Opinion Review Article | Open Access | Published 20th December 2023
Optimal facemask practices for the cleanroom: Learning the lessons from surgical research for bacterial control: Learning the lessons from surgical research for bacterial control
Tim Sandle, BPL | EJPPS | 284 (2023) | Click to download pdf
Abstract
Facemasks are an important part of personnel related microbiological contamination control measures for the cleanroom, especially for aseptic processing. Yet there are a number of variables that influence the performance of facemasks. These include mask design, the way the mask is worn, the maximum wear time, risks from increased saturation of the mask, and the relative health of the wearer in terms of respiratory conditions. This paper looks at a range of studies in the medical setting and draws out the pertinent points for pharmaceutical and healthcare managers to consider when reviewing and improving their cleanroom going protocols. This should include a maximum four hour wear time, the importance of training and prohibiting those with respiratory infections from entering the cleanroom.
Introduction
Facemasks are widely used in both cleanrooms and surgical units to reduce the spread of airborne particles originating from the nasopharynx region. Facemasks function as filters, allowing air exchange but capturing particles. Normal breathing produces particles through the processes of condensation and high-speed atomisation and many of these particles will be microbial carrying (1). Without the use of a facemask droplets and aerosolised particles will travel considerable distances (2). In particular face masks are effective at preventing downward dispersal of droplets and preventing atomised particles from being expelled (3). The degree of risk is dependent upon the number of particles released; the activities of the wearer; the effectiveness of the facemask filter; and the environmental state of the cleanroom.
Whilst there are several good practices embedded into cleanroom management relating to facemask use, poor mask control is one of the reasons for airborne deposition of bacteria. This may relate to inadequate mask design, especially facemask filter efficiency, or the way the mask is worn, especially where air leakage from the nose and mouth occurs. The mechanics of dispersal are complex and relate to such factors as turbulent dispersion forces, droplet phase-change, evaporation, particulate breakup, and droplet–droplet and droplet–air interactions. However, the activities of the mask wearer can influence this, especially in causing a greater abundance of particles to be released and for these to be moving at a greater velocity, such as from increased turbulent airflows, more vigorous vibration, and higher energetic movement, arising from the vocal cords during activities like talking, sneezing and coughing (4).
A further important consideration is with the quality of mask design. There are several different designs available, varying from the front facing features (flat or ‘budgie beaked, for example) and the way the mask is secured to the head (ties or circular elastic). These variances can affect the efficiency of masks with the same nominal bacterial efficiency rating. Add to this the aforementioned variables concerning the way the mask is donned (to which can be added taping or not taping the mask to the face) and the behaviours of the wearer (talking, coughing and so on) and the likelihood of bacterial dispersion becomes complex (5).
There are good practices that can be adopted by cleanroom operators and an assessment of facemask research can help to build a best practices framework. Both medical and cleanroom workers wear surgical masks, yet research into surgical mask use in the medical setting is more voluminous than research in the cleanroom setting. Hence, in setting out lessons to be drawn this paper assesses medical research (6). This paper presents an appraisal of the most important literature and presents findings for cleanroom managers working in pharmaceuticals and healthcare to consider.
Facemask function
The surgical face mask, as we would recognise it today, began to be used in the 1890s and became relatively commonplace in the operating theatres in Europe and the USA by the 1920s (7), although various forms of face coverings, of equally varying effectiveness, are traceable back to the plague pandemics of the Middle Ages. The surgical mask within the European Union is considered to be a medical device (sometimes referred to as a medical mask or a procedural mask), as per the Medical Devices Directive 93/42/EEC and Medical Devices Regulation (EU) 2017/745. The mask is typically formed from three layers of material: a melt-blown polymer (typically polypropylene) layer sandwiched between two layers of non-woven fabric (8). During manufacturing, 20 grams per square metre (GSM) of polypropylene fibres are produced by spinning bond technology, and 25 GSM non-woven sheets are fabricated by the melt-blown technology. The finished mask-form is pleated (9), to enable the mask to expand so that it fits the wearer more securely. With the three base components of the surgical face mask (10):
An innermost layer, designed to capture the moisture from the user’s breath.
