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Introduction
Data from the United Nations World Tourism Organization (UNWTO), indicated that tourism before the COVID-19 pandemic involved 1.5 billion international tourist arrivals worldwide. In addition to generating millions of direct jobs, tourism was the third most important sector in terms of exports, representing a worth of around 1.7 trillion dollars, thus being one of the fastest growing sectors in both advanced and emerging economies However, UNWTO estimates that between January and October 2020, international arrivals worldwide contracted up to 72 %, representing a loss of around 900 thousand tourist arrivals, while the economic impact is estimated in about 10 times greater than those caused by the 2009 global crisis, since the loss of direct jobs in this industry was then estimated between 100 and 120 million (UNWTO, 2021)
Data published by Oxford Economics showed that academic and business meetings tourism in 2017 represented around 1'500,000 million participants, who attended different tourist destinations in 180 countries, generating approximately 25.9 million of direct and indirect jobs (Oxford Economics, 2018). In the case of Mexico, in 2019 it was estimated that meeting tourism generated nearly 900,000 jobs and occupied 30 million rooms/night, which represented 18.8 % of the national occupancy; while the expenditure made by travelers to meetings was 94 % higher, compared to the vacation tourism. However, as of September 2020, it was estimated that in Mexico meeting tourism had lost revenues of about 11 billion (USD), as well as the loss of 408,000 jobs; it is estimated that in the first six months of the year 109 thousand events were cancelled, 12 million people stopped participating in mass events and 10 million rooms/night were not occupied (Alegria, 20021)
Pillai et al. (2021) suggest that the application of hygienic measures, cleanliness and safety protocols implemented in hotels have been important factors in the recovery of previous epidemics and pandemics. In addition, highlight the advantages in the use of diagnostic tests to detect SARS-CoV-2, as part of public policy not only to reduce the number of victims of infection, but also as a measure to mitigate the economic deprivation associated with the closure of businesses and establishments such as restaurants and hotels (De Walque, et al., 2020)
Nowadays, the most reliable method to know if a person is infected with the SARS-CoV- 2 is through the application of the qRT-PCR diagnostic test, which is based on the amplification of viral genes from nasopharyngeal swab samples of potentially infected individuals; Notwithstanding the above, this individualized molecular strategy is expensive and requires that the sample collection is performed by specialized personnel. Therefore, our research group validated and implemented a massive molecular diagnostic test based on the detection of SARS-CoV-2 using saliva as a suitable sample source. (Girón-Pérez et al., 2021)
The application of a massive strategy for the molecular detection of SARS-CoV-2 through saliva pools, firstly, allows reducing costs and permits to make viral detections to large groups of people, in addition to provide a reliable diagnostic tool to people belonging to groups that, for work, recreation, tourism or any other massive activity, need to concentrate in certain physical spaces.
The detection of SARS-CoV-2 through saliva has been analyzed in several works, in a court of 95 patients, where nasopharyngeal and saliva (deep throat) samples were analyzed, where no differences were found using both types of samples, as well as variations in the Cycle threshold (Ct) value are not affected (Leung et al., 2021) Furthermore, the detection of SARS-CoV-2 can be detected in patients with symptoms and asymptomatic in patients, so this should be an alternative for the detection of SARS-CoV-2 (Leung et al., 2021)
A meta-analysis of different studies for the detection of SARS-CoV-2 has revealed that the use of saliva pools has a sensitivity of 83.2 % and a specificity of 98.2 %, suggesting that this strategy should be considered for mass sampling in communities (Butler-Laporte et al., 2021). Therefore, saliva pools are a useful approach to stop the transmission chains in different workplaces or recreational settings.
The aim of this paper was to implement a strategy for mass molecular detection of SARS-CoV-2 in the saliva of people who attended the tourist complex, to provide evidence that no one was infected during the event. Hence, the use of this protocol allows decreasing costs in diagnostic tests and contributes to economic reactivation associated with the tourism industry
Material and Methods
Study model
In the present research, 120 people were analyzed (58 men and 62 women) with an average age of 22 years, wherein any of the tested individuals presented symptoms related to COVID-19. Participants stayed at the Nuevo Vallarta resort from November 4 to 6, of 2020.
The employed strategy was the analysis of 12 pools of saliva (10 individual saliva samples were mixed) before (1 day) and after staying at the resort (5 days) using the Real-Time Quantitative Reverse Transcription PCR (qRT-PCR) technique approved by the “Instituto de diagnóstico y referencia epidemiológica” (Indre) based on the Berlin protocol (Corman et al., 2020).
Saliva samples were collected by depositing the saliva sample in a sterile container, which was performed in the laboratory facilities, under the supervision of laboratory members (with a minimum volume of 2 mL), the patients were required to attend without previous oral hygiene and without lipstick, in order to avoid contaminating the samples. The saliva samples were correctly labeled and pools were made (of a minimum of 6 and a maximum of 10 persons) of which 14 µL was placed in a 1.5 mL Eppendorf tube, 10 saliva samples were then mixed each other to create a pool, the methodology used was previously reported by Girón-Pérez et al. (2021) The PCR test result was delivered on the same day of sample collection. In all cases, human gene (RNAseP) amplification was used as the internal control. The plasmid pT7 S10 RRV (containing the fragments of the genome encoding the E gene) was used as control.
