key: cord-0884292-5hstpvat
authors: Muscat Baron, Y.
title: Atmospheric PM2.5 before and after Lockdown in relation to COVID-19 Evolution and daily Viral Counts: Could Viral Natural Selection have occurred due to changes in the Airborne Pollutant PM2.5 acting as a Vector for SARS-CoV-2?
date: 2021-01-11
journal: nan
DOI: 10.1101/2021.01.10.21249548
sha: 93f4ddb9d122edd80924e5774ef1721a2ca8d8b4
doc_id: 884292
cord_uid: 5hstpvat

Background: Genes coding for SARS-CoV-2 have been detected on the microscopic airborne pollutant particulate matter, which has been suggested as a vector for COVID-19 transmission. Lockdown in China has been shown to be associated with significant reduction in pollution including the particulate matter component which coincided with the appearance of a viral mutant (Clade G) which steadily displaced the original Clade D after lockdown. The reason why Clade G developed a fitness advantage is as yet unknown. This paper examines the possible role of airborne particulate matter PM2.5 as selective pressure determining viral Clade predominance and further shedding light on the mode of SARS-CoV-2 transmission. Methods: The average levels of PM2.5 of a number of cities were obtained from the Air Quality Index (AQI), a real-time assessment of atmospheric pollution. The daily average PM2.5 levels were assessed between January 23rd and April 29th 2020 determined by the timeline when viral counts in Beijing and other cities were available. Daily viral counts of Clades D and G were available starting from the 12th February as determined by the scientific literature published in August 2020. The cities chosen were Beijing, Sheffield, Nottingham, Sydney and Cambridge because of their substantially elevated viral counts compared to other cities. Cities as opposed to vaster areas/nations were chosen as PM2.5 levels vary across regions and countries. Results: For the time period assessed, the Beijing PM2.5 pattern initiated with highly elevated mean PM2.5 levels of 155.8mug/m3 (SD+/-73.6) during high viral counts, followed by 82.1mug/m3 (SD+/-44.9) (p<0.04) when the viral counts decreased. In all the other cities assessed, the pattern differed whereby the PM2.5 levels increased significantly over the preceding baseline contemporaneously with the viral count rise. The changes in these cities PM2.5 levels were on average 31.5mug/m3 before viral counts rose and 56.35mug/m3 contemporaneous with viral count rise. The average levels of PM2.5 in these cities started to decrease one week after lockdown to 46mug/m3 when measured over 2 weeks post-lockdown. As regards the viral counts from data retrieved from Beijing, the latter part of the bell-shaped curve and a subsequent smaller curve of the viral count was available for evaluation. The average viral count for Clade D in Beijing was 11.1(SD+/-13.5) followed by a mean viral count for Clade G was 13.8(SD+/-9.2). Conversely in all the other cities besides Beijing, the viral counts averaged 45.8 for Clade D and 161 for Clade G. The variation in viral counts between cities suggests the strong possibility of variation in the availability of sampling between cities. The newer variant, Clade G demonstrated viral counts initially appearing in mid-February in Beijing to later displace Clade D as the dominant viral Clade. The appearance of Clade G coincided with the decreasing gradient of PM2.5 levels. A number of significant correlations were obtained between PM2.5 levels and the viral count in all the cities reviewed. Conclusion: COVID-19 viral counts appear to increase concomitant with increasing PM2.5 levels. Viral counts of both Clades correlated differentially with PM2.5 levels in all the cities assessed. The significantly highly elevated PM2.5 levels in Beijing resulted in correlating mainly with Clade D, however Clade G began to appear with decreasing PM2.5 levels, suggesting the beginnings for the initial SARS-CoV-2 Clade evolution. Clade G, the newer variant was able to flourish at lower levels of PM2.5 than Clade D. Clade G may possibly have utilized other sources of particulate matter as a viral vector, such as that derived from tobacco smoking, whereby 66% of Chinese males are smokers and 70% of the Chinese non-smoking population are exposed to 2nd hand smoking. Keywords: COVID-19; PM2.5; Vector; Viral counts; Clade Evolution; tobacco smoking;

For the time period assessed, the Beijing PM2.5 pattern initiated with highly elevated mean PM2.5 levels of 155.8µg/m3 (SD+/-73.6) during high viral counts, followed by 82.1µg/m3 (SD+/-44.9) (p<0.04) when the viral counts decreased. In all the other cities assessed, the pattern differed whereby the PM2.5 levels increased significantly over the preceding baseline contemporaneously with the viral count rise.

