key: cord-0894009-khufykgd
authors: Weil, A. A.; Luiten, K. G.; Casto, A. M.; Bennett, J. C.; O Hanlon, J.; Han, P. D.; Gamboa, L.; McDermot, E.; Truong, M.; Gottlieb, G. S.; Acker, Z.; Wolf, C. R.; Magedson, A.; Chow, E. J.; Lo, N. K.; Pothan, L. C.; McDonald, D.; Wright, T.; McCaffrey, K.; Figgins, M. D.; Englund, J. A.; Boeckh, M.; Lockwood, C. M.; Nickerson, D. A.; Shendure, J.; Bedford, T.; Hughes, J. P.; Starita, L. M.; Chu, H. Y.
title: Mapping the emergence of SARS-CoV-2 Omicron variants on a university campus
date: 2022-04-28
journal: nan
DOI: 10.1101/2022.04.27.22274375
sha: 38b36ab4ca5eef84fa38a16518f5f0404881ee8f
doc_id: 894009
cord_uid: khufykgd

Novel variants continue to emerge in the SARS-CoV-2 pandemic. University testing programs may provide timely epidemiologic and genomic surveillance data to inform public health responses. We conducted testing from September 2021 to February 2022 in a university population under vaccination and indoor mask mandates. A total of 3,048 of 24,393 individuals tested positive for SARS-CoV-2 by RT-PCR; whole genome sequencing identified 209 Delta and 1,730 Omicron genomes of the 1,939 total sequenced. Compared to Delta, Omicron had a shorter median serial interval between genetically identical, symptomatic infections within households (2 versus 6 days, P=0.021). Omicron also demonstrated a greater peak reproductive number (2.4 versus 1.8) and a 1.07 (95% confidence interval: 0.58, 1.57; P<0.0001) higher mean cycle threshold value. Despite near universal vaccination and stringent mitigation measures, Omicron rapidly displaced the Delta variant to become the predominant viral strain and led to a surge in cases in a university population.

Persistent SARS-CoV-2 circulation has led to the continued emergence of variants of concern (VOCs). On November 26, 2021 despite widespread population immunity, as evidenced by the exponential increase in cases over shorter time periods compared to prior VOCs [2] [3] [4] . There is also population-level, genomic, and in vitro evidence of decreased vaccine effectiveness against Omicron compared to the Delta variant and of partial evasion of vaccine-induced immunity by Omicron, leading to high numbers of breakthrough infections [5] [6] [7] [8] . Studies have shown mixed results on differences in Omicron viral load compared to the Delta variant, with evidence of either lower or comparable viral loads for Omicron [9] [10] [11] [12] . Omicron household transmission has been reported to have a higher attack rate and lower serial interval compared to Delta, although the majority of studies to date have not used genomic data to assess the serial intervals in intra-household transmission [13] [14] [15] [16] [17] [18] [19] .

There remain gaps in our understanding of the transmission dynamics and molecular epidemiology of VOC emergence in US populations.

Throughout the COVID-19 pandemic, university campuses have been sites of SARS-CoV-2 outbreaks [20] [21] [22] [23] . Many universities provide free, convenient testing to facilitate SARS-CoV-2 surveillance within campus communities 20, 22, 24 . Using data collected from September 2021 to February 2022 through a campus testing program, we describe the rapid emergence of Omicron in a highly vaccinated university community, and the clinical characteristics and transmission dynamics of the Omicron variant compared to the Delta variant. We used molecular epidemiology to track emergence of variants and examine intra-residence infections in congregate living settings.

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The copyright holder for this preprint this version posted  https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint

The Husky Coronavirus Testing (HCT) research study provides SARS-CoV-2 testing at the University of Washington (UW), a large public university in Seattle, Washington, USA 20 .

