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Personal protective equipment for surgeons during COVID-19 pandemic: systematic review of availability, usage and rationing

Abstract Background Surgeons need guidance regarding appropriate personal protective equipment (PPE) during the COVID-19 pandemic based on scientific evidence rather than availability. The aim of this article is to inform surgeons of appropriate PPE requirements, and to discuss usage, availability, rationing and future solutions. Methods A systematic review was undertaken in accordance with PRISMA guidelines using MEDLINE, Embase and WHO COVID-19 databases. Newspaper and internet article sources were identified using Nexis. The search was complemented by bibliographic secondary linkage. The findings were analysed alongside guidelines from the WHO, Public Health England, the Royal College of Surgeons and specialty associations. Results Of a total 1329 articles identified, 95 studies met the inclusion criteria. Recommendations made by the WHO regarding the use of PPE in the COVID-19 pandemic have evolved alongside emerging evidence. Medical resources including PPE have been rapidly overwhelmed. There has been a global effort to overcome this by combining the most effective use of existing PPE with innovative strategies to produce more. Practical advice on all aspects of PPE is detailed in this systematic review. Conclusion Although there is a need to balance limited supplies with staff and patient safety, this should not leave surgeons treating patients with inadequate PPE.


Introduction
In December 2019, clusters of patients presenting with severe pneumonia of unknown origin were reported in the city of Wuhan, Hubei Provence, China. Epidemiologically, these were linked to a seafood market in the city, and on 7 January 2020 the causative organism was identified, a novel coronavirus, now termed SARS-CoV-2 1 . In March 2020, the WHO declared a global pandemic 2 , which has gathered speed across the world despite increasingly more drastic non-pharmacological interventions (NPIs) to limit its spread. With one-quarter of the world's population now living under some form of government-mandated lockdown, and over three million documented cases worldwide, NPIs are the main public health measure that policymakers are using to reduce viral transmission 3,4 . Social distancing aims to flatten the curve of new infections, thereby avoiding a surge in demand on healthcare systems, but these effects may take weeks or months to manifest. Epidemiological modelling has shown that the pandemic could last for 12-18 months, and that social distancing may need to continue until a vaccine has been developed 3 .
The impact of this crisis on surgical services will be wide ranging 5 . Many thousands of patients worldwide have been deprived of surgical access, and are waiting to undergo elective and emergency surgical procedures. They will become part of the second and subsequent waves, with undoubted morbidity and mortality as a collateral effect of the COVID-19 pandemic 6,7 . Currently, the majority of evidence is of low quality, including case series and observational studies, with heterogeneous populations and surgical intervention groups. Fortunately, global collab-WHO modelling of personal protective equipment (PPE) for healthcare professionals has estimated that 89 million medical masks, 76 million gloves, 1⋅6 million goggles and 30 million gowns are required for the COVID-19 response each month 9 . China is the major producer and supplier of PPE globally, and its exports have come to a halt as the infection spreads domestically 10 . A combination of disruption to worldwide supply chains and international travel restrictions, combined with exceptionally high levels of demand, slow release of pandemic stocks as well as confusing and ever changing PPE guidelines, has led to a lack of PPE for frontline medical staff 11 , and confusion around when it is needed 12 . This systematic review summarizes the SARS-CoV-2 transmission risks for different surgical specialties, provides clarification on the appropriate use of PPE in the context of current specialty and national guidelines 13 , and discusses the ethical dilemma of PPE rationing that we are currently facing.

Methods
This systematic review was undertaken in accordance with PRISMA guidelines 14 . MEDLINE (via PubMed), Embase and WHO COVID-19 databases were searched. Newspaper and internet article sources were identified using a media database called Nexis (https://www.lexisnexis .com/en-us/products/nexis.page). The search terms used were: ('Surgeons'[mesh] AND ('personal protective equipment'[mesh] AND 'COVID-19'[mesh]). Appendix S1 (supporting information) shows the search strategy for MED-LINE, which was adapted for other databases. There was no restriction on publication type. This search was complemented by an exhaustive review of the bibliography of key articles. Results were restricted to articles in the English language.

Inclusion and exclusion criteria
All studies on the application of PPE in surgery during the COVID-19 pandemic were included. This included articles that reported on potential risks of transmission in surgery, types of PPE, specialty-specific risks and guidance. Articles that described PPE not in relation to surgery or COVID-19 were excluded, as were those not written in English.

