FIFA Arab Cup tournament with full capacity of spectators during the COVID-19 pandemic: a cross-sectional study

ABSTRACT Background We sought to assess the risk of COVID-19 and seasonal flu including respiratory syncytial (RSV) and influenza viruses during the FIFA Arab Cup 2021 in Qatar with full capacity of spectators. We also, evaluated the post-event attitude toward resumption of mass football events. Methods This was a cross-sectional study in which spectators (age ≥ 18 years) were invited for reverse-transcription PCR testing for COVID-19 and seasonal flu. At the same time, between 7 and 14 days after the event, the participants completed a self-administered questionnaire regarding their concerns during the tournament. Results The tournament included 16 international football teams from the Arab countries. As per the study protocol, 10,000 spectators were approached and 6,475 participated. Among the participants, 4,195 (65.1%), 2,253 (34.9%) and 27 (0.4%) were vaccinated with 2 doses, vaccinated with 3 doses, and recovered from SARS-Cov-2 infection, respectively. There were 61 (0.9%), 41(0.6%) and 11(0.2%) participants who tested positive for COVID-19, RSV and influenza (A/B), respectively. The average cycle threshold (Ct) value for COVID-19 positive cases was 26.1±7.3. Among those who were electronically approached, 6,102 completed the survey whereas 373 had incomplete survey. Overall, 2069 (33.9%) participants reported symptoms that theoretically could be related to COVID-19, of them 39 had positive PCR test (1.9%). Spectators (94.3%) were optimistic about returning sport events to the pre-pandemic status. Conclusions There was no significant increase in the daily COVID-19 cases during FIFA Arab Cup 2021 with a full capacity of spectators. Therefore, upcoming mass football events can be held safely.


Introduction
Worldwide, the coronavirus disease 2019 (COVID-19) pandemic has affected all the major professional sporting events given the risk of transmission and emergence of novel SARS-CoV-2 variants (Skinner and Smith 2021;Ilevbare and McPherson 2022).Although there has been progress towards the resumption of professional football events during the pandemic, there remain challenges.During the later pandemic phase, football leagues have resumed in numerous countries despite safety and health concerns (Gallego et al. 2020;Breidenbach and Mitze 2021;Marsh et al. 2021;Meyer et al. 2021;Pedersen et al. 2021;Rubin 2021;Savicevic et al. 2021;Schumacher et al. 2021;Toumi et al. 2021; National Project of Surveillance for Variants of Concern and Viral Genome Sequencing 2022).Initially, football tournaments were cancelled, postponed or organized with bio-secure resumption protocols without spectators.Subsequently, spectators could gradually participate in football events with strict preventive measures and limited capacity (Gallego et al. 2020;Schumacher et al. 2021).The Tokyo 2020 Olympic and Paralympic Games highlighted the requirement for public health interventions for decreasing and sustaining the transmission rates below epidemic levels in the host country to prevent disease transmission during mass gathering events (Borpujari 2021;Linton et al. 2021).
A previous study on the Amir Cup Football Final 2020 supported the phased resumption of football events with spectators in Qatar (Dergaa et al. 2021a(Dergaa et al. , 2021b)).This was allowed by mass COVID-19 vaccination drives across the country, which significantly decreased the risk of COVID-19 transmission among the community.Specifically, the initial COVID-19 National Mass Vaccination Project implemented at Qatar National Convention Center (18 February 2021, to 30 June 2021) administered approximately 628,752 vaccines.However, hosting mass gathering events remains challenging given the varying vaccination rates across countries and the possible emergence of highly transmissible COVID-19 variants (Borpujari 2021).During the first pan-European mass sports event in 2021, which was conducted when the Delta variant was spreading across Europe (Cuschieri et al. 2022), targeted preventive measures crucially contributed to the prevention of disease transmission in the presence of highly transmissible variant(s) and poor vaccination rates among the young population.
Notably, the transmission mechanisms of seasonal influenza and COVID-19 are similar; therefore, analysing both diseases can inform the development of targeted preventative strategies.A previous study on the spread of local seasonal flu during sports events reported an increase in the influenza mortality rate across cities in the United States during the COVID −19 lockdown (Cardazzi et al. 2020).Sporting events are substantially involved in the spread of seasonal flu, which should be considered when formulating policies for sports league reopening (Cardazzi et al. 2020).Moreover, the global decrease in the prevalence of seasonal influenza (Melidou et al. 2020)  However, the impact of football matches with spectators on the spread of COVID-19 infections, as well as the perception of community members regarding football events, remain unclear.This study aimed to assess the risk of COVID-19 and seasonal flu including RSV and influenza (A/B) during the football FIFA Arab Cup 2021 in Qatar, with a return to full spectator capacity.Additionally, we aimed to survey spectators regarding post-event symptoms related to COVID-19 and their attitude towards the resumption of football events during the COVID-19 pandemic.