A middle layer, designed to filter the air.
An outer layer, designed to be hydrophobic so that it does not allow water and moisture passage.
The outer layer and the innermost layer of this three-ply face mask design are formed from spun bond, non-woven materials. The middle layer is formed of melt-blown, non-woven materials. These melt-blown microfibres have a microporous structure and should be designed for good breathability. The three layers come together through acrylic bonding.
The mask is equipped with either elastic straps, to allow the mask to be tied or pulled around the head, or with ear loops. The purpose of the mask is to reduce the release of 'droplets' (particles larger than 5 or 10 µm in diameter) and aerosols (particles smaller than 5 µm) by retaining them within the mask material (11). Retention is through a combination of diffusion, interception, and impaction (12).
For the ‘surgical style’ mask (and hence conventional cleanroom masks) the European standard is EN 14683: 2019 (13). General manufacturing standards require an assessment for fluid resistance (resistance to penetration by synthetic blood under pressure (mmHg)), filter efficiency, differential pressure (assessed by the pressure drop across the mask as measured in mmH2O/cm2), and flammability. Within the European norm there are three classes of mask (Types 1 to 3) based on particle filter efficiency ratings, ranging between 95% and 98% in terms of the mask being able to filter particles of ≥3.0 µm; within cleanrooms, for sterile processing, the mask should be a Type 2 or 3 mask. The U.S. equivalent standard is ASTM F2100 (14). The U.S. standard describes an identical bacterial filter efficiency to the European one, although there is an additional requirement for a 0.1 µm particle filter efficiency rating (referred to as the ‘Particle Filtration Efficiency’ test). The bacteria filtration efficiency test is arguably of greater importance for working in cleanrooms. This test requires the use of Staphylococcus aureus as the challenge organism (probably because S. aureus is a bacterium of clinical relevance). To evaluate, the bacterium is challenged against a test mask in an aerosolised form at a flow rate of 28.3 L/m which simulates the range of normal respiration, and with a mean particle size of 3.0±0.3 µm. The test takes place with the inside of the face mask in contact with the bacterial challenge to simulate what the wearer may be exhaling. A suitable number of masks should be evaluated in order to establish confidence limits concerning the overall mask performance. The number of masks to be assessed varies between the European and U.S. standards. For the additional U.S. requirement for particle efficiency, this is assessed using a mildly degrading aerosol of sodium chloride (NaCl) with a maximum test challenge loading of 200 mg.
In terms of how such tests might relate to ‘real life’, the U.S. Centers for Disease Control and Prevention undertook studies in surgical units using settle plates and an Anderson impactor air sampler. This consisted of a comparison of the environment before surgeons entered, while surgeons simulated operations, and for comparing surgeons wearing face masks and not wearing face masks. This evaluation showed that wearing the surgical mark reduced wearer derived microbial contamination by 94% (15). Hence, the proportion of microbial carrying particles can be significantly reduced.
Yet facemasks, designed and tested to an appropriate standard, are still only effective when carefully managed and when they tightly fit the wearer (a point addressed below). Moreover, masks efficiency will degrade when the mask is subjected to physical, chemical, and thermal stresses. The integrity of the material can also be compromised during use by effects such as flexing and abrasion, and especially when the mask becomes wet, as might occur from water splashes or alcohol sprays or from the oral-nasal secretions of the wearer. A number of these factors are considered below; prior to this, it is useful to review the microbial challenges presented by the nasopharynx region.
Bacterial risks
It is perhaps overly obvious to state that facemasks are important due to the abundance of bacteria found within the nose and mouth and across the surface of the skin for this region of the human face. There are different populations found within the mouth, nose and on the skin.
