variant and changes in guidance by the CDC, CSU opted to require masks indoors regardless of vaccination status. Faculty, staff, and students could remove their masks if they were alone in their offices, rooms, or apartments, respectively. Contract tracing and the COVID-19 reporter remained mandatory.

The Omicron variant, a more transmissible SARS-CoV-2 variant, was reported in Larimer County, in January 2022, 2 weeks before the spring 2022 semester (Email; PPT, January 3, 202275). Mathematical models formulated by the CSU math faculty in conjunction with the Governor's Task Force predicted that there would be a COVID-19 spike from mid-January to mid-February.69,95 Everyone was required to one-time saliva screen upon return to campus; positives were required to isolate for 5 days as per CDC guidelines if they were symptom free and wore a mask for another 5 days. During winter break, the CDC modified the masking guidance to recommend 3-ply surgical masks or N95 respirators.67,96–98 CSU provided these masks at cost through their PPE website. Although masks were still required in CSU buildings, and the CDC guidance was noted, 3-ply surgical or N-95 respirators were not required.

One major CSU policy change was requiring COVID-19 vaccine proof or an exemption and boosters of all CSU students and employees once the Moderna COVID-19 vaccine was FDA approved on January 31, 2022.73–76 Anyone not vaccinated or with an exemption continued required screening twice weekly, with exceptions made for anyone not yet eligible for a booster due to the vaccine date, a current or recent COVID-19 illness, or who had received monoclonal antibody treatment in the last 90 days. Symptoms, exposures, and positive COVID-19 tests (including home tests) and contact tracing continued. CSU provided free Moderna boosters to students.

On February 28, 2022, the Larimer County COVID-19 positivity rate was 6%, corresponding to high community levels in CDC updates, but by March 3rd, the county transmission risk level was low (Emails; PPT, February 28, 2022, and March 2, 202299). Masks became optional, except at the Veterinary Teaching Hospital, in public transportation, and the CSU Health Network. After spring break in March 2022, saliva screening was replaced with voluntary antigen tests.100 Everyone was encouraged to continue best hygiene practices and disinfectant/sanitation stations remained in place. In mid-May, vaccinations or exemptions were still required (Email; PPT, May 11, 2022). Boosters were encouraged but were not required.

Microbiology Teaching Laboratories

During summer 2020, CSU instructors for laboratory courses made online teaching contingency plans, knowing that all fall 2020 laboratory classes were planned for face-to-face delivery. Since the spring semester had ended abruptly with online instruction, faculty members worked fervently to structure course learning materials in both in-person and online formats in case the pandemic forced them to switch to teaching remotely. Faculty members in the College of Veterinary Medicine and Biomedical Sciences participated in a 6-week “Summer Online Course Development” program to adopt best practices for online teaching, with the goal of optimizing student engagement and learning. TILT and CSU Online offered numerous workshops and short courses to 1300 faculty members for preparation of fall classes.83

Seven faculty and staff members formed the Biosafety in Teaching Laboratories Committee to develop best policies to reduce COVID-19 risks in microbiology teaching laboratories. Laboratory door signage designated entries and exits, assigned seating with 6-foot distancing was allotted, and seating charts were posted both online in course materials and in the classroom to facilitate contact tracing. Instructors measured 6 feet between benchtop chairs and marked all spaces with colored tape. Existing locker space was expanded with the purchase of additional lockers so that each student could store backpacks and coats in a separate space while in the laboratories. A video explaining the new procedures was sent to students before the beginning of the fall 2020 semester.

When students entered the laboratory, they immediately placed their materials in a locker labeled with their name. They washed their hands with soap and water, donned gloves and standard laboratory PPE (eye protection, laboratory coats), and disinfected their benchtop and chair with 70% ethanol. Students supplied their own mask and eye protection and stored these along with their laboratory coats in a student-designated drawer in the teaching laboratory.

Time spent in the laboratory was minimized by using a “flipped classroom” model where short 5-min lectures or laboratory procedure videos were prerecorded and placed online for student access before and after the laboratory. Safety practices such as donning and doffing gloves, PPE use, spill cleanup, fire blanket and spill kit location, eyewash operation, as well as standard laboratory procedures including aseptic technique, using a micropipette, pipetting large volumes, streaking bacteria on agar, preparing and plating serial dilutions, and Gram- and endospore staining were recorded. This allowed students to come to the laboratory, perform their experiments, and leave as soon as possible.

In pre-COVID laboratories, students gathered their materials/supplies from a single location and took them to their benchtop for their experiments. To reduce intermingling, students remained seated and supplies were prearranged at their desk before class or delivered during class. Each student had his or her own set of micropipettes, a handheld Pipetaid, Bunsen burner, Gram stain reagents, inoculating loops and needles, striker/flint, tube racks, and other materials, kept in their drawers, as well as an assigned microscope in the laboratory.