Study design and participants
A cross-sectional study was conducted during the FIFA Arab Cup 2021 tournament (30 November to 18 December 2021) with full spectator capacity.The tournament comprised of 16 teams and 32 matches were played at six different venues, which will also be used for the upcoming FIFA World Cup 2022.Eligible participants comprised all adult spectators (age ≥ 18 years) who were residents in Qatar, fully vaccinated (2 doses), fully vaccinated with a booster dose (3 doses) or recovered from previous COVID-19 infections and had no history of travel outside the country during and two weeks after the tournament.A total of 545,000 spectators attended the matches; among them, 10,000 spectators were randomly invited to participate in the study through SMS after 7-14 postattendance days.The available vaccines were BNT162b2 (Comirnaty, Pfizer), mRNA-1273 (Spikevax, Moderna) and ChAdOx1-S (Vaxzevria, AstraZeneca).
Figure 1 shows the study communication and testing workflow.Participants were identified from the spectators listed with FIFA ticketing (including phone number and Qatar ID) and matched with the electronic medical records (CERNER), with assistance from the Business Intelligence Unit at Hamad General Hospital.Using a convenience sampling method, we targeted 10,000 spectators based on the study manpower, budget and logistics.Notably, spectators who met the inclusion criteria and were willing to participate in the study received reminders through SMS/phone calls one week, three days, and one day before they visited the designated primary health care centres (PHCC).During the visit, participants underwent realtime reverse-transcription PCR (RT-PCR) testing for COVID-19 and seasonal flu infections (influenza A, influenza B, and respiratory syncytial virus [RSV]) using a single swab.Additionally, participants were asked to complete a selfadministered structured questionnaire regarding demographics, experienced symptoms, and their attitude/safety concerns regarding attending football matches.The questionnaire was sent through an SMS link; moreover, participants who had not completed it earlier were asked to complete it at the PHCC using dedicated tablets with a pre-loaded electronic questionnaire.The primary outcome measure was the incidence of tournament-related COVID-19 and seasonal flu symptoms.The secondary outcome measures were the frequency of COVID-related symptoms and the spectators' attitude towards the resumption of football events during the COVID-19 pandemic.
Participation was voluntary with no incentives or rewards.The study design and protocol (MRC-01-21-936) were approved by the Institutional Review Board Committee of the Hamad Medical Corporation (HMC), which waived the requirement for written informed consent as per 45 CFR 46.102.

COVID-19 PCR and seasonal flu testing
Laboratory analyses were performed at the laboratory facilities of HMC in Doha, Qatar.Before the routine use, the diagnostic assays for COVID-19 PCR testing were pre-validated as per the College of American Pathologists accreditation standards.Regarding seasonal flu tests, diagnostic assays were performed for Influenza A, Influenza B, and RSV.