Oral microbiome
Studies of the oral microbiome indicate that around 70 percent of the taxa are culturable, and 30 percent are unculturable. The main genera (from 16S rRNA gene-based and metagenomics analysis) are (16,17):
Gram positive:
Cocci – Abiotrophia, Peptostreptococcus, Streptococcus, Stomatococcus
Rods – Actinomyces, Bifidobacterium, Corynebacterium, Eubacterium, Lactobacillus, Propionibacterium, Pseudoramibacter, Rothia.
Gram negative:
Cocci – Moraxella, Neisseria, Veillonella
Rods – Campylobacter, Capnocytophaga, Desulfobacter, Desulfovibrio, Eikenella, Fusobacterium, Hemophilus, Leptotrichia, Prevotella, Selemonas, Simonsiella, Treponema, Wolinella.
Overall, streptococci and related species predominate. The oral microbiome is formed of different ecological niches: teeth, gingival sulcus, attached gingiva, tongue, cheek, lip, hard palate, and soft palate (18).
Nasal microbiome
Nasal bacterial density and microbiota composition is relatively diverse between people. The types of bacteria typically found in large proportions are: Corynebacterium, Cutibacterium acnes, and Staphylococcus epidermidis. These bacteria are found on around 9 out of 10 individuals, although the proportional abundance varies. Other bacteria commonly recovered, albeit in lower proportions, are: S. aureus (carried by between 25% and 60% of the population, depending on the country – medical papers are fairly wide ranging), Enterobacteriaceae—including Escherichia spp., Proteus spp., and Klebsiella spp., Moraxella spp. and Dolosigranulum spp (19).
Microbial carrying particles released from the nose and mouth
In terms of the risk of these organisms being expelled, most will be bound to particles or encased in droplets. Droplets are classified by the World Health Organisation (WHO) as being of ≥5.0 µm (20) and particles of this size have a propensity to settle quickly to the ground, usually within 1 metre of the site of generation, depending on the airflow dynamics (21). Aerosolised particles, from the WHO infection control perspective, are defined as particles ≤5.0 µm. These particles can remain suspended in the air for prolonged periods and are transferred a greater distance from the source.
Healthy individuals generate particles between 0.01 and 500 μm through normal respiration, and individuals with infections produce more particles of a slightly larger size - between 0.05 and 500 μm. This means that both airborne and droplet transmission present risks without a mask being worn. Since the 1940s it has been established that time is the major determinant of infection transmission (more so than distance); that is aerosolised particles released from one individual will travel an infinite distance, but they will remain in the air for a prolonged period of time. For example, a typical sneeze will expel particles around 3 metres from the source; however, the particles expelled will remain within the zero to 3 metre range for at least 20 minutes (22). This has been supported by studies undertaken during the COVID-19 pandemic where the risk of contracting the coronavirus increased the longer an infected person and a non-infected person spent together, as shown by studies on rail and aircraft journeys. Within a cleanroom, with effective mechanical ventilation designed to expel air from the cleanroom, such time periods can be significantly lowered but they will exist for a period of time. This is why, for instance, some facilities practice a time delay as personnel move through changing areas to enable any deposited particles to clear in accordance with the air change rate before the next group enters.
The size and quantity of aerosol and droplet release is dependent upon the respiratory activity. Influencing factors that can lead to fewer or more particles being released include relative humidity, particle aggregation and mucus properties within the human body. Humidity is also an influencing factor in terms of room environmental parameters as it affects the distance travelled, with increases in vertical and lateral particle movement being associated with a lower room relative humidity (below 50%) (23). Another factor is the behaviour of the mask wearer.
Limitations of culturability
What is apparent from the above reviews is that the diversity of microbial types that could be dispersed from the nose and mouth is wider than what is commonly recovered from cleanrooms (24). This is more reflective of the limitations of culture media and of culturability (issues that have been explored in related papers) (25) than necessarily confidence that masks are always worn and used correctly. Tryptone soya agar, for example, is the most common medium used for environmental monitoring and while it is effective at recovering Staphylococci and Micrococci (26), it is more limited at recovering Streptococci and other oral bacteria. These types of bacteria generally require agar supplemented with a blood base) (27).