Data extraction and assessment of study quality
Two authors independently assessed the articles for inclusion and exclusion criteria and extracted data, with a third author resolving any differences. The data extraction was independently checked by the senior author. The following baseline data were extracted from each study: first author, year of publication, data collection period, geographical location and surgical specialty. Data were extracted on the sources of transmission in surgery, types of PPE recommended, surgical specialty-specific risks and considerations, PPE shortages and rationing.

Narrative synthesis
Given the marked heterogeneity in study design and types that have been published during the emerging COVID-19 pandemic, a narrative synthesis was performed according to the guidance on the conduct of narrative synthesis in systematic reviews 15 . Three authors systematically summarized each article using bullet points to document key aspects of each study, focusing specifically on the availability, usage and rationing of PPE in surgery. The senior author identified and grouped common themes, divided larger themes into subthemes, tabulated a combined summary of the article, and synthesized a common rubric for each theme.

Results
A total of 1329 articles were identified from all literature sources, leaving 1024 for screening of titles and abstracts following removal of duplicates. Ninety-five studies met the inclusion criteria and were included in the narrative synthesis ( Fig. 1 and Table 1).

Sources of transmission during surgery
Transmission of SARS-CoV-2 takes place via particles or droplets containing the virus (larger than 5 μm, travel less than 1 m) as well as aerosol (smaller particles less than 5 μm, travel more than 1 m), via fomites and subsequent direct contact (touching eyes, nose or mouth) 16,17 . This is recognized to be especially high risk for healthcare professionals performing resuscitation 18 . PPE requirements have largely been defined based on whether a procedure is aerosol-generating or not 19 . Although airway procedures such as intubation, extubation and suctioning are widely recognized to generate aerosols, specific aerosol-generating procedures (AGPs) have been less well described, but are critical to identify during the COVID-19 pandemic to guide where extra PPE precaution is indicated ( Table 2) [20][21][22][23][24][25][26] . A study 27 showed that SARS-CoV-2 RNA from sewage samples was positive from inlets of the sewage disinfection pool and negative from the outlet of the last sewage disinfection pool, suggesting that strict disinfection and hand hygiene could decrease the hospital-associated COVID-19 infection risk to staff in isolation wards 27 .  Other than AGPs, the risks of transmission include the fumes released during surgery and contaminated body fluids. Owing to the novelty of COVID-19 there is no definitive evidence to quantify the risks of transmission via smoke derived from open or laparoscopic surgery. However, there is enough evidence based on previous studies to support steps being undertaken to manage the potential risks 28 .
Electrocautery creates particles with the smallest mean size of 0⋅07 μm; laser tissue ablation generates larger particles with a mean size 0⋅31 μm, and the largest particles are generated by the ultrasonic (harmonic) scalpel, at 0⋅35-6⋅5 μm 29 . The smaller the particles, the further they travel. Smaller particles are more chemically based, but as the particulate matter increases in size, it poses more of a biological hazard, acting as a vector for pathogen transmission, with larger particles travelling up to 1 m from the operative field 30 . The majority of smoke evacuation and filtration modes facilitate capture of particles larger than 0⋅01 μm. As the SARS-CoV-2 aerodynamic size is described in the range of 0⋅06-0⋅15 μm 29,31 , the use of devices with smoke evacuation filters theoretically reduces local inoculation. Previous work has confirmed viral content (papillomavirus and human immunodeficiency virus) within surgical smoke 32,33 , and documented operator contraction of a papillomavirus using carbon dioxide laser 34 .
There are also risks of transmission owing to urine spillage and aerosolization in open and minimally invasive urological interventions, with Ling et al. 35 reporting persistence of SARS-CoV-2 nucleic acid in urine. Although disease transmission of COVID-19 through urine has not yet been demonstrated, the European Association of Urology Robotic Urology Section 36 stated that urethral or ureteral catheterization during laparoscopic and robotic procedures should be treated with caution. The British Association of Urological Surgeons has described the risk of operator contamination from urine splash as minimal and stated that aerosol risks are more significant from patients coughing during intimate procedures, such as catheterization, or following intubation/extubation. Furthermore, SARS-CoV-2 RNA has also been identified in faeces 37 .
Many studies have found that SARS-CoV-1 RNA can be detected in plasma, since the first report on 10 April 2003 [38][39][40] . Overall, 78 per cent of patients had detectable viral RNA in the first week of their illness 41 , in line with data on MERS-CoV 42 and SARS-CoV-2 43 . Owing to the risk of asymptomatic carriage and the presence of Verbeek et al. 24 2020 Cochrane Database Systematic Reviews Personal protective equipment for preventing highly infectious diseases due to exposure to contaminated body fluids in healthcare staff virus in the blood, the European Centre for Disease Prevention and Control (ECDC) and the American Association of Blood Banks have published rapid risk assessments regarding blood safety during the pandemic. The ECDC implied a precautionary deferral of donation of blood and cells for 21 days after possible exposure to a confirmed patient or by anyone who returned from Wuhan, China, applying the approach used for SARS-CoV-1 and MERS-CoV 44 .