Diagnostic assays
Universal Transport Medium containing the sample swab was extracted using Bioneer ExiPrepTM 96 Virus DNA/RNA kits (Catalogue No K4614; Bioneer, South Korea) and tested through RT-PCR performed using the TaqPath COVID-19, Flu A/B, and RSV Combo kit (Thermo Fisher, USA), which targeted the SARS-CoV-2 S and N genes; Influenza A/B matrix gene, and RSV A/ B N and M genes, respectively.Thermal cycling was performed on ABI 7500 instruments (Thermo Fisher, USA).
The test results were interpreted based on the amplified target gene's respective cycle threshold (Ct).A COVID-19 PCR test was considered 'positive' and 'reactive' if the Ct value was < 30 and ≥ 30, respectively, and 'negative' if there was no gene amplification.The participants immediately received their COVID-19 test results via the national COVID-19 monitoring phone application (the application is mandatory for all the people living in or visiting Qatar).Additionally, population reference data were extracted from the daily COVID-19 numbers officially reported by the Ministry of Public Health during the study period.The national incidence rate of COVID-19 cases in Qatar was determined as the daily number of PCR-positive cases per 100,000 population based on the entire population of Qatar (2.9 million) before and after the tournament.

Materials
The following data were collected using a structured electronic questionnaire: (a) demographic characteristics, including age, sex, nationality, recovery from SARS-CoV-2 infection, vaccination status for COVID-19 (fully vaccinated with or without booster dose), vaccine name, and laboratory findings, (b) the reporting of post-event COVID-19 symptoms, and (c) the spectators' attitude towards the resumption of football events during the COVID-19 pandemic.

Reporting of COVID-19-related symptoms
COVID-19 related symptoms were assessed using 19 items in the electronic questionnaire and grouped as follows: nose and throat symptoms, chest and other head/neck symptoms, and whole-body symptoms.The participants were asked to respond either yes or no to the symptoms.

The spectators' attitudes towards the resumption of football events
The spectators' attitude towards the resumption of football events during the COVID-19 pandemic was assessed using a 12-item electronic questionnaire, which took approximately 15 minutes to complete.This questionnaire was adopted with several modifications from the Innovative Institute for Fan Experience (https://www.surveymonkey.com/r/WV65HCB) and a recent published study (Takamatsu 2021).It implemented a five-point Likert scale (1 = strongly disagree, 5 = strongly agree).Additionally, a reliability test based on Cronbach's alpha was performed to check measurement stability and ensure no contradiction between the survey's outlines.The reliability test confirmed the reliability of the instrument's model with a Cronbach's alpha value of 0.802, indicating a good level of internal consistency.

Statistical analysis
Continuous data are presented as mean and standard deviation while categorical data are expressed as frequency and percentage.The number of participants and the corresponding percentage were calculated for each questionnaire item.Chisquare test was performed for the analysis of differences in COVID-19 test findings (categorical variable) between spectators fully vaccinated vs. fully vaccinated with booster dose and symptomatic vs. asymptomatic spectators.The continuous variable (Ct value) between fully vaccinated vs. fully vaccinated with booster dose was compared using student's t test and a two-tailed p value < 0.05 was considered as significant.Microsoft Excel was used for data entry, editing, and sorting.Graphs were plotted using GraphPad Prism software.Statistical analyses were performed using Statistical Package for the Social Sciences 21.0 (SPSS Inc.USA).This study follows the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist (Supplementary file).

Results
The survey (COVID-19, RSV and Flu testing and questionnaire) was conducted between 7 December 2021, to 3 January 2022.Among the 10,000 invited spectators, a total of 6,475 agreed to participate in this study (response rate = 65%).Table 1 presents the demographic characteristics of the participants.Among 6,475 participants, 41.9%, 85.0%, and 97.7% were aged ≥ 40 years, males, and expatriates, respectively.All participants were fully vaccinated with 2 doses (n = 4,195), fully vaccinated with booster dose (n = 2253) or recovered from previous COVID-19 infection (n = 27).After the match, follow-up for COVID-19 infections was tested by using PCR (n = 6,475); symptom screening was conducted over a period of 14 days.
Table 3 presents the item responses regarding the spectator's attitudes toward the resumption of football events during the COVID-19 pandemic.Among the participants, 42% and 40% agreed and strongly agreed, respectively, that they were satisfied with the current tournament-organizing committee and/or venue facilities.Moreover, 47% and 24% of the participants agreed and strongly agreed, respectively, that it is safe to attend matches in stadiums during the COVID-19 pandemic.A minority of the participants (~2%) were still not comfortable with attending matches in stadiums.Moreover, most participants (94.3%) were optimistic about the return of sports to the pre-pandemic status.

