Viral Infections Acquired Indoors Through Airborne, Droplet Or Contact Transmission Reviews Giuseppina La Rosa, Marta Fratini, Simonetta Della Libera
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124 Ann Ist Super Sanità 2013 | Vol. 49, No. 2:124-132 DOI: 10.4415/ANN_13_02_03 Viral infections acquired indoors through airborne, droplet or contact transmission REVIEWS Giuseppina La Rosa, Marta Fratini, Simonetta Della Libera, AND Marcello Iaconelli and Michele Muscillo Dipartimento di Ambiente e connessa Prevenzione Primaria, Istituto Superiore di Sanità, Rome, Italy ARTICLES Abstract Background. Indoor human environments, including homes, offices, schools, workplac- Key words es, transport systems and other settings, often harbor potentially unsafe microorganisms. • viruses RIGINAL Most previous studies of bioaerosols in indoor environments have addressed contamina- • indoor O tion with bacteria or fungi. Reports on the presence of viral aerosols in indoor air are • droplet scarce, however, despite the fact that viruses are probably the most common cause of • droplet nuclei infection acquired indoor. • fomites Objective. This review discusses the most common respiratory (influenza viruses, rhino- viruses, coronaviruses, adenoviruses, respiratory syncytial viruses, and enteroviruses) and gastrointestinal (noroviruses) viral pathogens which can be easily transmitted in indoor environments. Results. The vast majority of studies reviewed here concern hospital and other health facilities where viruses are a well-known cause of occupational and nosocomial infec- tions. Studies on other indoor environments, on the other hand, including homes, non- industrial workplaces and public buildings, are scarce. Conclusions. The lack of regulations, threshold values and standardized detection meth- ods for viruses in indoor environments, make both research and interpretation of results difficult in this field, hampering infection control efforts. Further research will be needed to achieve a better understanding of virus survival in aerosols and on surfaces, and to elucidate the relationship between viruses and indoor environmental characteristics. INTRODUCTION or exhale during conversation or breathing (primary Private and public indoor environments, including aerosolization). A single cough can release hundreds homes, offices, schools, workplaces and transport systems of droplets, a single sneeze thousands (up to 40 000) contain numerous potentially harmful pollutants. Research at speeds of up to 50-200 miles per hour, each droplet on exposures to indoor pollutants has so far focused mainly containing millions of viral particles (although the number on chemical compounds. Recently, exposure to biological varies greatly in the course of infection). Aerosol droplets agents, mostly bacteria and fungi, has aroused growing travel only short distances (1-2 meters) before settlings interest, but reports on the presence of viral aerosols in on surfaces, where viruses can remain infectious for indoor air remain scarce. hours or days. Virus survival on fomites is influenced by Viruses are small (20-400 nm), obligate intracellular temperature, humidity, pH and exposure to ultraviolet parasites. They represent a common cause of infectious light. Hands that come into contact with these surfaces disease acquired indoors, as they are easily transmitted become contagious (through later contact with mucous especially in crowded, poorly ventilated environments membranes). Secondary aerosolization can occur when air [1, 2]. During and after illness, viruses are shed in large displacements disperse the viruses back into the air from numbers in body secretions, including blood, feces, urine, contaminated surfaces. Droplet transmission is not to be saliva, and nasal fluid. Consequently, viral transmission confused with airborne transmission. Droplets do not routes are diverse, and include direct contact with infected remain suspended in the air. On the other hand, airborne persons, indirect contact with contaminated surfaces, transmission depends on virus-containing droplet nuclei fecal-oral transmission (through contaminated food (small-particle residue ≤ 5 µm) of evaporated droplets or and water), droplet and airborne transmission. Droplet dust particles that can remain suspended in the air for transmission occurs when viruses travel on relatively large long periods. Viruses contained within the droplet nuclei respiratory droplets (> 10 µm) that people sneeze, cough, can be transported over considerable distances by air Address for correspondence: Giuseppina La Rosa, Dipartimento di Ambiente e connessa Prevenzione Primaria, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Rome, Italy. E-mail: [email protected]. 