Face mask controls
Wearing a face mask reduces the transfer of bacteria, in the form of aerosolised particles and droplets, from the wearer into the cleanroom space and onto surfaces or into product. This is provided:
Masks are of an appropriate design
Masks are worn correctly
Masks do not become wet or damaged
Masks are not worn beyond their maximum wear time
Masks are sterile, when required
The wearer does not talk or shout excessively
The health of the wearer is not adverse as to compromise the mask efficacy (such as suffering with respiratory illnesses triggering coughing and sneezing).
Each of these provisions are discussed below.
1.Appropriate design
Not all surgical facemask designs are equivalent and experimental studies suggest that between masks with equivalent filtration efficiency different designs may result in an increase or decrease in bacterial dispersion (28, 29). The type of material and the quality of the material are important determinants. As well as polypropylene, other fibres used in facemasks include polycarbonate, polyester, polystyrene, and polyethylene (30). The supporting material should be strong enough to maintain the filter properties during the mask usage (the thickness of fibre ranges from <1 to 10 µm). The most effective designs are multi-layered masks that fit tightly to the face, and which do not lead to any ‘dead space’ between the user and mask.
To support good design, the method of manufacture also needs to be consistent since variances in the manufacturing method, especially with the uniformity of the web structure (the cross-sectional shape of the fibre) (31), can affect the outcome. Achieving the correct weight of the middle layer is the most important determinant of efficiency. This is best achieved through superior manufacturing methods like electrospinning nanofibers (32). Simply put, just because a mask is labelled as a ‘surgical mask’ this does not mean it meets the required criteria and a degree of supplier oversight is required.
2.Wearing correctly and appropriate fitting
For a facemask to be effective, it not only needs to have the appropriate microbial filter efficiency and to maintain pressure during respiration, the mask also needs to fit the wearer securely (33). Standard cleanroom facemasks are designed to fit the ‘typical face’ according to the regional market (this is often ill-defined and variable). It is important that cleanroom operators ensure that the facemask allocated is suitable. Where a mask does not fit securely this leads to the phenomenon of deflection, where exhaled air and droplets are directed through a fine gap between the mask and skin, leading to outward leakage around the ‘face-seal’ perimeter.
To examine this effect of an ill-fitting mask, scientists at the U.S. Department of Energy's Center for Nanoscale Materials undertook a series of experiments. It was found that a 1% gap (of around one millimetre) reduced the filtering efficiency of all masks evaluated by 50% or more (34). This can arise from the way the mask is worn or due to a design deficiency. Incorrect wearing is a common issue in practice; one study assessed how well people in the medical field wore their face masks. The review of 1000 surgical unit staff found only 18% of personnel wore their surgical masks correctly) (35).
To improve mask fitting, this can be strengthened by the practice of double twisting the tie of the mask over the ear (bringing together the corners and ear loops on each side, knotting the ears loops together where they attach to the mask, and then tucking in and flattening the resulting extra mask material to minimize the side gaps). Double masking can also ensure a good fit, and this raises the pressure differential across the mask, although the discomfort factor for the wearer would need to be assessed (36).
An alternative method involves securing the nose bridge section with adhesive tape, with reduces the release of particles towards the eye. A Wills Eye Hospital study (Pennsylvania, USA) explored the following scenarios, with the participants required not to talk:
No mask worn.
Loose fitting surgical mask worn.
Tight fitting surgical mask worn.
Tight fitting surgical mask fixed with tape (across the nose bridge) worn.
Each stage was assessed after two minutes by sampling the release of bacteria on each subject’s forehead. It was found those wearing a tight-fitting surgical mask with tape recorded fewer bacterial counts compared with subjects wearing the same mask without tape (the difference was 0.93 CFUs [95% confidence interval 0.32-1.55]; P = .003); high counts were recorded under the other scenarios (37). The use of tape across the nose bridge has been demonstrated to be beneficial in other studies (38).