The changes in these cities' PM2.5 levels were on average 31.5µg/m3 before viral counts rose and 56.35µg/m3 contemporaneous with viral count rise. The average levels of PM2.5 in these cities started to decrease one week after lockdown to 46µg/m3 when measured over 2 weeks post-lockdown.

As regards the viral counts from data retrieved from Beijing, the latter part of the bellshaped curve and a subsequent smaller curve of the viral count was available for evaluation. The average viral count for Clade D in Beijing was 11.1(SD+/-13.5) followed by a mean viral count for Clade G was 13 COVID-19 infection has reappeared in most countries, the recrudescence delineated as the "2nd wave". This increase has been attributed to the reversal of certain measures endorsing social distancing which was legally enforced in most countries affected. Concomitant with the increase in COVID-19 infection incidence, the previous reduction in atmospheric pollution following national and regional lockdowns has been shown to have been partially reversed. This reversal also involved a recrudescence of elevated levels of the pollutant particulate matter PM2.5.

In the United States, a nationwide study by Wu et al 2020 indicated a link between long-term exposure to particulate matter PM2.5 and COVID-19 related mortality. 1 Genes coding for SARS-CoV-2 have been found to be adherent to particulate matter. 2 A study of a large number of Chinese cities demonstrated a 2% increase in COVID-19 new cases, with every 10μg/m3 increase in atmospheric PM2.5. 3 A paper by Comunian et al (2020) suggested that through two avenues, particulate matter may encourage COVID-19 infection and transmission. 4 The first avenue suggests that the deleterious effects of particulate matter on pulmonary microbial defences encourage COVID-19 to colonize and infect the respiratory system. The second suggests that particulate matter may actually act as a vector for transmission of COVID-19

infection.

This paper examines the possibility that pollution changes catalyzed COVID-19 infection and also its evolution, strengthening the hypothesis that particulate matter may act as a vector and co-factor for the Coronavirus Pandemic.

The average levels of particulate matter PM2.5 of a number of cities were obtained from the Air Quality Index. The Air Quality Index is a real-time measurement of atmospheric pollutants, including PM2.5. 5 The daily average PM2.5 levels were assessed between January 23rd and April 29 th 2020 determined by the timeline when viral counts in Beijing occurred. The 23 rd January 2020 was chosen as a starting point when the lockdown was implemented in the Hubei Province of which Wuhan is the principal city. April 29 th was the day when the viral count in all cities chosen had decreased significantly.

Daily viral counts of Clades D and G were obtained from a paper by Korber et al. 6 This paper obtained viral samples from a large number of centres across the globe in varying numbers. The cities chosen were Cambridge (U.K.), Sheffield (U.K.), Nottingham (U.K.), Sydney (Australia) and Beijing (Temple of Heaven) because of their substantially elevated viral counts compared to other cities. The substantial number of viral counts reduced the error from sampling bias. Cities as opposed to . 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. (which was not certified by peer review)

The copyright holder for this preprint this version posted January 11, 2021. ; https://doi.org/10.1101/2021.01.10.21249548 doi: medRxiv preprint vaster areas were chosen as particulate matter PM2.5 levels vary across regions and countries.

The daily viral counts of Clades D and G obtained from the paper by Korber during elevated viral counts. When the viral counts in Beijing decreased, the PM2.5 also decreased by a margin of 36% to 82.1µg/m3 (SD+/-44.9) (p<0.04).