Incidence rate of COVID-19 cases
Figure 2 shows the annual trend of diagnosed COVID-19 cases in Qatar per 100,000 population.Figure 3 shows the daily incidence rate of COVID-19 cases (a) prior to the event, during the event and up to two weeks post-event.The incidence rate was estimated per 100,000 of the population of Qatar (the total population of Qatar is around 2.9 million residents).One week before the tournament started, the average incidence of newly diagnosed COVID-19 cases in Qatar was 5 per 100,000 population (Figure 3a), which increased to 5.41 per 100,000 population on the first tournament day (30 November 2021) (Figure 3b).This number remained steady, with a slight increase to 6 per 100,000 population at the end of the tournament (18 December 2021).During the study period, the average incidence rate of COVID-19 positive cases in Qatar was recorded as 5.6 per 100,000 population.The average incidence rate of newly diagnosed COVID-19 cases two weeks after the event (extended to January 2022) showed a gradual spike to 11.02 per 100,000 population (Figure 3c). Figure 4 summarizes the study design and results including the post-event follow up (Arab Cup-2021) for RT-PCR, virology panel testing and self-reported symptom among the spectators.

Discussion
This study described the first FIFA regional (including 16 teams from 16 Arab countries) football tournament in the Middle East that has been undertaken in stadiums with full capacity of spectators during the COVID-19 pandemic.During the later phase of the COVID-19 pandemic, several professional sports leagues decided to resume sports events.Some events allowed a small number of spectators (Pedersen et al. 2021;Toumi et al. 2021;Dergaa et al. 2021b), with concerns being raised that they would be "super spreader' events (Bond et al. 2020;Carmody et al. 2020;Ruiz-Lozano et al. 2020;Sassano et al. 2020).However, the impact of the attending spectators on the local incidence rate of COVID-19 remains unclear.
Currently, professional soccer leagues have been successfully resumed during the pandemic, without substantial COVID-19 transmission.In Germany, the resumption of the professional soccer league has suggested that football matches can be safely played during a pandemic, even with a high burden of viral transmission within the general population (Meyer et al. 2021;Schumacher et al. 2021).Data from the US National Football League in 2020 suggested that professional sports can be safely conducted (Mack et al. 2021).
In our study, 61 (0.9%) spectators tested positive for COVID-19, with all of them being fully vaccinated or having recovered from previous COVID-19 infections.This could be attributed to the fact that the tournament was held when the epidemiological landscape of the COVID-19 pandemic was changing.Specifically, countries were relaxing their mitigation measures and allowing increased cross-country mobility, with ongoing COVID-19 vaccination drives.Moreover, the highly transmissible Omicron  Worldwide, mask mandates were being removed, especially among vaccinated individuals, with masks being among the effective non-pharmacological interventions for reducing the spread of COVID-19 (Brooks and Butler 2021;Bundgaard et al. 2021).Additionally, increased migration across countries increases the incidence rate of COVID-19 (Linka et al. 2020).We observed a gradual increase in the COVID-19 cases (11.02 per 100,000 population) two weeks after the event.However, this spike could be attributed to increased crosscountry mobility during the winter holidays and the possible emergence of the Omicron variant.