Another variable that affects how well a mask fits is the presence of facial hair, such as beards and certain hairstyles and certain facial features, such as the double chin. These can lead to displacement and deformation of the mask, especially during talking (39). Mask designs not only need to be flexible for different facial features, but the mask also needs to be comfortable. Discomfort affects users’ compliance and frequent readjustments by the worker presents a contamination control hazard.
3. Avoidance of damage
Damage to a mask, or with the mask becoming wet (such as fluid splashed onto the mask), will compromise the efficiency of the mask. In such circumstances, the mask should be changed through personnel exiting from the cleanroom and going through the appropriate change process. When it becomes wet, a mask can lose its protective filtration quality over time as a result of fluid exposure from both sides, and thus become a nidus of microbial accumulation. Airborne microorganisms can subsequently penetrate through the wet fabric by a process called “wicking” (40). Under the EN 14683 standard, masks which carry the letter ‘R’ as part of their labelling have passed a test for splash resistance (this applies to Types 2 and 3 only, Type 1 masks are never manufactured to be splash resistant).
4. Maximum wear time for a face mask
Any material-based filter will only operate for a finite period of time and the same applies to surgical facemasks (41). The mask efficiency deteriorates over time due to saturation effects. In particular, released droplets breakup and coalescence on the fabric, leading to a liquid film barrier developing over the fibrous porous surface of the face mask. When this builds up within the pore, the microstructure becomes blocked. The more pores that are filled, the less effective the mask becomes. This worsens with coughing (a condition that is explored below) since the saliva droplet composition rises as a result of cough dynamics.
A French study concluded that the typical surgical mask (meeting the criteria of the standard EN 14683) must be changed at least every 4 hours at the most (42). This four-hour maximum time is also recommended by WHO (43) as well as being backed by a British study (44). These studies determined that after four hours the surgical facemask no longer functions as an effective microbial barrier. Such findings are useful for cleanroom managers when proceduralising maximum mask wearing times. Reductions in wear time may need to be made under conditions of increasing temperature and humidity.
In addition to wear time, manufactured masks will only maintain their integrity for a finite period of time. Face masks are subject to natural ageing and will reach a date from manufacture beyond which their effectiveness cannot be guaranteed. This places an importance on expiry dating. Research generally indicates a two-year expiry, although this will vary between manufacturers, manufacturing method, and the source material (45).
5. Sterile face masks
For aseptic processing activities, the face mask needs to be sterile along with other clothing worn by the operator. There is nothing specific about the sterilization process that improves mask efficiency, and it is not inconceivable that some sterilisation processes might adversely affect efficiency, therefore the supplier of the mask should perform some of the efficiency tests using sterilised material. For the purchaser, an assessment of the sterility process and a review of the validation documentation should be performed as part of the supplier auditing process.
6. The effects of talking or shouting
It is regarded as good practice to minimise speaking within the cleanroom and to enforce this within aseptic processing areas (especially within EU GMP Grade A, where speaking should never be permitted). This is based on the expectation that bacterial release will be greater when talking occurs. This is supported by surgical unit studies, showing how the dispersion of oral flora reduces by minimizing speaking during a procedure (46), even under conditions where the duration of talking would be for less than five seconds (47).
The increased effectiveness of facemasks during “no talking” situations has been further evaluated. In one study, to assess the “talking” situation, each subject was given a script to read for two minutes at their normal speaking level with the data compared to scenarios where there was no talking for two minutes. Comparing the “no talking” scenarios and “talking scenarios” the difference was 1.1 CFU, with higher counts recorded under the “talking” condition. This was repeated using different facemasks. Irrespective of the type of mask used, subjects in the speech scenarios had significantly greater bacterial growth compared with the no talking scenarios. As well as concentration, there are also alterations of particle size. In situations where there was no talking, particle sizes released from normal respiratory processes are 0.8 μm at average; whereas particles averaged within the range 3.5 and 5 μm when subjects were talking (48).