In the British cities and in Sydney, the pattern differed from that of Beijing, whereby the PM2.5 levels increased significantly over the preceding baseline concomitant with . 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 levels of PM2.5 in these cities altered after regional and national lockdown. The levels of PM2.5 in these cities decreased significantly one week after regional and Table 1 . . 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 January 11, 2021. ; Viral counts varied between the five cities included in this study. As regards the viral counts from data retrieved from Beijing, the latter part of the bell-shaped curve and a subsequent smaller curve of the viral count was available for evaluation. The average viral count for Clade D in Beijing was 11.1(SD+/-13.5) followed by a mean viral count for Clade G was 13.8(SD+/-9.2). Conversely the initial full bell-shaped curves of viral counts were available for the cities of Sheffield, Nottingham, Sydney and . 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 January 11, 2021. ; Similar significant correlations were obtained when the PM2.5 was compared with viral counts assessed a week later. This exercise was done to allow for the viral incubation period to take root. In the case of Cambridge the correlation between PM2.5 and the Clade G viral count one week later was significant (R=0.62 p<0.002).

The data was analysed for normality and all the data were found to be nonparametric.

The Mann Whitney U test was applied for comparing nonparametric variables of both groups of cities and the Spearman Rank test was applied for nonparametric correlations.

Earlier this year the genome of COVID-19 was sequenced and was found to consist of a single RNA strand containing approximately 30,000 purine and pyrimidine bases.

Following the first sequence more than 100,000 SARS-CoV-2 genomes have been sampled indicating that over 13,000 mutations have occurred over a period of nine months. 7 The rate of genomic modification for SARS-CoV-2 has been estimated to occur around twice a month, significantly lower than that of Influenza virus. 7 Through these mutations, there exists the possibility of natural selection occurring as an adaptation to the environmental milieu, including the atmospheric levels of particulate matter. This . 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 January 11, 2021. ; https://doi.org/10.1101/2021.01.10.21249548 doi: medRxiv preprint may be of singular importance if particulate matter is proven to be a vector for COVID-19, especially if the particulate matter implicated originates from tobacco smoking. 8, 9 A prominent mutation that has dominated the COVID-19 genomic landscape involves the viral spike protein gene at D614G position. The D614G mutation involves a single genomic alteration with the replacement of aspartic acid by glycine at the amino acid D614 position of the spike protein. In vitro, the D614G mutation has demonstrated increased cellular infectivity, however this does not seem to be consistently the case in vivo. 7 The modification in the Clade genome appears to result in an alteration in the phenotype of the spike protein peptide configuration. The original Clade D has its spike protein's three peptides aligned in a "closed" configuration whereas the Clade G spike protein peptides are consistently found in an "open" orientation. 10 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 January 11, 2021. ; https://doi.org/10.1101/2021.01.10.21249548 doi: medRxiv preprint receptor-binding domain of the COVID-19 Spike protein and the angiotensin II receptor. 12 Consequently, the salt and water content of the viral environs, including a potential vector, may be relevant to the viral pathogenic behaviour.

This review indicated that prior to the viral count increase, the PM2. . 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 January 11, 2021. ;

Following the January 2020 lockdown in China, there was a steady decline in airborne particulate matter due to the diminution in the incineration of coal. 13 Coal consumption in China decreased by approximately 50% following lockdown, from 80 thousand tonnes daily to 40 thousand tonnes per day and consequently was associated with a reduction in atmospheric pollution. 14 All three cities demonstrated an elevated reproduction number (R 0 ) confirming a high transmission rate. 14 Comparing COVID-19 to the Influenza virus, at its zenith the R 0 of the H1N1 influenza is 1.4-1.6 while that of COVID-19 was 5.7 at its peak to settle to 3.28. 16, 17 This elevated R 0 may suggest that there may be another variable accelerating COVID-19 transmission besides human to human transmission.