125 VIRUSES IN INDOOR ENVIRONMENTS currents to be inhaled by a susceptible host, penetrating also available. Both protocols are continuously updated at deep into the respiratory system due to their small size. the international level. Particles between 5 and 10 µm in diameter represent an The first reviews on viruses in indoor environments intermediate stage; most particles in this size range will were published in the 1980s [5, 6]. Adenovirus (type be trapped in the nose, although some will penetrate to 4), the first virus to be isolated from indoor aerosol, was below the larynx. identified in 1966 in aerosol samples from the quarters of Roy and Milton proposed a classification for pathogen military recruits infected with Acute Respiratory Disease airborne transmission: obligate, preferential, or [7]. Enterovirus (coxsackievirus A-21) was identified in REVIEWS opportunistic [3]: 1970 in aerosol samples from the barracks of soldiers 1) obligate: refers to an infection that, under natural affected by acute respiratory infection [8]. Since then, conditions is initiated only through aerosol (droplet nuclei) human infections due to viral aerosol (or contact with AND deposited in the distal lung. The best known obligate contaminated surfaces) have been studied in various airborne microorganism is Mycobacterium tuberculosis. No environments, including office building, hospitals, groups of viruses belong to this category; restaurants, transport systems and schools [3]. 2) preferential: refers to pathogens that can initiate This review discusses the most common respiratory ARTICLES infection by multiple routes, but are predominantly (influenza viruses, rhinoviruses, coronaviruses, transmitted by droplet nuclei (e.g. chickenpox and adenoviruses, respiratory syncytial viruses, and measles); enteroviruses) and gastrointestinal viruses (noroviruses) 3) opportunistic/rare: refers to pathogens transmitted for which evidence exists on transmission in indoor mainly via other routes but able to spread via droplet environments. We will mainly focus on airborne RIGINAL nuclei or dust in certain circumstances. transmission, a route with the potential for infecting a O The vast majority of respiratory and enteric viruses belong large number of hosts over long distances from the source to the third group. Viruses able to transmit infection via of viral contamination. the airborne route can almost ever transmit infection also over short ranges and through direct contact. The most INFLUENZA VIRUS important source of potentially pathogenic viral aerosol Influenza virus infection is one of the most common is other humans (ill or in incubation period). Airborne and highly contagious infectious diseases and can occur viral particles can also spread by other means. The in people of any age. The virus, belonging to the Ortho- flushing of a toilet, for example, can aerosolize significant myxoviridae family, can cause mild to severe acute febrile concentrations of airborne viruses [3]. Once released in illness, resulting in variable degrees of systemic symptoms, indoor environments, the movement and fate of viruses ranging from mild fatigue to respiratory failure and death. in the air is a complex process, involving many factors: the About 50% of all infections may be asymptomatic. As- mechanism and speed by which the droplets are ejected ymptomatic patients however, shed virus and can trans- from the infected person, the concentration of viruses in mit the disease, thus creating a reservoir for the virus. In respiratory secretions, the presence of particulates/organic most cases, the influenza virus is transmitted by droplets, matter, environmental factors affecting the infectivity through the coughing and sneezing of infected persons, and viability of viruses (e.g temperature and humidity), but it can also be transmitted by airborne droplet nuclei and ventilation, heating, or air conditioning. Morawska as well as by contact, either through direct skin-to-skin reviewed the influence of these parameters on airborne contact or through indirect contact with contaminated en- viral transmission [4]. The dynamics of survival and vironments. Controversy exists with regard to the impor- dissemination of viruses in aerosols indoors, as well as the tance of the airborne route as compared to droplet or con- role of ventilation and other environmental factors are still tact transmission. In clinical studies, virus-laden particles poorly understood. within the respirable aerosol fraction have been detected Crowded indoor environments, especially when poorly in exhaled breaths of patients with influenza and in the ventilated, represent greater risks for viral transmission. air samples from healthcare settings during seasonal peak Hospitals in particular, are environments where viral [9]. Moreover, the scientific literature presents evidence aerosol can be particularly hazardous, since patients tend in support of a contribution of aerosol transmission to the to be especially