COVID-19 mitigation strategies in stadiums are limited by several factors such as the presence of high number of spectators, seating proximity, and the possibility of high contact level among spectators and also among athletes in the field.Some investigators González-Val andMarcén 2022 andCardazzi et al., 2020) have determined the impact of sporting events as super spreaders.González-Val and Marcén 2022 found that massgathering events during the pandemic in Spain led to approximately 31% increase in the daily reported COVID-19 cases per 100,00 people.A previous Danish study reported that although COVID-19 transmission was linked to matches held at stadiums with spectators, the infectivity rate could not be classified as a 'super spreader'(dk 2022).Moreover, studies reported a general spike in the COVID-19 positivity trend following a week of EURO2020 matches across most countries and host cities (Marsh et al. 2021;Cuschieri et al. 2022).
However, we did not observe a similar trend after the FIFA Arab Cup 2021, which might be attributed to the fact that all the spectators were fully vaccinated, and they followed mandatory face mask wearing throughout the tournament.Nonetheless, COVID-19 transmission can still occur even with the various mitigation measures and among vaccinated individuals (Subbaraman 2021;Chen et al. 2022;Kuhlmann et al. 2022), especially with non-adherence to basic measures of personal hygiene and mask-wearing (Breidenbach and Mitze 2021;Schmitt and Wang 2021).
In our study, those who were fully vaccinated with an additional booster dose were less likely to acquire breakthrough COVID-19 infection as compared to fully vaccinated spectators (two shots of vaccine) without booster which might not have lasting protection against infection.This could be attributed to the fact that a booster dose enhances the immunity averting serious illness and may help prevent breakthrough COVID-19 infections.
A recent study (Accorsi et al. 2022) showed that for both Delta and Omicron strains of COVID-19, the median Ct values were considerably higher among individuals who received 3 doses of mRNA COVID-19 vaccine as compared to 2 doses.Consistent with these observations, the Ct value was nonsignificantly higher among fully vaccinated spectators with booster dose as compared to fully vaccinated individuals in our cohort.Recent studies have reported atypical clinical manifestations of some COVID-19 cases which remain asymptomatic despite positivity (Mei et al. 2020).Our findings suggest that COVID-19 positivity rate is higher among the symptomatic spectators than those who remains asymptomatic.Toumi et al.,2021 andChen et al. 2022 reported that games held with limited in-person attendance did not lead to a consistent increase in the daily COVID-19 cases per 100,000 USA residents.
Additionally, we investigated the impact of professional sporting events on local infection rates of seasonal influenza and RSV during the event.Previous studies have demonstrated that sports-related mass gatherings were associated with a spike in influenza infections during the 2006 winter Olympics andFIFA 2006 World Cup (Gundlapalli et al. 2006;Williams et al. 2009).However, we observed a very low incidence rate (proven infections or possibly seroconversions) of seasonal respiratory viruses [0.2% Influenza (A/B) and 0.6% RSV].
The future of sports involving spectators remains uncertain given the observed situation resulting from the emergence of novel COVID-19 variants.Nevertheless, on March 2022, 88.6% of the Qatar population aged ≥ 16 years had already received two vaccine doses with > 6.5 million jabs administered National Covid-19 Vaccination Program Data, Ministry of Public Health (MOPH) 2022.In our study, 71% and 87% of the spectators felt safe attending matches in stadiums and were optimistic about sports returning to the pre-pandemic state, respectively.The vaccination program could facilitate events such as the one discussed in our study.This could ensure safety and allow fans to psychologically overcome hesitations about being in mass gathering events after such an extended period of social isolation.

