• Sign Up

Airborne Precautions


Airborne Precautions

Article Author:
Binish Ather
Article Author:
Taaha Mirza
Article Editor:
Peter Edemekong
Updated:
6/28/2020 2:03:33 PM
For CME on this topic:
Airborne Precautions CME
PubMed Link:
Airborne Precautions

Introduction

An airborne disorder is any disease that is caused by a microorganism that is transmitted through the air. Many clinically important airborne diseases are caused by a variety of pathogens including bacteria, viruses, and fungi.[1] These organisms may be transmitted through sneezing, coughing, spraying of liquids, spread of dust, talking, or any activity that results in the generation of aerosolized particles. It is important to be aware that airborne diseases, in general, do not include disorders caused by air pollution, poisons, smog, and dust.[2][3]

According to the World Health Organization, “Airborne transmission of infectious agents refers to the transmission of disease caused by dissemination of droplet nuclei that remain infectious when suspended in air over long distance and time.” Airborne transmission can be characterized as obligate or preferential depending on whether it is only transmitted via droplet nuclei or if it has multiple other routes of transmission. [4]

The microorganisms transmitted by an airborne route may be spread via fine mist, dust, aerosols, or liquids. The aerosolized particles are generated from a source of infection such as an infected patient or animal. In addition, aerosols may be generated from biological waste products that accumulate in garbage cans, caves, and dry arid containers. In aerosolization, the microorganisms that are less than 5 micrometers in size float in the air. These microorganisms, contained in droplets, are then dispersed via air currents to varying distances and can be inhaled by susceptible hosts.[5][6][7] Although a majority of the particles will drop off within the vicinity, the infected aerosolized particles often remain suspended in air and may even travel considerable distances, . As the distance between the source and susceptible individuals increases, the rate of transmission decreases. Airborne transmission necessitates the use of available interventions in healthcare facilities to break the transmission of airborne particles from patient to patient and patient to healthcare workers. Airborne particles are considered highly infectious as they often remain suspended in the air and travel by air currents to different parts of the hospital where there is a potential of them being inhaled by others. In some cases where there is inadequate ventilation, the airborne particle may remain in the hospital room for extended periods and may even be inhaled by a newly admitted patient.

The control and prevention of airborne transmission of infections is not simple; it requires the control of airflow with the use of specially designed ventilation systems, the practice of antiseptic techniques, wearing personalized protective equipment (PPE), and performing basic infection prevention measures like hand washing. [8][9][10]

Airborne Organisms

In almost all cases, airborne pathogens cause an inflammatory reaction of the upper airways affecting the nose, sinuses, throat, and lungs. The involvement of these structures may result in sinus congestion, sore throat, and lower respiratory tract symptoms. Any coughing or sneezing activity may then generate aerosolized particles leading to airborne transmission. Some of the common pathogens that may spread via airborne transmission are:

  • Anthrax
  • Aspergillosis
  • Blastomycosis
  • Chickenpox
  • Adenovirus
  • Enteroviruses
  • Rotavirus
  • Influenza
  • Rhinovirus
  • Neisseria meningitidis
  • Streptococcus pneumoniae
  • Legionellosis
  • Measles
  • Mumps
  • Smallpox
  • Cryptococcosis
  • Tuberculosis
  • Bordetella pertussis
  • Severe acute respiratory syndrome (SARS)
  • Middle East Respiratory Syndrome (MERS)
  • Coronavirus Disease 2019 (COVID-19)

This is a non-exhaustive list that only encompasses some of the common diseases that have been implicated in airborne transmission.[11] A special note to be made is regarding COVID-19, the 21st century pandemic which is thought to spread through airborne routes (among other routes).[12] Active measures to prevent airborne transmission has shown to curb its spread.