Types of personal protective equipment
Recommendations made by the WHO regarding the use of PPE in the management of patients who have, or are suspected to have, COVID-19 in community and hospital settings have evolved alongside developing evidence regarding transmission 13 . The standard PPE guidance from Public Health England (PHE) for healthcare workers involved in the direct care (within 1 m) of patients with confirmed or suspected COVID-19 include: disposable apron, gloves, a fluid-repellent surgical mask and eye protection comprising either goggles or a face shield 45 . When working in high-risk units (ICU, high-dependency unit, accident and emergency, resuscitation, wards with non-invasive ventilation or continuous positive airway pressure ventilation, operating theatres, endoscopy units) or in the operating theatre where AGPs are being undertaken, a respirator (N99 or FFP3 equivalent, which can be either valved or unvalved) is recommended instead of a surgical mask, along with a fluid-repellent long gown 46 and full-face shield or visor 13,45,46 (Fig. 2). PHE is in support of full PPE in relation to AGPs conducted in any patient; given the high asymptomatic carrier rate of 16-50 per cent reported in some populations 47 , the assumption should be made that all patients, regardless of symptoms, are COVID-19-positive. Respirator masks are categorized according to their ability to filter fine particles in the scale of 0⋅01-1 μm in size according to the European Union (EU)-defined Filtering Face Piece (FFP) scale, whereas SARS-CoV-2 measures 0⋅07-0⋅09 μm in diameter on electron microscopy 48 . FFP3 masks represent the standard of precaution, able to filter over 99 per cent (offering 100-10 000-fold protection), compared with 63 per cent (6-fold) for standard surgical masks 49 (Fig. 3). Constraints within the National Health Service (NHS) have been recognized, and both FFP2 or N95-equivalent respirators offer high levels of protection if fitted well, with a minimum efficiency of 92-98 per cent (offering 100-fold protection) (Fig. 4). Protection using FFP2/3 respirators has been reported to last up to 8 h and current guidelines support sessional use in the care of multiple patients in red zones 50 , whereas protection has been reported to last 30 min for fluid-repellent surgical masks 51 . It is important to note that masks alone are not the panacea, and need to be combined with correct fitting via fit tests, avoidance of face/mask touching, regular hand washing and social distancing to minimize transmission 13 .

Surgical specialty guidance for personal protective equipment
The current advice from UK surgical professional bodies is summarized in Table 2. Emerging evidence has highlighted that certain subspecialties are at higher risk based on their potential exposure to high viral loads in mucosal membranes of the nasopharynx and oropharynx, such as ear, nose and throat (ENT), maxillofacial, and plastic and reconstructive surgery of the head and neck 52,53 . Most specialty guidelines recommend avoidance of AGPs wherever possible, but full PPE is advised if this is required.
The British Association for Paediatric Otolaryngology and ENT UK in conjunction with the National Tracheostomy Safety Project have outlined measures for tracheostomies in an effort to reduce potential risks. The documents highlight the requirement to balance the need for a tracheostomy versus the potential risks to both the patient and staff 54 . Many further publications relating to changes in ENT practice have been published [55][56][57][58][59][60] . The British Association of Oral and Maxillofacial Surgeons guidance recommends full PPE for all close face-to-face contact with patients, not only during treatment but also examination, until the current trajectory has flattened 61,62 . This can be applied to other surgical specialties such as plastic surgery and ENT, which involve examination and treatment of the head and neck area when managing trauma or cancer near the aerodigestive tract [63][64][65] .
In other specialties there has been a drive to identify high-risk procedures and minimize their use where possible 66 . In general surgery, laparoscopy and endoscopy should be performed only where there is no alternative and laparotomies carried out wearing full PPE [67][68][69][70] . Similar changes in guidance have been seen in gynaecology 71,72 , paediatric surgery 73 , urology 74 , orthopaedics 75,76 , head and neck cancer 77 and neurosurgery 78 .