University-wide mitigation policies during this study period included indoor masking, air filtration, limitations in size of gatherings, and mandatory vaccination for faculty, staff, and students, resulting in completion of the primary vaccine series for 98.6% of students, 98.9% of staff, and 99.7% of faculty by January 2022 25 . Individuals were eligible to enroll in the study if they were faculty, staff, or students at the university and were English-speaking. Clinical symptoms and vaccination status were collected through electronic questionnaires. Participants completed a daily attestation via email or text message, and those who reported new symptoms, exposure to a known SARS-CoV-2 case, or recent travel were offered SARS-CoV-2 testing. Additionally, participants could request testing for any reason. Data were collected using Project REDCap 26, 27 . Swab collection. Testing was performed through three mechanisms: observed self-swab at a staffed kiosk, unobserved self-swab returned to a campus testing dropbox, or unobserved selfswab returned to the laboratory via courier 28 . Two swab types were used; a US Cotton #3 swab (SteriPack Polyester Spun Swab), returned in a 10mL tube, was used for all unobserved collection returned via courier, and for some observed collection testing at times of supply chain issues. The RHINOsticTM Automated Nasal Swab (Rhinostics RH-S000001), returned in a MatrixTM 1.0mL ScrewTop Tube (Thermo Fisher 3741), was used for observed kiosk and unobserved dropbox swab collections.

Laboratory methods. All swabs were stored dry, with no preservative or media, and eluted with 1mL Tris-EDTA for US Cotton #3, or 300µL Tris-EDTA for RHINOsticTM. 50µL of eluate was treated with proteinase K and heat for direct RT-qPCR (Swab-Express RT-qPCR) as previously . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint described 29 . The RT-qPCR assay employs custom probe sets for SARS-CoV-2 Orf1b and S gene designed against the ancestral strain that are multiplexed with a probe set for human RNase P 29 . Briefly, 5uL of prepared eluate was transferred to four multiplexed RT-qPCR reactions, two Orf1b-FAM plus RNase P-VIC and two S-FAM plus RNase P-VIC. Positive samples had SARS-CoV-2 targets detected in three or four reactions and an internal control RNase P amplification detected in at least three reactions; however, the 157-158 deletion in Delta variants results in S gene target failure or delay in our assay.

Genomic sequencing. Viral genome sequencing was attempted on SARS-CoV-2 positive specimens with a high quantity of SARS-CoV-2 RNA, generally having Orf1b cycle threshold (Ct) ≤30. Nucleic acids were extracted (Magna Pure 96, Roche) and sequencing libraries prepared (Illumina COVIDSeq kit). Genomes were sequenced (Illumina NextSeq2000 P200 kit) and consensus genomes were assembled against the SARS-CoV-2 reference genome Wuhan/Hu-1/2019 (Genbank accession MN908947) using a modified iVar pipeline 30 . Consensus sequences were deposited to GenBank and GISAID (see Supplementary Materials). We considered "BA.1" to include the parental lineage and all BA.1 sublineages, and "BA.2" to include the parental lineage and all BA.2 sublineages.

Statistical Analysis. We used the term "infection date" to describe the collection date of each person's first SARS-CoV-2 positive sample, and to represent the first known date of infection regardless of symptom status. For participants who tested positive for SARS-CoV-2 more than once between September 10, 2021 and February 14, 2022, the first infection was included in our analysis. The proportion of cases reporting various symptoms were compared by variant using Pearson's chi-squared tests. Median serial interval of symptomatic participants in clusters were compared by variant using a non-parametric Mann-Whitney U test.

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The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint COVID-19 vaccination status was collected at enrollment, updated monthly, and updated at or after collection of the SARS-CoV-2 positive samples. Participants self-reported vaccine manufacturer name, dose number, and date of receipt. Vaccination status for participants is dynamic, and in this manuscript the term "vaccination status" reflects the status on the date a positive swab was taken. Fully vaccinated was defined as completion of the primary series at least two weeks prior to the positive test date. Partially vaccinated was defined as an incomplete two-dose primary series or less than two weeks since completion of the primary series.

Unvaccinated was defined as confirmed no vaccination. Vaccination was defined as unknown for participants who reported invalid dates or no information at all. A participant was considered boosted if they received a booster dose at least two weeks prior to the positive test date, partially boosted if fewer than two weeks, and not boosted if no booster was received by the positive test date.

