The coronavirus disease 2019 (COVID-19) pandemic has required modifications to both clinical care and research. Cardiopulmonary exercise testing (CPX) with gas analysis is a valuable clinical tool and common measurement outcome in research protocols. Clinically, a CPX test has numerous indications, including the determination of exercise intolerance, disease risk and diagnosis, prognosis, and in evaluating surgical candidates (1–5). Researchers often use CPX to objectively describe fitness levels, prescribe exercise, and measure changes in fitness and outcomes following an intervention in both healthy and disease populations (5–11). Therefore, it is desirable to continue performing this valuable test during the COVID-19 pandemic. As clinical volume gradually returns to normal and research protocols are approved to restart, the safety of the patients, subjects and testers must be addressed by precautions to prevent the spread of the disease when performing a CPX test (12,13). Although there is an abundance of available information on general COVID guidelines provided by the Centers for Disease Control (CDC) (https://www.cdc.gov/coronavirus/2019-ncov/index.html), information on how to safely set-up and perform CPX testing is lacking. When modifying a CPX protocol for the COVID-19 era, both government guidelines and local institutional requirements must be considered. Despite the need to continue CPX testing with the use of modified protocols to ensure safety for all involved, the specific means by which to maintain safety largely remain unaddressed. The purpose of this article is to describe recommended steps to maximize the safety of all involved that should be taken — from prescreening to posttesting.
Setup, Workflow, and Planning for a Safe Environment
Prior to initiating any modifications, an objective analysis of the testing area, workflow, and available resources should be performed. For the purpose of minimizing risk, liability, and to follow guidelines within each individual institution, it is advisable to have several planning meetings between relevant stakeholders. This should include representation from the CPX laboratory who is familiar with testing and an infectious disease consultant from the institution or local medical facility. So all are aware of the testing environment, it is highly recommended that an on-site walk-through be included in planning. Facility preparations may include improving ventilation, adding a high-efficiency particulate air (HEPA) purifier, determining the maximal number of staff allowed in the CPX testing room, adjusting equipment or furniture to maintain social distancing whenever possible, minimizing other activities or foot traffic occurring during the testing times, and constructing a check-in kiosk with COVID-19 screening (for contact tracing, temperature, etc.) at the entrance. In addition, planning for personal protective equipment (PPE) must be considered and ordered prior to testing as well as staff training on proper use of the PPE. Safety of staff must be considered by assessing potentially high-risk individuals or offering staff discretion not to perform testing without penalty. To properly sanitize the equipment and environment, a mock run-through should be performed to determine work flow and necessary time in between tests. A system of COVID-19 screening questionnaires, by both verbal scripts and written documents, also should be created as part of a standard operating procedure (SOP). It is helpful to create a shared folder on a password protected network for team members to access information on purchased PPE, SOP protocols, screening forms, institutional policies, and other information unique to COVID-19 CPX testing (e.g., relevant CDC or United States Environmental Protection Agency (EPA) web sites listing approved disinfectants).
The COVID-19 virus can be transmitted through aerosols and droplets by talking, coughing, sneezing, and laughing, in which the virus can remain stable and infectious across a wide range of environmental conditions for a considerable length of time (14). Because of the increased ventilation and bodily fluids naturally occurring during exercise, the necessity for staff to shout instruction or motivation to the exerciser and the potential for the patient or client to display aggressive body movements at high intensities of exercise, a CPX is associated with increased risk for all parties involved (15). Therefore, any precautionary measure that can potentially reduce the exposure to either airborne particles or through surface contact is of benefit. The primary equipment of interest can be grouped into three general categories; PPE, screening, and disinfecting, and the metabolic cart. The equipment and estimated costs are listed in the Table. Pricing may differ depending on brand, quality, and volume of purchase. The Table should be used as a starting point to plan specific laboratory needs. If possible, one should explore off-setting costs through negotiation with administration, grant budgets or as a through charge passed on to a contractor or client. A brief description of each equipment's use and importance is below.