Shortages of personal protective equipment
In the short history of this pandemic, medical resources have already been rapidly overwhelmed, including PPE. In recent days, there have been well reported critical shortages of gowns 79 and masks [80][81][82] in particular, with famous businesses supporting the national need in addition to other philanthropic donations 83,84 . In response to the shortage, there have been reports of healthcare workers resorting to procuring their own PPE 85 . The recognition, by the WHO and others, that the current global stockpile of PPE is inadequate to meet not only the current need but also future escalating demand 13 , has resulted in multiple changes to PPE guidelines published around the world, including PHE, which has been criticized for basing guidance on availability of resources rather than maximizing the safety of healthcare professionals 86 . The most recent changes, dated 17 April 2020, include PHE suggesting three options if the supply runs out, including sessional use of PPE, reusing it or using alternatives to standard PPE 87 . The shortage of PPE combined with unclear and changing guidance has resulted in anxiety and confusion for healthcare workers.
The Royal College of Surgeons of England (RCS) found that almost one-third (32⋅5 per cent) of UK surgeons do not have access to enough masks, gowns or eye protection, from a survey of 1978 surgeons and surgical trainees, and has described a widespread lack of PPE for frontline staff [88][89][90][91][92] . The RCS recognizes that surgeons should not risk their health if they have inadequate PPE [93][94][95] . In response to the PPE shortage, ENT UK 61 highlighted that although 'FFP3 masks are a precious life-saving and protecting resource, clinical staff are also life-saving resources and deserve the best protection we can offer'.
The medical workforce is at high risk of exposure as well as increased viral infective dose, thought to translate to viral load, an independent factor in the severity of the illness. In Italy, healthcare workers including several surgeons experienced high rates of infection and death owing an early lack of PPE 96 . There have also been early deaths, again including surgeons, among healthcare workers reported in the USA and the UK 97,98 . There is good evidence that improved access and use of PPE vastly reduced healthcare worker infections in both Italy and China 99 . Data extracted from Langrish et al. 49 and graphs modified from https://smartairfilters.com/en/blog/comparison-mask-standards-rating-effectiveness/.

Ethical dilemma of personal protective equipment rationing
Healthcare resource allocation has political, economic and moral dimensions, and rationing is inevitable in a system where there are limited resources. The National Institute for Health and Care Excellence routinely rations treatments based on quality-adjusted life-years (QALYs), which represent beneficial health activity; the lower the cost per QALY, the more efficient the healthcare activity 100 . Rationing of PPE adds a new dimension to modern healthcare practice. We are no longer rationing between patients but between healthcare workers, with organizations having to respond to the changing situation on the ground 66,77,78,101 . Ethical guidance regarding justice within healthcare rationing has often been written by health economists 102 ; professional philosophers have been reluctant to tackle day-to-day policy questions, reflecting the great difficulty in forming ethically sound answers 102 . There has always been an acceptance that working in a healthcare setting carries a level of personal risk; however, it would seem unreasonable for a healthcare worker to carry out a healthcare activity if there were a high risk of death 103 . In the Ebola crisis, 58⋅3 per cent of healthcare workers infected with Ebola died in the three worst affected countries 104 . In reference to the General Medical Council's best practice of 'making the care of your patient your first concern', in his book Tough Choices, Sokol 105 stated that in 'extreme circumstances -such as epidemics, where treating patients involves a high risk of infection and modest benefits to patients -doctors' obligations to their children, parents, siblings and loved ones take priority over the care of patients'.
A doctor's duty of care creates an implicit and explicit social contract with both patients and society as a whole, to care for and treat patients despite a degree of personal risk 102 . PHE and other public health bodies have suggested a minimum level of PPE for specific interactions with patients with, or suspected to have, COVID-19 (Fig. 2) and, combined with variations in guidance from different national and international bodies with differing local interpretations of guidance and poor communication, a sense of fear has understandably been created among healthcare professionals.
Guidelines for the rationing of PPE should follow the scientific evidence and also be morally defensible. A utilitarian approach, where the greatest good for the greatest number is promoted, provides a valuable ethical framework and is intuitively scientific as it focuses on the consequences, as being the morally significant entity. It is scientifically justifiable to provide maximal PPE for higher-risk procedures such as AGPs. Some clinicians are better placed to treat patients with COVID-19 than others. A utilitarian approach would support protecting these people who could provide the most benefit. Other clinicians may be offered lower levels of protection or their work activities reduced to limit the demand on PPE supplies. To limit certain activities is acceptable; however, to discriminate between clinicians would be a difficult moral calculation and likely to cause considerable distress 106 .
Other ethical considerations such as reciprocity and social worth have also been proposed 106 . Reciprocity involves giving more protection to clinicians who are most vulnerable owing to the higher level of risk that their job entails. For example, intensivists and anaesthetists who regularly perform aerosolizing procedures may deserve the maximum level of protection, not just from a scientific perspective but also a moral one. Social worth is not typically seen as a morally permissible way of allocating resources. In extreme situations, such as a pandemic, where certain roles are essential for the functioning of society, it may become permissible. The idea of key workers being allowed to work and receive special benefits has been derived from this concept.
Protecting the vulnerable is another important ethical consideration. People with significant underlying health conditions, such as cancer or immune deficiencies, have been advised to shield and stay home, and lifting lockdown too early will result in an excessive number of deaths 107 . However, with emerging evidence that black, Asian and minority ethnic (BAME) groups are at higher risk of severe COVID-19 infection, it is imperative that this is urgently investigated, and guidance is developed to protect healthcare workers in at-risk groups 108 .
A utilitarian perspective, using scientific evidence and principles such as social worth, reciprocity and protection of the vulnerable, provides a useful framework for making difficult rationing decisions regarding PPE 106 . No one system of allocation will be acceptable to all 109 . Recent reports of reusing/washing gowns in circumstances of acute shortages of PPE and delays in international shipments 96,110 have brought into sharp focus the difficult decisions that lie ahead. It is imperative that decisions and the rationale behind them are transparent and collaborative with all relevant national bodies. This will limit the amount of moral residue and help with rebuilding after the pandemic is over 105 .