Shared residence was defined as the same apartment, dorm room, or unit number, or by the same street address for single-unit residences. Clusters of positive cases were defined as living within a shared residence with identical SARS-CoV-2 sequences. An index date and serial interval were calculated for each cluster with at least two symptomatic individuals. Serial interval was defined for each non-index individual in a cluster as the duration of time between the index symptom onset date to non-index individual's symptom onset date. Symptom onset date was defined as the earliest symptom onset date within one week before or after each individual's positive test. Individuals were considered asymptomatic if they reported no symptoms within one week before and after testing positive.

Multiple linear regression models were used to estimate mean difference in Ct between Omicron and Delta variant cases, adjusting for age, symptom status (symptomatic versus asymptomatic), average RNase P gene value, days since symptom onset among those with symptoms, and vaccination status (primary series vs. booster) and days since last COVID-19

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The copyright holder for this preprint this version posted Maximum likelihood phylogenetic trees were constructed using the Nextstrain Augur software package 31 using default parameters for SARS-CoV-2 as outlined on the Nextstrain GitHub webpage 32 . Nextstrain Auspice software was used for tree visualization. Our genomic analyses also included publicly available SARS-CoV-2 genomes for other Washington state samples from the GISAID EpiCoV database 33 , which were screened using Nextclade version 1.10.0 34 . Any sequences deemed to be of "bad" or "mediocre" quality by this tool (due to missing data, mixed sites, private mutations, mutation clusters, frameshifts, or stop codons) were excluded from further analyses.

To estimate the number of Delta viral introduction events onto campus represented by the 209 sequenced Delta samples, we created a tree that included these samples along with all GISAID Delta genomes from samples collected in Washington state between September 1, 2021, and February 14, 2022, meeting our quality criteria (N=15,406). The Nextstrain Augur "traits" subcommand was used to infer campus versus non-campus states for all internal nodes. An introduction event was presumed to have occurred in all cases in which a Washington state non-university campus parent node connected with an on-campus child node. To assess the accuracy of this estimate given the number of Washington state Delta genomes available, we re-calculated the introduction event number using 15 subsamples of the total pool of available non-study genomes varying in size from N=1,000 to N=15,000. We repeated this process with a tree which included the 1,730 sequenced Omicron samples and all GISAID Omicron samples . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

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Using all sequenced study samples and overall daily case counts over the study period, we estimated variant-specific effective reproduction numbers (Rt) for Delta and Omicron. To do this we reconstructed variant-specific incidence from observed daily variant proportions using a multinomial likelihood for variant proportion and negative binomial likelihood for cases. This reconstructed incidence was used to compute the effective reproduction number for Delta and Omicron while reflecting the observed shorter serial interval of Omicron versus Delta 35 .

The UW IRB approved this study (#00011148).

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The median age of participants with infection was 20 years (range 18-66) for Delta and 21 years (range 17-79) for Omicron ( Table 1) . Most SARS-CoV-2 cases were among students (90.9% of Delta cases, compared to 87.9% of Omicron cases). Residing in a household with a density of ≥6 was reported for 34.0% of Delta and 23.8% of Omicron cases. 18.2% of Delta and 18.3% of Omicron cases were asymptomatic at the time of swabbing. Among symptomatic cases, the most reported symptoms were rhinorrhea/congestion (69.6% and 62.4% for Delta and Omicron, respectively), cough (59.1% and 61.5%), and sore throat (56.1% and 69.2%). Loss of sense of taste or smell was more common among Delta cases (11.1% of those with Delta vs. 2.8% of those with Omicron, P<0.001). Myalgias, fever, and chills were more prominent in Omicron Table 2) . We did not find a difference in semiquantative viral load comparing Omicron Pango lineages BA.1 and BA.2 (N = 1,688, Supplemental Table 1) .

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The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint Among the 1,939 SARS-CoV-2 genomes, we identified 13 residences with multiple sequenced Delta cases and 136 residences with multiple sequenced Omicron cases. Phylogenetic and pairwise distance analyses of these genomes indicated that many cases within the same residence were likely the result of more than one introduction event. Thus, we restricted analysis to 78 clusters including 173 individuals with identical viral genomes within the same residence (N=25 residents for Delta, and 148 for Omicron).