Airborne diseases are not exclusive to humans and can also infect animals. A notable example is of poultry that is often affected by an avian disorder (Newcastle disease), that is also transmitted via an airborne route. However, it is important to understand that exposure to an animal or a patient with an airborne disease does not automatically ensure disease transmission. The infection also depends on the host immunity, the amount of exposure, and the duration of exposure to the infected patient. [4][7][13][14]

Airborne Particles Generated from Medical Equipment

Besides patients, several medical and surgical procedures may also generate aerosolized infectious particles. In most cases, these airborne particles are generated during the manipulation of the lung airways. These include:

  • Manual ventilation with a bag and mask
  • Intubation
  • Open endotracheal suctioning
  • Bronchoscopy
  • Cardiopulmonary resuscitation
  • Sputum induction
  • Chest physiotherapy
  • Lung surgery
  • Nebulizer therapy and steam inhalation
  • Non-invasive positive pressure ventilation (BIPAP, CPAP)
  • An autopsy of the lungs

Care must be taken while performing the above medical procedures on patients known to have diseases with high transmissibility through airborne routes.[15]

Issues of Concern

Factors that influence airborne transmission

Airborne transmission depends on several physical variables characteristic to the infectious particle and the environment.[5][8][9][10][14] Factors that influence the spread of airborne infections include the following:

  • Temperature: Certain viruses are more active at lower temperatures. For example, influenza tends to spread more easily in cold climate conditions. In contrast, the infectivity of bacterial pathogens decreases in cold temperatures as they are less resistant and thus remain in a state of dormancy.
  • Amount of sunshine: Ultraviolet (UV) rays of the sun are harmful to both bacteria and viruses. The strength and duration of UV light exposure can determine the survival of infectious pathogens in the air. Countries that have a higher average daily sunshine are thus less prone to airborne transmission.
  • Humidity: The percentage of water vapor in the air also determines the effectiveness of airborne droplet nuclei to spread from person to person. It has been studied that high humidity levels are protective against UV light destruction as water vapor forms a protective barrier around the droplet nuclei.
  • Wind: Air currents are known to increase the distance traveled by infectious airborne particles. Wind also however decreases the concentration of droplet nuclei thus decreasing the airborne infectivity.

Other Factors

  • Tropical Storms: Several studies have shown that tropical storms decrease the quantity of fungal spores in the air. The number of fungal spores does however increase after a few days.
  • Socioeconomic and living conditions: Like infectious diseases that are spread via contact, the role of living conditions and socioeconomic factors also plays a key role in airborne transmission. Housing and the number of people residing in one room/area is an important determinant of airborne transmission. Room ventilation and aeration are also key factors. Airconditioning is also considered as a culprit for the increased airborne spread in closed environments.
  • Rural vs Urban: In urban areas, close living conditions results in increased transmission of bacterial and viral pathogens. In contrast, rural areas are more prone to airborne transmission of fungal spores.
  • Inadequate sewage and drainage systems: Biowaste accumulation also increases the risk of formation of airborne particles and thus their spread.

An article published in 2009 highlights how every pathogen has its own set of ideal environmental conditions for airborne transmission. Generalization of the unfavorable conditions for aerosol transmission may be misleading. Each pathogen should be separately studied in this regard.[16]

Management Principles

When patients are seen in the emergency room or admitted to the hospital, it is impossible to know immediately if there have an infection that is transmissible via the airborne route.[17][18] Thus, healthcare workers need to maintain a high degree of suspicion in patients who present with signs and symptoms that are compatible with such an infection. The earlier the airborne prevention methods are adopted, the lower the risk of transmission to other patients and healthcare staff. [14][19]

Airborne Isolation Room

This is a single patient room equipped with special air handling (negative pressure) and ventilation capacity. An airborne isolation room is also known as a negative pressure room. This negative pressure room is usually a single-occupancy patient-care room frequently used to isolated individuals with confirmed or suspected airborne infection.[20][21][22]

Elements of an Airborne Isolation Room

The following are some elements of an airborne isolation room.[7][10][14]

  • Negative pressure ventilation that creates inward directional airflow from corners of the room
  • The airborne isolation room should have a toilet and sink for the patient, and a designated handwashing sink for healthcare workers.
  • Have monitoring equipment including alarms.
  • Transmit exhaust of air from the hospital room to the outside of the building
  • Recirculate air through a HEPA filter before being returned to the general circulation
  • The door to the room must be kept closed to maintain negative pressure even if the patient is not in the room.
  • The windows in the room should remain closed at all times; opening the window may cause the reversal of airflow, which counters the benefits of a negative pressure room.
  • All healthcare providers who enter the isolated negative pressure room must be fit tested for an N95 respirator.
  • Only healthcare providers immunized to the organism in question should enter a room where airborne precautions are in place for varicella or measles. A respirator is not necessary for immunized individuals but is required for non-immunized workers who provide care.
  • One should also have a point of care evaluation for every patient interaction so that one can determine the need for additional precautions.