Recommended additional equipment and approximate cost for safe CPX testing.
||Approximate Cost ($)
||• Daily use, unless soiled
• Multiple layering
• N95 preferred
||$3 to 7 each
||• Daily use, clean after each CPX test
• Universal fit/full cover visor
|Polyethylene isolation disposable gowns
||$50 to 150/10 to 150 count
||• Discard after one CPX test
• Level 2 (low risk) recommended
• Elastic cuff recommended
||$20 to 30/100 count
||• Discard after one CPX test
• Recommend ordering multiple sizes
|Screening and disinfecting
|Noncontact infrared forehead thermometer
||$100 to 150 each
||• Manufacturer guidelines
|HEPA air filter
||$200 to 400 each
||• Manufacturer guidelines
|Purell hand sanitizer
||$20; extra-large (67.6 oz) hand pump
||• Use frequently and liberally
|Clorox disinfecting bleach-free wipes
||$12/75 wipes/tub; 3 tubs/pack
||• Check on EPA website to insure kills COVID-19; https://www.epa.gov/pesticide-registration/list-n-disinfectants-use-against-sars-cov-2-covid-19
|70% Isopropyl alcohol wipes
||$10 to 15/50 to 200 counts
||• Does not leave residue when wiping face shield
• Kills COVID-19 in 30 to 60 s
|Oxivir replacement wipes
||$120/160 wipes/pack; 4 packs/case
||• Alternative wipe
• Use on all equipment after each CPX test
|Virex II disinfectant spray
||$30/32 oz. (4 pack)
||• Alternative wipe
||• Discard after one CPX test
||• Discard after one CPX test
|Silicone membranes (leaflets)
||$24 each/ sold as individual units
||• Discard after one CPX test
|Hose (9 ft or 2.74 m)
||$30 each or $25 > 10
||• Discard after one CPX test
|Water trap filter
||$24 per pack/6 filters in a pack
||• Discard after one CPX test
aDependent on vendor, institution discount, and metabolic cart manufacturer.
bContain only antimicrobial ingredients (e.g., hydrogen peroxide, ethanol) that are not known to cause occupational asthma or cancer. These surface disinfectants can often replace chlorine bleach or quaternary ammonium chloride compounds, which have been linked to these adverse human health effects.
It should be noted that the CDC does not routinely recommend using gloves over hand hygiene or gowns in patient care tasks that do not involve patients under active droplet/respiration precautions. Shield use is recommended only in areas where COVID transmission rates are high, but not necessarily recommended if transmission rates are low. However, we recommend using surgical face masks or N95 respirators, gloves, and gowns to be overly cautious if resources are available.
Surgical face masks act as a protective barrier to prevent splashes, sprays, large droplets, or splatter from entering the wearer's mouth and nose (16). N95 respirators (filtering face piece) are preferable, however cost and availability may be limiting. Therefore, surgical face masks are a secondary option. In addition, N95 users should be fit tested by the institutional safety office (e.g., occupational and environmental safety office) to determine the proper mask size ensuring there is a good seal. Specific to a CPX test, it is recommended that staff wear face masks and face shields because of the close proximity required when prepping a client (e.g., applying electrodes, taking blood pressure and constructing the head gear) and the potential of aerosol or droplet spread when removing the mouthpiece immediately after the CPX and the unavoidable deep exhalations and loud talking that occur throughout the test. Surgical face masks also help prevent the wearer from spreading respiratory droplets. Surgical face masks should be worn in accordance with parameters in FDA's Model Food Code sections 4-801.11 Clean Linens and 4.802.11 specifications, and be single-day use. Everyone (including the client when not fitted with metabolic cart head gear) should wear a face mask at all times to reduce the spread of illness. To prevent contamination, the mask should not be touched while in the patient environment, and the mask should not come in direct contact with any surface in the patient environment. If either of these situations occur, the mask should be disposed of and a new one obtained.
Face shields add an additional protective barrier to minimize eye or face exposure from potential splashes and sprays, or aerosols generated during exercise and prolonged face-to-face or close contact with a client during pretesting and posttesting activities. Provided the shield is not contaminated with bodily fluids and structural integrity remains intact, staff members may reuse their face shield for each CPX test in a given day provided they are thoroughly cleaned between each test with an approved disinfectant or alcohol. The disinfectant should be allowed to dry prior to reuse of the face shield. If streaking has occurred, use paper towels to remove any residue left on the face shield. To do this, first use a damp paper towel and then follow it with a dry paper towel. If personnel touch their recycled face shield, they should immediately sanitize their hands or change gloves.
Nonsterile, disposable protective gowns should be worn at all times in the testing area to prevent pathogens from contaminating clothing. Nonsterile, waterproof gowns are advised for use in the posttesting equipment disassembly and cleaning area to protect clothing from contaminants and chemicals used in the high-level disinfection process. Gowns should be changed out (discarded) between each test. It is recommended to use gowns that meet the Association of the Advancement of Medical Instrumentation level 2 standard. A detailed description of gown standards can be found at https://www.fda.gov/medical-devices/personal-protective-equipment-infection-control/medical-gowns.