Thirty individuals reported that symptoms began on the same day as another individual in the cluster and 53 collected their first positive sample on the same day as another individual in the cluster. All identical viral genomes within a single household were detected within a maximum serial interval of 15 days. Forty-four clusters included more than one symptomatic individual and more than one unique symptom onset date. Among these clusters, the median serial interval between symptom onset of the index and a subsequent case was longer for 8 subsequent cases in 7 Delta clusters (median 6 days, range [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] ) compared to for 43 subsequent cases in 37 Omicron clusters (median 2 days, [1] [2] [3] [4] [5] [6] [7] [8] [9] ) (P=0.021, Supplemental Figure 1 ).

A phylogenetic tree shown in Figure 3A includes all 209 Delta genomes shown with 1,174 randomly selected genomes from samples collected in Washington state over the same time period. A phylogenetic tree containing all 1,939 sequenced viral genomes is shown in Figure   3B , illustrating rapid replacement of Delta by Omicron on the university campus in December 2021. Three monophyletic clusters containing exclusively or almost exclusively study genomes (N=35, 24, 66 total genomes and N=35, 23, 66 HCT genomes) are boxed in Figure 3A ;

approximately 60% of all study Delta genomes fall into one of these 3 groups. The maximum pairwise distance between two study Delta samples was 60, and average distance was 18.54.

One hundred sixteen (56%) of these samples were genetically identical to at least one other study sample. The tree in Figure 3C includes all 1,730 Omicron genomes with 1,512 randomly . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

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The copyright holder for this preprint this version posted showed that the estimate of Delta introduction events would be unlikely to change even if more Washington state genomes were available, though it was unclear if this was the case for the Omicron estimate (Supplemental Figure 2) .

To quantify the degree to which each variant impacted on-campus transmission rates, we estimated variant-specific transmission dynamics following previously established methods 35 .

Here we find that the Rt associated with the September to October Delta outbreak peaked at 1.8 (95% credible intervals [CI] 1.3-2.4) and declined rapidly below 1, while the Rt associated with the December to January Omicron outbreak peaked at 2.4 (95% CI 1.9-2.8) and declined below 1 over a longer period (Figure 4) . These differences in Rt are reflected in the relative magnitudes of the September to October Delta outbreak compared to the December to January Omicron outbreak (Figure 4 ).

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In a large, urban university campus with widely available testing, stringent mitigation measures and near-universal vaccination, the Omicron variant rapidly displaced the Delta variant to become the predominant viral strain over a two-week period. Fever, myalgia, and chills were more commonly reported in Omicron cases and loss of taste and smell in Delta cases. Ct values were on average higher for Omicron cases. Using genomic analyses, we observed shorter serial intervals in case clusters and faster spread for Omicron relative to Delta. These findings highlight the importance of integrating genomic surveillance into university testing studies to better characterize VOC community spread.

Variants have continuously altered our understanding of SARS-CoV-2 genomic epidemiology.

The adaptation of public health recommendations to this quickly changing landscape relies on rapid data collection, and university testing programs are uniquely positioned to collect data which may be more broadly representative of community dynamics than hospital-based surveillance strategies. Using symptom and exposure-based testing, we identified Omicron . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint Our findings suggest a median serial interval of 2 days and 6 days among persons with Omicron and Delta, respectively. In contrast to other analyses examining serial intervals within households or other clusters [13] [14] [15] 17, 19 , we used viral genomic data to minimize confounding of the serial infection interval by co-incident exposures during periods of high community transmission. By using only identical genomes to calculate the intra-residence serial interval, we decreased the likelihood that clusters are the result of more than one index case (although we cannot eliminate this possibility). Our finding of reduced serial interval between index and subsequent household infections for Omicron compared to Delta cases is consistent with other studies in the US (median serial interval of 3 days for Omicron) 13 

South Korea (reported mean serial intervals from 2.8-3.5 days for Omicron and 3-4.1 days for Delta) [16] [17] [18] [19] . Our estimated median serial interval of 2 days for Omicron is lower than these studies and this may be due to our study population being on average younger and more highly vaccinated and only one other study using genomic sequencing to identify household transmission 16 .