A characteristic common to the three cities of Wuhan, Qoms and Bergamo, was the elevated atmospheric levels of particulate matter. 15 Research from the Italian city of Milano detected COVID-19 genes present on particulate matter. 2 This study showed that compared to control air samples of particulate matter, 34 RNA extractions for the . 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 January 11, 2021. 

The highest concentration of particulate matter humans are exposed to in a short period of time is during tobacco smoking. 19 With more than 66% of Chinese males smoking and 70% of the non-smoking population exposed to 2 nd hand smoking, 20 it may well be that the Clade G found a favourable pabulum for COVID-19 transmission and infection through carriage on particulate matter derived from tobacco smoking. 15 The rate of smoking in adults in the other cities besides Beijing is significantly lower: Cambridge 17.7%, Sheffield 13.9%, Nottingham 20.9%, Sydney 10.5%. 21, 22 This to some extent may explain the significant differential correlations obtained between PM2.5 and both viral Clade counts between all four of these cities.

. 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 January 11, 2021. ;

The adverse effects of particulate matter PM2.5 on respiratory health have been well demonstrated in the scientific literature. 23 Particulate matter settling in the lung creates free radicals causing oxidative stress on the respiratory epithelium. 24, 25 Alveolar macrophage cell oxidative stress occurs with exposure to the metallic components of subway PM2.5. 26, 27 Cellular infiltrates follows particulate matter lung exposure resulting in an increase in pulmonary infiltration with neutrophils, eosinophils, T cells and mastocytes. 28, 29 This consequent pulmonary cellular infiltrate can escalate into a cytokine storm which has been implicated in a significant number of SARS-CoV-2 related deaths. 30 Besides the deleterious effect of particulate matter on anti-microbial respiratory defences and the potential carriage of SARS-CoV-2, there may also be synergism between PM2.5 and the COVID-19 exacerbating lung pathology. 15 Inhaled particulate matter can result in pulmonary pathology by causing severe inflammatory reaction in lung tissue. Particulate matter appears to influence the renin-angiotensin system which modulates pulmonary inflammatory response. In preclinical studies, lack of angiotensin converting enzyme II was associated with delayed lung repair following PM2.5 induced injury. 31 The pulmonary port of call for SARS-CoV-2 appears to be the angiotensin converting enzyme II receptor on respiratory epithelial goblet cells. 32 Tobacco smoking results in an increase in pulmonary goblet cells which in turn increase angiotensin converting enzyme II. 33 Animal studies have shown that PM2.5 caused vascular oxidative stress in the pulmonary vasculature and heavy metal enhanced protein expression in the pulmonary arterial system. 34 The finding of COVID-19 genes on particulate matter . 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 January 11, 2021. ; https://doi.org/10.1101/2021.01.10.21249548 doi: medRxiv preprint may suggest that the PM2.5/COVID-19 complex is a potential independent pathological entity. Both components of the PM2.5/COVID-19 complex may act in concert to accelerate pulmonary pathology both in the lung parenchyma and vasculature. 15 The adverse health effects of particulate matter derived from tobacco smoking and 2 nd hand smoking are well established. 35, 36 A study has indicated that USA States with lower restrictions on smoking in public and a higher percentage of the smoking population had a 23% higher incidence of SARS-CoV-2 infection rates than States with more restrictive smoking bans and lower percentage smoking populations. 37