Disposable medical gloves should be worn at all times and changed between each test. Personnel should minimize the amount of hand contact with objects and individuals (both clients and self) at all times. Those handling the breathing equipment (after the test) should dispose of their gloves immediately when finished with this task.
Screening and Disinfectant Equipment
Due to the necessary close proximity between individuals during test preparation (electrode and head gear preparation) and the unavoidable volume of air being moved during a CPX test, it is paramount care be taken both prior and during the CPX test to minimize potential transmission. Furthermore, recent research demonstrates the COVID-19 virus can remain airborne longer and travel farther than earlier predicted in the COVID-19 pandemic (17). While SARS-CoV-2 virions are around 60 to 140 nm in diameter, larger respiratory droplets and air pollution particles (>1 μm) have been found to harbor the virions. HEPA filters are very effective, and are certified to capture 99.97% of particles that are precisely 0.3 μm in diameter. The COVID-19 particle is ~0.125 μm; however, the droplets it travels in — when people cough, talk, or breathe — initially are larger, ~1 μm. A particle size of 1 μm is easily captured by HEPA filters. Although there is no direct evidence that air filtration works to prevent the transmission of COVID-19, there is theoretical evidence for its use (18). This evidence comes from similar viruses, like SARS. During the SARS outbreak in 2003, both the United States CDC and the Hong Kong Hospital Authority recommended use of portable air purifiers with HEPA filters to help reduce viral concentrations and disease transmission to health care workers if isolation wards were not available. Furthermore, recent research suggests that air filtration can reduce the risk of transmission of viral particles such as viral influenza (19,20).
When purchasing disinfectant products, first check with your institution for a preapproved list of products. It is recommended that only EPA-approved sanitation wipes that kill CoV-19 type 2 (COVID-19) be used. These can be found at https://www.epa.gov/pesticide-registration/list-n-disinfectants-use-against-sars-cov-2-covid-19. It is important that team members follow the instructions for use, allowing sufficient contact time to pass (up to 30 min) for the disinfectant to be effective before proceeding to use on another patient.
Metabolic Cart Equipment
Our human performance laboratory has identified several pieces of equipment that can potentially become contaminated and contribute to virus transmission. These include the mouthpiece, nose clip, silicone membranes (leaflets), hose, and water filter trap. Because of this added risk, we have chosen to change out and discard each piece of these equipment components between tests. Although this is a conservative approach that adds cost and time, we believe the infection risk reduction outweighs this burden. However, it is understandable if this view is considered wasteful and environmentally unfriendly. We advise consultation with institutional infectious disease experts and bioengineering in making this decision. Other pieces of equipment should be sanitized per manufacturer and institutional standards as usual (e.g., housing (valve body), inhalation/exhalation port, diaphragm O-ring, saliva catch, and headgear). Some metabolic carts use breathing masks instead of mouthpieces. If a breathing mask is used, it should be cleaned or discarded depending on resources available and manufacturer guidelines on disinfecting.
Prescreening of Patients and Subjects
It is very difficult, if not impossible, to definitively rule-out COVID-19 in light of testing sensitivity. Comparable to other PCR infectious disease based tests, there is a window period whereby a test is negative, yet the person is infectious. This window period for the viral, PCR-based, COVID-19 test is approximately 3 d. Although this may be considered a false negative, it is more accurately described as a period when the RNA level is below the threshold of detection (21). Each institution should abide by their institution's clinical protocols, if applicable. Since a CPX test is an aerosol-generating procedure, it should be avoided in an active COVID-19 patient. In a recovering COVID-19 patient, it is recommended that consultation with the caring physician be used to determine when to perform a CPX. Within 24 h of a scheduled appointment, clients should be screened by phone using an institutionally approved screening form or questionnaire involving symptom status, interaction with others, and potentially recent travel. If applicable, one should consider an online screening tool that can be accessed prior to the appointment. If the purpose of the CPX is research-oriented, a virtual informed consent may be utilized with Institutional Review Board approval. An example of a screening form is included in Figure 1, as was adapted to contain CDC screening guidelines (22). If the client screens negative, they should be provided a contact to call immediately if they develop symptoms before their in-person visit. If the client screens positive, the appointment should be postponed or canceled, and the individual should be advised to self-isolate until given further medical guidance.