Faculty were initially instructed to keep a 12-foot distance from students to minimize contact and possible disease transmission. The Biosafety in Teaching Laboratories Committee realized that it would be impossible to teach students basic microbiology skills such as streaking bacteria onto plates, colony morphologies, and focusing the light microscope at this distance. Face shields were supplied to help mitigate disease transmission and allow instructors to demonstrate techniques and assist students at close range. Everyone was required to wear a mask, eye protection, and a face shield. Faculty struggled with speaking loud enough and students struggled with hearing them. Instructors were subsequently provided portable microphone systems, with a separate mouthpiece for each instructor. CSU instructors unanimously agreed that microphones were essential for the success of their classes.

Absenteeism was a significant challenge during the pandemic, particularly in microbiology laboratory courses that relied on growing microbes, performing experiments, and timely data collection. Students who were COVID-19 positive or had an exposure were not identified to instructors and instructors were not allowed to ask a student his or her COVID-19 status. However, students always informed the instructors if they had COVID-19, so that they would remain up to date with the laboratory exercises. When a student self-reported, his or her laboratory bench and chair were disinfected with 70% ethanol to prevent possible transmission. Students positive for or exposed to a COVID-positive individual were contacted by the Larimer County Public Health Department or the CSU Public Health Office for contract tracing and appropriate response.

Conclusion

A December 2020 report by The New York Times indicated that a “survey of more than 1900 American colleges and universities revealed more than 397,000 COVID-19 cases with at least 90 deaths.”101 To mitigate the risk of transmission, morbidity, and mortality, universities and colleges used strategies comparable with those used by the CSU to continue teaching, research, and operations during the pandemic.102–105 Some variations noted were the time of testing upon return to campus (immediately on check-in vs. a 7-day period), degree of masking requirements (in some classrooms vs. all classrooms), use of wastewater surveillance, movement to online classes versus hybrid or in-person, and providing safety kits.

At the time of this writing (May 2022), CSU is very fortunate to report that there have been no documented cases of classroom transmission of COVID-19 at CSU-Fort Collins.69 There have been 8770 COVID-19 total cases from May 2020 to present, with 5953 cases for spring 2022 beginning with January 14, 2022.106 This compares with a total number of cases in Larimer County of 82,403, and 1,418,901 cases in Colorado (May 22, 2022). CSU has performed 251,052 saliva screens, with 211,149 saliva samples screened in spring 2022. As of May 2nd, 99% of the 24,105 on-campus students had submitted vaccine proof to the portal, 91.7% were fully or partially vaccinated, 56.2% reported boosters, and 8.2% had vaccine exemptions.107 Of 8341 employees (including employees across the state who might not be on campus), 95.7% had submitted to the portal, 88.6% were fully or partially vaccinated, 62.2% had boosters, and 7.1% had exemptions.

Factors supporting this success are the intense, selfless collaboration of numerous entities, leaders, researchers, instructors, the CSU and Fort Collins community, and local and state health officials. It is impossible to list all the CSU employees and people who have been and are continuing to be involved in this endeavor. The social norming campaign, the willingness of students and the CSU community to comply with public health requirements, and the ability to quickly screen and perform effective contact tracing were crucial to keeping the number of cases low. The availability of vaccines and boosters, compliance with vaccine mandates, and a relatively low level of community transmission kept the numbers of cases under control and assisted CSU with returning to mostly in-person instruction. One of the important realizations is that we must stay alert, not drop our guard, and remain flexible in our responses to future challenges.

Acknowledgments

All photographs are courtesy of Colorado State University. The information in this article was obtained from the authors' email messages, CSU messages, and town hall meetings, and interviews with key participants at the CSU. The authors wish to thank the CSU community members for their commitment to the CSU students, faculty, and staff to mitigate the risks of the coronavirus. They especially thank Steve Burn, Jonathan Cumpsten, and Facilities Management for information on the pandemic response. It is important to note that this article does not include all the efforts contributed by the CSU, state, and local individuals. The authors apologize in advance for any omissions.

Authors' Contributions

C.G.-W.: investigation, project administration, writing original draft, and review and editing; D.R.C.: writing original draft, and review and editing; M.B.: validation, and review and editing; K.L.: validation, and review and editing; L.L.: validation, and review and editing; H.P.: validation, and review and editing; K.Q.: validation, and review and editing; B.W.: validation, and review and editing.

Authors' Disclosure Statement

The authors declare no competing interests, including personal financial interests, funding, employment, or any other interests.

Funding Information

This article was not supported financially and the authors declare no conflict of interest.

References


Articles from Applied Biosafety: Journal of the American Biological Safety Association are provided here courtesy of ABSA International and Mary Ann Liebert, Inc.

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