What is an Anteroom?

This is relatively clean and is a frequently used area to transition patients/healthcare workers in and out of the airborne isolation room when it is under negative pressure.[10][21] An anteroom is frequently used as a transitional space between the airborne isolation room and the hallway. It is in this transition area where healthcare workers store their PPE and put on their PPE before entering the airborne isolation room.

  1. The laundry hamper is usually located inside the patient room.
  2. The sink is usually in the anteroom location.
  3. The only items that are stored in the anteroom are the procedure or surgical masks, N95 respirator, eye protection devices, gloves, and gowns.
  4. At the handwashing sink, an alcohol-based hand sanitizer and disinfectant wipes should be available.
  5. Posters showing how to perform handwashing must be placed near the sink.

Clinical Significance

Personal Protective Equipment (PPE)

Personal protective equipment forms a cornerstone of protection against airborne diseases. [7][14][21] All healthcare workers who enter the negative pressure room should wear an appropriately fit-tested N95 respirator. The N95 respirators are individually fitted and can filter particles one micron in size. Studies show that the mask has a 95% filter efficiency and provides a tight facial seal with less than a 10% leak.

To use the respirator appropriately, one should do the following:

  • Hand hygiene should be performed before putting on a respirator.
  • Perform a seal check. This may be done by covering your respirator with both hands and exhaling sharply. If air blows on out from the edges, sealing should be repeated.
  • To avoid self-contamination after use, remove the respirator using the straps. Avoid touching any part the part which may have microorganisms on it.
  • When the respirator is not in use, it should not be dangled in front of the neck or top of the head.
  • If the respirator becomes soiled, wet, or is splashed with body fluids, it should be promptly removed.
  • After use, the respirator should be removed, and one should thoroughly wash hands.
  • The N95 respirator must be fit tested for all healthcare workers assigned to treat the particular patient.
  • All N95 respirators must be cited by the Occupational Safety and Health Administration (OSHA) and have an efficiency rating.

Patient Movements

In hospitals, patients admitted to the negative room often have to be transported to other departments like radiology, physical therapy, the pulmonary laboratory, or even another hospital. Before transferring a patient with an airborne infection, one must always communicate with the relevant department first. The guidelines for transportation are as follows:

  • During transport, the patient should wear a surgical mask.
  • There may be situations when during the transport the patient may not be able to wear a mask. In such scenarios, the transport should be performed in a way to limit the exposure to other patients or staff. This means the transport staff should not wait in the reception area or leave the patient in a holding area.
  • The patient should preferably be transported in an empty elevator, and the personnel that is transporting the patient should be told to maintain infectious disease precautions throughout the transportation. These include appropriate N95 respirators and personal protective equipment.
  • If the patient is intubated, call respiratory therapist ahead of time to ensure that the transport is done according to respiratory guidelines.

Patient and Family Education

Patients who require isolation due to the risk of airborne transmission need to be counseled regarding their condition and infectivity. Their family members, caretakers, and visitors must also be educated so that they may abide by preventive guidelines to ensure that the disease is not transmitted. The patient should be educated on coughing etiquettes to ensure the minimum spread of aerosolized particles in the isolation room. Face tissues and handkerchiefs must be properly and appropriately disposed of to further decrease the chances of transmission. Furthermore, a sign recommending infectious precautions should be placed outside the isolation room so that all visitors may be apprised by the guidelines. Unnecessary visits should be avoided and all immunocompromised individuals must refrain from entering the isolation room. The use of N95 respirators and hand hygiene must be followed by all visitors without lapses.