Day of Appointment Prescreen
If not in a hospital setting with the infrastructure of a check-in desk (e.g., exercise physiology laboratory), it is advised to create a check-in kiosk at the building entrance equipped with a noncontact infrared thermometer, log-in sheet, screening forms, additional face masks, and hand sanitizer. It is recommended the check-in station be outfitted with a plexiglass barrier between clients and staff for additional protection. Patients or subjects should be instructed to arrive at a check-in point wearing a face mask. If they do not have a face mask, the staff should be prepared to provide one for them. No visitors should be allowed to accompany the patient or subject into the testing area. Staff should request the client use an institutionally approved alcohol-based hand sanitizer at the entrance. Handshakes or other contact greetings should not be performed and social distancing maintained. At this time, staff should conduct an on-site screening survey similar to the 24-h prescreening questionnaire. In addition, their temperature should be taken. Anyone presenting with a reading of ≥99.5 F is considered a positive screen and should be dismissed. Because the definition of fever can vary by age, sex, time of day, and type of thermometer, CPX laboratories should seek consult from their medical staff to determine a disqualifying body temperature. If a person screens positive upon arrival, their appointment should be canceled and they should be asked to leave. Guidance for the individual should include instruction to self-isolate and either contact their primary care provider or a central hotline established by the institution. It is recommended that staff reiterate they also have passed a screening questionnaire that day, had their own temperature measured upon reporting to work and that they are practicing hand hygiene and social distancing. All information should be logged (including time of check-in, temperature, who signed the guest in, and contact information) in the scenario that contact tracing is necessary. To further instill confidence that all precautions are being practiced, staff should reiterate that the building is sanitized every evening by the institution's janitorial staff or cleaning services. This includes wiping down surfaces, door handles and other high touch areas, along with immaculate cleaning of the restrooms. In addition, staff should clean between each patient to sanitize surfaces and equipment using wipes that are virucidal, bactericidal, fungicidal, and tubercucidal, as well as discard equipment that cannot be properly disinfected (Fig. 2).
During the CPX
In a case that the client has acutely recovered from COVID-19, it is highly recommended the CPX test be medically supervised. This recommendation comes from the growing evidence that the virus can have long-lasting effects on the heart, specifically myocarditis, and events have occurred in recovered patients during exercise (23–25).
Multiple exercise tests should not be performed simultaneously in order to decrease population density and limit staff, patient, and subject exposure. In addition, staff in the testing room should be limited to two technicians and potentially a physician for medical coverage along with the patient or subject. If for any reason there is an extended time period between tests, staff should maintain social distancing during this time. If conducting serial testing, adequate time should be allotted between tests for staff to thoroughly disinfect the space and to eliminate lingering aerosols. Our laboratory allows 90 min between tests.
Because of the close proximity necessary to acquire the measure, unless there is known hypertension or hypotension, or other relevant risk, exercise blood pressures should be kept to a minimum. An exercise blood pressure should be taken early in the test to make sure there is not a drop in systolic blood pressure or an excessive rise in blood pressure. If symptoms develop during the test, a blood pressure can be performed. A pretest resting blood pressure should be obtained and an immediate postexercise blood pressure may serve as a maximal reading.
It Has Been Demonstrated That the COVID-19 Virus Can Travel 6 Ft
Due to the mouthpiece and intense exercise demands, maximal CPX testing procedures require close interaction within 6 ft with an unmasked participant; therefore, staff should be expected to wear a face mask (N95, if available), face shield, gown, and gloves (26). These procedures are more intensive than a standard exercise tolerance test without gas analysis, involving equipment that comes into direct contact with the subject's mouth and nose. This equipment is placed by staff preexercise and removed quickly postexercise while the participant is still breathing heavily from maximal exercise exertion. The participant should continuously wear a face mask for as long as possible, up to the point of placing the CPX headset, and replace their face mask as soon as reasonably possible during their test recovery. All testing personnel should wear PPE to protect themselves and the client.
After the CPX
Following the CPX test, all linens should be properly and immediately placed in a soiled linen container. All furniture, doorknobs, tabletops, keyboards, and monitors should be thoroughly wiped down with disinfectant. Stethoscopes, blood pressure equipment, and the exercise modality (treadmill, bike) should be disinfected. If ECG leads or heart rate monitors were used, all wires and belts should be wiped thoroughly. The previously mentioned metabolic cart equipment should be discarded after each test and replaced with new components while the remaining reusable components are prepared for high level disinfection. This will protect the client (and staff) by minimizing virus spread by eliminating residual contaminants from a previous test. Doors, and if available, windows should be opened to increase ventilation in the testing space. Staff should not congregate between tests. It is recommended that 90 min be allotted between scheduled tests. Although discarding and wiping down equipment may not require the entirety of this time, some disinfectants take up to 30 min to kill a virus.