Similar studies have noted how the variety of oral microbiota increases under the “talking” scenario (49). Under “no talking” scenarios, the most common bacteria recovered are Staphylococcal species (at around 64% of recovered bacteria). This probably indicates that these organisms have most probably been released more from the nose than from the mouth). In contrast, in the “talking” scenarios the proportion of Staphylococcal species reduced to 51% and the proportion of Streptococci increased (particularly Streptococcus mitis and Streptococcus viridans). Hence, when taking, the contribution of bacteria released from the mouth rises relative to those released from the nose alone.
Head and mouth movements
When wearing a mask for critical operations, such as interacting with a Grade A / ISO class 5 environment, movements should be kept to a minimum. Although masks will capture most of the released contamination, dermabrasion and skin shedding will occur at a faster rate and this increases with rapid movements through the mask to rubbing against the face and neck (50). Supporting studies have reported that a tendency of wearers to wiggle their faces beneath a surgical mask also increases bacterial dispersion (51).
7. Health of the wearer
It is good practice, especially for aseptic environments, for personnel with coughs, colds, and other respiratory infections not to enter the cleanroom. Such conditions affect facemask efficiency.
Cough cycles
The penetration dynamics of airborne droplet transmission are influenced by coughing and consequently the more a person coughs, the less effective the mask becomes. This relates to increased particle bombardment, displacement of aerosol emission upward and downward from the mask (52), lateral dispersion, and increased mask material saturation. Determining the impact of coughing on the mask is not straightforward since cyclic coughing incidents encompass complex fluid dynamics. Studies indicate that occasional coughing does not affect the mask performance (53); however, persistent coughing severely challenges the filtration efficiency of the mask (54). Persistent coughing was defined as ten cough cycles during the total wear time, and this led to the mask efficiency decreasing by around 8% (hence to a bacterial retention efficiency of below 90%). The variables controlled in the study were, for the room: zero wind speed, ambient temperature 2 °C, pressure one atmosphere, relative humidity 50%. With the test subjects, their mouth temperature averaged at 34 °C and their face skin temperature averaged at 32°C.
Sneezing
Similar effects occur with sneezing as they do with coughing (55). While the containment of the sneeze is easier, the discharge can present a concern in terms of moisture content, something that is influenced by the level of mucus.
Discussion
Within the cleanroom, while the use of a surgical facemask will not provide complete prevention from airborne droplet transmission, it reduces contamination levels significantly, provided masks from reputable vendors manufactured to an appropriate standard are purchased. These should be Type 2 or 3 masks (as per the European standard), splash proof, and sterile where required. When used correctly, facemasks contribute to a synergetic personnel contamination control effect in conjunction with other control measures.
This paper has considered the most important factors impacting upon facemask performance from design to their use in a practical setting. This has chiefly been by drawing on medical literature and considering this within the cleanroom context. There are many points of interest from the review, the most pertinent being:
Failure to wear a mask correctly leads to the potential release of droplets. Many people habitually do not wear masks correctly, thereby placing an emphasis upon training.
The use of surgical tape across the nose bridge improves the fit of the mask.
Wearing a mask for too long decreases the ability of the mask to contain aerosolised particles.
Those with respiratory illnesses will provide a significantly greater particle challenge to the mask, decreasing its relative efficiency as well as decreasing the maximum wear time.
We cannot grow all of the microorganisms associated with the nose and mouth on conventional media used for environmental monitoring, therefore we should not place and over-reliance upon monitoring and instead we need to focus on the control factors.
Given that talking increases the potential release of Streptococcal organisms, there is the real possibility that personnel talking within Grade A – even when wearing a mask – could release microbial carrying particles which would be severely underestimated using conventional monitoring methods.
Facemask efficiency needs to be thought of as something dynamic (and which is not necessarily constant). Efficiency will decrease over time and is particularly affected by the respiratory health of the wearer.
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Author Information
Corresponding Author: Tim Sandle, Head of Microbiology
Bio Products Laboratory ,
UK Operations, England
Email: timsandle@btinternet.com
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