Duration of Precautions

In general, airborne precautions can be discontinued once the patient shows no signs or symptoms of an infection. [10][21][23][24]

However, one also has to be aware of the period of incubation and if unsure, always consult with an infectious disease expert

  1. Anthrax is caused by exposure to aerosolized B. anthracis spores. It needs to be treated with at least 8 weeks of antimicrobial therapy. This is a serious infection with very high mortality if the diagnosis is missed. An infectious disease consult should be involved in the management of patients with anthrax. The patient usually remains infectious while symptoms remain. Since this is a potential agent for bioterrorism, it is important to seek advice from the CDC. Patient isolation is mandatory, and all traffic in must be curtailed.
  2. Chickenpox is caused by varicella-zoster virus. Individuals remain infectious for 5 to 7 days after the rash develops. By this time most of the vesicles have dried up, and the risk of transmission decreases.
  3. Influenza is a common cause of upper and lower respiratory tract infections. Patients with influenza are considered infectious even before the onset of symptoms. In most cases, viral shedding occurs at the time of the symptoms and continues for 5 to 10 days. Data indicates that younger children and infants may shed the virus for a week or two, thus placing other individuals at risk for acquiring the infection. In patients who are immunocompromised, the shedding may last for up to 12 weeks.
  4. Measles (rubeola) is the most contagious infectious diseases, with a secondary infection rate in susceptible domestic contacts over 90 percent. The majority of patients are contagious 1 to 2 days before the onset of symptoms. Younger patients may remain contagious 4 to 5 days before and after the rash.
  5. Smallpox is not a concern in many parts of the world, but it is a contagious infection. However, unlike measles, influenza, and pertussis, the transmission rate of smallpox is low. Once smallpox is acquired, the patient remains contagious from the onset of the fever and rash. The highest viral shedding occurs during the first 2 weeks of the rash. Infection rates of anywhere from 40% to 80% have been reported.
  6. Cryptococcosis is being diagnosed more often now because of the widespread of organ transplantation. The risk of acquiring or developing an infection, however, is very low in immunocompetent and healthy individuals. An infectious disease consult is necessary to determine the period of isolation.
  7. Tuberculosis is a common disease, but it is not considered as contagious as measles or influenza. Even when acquired, only 5% of the individuals develop clinical disease. The risk of disease transmission is most common in close living quarters. Data reveals that about 20% of household contacts do develop a positive skin test to purified protein derivative testing (PPD). The patient usually remains infectious while symptoms are present, which can be a few weeks.

Managing Deceased Patients

When a patient is deceased, airborne precautions remain necessary when handling and preparing the body during transfer to the morgue. Similarly, performing an autopsy also warrants proper personal protective equipment and the use of N95 respirators.

Managing specimens and rooms of patients and with airborne infections

When a patient with an airborne transmissible disease has been discharged, it is important to continue airborne precautions while decontaminating the room. The door must remain closed and negative air flow must be maintained until all air in the room has been recirculated and replaced. This process usually requires 45 to 60 minutes depending on the size of the room. Soiled linen should be handled with gloves with minimal agitation to prevent dispersion of microorganisms into the air. The laundry hamper should be close to the location so that the linen can be placed inside rather than carried a long distance. If there is obvious contamination with body fluids, the linen should be placed in a plastic bag. Proper handling and transport of specimens: All body specimens should be considered to be infectious and handled safely.

Other Issues

Due to the pandemic caused by COVID-19, there has been an acute shortage of personal protective equipment and N95 respirators. This has made hospitals, doctors, and public resort to alternate precautions for airborne transmission. According to the Center for Disease Control and Prevention (CDC), N95 respirators are not recommended for daily wear by the public. Instead, the CDC recommends that the public may use a simple face cloth covering to protect themselves and others from COVID-19. Alternatively, simple surgical masks are also considered effective at blocking large-particle droplets, splashes, and splatters that may contain viruses and bacteria. Surgical masks can also help reduce the dispersion of one's own saliva and respiratory secretions to others, thus proving important to contain the spread of pathogens. While considered important, surgical masks do not filter or block small particles in the air that may be transmitted by coughs, sneezes, and other medical procedures (intubation). Thus, N95 respirators are considered the protection of choice for healthcare workers when dealing with patients diagnosed with diseases that may be airborne. N95s are designed to ensure a tight fit around the nose and mouth so that they can efficiently filter out 95% of the particles sized 0.3 micrometers or more without leakage of air. Due to their tight fit and filtering capabilities, breathing in an N95 respirator is associated with heat build-up and distress. To make breathing easier, some models of N95 respirators come with exhalation valves that make breathing out easier. Care must be taken to not use those valves when sterility is required. Due to the immense shortage of N95 masks during the COVID-19 pandemic, U.S. Food and Drug Administration (FDA) has issued the emergency use authorizations of decontaminating proecedures for some respirators, provided there are insufficient supplies of new ones. Multiple methods for decontamination have been described by the CDC including the use of ultraviolet radiation, vaporous hydrogen peroxide, moist heat, microwave generated steam, and ethylene oxide. Alternatively, CDC also recommends that 5 N95 respirators may be issued to each healthcare professional so that they may wear one respirator each day and store it in a breathable paper bag at the end of each shift to decontaminate it using time. This guideline is based on the study that outlines that SARS-CoV-2 is able to survive for up to 72 hours on various surfaces.[25]  Other studies are also determining whether using a surgical mask on top of an N95 respirator extends the life of the respirator. [26] Due to the COVID-19 pandemic, another respirator gaining popularity is the KN95 mask. This is manufactured in accordance with the standards of China. It is claimed that the KN95 masks are similar to the N95 respirators for filtering non-oil-based particles. Despite these claims, the FDA has not yet authorized the use of KN95 respirators.