Innovation
Owing to global issues with the supply chain of PPE, many countries have looked to innovative solutions. An initial focus has been on producing reusable PPE, to reduce both the economic and environmental impact (28 per cent reduction in natural resource energy consumption and 93 per cent reduction in solid waste generation) 110,111 , alongside the exploration of simple measures that could aid personal ownership of items and tracking of individual use in hospital settings, increasing the acceptance of resterilized items 112 .
The European Association for Additive Manufacturing has responded to a request from the European Commission to help produce medical equipment for hospitals tackling the COVID-19 outbreak 113 and, in the UK, emergency working groups have been set up: the Sustainable Hub for Innovation, Execution, Launch and Distribution in England, and the South Wales Additive and Rapid Manufacturing Consortium in Wales. These groups have brought industry leaders, scientists and government together in an umbrella collaboration to create innovative solutions to meet the PPE demand, including cutting edge printing hubs. In addition to producing new equipment, novel repurposing of existing theatre equipment has been undertaken, such as adaptation of orthopaedic helmet systems used for elective arthroplasties, where manifolds were 3D-printed and hoods sewn on to the helmet 114 .
There have even been attempts to create electronic PPE by using telemedicine tools to perform electronic medical screening examinations, which has the potential to conserve PPE and protect providers while maintaining safe standards for medical screening 115 .

Discussion
In the short history of this pandemic, medical resources have been rapidly overwhelmed. There has been a huge focus both in the NHS itself and the national press regarding PPE. Lessons from China showed that high healthcare worker infection rates were only improved once PPE was adequate. As a nation, we have had time to plan for this pandemic compared with other less fortunate countries such as Italy and China, where relatively large numbers of healthcare workers succumbed to COVID-19. Such planning has been widely criticized in the scientific press 116 , and in recent days there have been well reported critical shortages of PPE in the UK including gowns and masks. After missing out on an opportunity to join the EU joint procurement scheme to bulk-purchase PPE, there has been an ever more urgent need to secure and coordinate supply chains 117 . Boris Johnson has recently appointed a PPE 'tsar', former London Olympics chief executive Paul Deighton, to coordinate, source and boost manufacturing of protective equipment needed to protect NHS staff.
The medical workforce is at high risk of exposure as well as increased viral load and, although there is a need to balance limited supplies with staff and patient safety, this should not leave the healthcare professionals treating patients with inadequate PPE. The British Medical Association, RCS and Royal College of Nursing have all spoken out, saying that their members should not be in this position. We are learning more about the novel pathogen SARS-CoV-2 as worldwide research is carried out and shared, including identifying the staff most at risk -men, those with high BMI, increased age and co-morbidities, and those from the BAME community 118 . National guidelines must keep pace as new information comes to light to protect those most at risk.
These are unprecedented times when difficult decisions need to be made. However, in the case of rationing PPE, these decisions should be transparent, collaborative, accountable and adaptable as evidence of the pandemic evolves, rather than disguised as guidelines with the minimum level of protection. Changes in guidelines should be communicated honestly and clearly to the public and frontline healthcare professionals without political spin or ambiguity. Making morally sound policies is equally as important as following the scientific evidence to maintain trust, solidarity and a functioning society. Until there is a vaccine or proven treatments available, the requirement for surgeons to limit their workload and take sensible precautions is imperative in reducing transmission, flattening the curve, protecting themselves and patients, and reducing the death toll.