This study showed that exposure to high levels of PM2.5 in the years preceding the COVID-19 pandemic was associated with the higher incidence of SARS-CoV-2 infection and mortality due to COVID-19 but without affecting the case-fatality rate (Deaths/cases*100) in Metropolitan Lima, a city that is considered one of the most polluted in Latin America . This suggests that the current incidence of COVID-19 is associated with a chronic exposure to air pollution. The association was maintained including after controlling by population density, age, sex and number of food markets.
This is an important finding that explain why cases of COVID-19 increased in Lima despite Peru had one of the earliest COVID-19 lockdowns in Latin America applying a quarantine, with much of the activities closed (schools, universities, churches, ban of public events) soon after the first case of COVID-19 was detected.
A previous systematic analysis showed that the incidence of and the risk of morbidity and mortality from COVID-19 increase with chronic and acute exposure to air pollution, particularly to PM (PM2.5 and PM10) and nitrogen dioxide [8; 25; 26; 27].
The values of PM2.5 ranged for all districts from 14.50 to 41.69 µg/m3, all of which were higher than the annual mean value declared by the WHO (10 µg/m3). Thus, as it was previously shown that PM2.5 was associated with an increasing risk for respiratory infectious diseases , the present situation with the COVID-19 spread demonstrates an increasing trend. We have assessed the association with long-term PM2.5 exposure; however, the impact of short-term exposure needs to be addressed in further research.
An analysis of the distribution of COVID-19 cases worldwide demonstrates a remarkable asymmetry with respect to the countries/regions [28; 29]. This is exactly the pattern that we have observed in Metropolitan Lima. From the 24 districts assessed, those with higher PM2.5 concentrations during 2012–2016 showed more COVID-19 incidence than did those with less concentrations of the pollutants (Supplementary Table 2). Nationwide, 220749 SARS-CoV-2 positive cases and 6,308 deaths due to COVID-19 have been reported since the first case was reported. Lima has 58.3% of the national cases and 38% of deaths. However, Lima represents only 28% of the total Peruvian population.
Human pathogenic corona viruses, which include SARS-CoV-2 that is responsible for COVID-19, bind to their target cells through the angiotensin-converting enzyme 2 (ACE2) receptor expressed by epithelial cells of the lung, intestine, kidney, and blood vessels . It is possible that PM2.5 may induce the elevation of ACE2 activity.
Active cigarette smoking up-regulates ACE-2 expression in the lower airways, which may partially explain the increased risk of severe COVID-19 in these populations . If air pollutants act similarly as the agents released during smoking, it is probable that individuals with chronic exposure to these compounds would have low ACE-2 activity or greater susceptibility to the infection .
This study in Metropolitan Lima that used data of PM2.5 from 2012 and 2016 for 24 districts showed that the case-fatality rate did not increase with the increasing values of PM2.5. This is an interesting finding because a crude analysis of the data showed that deaths are higher when PM2.5 concentrations are higher. However, when the data are calculated as the amount of deaths/number of cases due to COVID-19 (case-fatality rate), there was no observable association with PM2.5. However, the results suggest that PM2.5 does not affect the case-fatality rate. This agrees with the data observed in New York after short-term exposure to air pollutants .
The national COVID-19 case-fatality rate was 2.58%, and 1.93% for Lima. The highest rate in the rest of Peru respect to Lima may reflect the deficiencies in the healthcare system in the different provinces of Peru. The COVID-19 case-fatality rate was higher in men and increased with age, thus confirming previous results .
In average, the age at infection was around 42 years in Peru. After end of quarantine, it is possible that age at infection will lowered. This due to that more of young people will be exposed.
At national and at province level (Lima), the age at infection was 20 years lower than the age at death due to COVID-19. This higher mortality risk for older people has been reported previously [34; 35]. In our study, the association between older age and COVID-19 mortality risk was unaffected by increasing levels of PM2.5, suggesting that the factors that explain the higher mortality risk with age are independent of PM2.5 exposure. In fact, PM2.5 did not modify the COVID-19 case-fatality rate in Lima.
Lima has an average of 13% elderly population and 22% under 19 years of age. The districts of the suburbs (Ate, Puente Piedra, Carabayllo, VES and VMT) have the lowest elderly population and therefore more young people. The largest population (19–64 years) is similar in all districts, and those who move around the city for work, shopping, entertainment, are the most exposed to infection .