Enhancing Healthcare Team Outcomes

The management of airborne infections is with an interprofessional team aided by hospital guidelines and rules. All healthcare workers including the nurse have a vital role in preventing airborne infections. an interprofessional team approach involving clinicians and nurses will produce the best results in preventing the spread of infections. The following principles should apply:

  1. Mostly, antibiotics or antiviral drugs are not usually prescribed to prevent or control infections caused by viruses. However, antibiotics may be prescribed to a patient with the flu, to control or prevent secondary bacterial infections.
  2. Recommendations from the CDC for the public include maintaining careful hygiene and sanitation protocols and getting vaccinated against the organisms associated with airborne infections.
  3. If the number of negative pressure rooms is limited, set priority for use. For example, infectious tuberculosis is the highest booty followed by measles, then variceal disseminated zoster and finally extensive localized zoster.
  4. In emergencies, when there is no airborne isolation room, at least, pull the privacy curtains and require all personnel to wear an N95 respirator. Ask visitors and other patients to leave the area.
  5. One may also use UV air purification devices that are EPR certified and FDA approved to inactivate a wide range of airborne infectious disorders.
  6. It is important that all health care workers be aware of their immune status. Individuals who have problems with immunity or have not been vaccinated should not be allowed to take care of patients with vaccine preventive airborne infections like chickenpox or measles.