Model interpretation
Negative detection of the SARS-CoV-2 virus occurs when the E gene is not amplified or is detected above cycle 38, meaning that none of the individuals included in the saliva pool is a SARS-CoV-2 carrier. On the other hand, when gene E is amplified below cycle 38, it indicates that at least one individual is positive and therefore, each saliva sample must be individually tested to identify the infected person.
Hotel sanitary measures
The use of face masks in common areas (bars, restaurants, event rooms) in addition to hand sanitization using hydroalcoholic gel, placed in common areas (reception, lobby, rooms and other common spaces), was required. In addition, the maximum capacity of the hotel (1300 people) was reduced to 50 % (the hotel allowed only 650 people), which emphasizes the relevance of preventive measures for the creation of safe environments and the potential economic reactivation in this sector, at least partially
Results
Obtained data indicate that all participants attending the mass event were not carriers of the SARS-CoV-2 prior to arriving, as well as ensuring that during the event, the participants were not infected with the virus causing COVID-19 (Table 1).
Table 1 Results of tourist in hotel resort
| No of person/No of Pools | Date of Sample | Results |
|---|---|---|
| 120/12 | Before of travel (November 3th 2020) | Negative pools |
| 120/12 | After of travel (November 11th 2020) | Negative pools |
The E gene amplification curves of the individuals who attended the resort, as well as experimental controls are shown in Figure 1.
For SARS-CoV-2 as measured both before and after arriving at the event, indicating that this model is a helpful tool for monitoring large groups of individuals for SARS-CoV-2.
Discussion
The use of saliva for SARS-CoV-2 detection has been extensively analyzed in several studies (To et al., 2020; Pasomsub et al., 2021; Williams et al., 2020) showing that it is a reliable source for obtaining the virus and can be used as an alternative source; in addition, the sensitivity ranges from 81 %-99 %, which is indispensable to break viral chains of contagion (Braz-Silva et al., 2021).
This strategy can be used for the reactivation of the tourism industry worldwide due to the fact that this strategy significantly decreases the molecular testing associated cost, since as mentioned, in this case 12 qRT-PCR reactions allowed the analysis of 120 people, obtaining affordable, reliable and sensitive results. In addition, the application of this massive test also permits to discard asymptomatic carriers of the virus, who, even not showing signs and symptoms of COVID-19, are able to transmit the pathogenic agent to other individuals.
The application of sanitary measures is imperative for the reactivation of tourism in Mexico and worldwide, including hand washing and the use of hydroalcoholic gel (with ethanol) are recommended by the Center for Disease Center (CDC), since both can eliminate several kinds of pathogens and exert virucidal activity; Additionally, the reduction in hotel capacity may be an option to ensure safe places to vacation (Berardi et al., 2020). The use of a face mask is mandatory, since it avoids the passage of particles and sprays generated from the respiratory tract, promotes physical distancing, and reduces the rate of virus transmission (Howard et al., 2021).
The SARS-CoV-2 detection and the application of sanitary measures should continue to be applied despite the vaccination process, since immune protection after vaccination could be partial, and given that the emergence of new variants of COVID-19 has been reported, thus the vaccinated person still has the potential to transmit and spread the virus. Likewise, there are new variants of the SARS-CoV-2, on which available vaccines may not be effective (Delta-variant) (CDC, 2021).
Saliva pools have been widely proposed as a model to expand the sampling capacity for SARS-CoV-2 detection; besides having advantages due to the fact that it is non-invasive, it has a very high sensitivity (Huang et al., 2021); however, one of the negative aspects is that the sensitivity decreases depending on the time the sample is processed.
The temporality is one of the reasons for the lack of approval by the Food and Drug Administration (FDA) (US, FDA 2020), as well as the lack of an adequate viral transport medium (to maintain this sensitivity). The implementation of pools should be carefully planned, since small pools smaller than 11 indicate a low percentage of false positives (2 %), while larger pools (larger than 11 pools) the error is close to 14 % (Watkins et al., 2020).
In conclusion, the use of the saliva pool strategy for the mass detection of SARS-CoV-by PCR allowed the monitoring of individuals on a quick and economical basis, which, together with the follow-up of established sanitary measures, can contribute to the reactivation of the tourism industry
Study limitations
The most important limitation is the type of patient, since we only have access to ambulatory patients (it is not a heterogeneous group), also more age groups are missing, since the patients are between 18 and 25 years old (young); likewise, the symptomatology (respiratory diseases, bacterial infections) was not taken into account, which can affect the amount of enzymes (RNases), the number of cells or if it has the presence of bacteria. The strengths of this work is to set up a sensitive, fast and safe methodology; besides, it can be implemented in universities or work centers.