There is evidence of the role of PM pollutants in SARS-CoV-2 transmission. PM2.5 and other small PM can act as disease vectors and facilitate the airborne transmission of viable virus particles, and these have been incriminated in the spread of measles and SARS .
Social distancing is an important preventable measure to decrease the spread of COVID-19. This was demonstrated in 28 European countries, where the most probable point of change during the COVID-19 epidemic showed a dose-response association of the observed flattening of the epidemic curve with an increasing social distancing index (SDI). Countries in the highest SDI quartile achieved a statistically significant decline in the incidence and prevalence of the epidemic .
In Brazil, according to a recent report, social distancing measures that were adopted by the population appeared effective, particularly when implemented in conjunction with the isolation of cases and quarantining of contacts .
In numerical simulations, in a city within Brazil, three scenarios were compared: first was the vertical distancing policy, where only older people was distanced; the second involved the horizontal distancing policy where all age groups adhered to social distancing; and the third involved a control scenario wherein no intervention was undertaken to distance people. Horizontal distancing, if applied with the same intensity in all age groups, significantly reduced the total number of infected people by "flattening the disease growth curve"; however, vertical distancing or non-distancing did not show this effect .
Doubtless, social distancing measures appear to be the most effective intervention to slow the disease spread of COVID-19. Though studies unanimously confirm the mitigating effect of social distancing on disease spread, the reported effectiveness varies from 10% to a more than 90% reduction in the number of infections . The changes of mobility in public places, such as retail and recreation centers (e.g., restaurants, cafes, theaters, etc.), grocery stores and pharmacies, transit hubs (e.g., airports, bus stations, subways, etc.), and parks, are the most important determinants of the disease-transmission rate .
In Peru, some specific factors could contribute to the spread of COVID-19 during quarantine. These include the easy availability of food markets, banks, and public transport. In Peru, the food markets remained open during the quarantine period to ensure food availability for the population.
According to the findings of this study, in districts where there were more markets, there were higher numbers of cases and deaths. This may explain the high spread of the COVID-19 cases in Lima, in a situation in which individuals are susceptible to the virus by previous exposure to air pollutants.
It is well known that the highest risk of SARS-CoV-2 transmission occurs prior to symptom onset. A recent paper provides evidence of the effectiveness of mask use, disinfection, and social distancing in the prevention of COVID-19 .
In this study, the number of markets was unrelated to the PM2.5 concentration, which suggests that both factors are independently associated with the spread of COVID-19. Moreover, after controlling for different variables including number of food markers, PM2.5 remains associated to the number of cases of COVID-19.
From a long-term perspective, the reduction of air contamination should be considered a part of the integrated approach for sustainable development, human health protection, and for reducing the spread of a disease during an outbreak, epidemic, or pandemic. However, although reducing air pollution is important to reduce morbidity and mortality due to different diseases, the findings of this study suggest also the importance of social isolation to reduce the incidence of COVID-19 . The magnitude of contagion in the food markets is an example that policies that are aimed at reducing crowding could be important for preventing the spread of COVID-19.
The limitations of the study are lack of data on number of people attending the food markets during the quarantine period. We were also unable to obtain data on people attending banks, and public transport within the same period. Data also on accomplish of social distancing and use of mask is also lacking.
The study makes a significant contribution to the literature because the findings indicate that higher PM2.5 levels are associated with higher incidence of infections with SARS-CoV-2 and mortality of COVID-19. However, the case-fatality rate did not increase with the increase in PM2.5 levels.
The findings of this study are generalizable to regions with similar population density and PM2.5 levels in the setting of respiratory epidemics or future pandemics. This study will be a support tool for decision-making in the country's health policy, since having a study in which PM2.5 is associated by district, age, sex, markets of stocks in the number of cases of COVID-19 and deceased, will allow to rethink the measures used by the Peruvian government, and other countries characterized by high air pollution.
In conclusion, the present study demonstrated that the higher rates of spread of COVID-19 in Metropolitan Lima (Peru) were associated to the previous long-term PM2.5 exposure. Men and older people were at higher risk of death due to COVID-19. Reduction of air pollution since a long-term perspective, and social distancing are needed to prevent spreads of virus outbreak. These results must be considered by officers of the Governments to be applied in the health policies aimed to prevent or reduce epidemic viral spread. The strategies taken to confront the pandemic must consider previous environmental indicators to intensify efforts in areas with higher air pollution.