References

[1] Fernstrom A,Goldblatt M, Aerobiology and its role in the transmission of infectious diseases. Journal of pathogens. 2013;     [PubMed PMID: 23365758]
[2] Gammon J,Hunt J, A review of isolation practices and procedures in healthcare settings. British journal of nursing (Mark Allen Publishing). 2018 Feb 8     [PubMed PMID: 29412028]
[3] Broussard IM,Bhimji SS, Precautions, Universal null. 2018 Jan     [PubMed PMID: 29262198]
[4] Seto WH, Airborne transmission and precautions: facts and myths. The Journal of hospital infection. 2015 Apr     [PubMed PMID: 25578684]
[5] Brouqui P,Boudjema S,Soto Aladro A,Chabrière E,Florea O,Nguyen H,Dufour JC, New Approaches to Prevent Healthcare-Associated Infection. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2017 Aug 15     [PubMed PMID: 28859352]
[6] MacIntyre CR,Chughtai AA,Rahman B,Peng Y,Zhang Y,Seale H,Wang X,Wang Q, The efficacy of medical masks and respirators against respiratory infection in healthcare workers. Influenza and other respiratory viruses. 2017 Nov     [PubMed PMID: 28799710]
[7] Moriceau G,Gagneux-Brunon A,Gagnaire J,Mariat C,Lucht F,Berthelot P,Botelho-Nevers E, Preventing healthcare-associated infections: Residents and attending physicians need better training in advanced isolation precautions. Medecine et maladies infectieuses. 2016 Feb     [PubMed PMID: 26654322]
[8] Baseer MA,Ansari SH,AlShamrani SS,Alakras AR,Mahrous R,Alenazi AM, Awareness of droplet and airborne isolation precautions among dental health professionals during the outbreak of corona virus infection in Riyadh city, Saudi Arabia. Journal of clinical and experimental dentistry. 2016 Oct     [PubMed PMID: 27703605]
[9] Ito Y,Nagao M,Iinuma Y,Matsumura Y,Yamamoto M,Takakura S,Igawa J,Yamanaka H,Hashimoto A,Hirai T,Niimi A,Ichiyama S,Mishima M, Risk factors for nosocomial tuberculosis transmission among health care workers. American journal of infection control. 2016 May 1     [PubMed PMID: 26777287]
[10] Lindsley WG,Noti JD,Blachere FM,Szalajda JV,Beezhold DH, Efficacy of face shields against cough aerosol droplets from a cough simulator. Journal of occupational and environmental hygiene. 2014     [PubMed PMID: 24467190]
[11] Tang JW,Li Y,Eames I,Chan PK,Ridgway GL, Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises. The Journal of hospital infection. 2006 Oct;     [PubMed PMID: 16916564]
[12] Morawska L,Cao J, Airborne transmission of SARS-CoV-2: The world should face the reality. Environment international. 2020 Jun;     [PubMed PMID: 32294574]
[13] Beam E,Gibbs SG,Hewlett AL,Iwen PC,Nuss SL,Smith PW, Clinical challenges in isolation care. The American journal of nursing. 2015 Apr     [PubMed PMID: 25811520]
[14] Paton R,Tolhurst N,Perisa M,Dempsey K,Tallon J, What mask to use? Australian nursing     [PubMed PMID: 29235820]
[15] Tran K,Cimon K,Severn M,Pessoa-Silva CL,Conly J, Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: a systematic review. PloS one. 2012;     [PubMed PMID: 22563403]
[16] Tang JW, The effect of environmental parameters on the survival of airborne infectious agents. Journal of the Royal Society, Interface. 2009 Dec 6     [PubMed PMID: 19773291]
[17] Peterson K,Novak D,Stradtman L,Wilson D,Couzens L, Hospital respiratory protection practices in 6 U.S. states: a public health evaluation study. American journal of infection control. 2015 Jan     [PubMed PMID: 25564126]
[18] Katz LM,Tobian AA, Ebola virus disease, transmission risk to laboratory personnel, and pretransfusion testing. Transfusion. 2014 Dec     [PubMed PMID: 25403825]
[19] Tajima K,Nishimura H,Hongo S,Hazawa M,Saotome-Nakamura AI,Tomiyama K,Obara C,Kato T, Estimation of secondary measles transmission from a healthcare worker in a hospital setting. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases. 2014 Jul     [PubMed PMID: 24780918]
[20] Patrick MR,Hicks RW, Implementing AORN recommended practices for prevention of transmissible infections. AORN journal. 2013 Dec     [PubMed PMID: 24266933]
[21] Hines L,Rees E,Pavelchak N, Respiratory protection policies and practices among the health care workforce exposed to influenza in New York State: evaluating emergency preparedness for the next pandemic. American journal of infection control. 2014 Mar     [PubMed PMID: 24457143]
[22] Seto WH,Conly JM,Pessoa-Silva CL,Malik M,Eremin S, Infection prevention and control measures for acute respiratory infections in healthcare settings: an update. Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majallah al-sihhiyah li-sharq al-mutawassit. 2013     [PubMed PMID: 23888794]
[23] Benson SM,Novak DA,Ogg MJ, Proper use of surgical n95 respirators and surgical masks in the OR. AORN journal. 2013 Apr     [PubMed PMID: 23531312]
[24] Silkaitis C,Bardowski L,Coomer C,Trakas K,Lavin MA,Reddy S,Bolon MK,Zembower TR, Use of acid-fast bacilli staining to determine the need for airborne infection isolation precautions: a comparison of respiratory specimens. American journal of infection control. 2014 Nov     [PubMed PMID: 25248484]
[25] van Doremalen N,Bushmaker T,Morris DH,Holbrook MG,Gamble A,Williamson BN,Tamin A,Harcourt JL,Thornburg NJ,Gerber SI,Lloyd-Smith JO,de Wit E,Munster VJ, Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. The New England journal of medicine. 2020 Apr 16     [PubMed PMID: 32182409]
[26] Roberge RJ, Effect of surgical masks worn concurrently over N95 filtering facepiece respirators: extended service life versus increased user burden. Journal of public health management and practice : JPHMP. 2008 Mar-Apr     [PubMed PMID: 18287908]