Implications of the study findings with reference to the upcoming FIFA World Cup 2022, other mass events and football tournaments
Our findings demonstrated the importance of a holistic approach to reopening public events during or following a major infectious disease outbreak at the national level.This study provides evidence that the large numbers of vaccinated fans at the FIFA Arab Cup 2021 games did not lead to a substantial spike in the incidence of local COVID-19 cases.The protocols and policies implemented by the ministry of public health (MoPH) can be applied to other sports events involving mass gatherings, including the next FIFA World Cup.Relaxation of mitigation measures, especially the lack of social distancing and mask-wearing, increases the risk of transmission, even among vaccinated individuals.Our findings demonstrate that policymakers should consider implementing preventive measures (mask-wearing, a mandatory COVID-19 vaccination certificate showing a second/booster dose within 6 months or a recent COVID-19 infection certificate) during the upcoming FIFA World Cup.Given the limited evidence regarding the long-term immunity persistence in either vaccinated or previously infected individuals, the measures could further reduce the rate of COVID-19 infection during mass gathering events.It is important to consider the possibility of highly transmissible variants when formulating policy and implementing mitigative measures.This is because even in countries where the surge of COVID-19 infections has initially been contained, there has been a subsequent wave of new infections involving new strains (Salyer et al. 2021;Accorsi et al. 2022).In such a scenario, robust infection mitigation measures are necessary to allow the safest possible environment for allowing spectators in professional football.It was demonstrated that mass events like football tournaments can be played and carried out without an increased incidence rate of COVID-19.This was most likely due to the high vaccination rate of spectators and players.

Limitations
To the best of our knowledge, this is the first study evaluating the effect of allowing fully vaccinated and COVID-19-recovered spectators to attend an international mass football event during the COVID-19 pandemic.However, there are several limitations.First, we could not determine the cause-effect relationship between the spectator who attended matches and the increase in cases over the following weeks.Specifically, we could not determine whether the increase in COVID-19 cases was directly due to spectators' attendance at the stadium, tailgating around the stadium, or individuals congregating in their homes with family and friends.Our study design could not identify causative and confounding factors contributing to the COVID-19 situation.The use of a threshold of Ct 30 to distinguish between infected and non-infected individuals could be a debatable aspect in our analysis.In fact, this threshold is typically interpreted as indicator for contagiousness but not for infection status.Future studies may be warranted to assess the effects of these various protocols in other mass gathering sport events to determine their effectiveness for implementation in future public health scenarios.

Conclusions
The FIFA Arab Cup 2021 represented the first event in Qatar where fully vaccinated spectators could enter stadiums with full operational capacity.Our findings demonstrated that this event was not associated with increased COVID-19 cases in local settings.It is important to resume important sports activities without causing a spike in COVID-19.Notably, our findings demonstrate the important policy-related recommendations that can be implemented to allow safe return to other sporting and large-scale entertainment events.

Disclosure statement
No potential conflict of interest was reported by the author(s).

Funding
The author(s) reported there is no funding associated with the work featured in this article.No funding is associated with this study.
and respiratory syncytial virus (RSV)(Di Mattia et al. 2021) during the COVID-19 pandemic could be attributed to mitigation measures for SARS-CoV-2 transmission.According to reports from the United States, the United Kingdom, Italy, Finland, and Belgium the RSV epidemic season declined abruptly with implementation of COVID-19 restrictions in March 2020 (Di Mattia et al. 2021).
variant was rapidly spreading across Europe, Africa, and Asia, with vaccinated individuals showing less protection against the Omicron variant (Brandal et al. 2021; Espenhain et al. 2021; Mallapaty 2021; Subbaraman 2021; Eggink et al. 2022).Similar circumstances applied to Qatar, which experienced a SARS-CoV-2 Omicron wave that peaked in mid-January 2022 and began on 19 December 2021 (Chemaitelly et al. 2022; National Project of Surveillance for Variants of Concern and Viral Genome Sequencing 2022).

Figure 2 .
Figure 2. The annual trend of diagnosed COVID-19 cases in Qatar per 100,000 population.

Figure 3 .
Figure 3.The daily incidence of COVID-19 cases (a) prior to the event, (b) during the event and (c) up to two weeks post-event.The incidence was estimated per 100,000 of Qatari population (2.9 million residents).

Figure 4 .
Figure 4. Schematic of the study design and results including the post-event follow-up (FIFA Arab Cup-2021) for RT-PCR, virology panel testing and Self-reported symptoms among spectators.

Table 1 .
Demographic characteristic and post event COVID-19, seasonal flu related information of the spectators (n = 6475).
*373 participants did not fully complete the self-administered symptom reporting