Particulate matter possesses several species differentiated by their elemental composition. The PM species' components are determined by particulate matter environmental origins. 38 Similarly particulate matter water content is differentially determined by particulate matter's main hydroscopic salt components of sodium chloride, ammonium nitrate and ammoniated sulphate. 38 The ratio of these salts depends on the environmental origin of the particulate matter e.g. particulate matter close to the sea has a higher proportion of sodium chloride. Pulmonary pathology may be exacerbated by the PM predominance of ammonium nitrate and ammoniated sulphate salt components which are certainly more toxic than sodium chloride. 34 The presence of sodium chloride in the respiratory tract assists in pulmonary anti-. 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 January 11, 2021. ;  microbial defences making bronchial mucus less viscous, encouraging epithelial cleansing ciliary movement. 39 Particulate matter may have had a bearing on the different geographical distribution between the 1 st and 2 nd waves of SARS-CoV-2. Coastal cities and islands appear to have been spared the 1 st wave in March, only to succumb to the 2 nd wave later in August. 40, 41 Coronavirus' spike protein possesses hydrophobic sites on its N-terminal peptide and the sodium chloride derived-particle based water may have deterred viral adherence to particulate matter. 42, 43 This may not be the case with the 2 nd wave whereby Clade G achieved near complete dominance. 7 The different orientation of Clade G trimeric spike peptides may influence the hydrophobic behaviour of the Nterminal portion of the spike protein peptide.

Particulate matter originating from exhaled tobacco smoke demonstrates a 1.5 times volumetric increase due to the added particle based water attained during its passage through the bronchial tree. 44 It may well be that if Clade G N-terminal peptide is less hydrophobic than Clade D, that the variant would find particulate matter originating from tobacco smoking a more favourable viral vector. A putative inference is that potentially the asymptomatic SARS-CoV-2 positive smoker may present as a superspreader to both smokers and nearby nonsmokers alike. Moreover the protective effect of masks is lacking during the act of smoking, as obviously face protection has to be removed while smoking, encouraging further COVID-19 transmission. 45 Other components of particulate matter may also have influenced SARS-CoV-2 adherence to particulate matter. The major component (>60%) of atmospheric . 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 January 11, 2021. ;  particulate is carbon. Subway travel has the highest indoor airborne concentration of particulate matter. Particulate matter found in the environs of subways has a significant haematite component as opposed to the surface carbon-rich particulate matter matter. In the absence of carbon's adsorbance properties, viral release in the respiratory system may be facilitated by corona-laden haematite rich particulate in subways. 46

There was a significant difference in viral counts obtained between cities included in this review. This suggests the strong possibility of variation in the availability of sampling of viral counts between cities. The Beijing data retrieved the latter part of the bell-shaped curve. The assumption that viral counts were higher in Beijing is an extrapolation of the viral count curve. This extrapolation is given greater credence when the curve in Beijing is compared to the other complete curves of the other cities and also correlates with the elevated PM2.5 levels in Beijing in early February and late January 2020. The average daily PM2.5 levels are taken in this study and it must be mentioned that there may be wide variations between the maximum and minimum levels of particulate matter throughout the day including when there may be human exposure to this pollutant. Exposure to atmospheric PM2.5 does not necessarily equate that to humans being similarly exposed to the same levels indoors. Indoor levels may actually be higher if fossil fuels are used for heating purposes. In Wuhan over the past year, natural gas consumption for heating purposes increased 2.8 times this fossil fuel's utilization by the traditional stove and water heater, potentially . 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. (which was not certified by peer review)

The copyright holder for this preprint this version posted January 11, 2021. ; https://doi.org/10.1101/2021.01.10.21249548 doi: medRxiv preprint producing another indoor source for particulate matter. 47 The assumption that Clade G utilized particulate matter derived from tobacco smoking is a hypothesis based on the fact that the variant emerged when PM2.5 plummeted in China, combined by the fact that as mentioned earlier more than 66% of Chinese males smoke and 70% of the non-smoking population are exposed to 2 nd hand smoking. 20

This study suggests that there appears to be an association between PM2.5 levels and COVID-19 infection. The correlations between viral counts and particulate matter may indicate that besides PM2.5's deleterious effects on pulmonary defences, there may be a viral vector effect that exacerbated the pandemic. Moreover there may be an association with SARS-CoV-2 Clade evolution. The initial Clade D predominated when the PM2.5 were elevated, only to be displaced by Clade G when the atmospheric PM2.5 levels decreased. It may also be inferred that Clade G utilized other sources of this pollutant closer to human respiratory tract, such as particulate matter derived from tobacco smoking employed as a vector for COVID-19 transmission.

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