Semiquantitative viral loads were lower for Omicron compared to Delta variant infections, supporting the theory that increased transmissibility of the Omicron variant is not due to viral load and in agreement with other studies in the setting of highly vaccinated populations and routine testing of asymptomatic and mildly ill individuals, including three other US universities and the US National Basketball Association's occupational health program 9,12 . In contrast, a US study of hospital patients tested as part of routine clinical care and a Swiss study of symptomatic outpatients with only eighteen Omicron cases did not find a difference in viral load between Omicron and Delta variants 10, 11 .

The Omicron variant swiftly replaced Delta on campus, despite high rates of vaccination and broad campus mitigation measures in place. Due to the availability of rapid whole genome sequencing 38,39 , we quickly identified the emergence of Omicron. The rapid rise of Omicron may . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted April 28, 2022. Omicron cases is limited likely due to the limited genomic variation among Omicron viruses and the fact that study genomes currently make up about 10% of the available Omicron genomes from Washington. This estimate does suggest that most Omicron introduction events resulted in a single sequenced case. Our analyses indicate that the same is true for Delta introduction events. However, for Delta, it was also clear that most sequenced cases were the result of introduction events that resulted in multiple cases, and that most on-campus SARS-CoV-2 cases due to Delta variant viruses were the result of campus-related transmission. It is particularly notable that most sequenced Delta cases were due to just one of three putative introduction events while the highest number of cases due to a single putative Omicron . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint introduction event (for the analysis including all Washington state Omicron sequences) was 41 (or 2.4% of the total number of sequenced cases), which may suggest differences in patterns of Delta and Omicron transmission on campus. Unfortunately, the considerable degree of uncertainty in the Omicron phylogenetic tree limits our ability to directly compare transmission patterns of the two variants.

Our study limitations include the lack of routine surveillance testing of the entire campus population. Follow-up symptom data was missing for some individuals and therefore we do not know if some asymptomatic cases were pre-symptomatic. We rely on self-report of vaccine status and could not reference state registries. However, state registry data may be incomplete or delayed, especially for students from other states. A limitation of our Ct analysis is the change in swab type during the study which may impact viral load, and we therefore restricted our viral load analysis to only one swab type. We also did not account for repeat infections.

Finally, this study included only people on a single university campus who participated in the research study, and who are on average, younger, healthier, and more educated than the general population.

In conclusion, we found rapid replacement of the SARS-CoV-2 Delta variant with the Omicron variant within a highly vaccinated university population. As we move into the next phases of the pandemic, real-time data around viral kinetics and genomic epidemiology of emerging variants will be important to guide our national strategies on mitigating respiratory virus spread.

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The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint 1. Race is divided into mutually exclusive groups 2. Multiple races included participants reporting more than one of these groups 3. Household density was defined as the number of people sharing the same kitchen or living space 4. A household density of 6 was assumed for participants who reported more than 6 household members 5. COVID-19-like illness (CLI) was defined as self-reported fever, chills, and/or shivering, with cough and/or shortness of breath 6. Influenza-like illness (ILI) was defined as self-reported fever, chills, and/or shivering, with cough and/or sore throat 7. Duration between symptom onset and first SARS-CoV-2 positive result in symptomatic participants 8. Unique symptoms reported by a participant within 7 days before and after collecting their first SARS-CoV-2 positive swab.

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The copyright holder for this preprint this version posted (C) Posterior estimates of variant-specific effective reproduction numbers. Shaded intervals in all plots correspond to 50%, 80%, and 95% credible intervals.

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The copyright holder for this preprint this version posted Regression was restricted to Omicron cases detected using RHINOstic TM swabs (42 Omicron cases detected using US Cotton #3 swabs).

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Cryptic transmission of SARS-CoV-2 in Washington state

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The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted April 28, 2022. ; https://doi.org/10.1101/2022.04.27.22274375 doi: medRxiv preprint