Staff Ability to Work
Staff should not come to work if they have: fever ≥99.5 F (37.7 C), shortness of breath or difficulty breathing, cough, nasal congestion, or runny nose (within the last 2 wk), sore throat, muscle pains or aches, chills, headache, loss of taste or smell, nausea, vomiting, diarrhea, abdominal pain, rash, red eye, or weakness. If any of the foregoing occurs during a shift, staff should mask, leave, inform their supervisor, and follow institutional guidance for assessment (likely an institutional hotline) and COVID-19 testing. By contacting the hotline, staff will register with an appropriate employee occupational health and wellness (EOHW) entity. Staff must self-isolate until cleared by EOHW to return to work. Staff should follow institutional guidelines when at work and outside of the CPX testing laboratory, adhere to local government guidelines for public safety when not at the workplace, and be aware of COVID-19 hotspots when considering travel.
The COVID-19 pandemic has necessitated many protocol modifications to ensure safety in both the clinic and research environments. As long as COVID-19 remains a serious risk, exercise physiology human performance or clinical diagnostic laboratories must take additional precautions in order to continue testing. Preparing for these modifications includes reviewing federal and local guidelines, as well as working closely with specialized offices within individual institutions, such as the Occupational and Environmental Safety Office. It is recommended that modifications be made by acquiring PPE, training staff on the proper way to don and doff PPE, altering workflow, thoroughly sanitizing equipment, and screening staff, patients, and research subjects. These precautions will mitigate risk of exposure for all while allowing testing to continue in the laboratory.
The authors declare no conflict of interest and do not have any financial disclosures.
1. Guazzi M, Bandera F, Ozemek C, et al. Cardiopulmonary exercise testing: what is its value?J. Am. Coll. Cardiol
. 2017; 70:1618–36.
2. Older PO, Levett DZH. Cardiopulmonary exercise testing and surgery. Ann. Am. Thorac. Soc
. 2017; 14(Suppl. 1):S74–83.
3. Malhotra R, Bakken K, D'Elia E, Lewis GD. Cardiopulmonary exercise testing in heart failure. JACC Heart Fail
. 2016; 4:607–16.
4. Mezzani A. Cardiopulmonary exercise testing: basics of methodology and measurements. Ann. Am. Thorac. Soc
. 2017; 14(Suppl. 1):S3–S11.
5. Guazzi M, Arena R, Halle M, et al. 2016 Focused update: clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Eur. Heart J
. 2018; 39:1144–61.
6. Kaminsky LA, Arena R, Myers J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing: data from the fitness registry and the importance of Exercise National Database. Mayo Clin. Proc
. 2015; 90:1511–23.
7. Kraus WE, Torgan CE, Duscha BD, et al. Studies of a targeted risk reduction intervention through defined exercise (STRRIDE). Med. Sci. Sports Exerc
. 2001; 33:1774–84.
8. Duscha BD, Slentz CA, Johnson JL, et al. Effects of exercise training amount and intensity on peak oxygen consumption in middle-age men and women at risk for cardiovascular disease. Chest
. 2005; 128:2788–93.
9. O'Connor CM, Whellan DJ, Lee KL, et al. Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA
. 2009; 301:1439–50.
10. Keteyian SJ, Brawner CA, Savage PD, et al. Peak aerobic capacity predicts prognosis in patients with coronary heart disease. Am. Heart J
. 2008; 156:292–300.
11. Ross R, Blair SN, Arena R, et al. Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation
. 2016; 134:e653–99.
12. The Lancet. COVID-19: protecting health-care workers. Lancet
. 2020; 395:922.
13. Dorr R. Protecting patients and healthcare personnel from COVID-19: considerations for practice and outpatient care in cardiology. Herz
. 2020; 16:1–2.
14. Sommerstein R, Fux CA, Vuichard-Gysin D, et al. Risk of SARS-CoV-2 transmission by aerosols, the rational use of masks, and protection of healthcare workers from COVID-19. Antimicrob. Resist. Infect. Control
. 2020; 9:100.
15. Faghy MA, Sylvester KP, Cooper BG, Hull JH. Cardiopulmonary exercise testing in the COVID-19 endemic phase. Br. J. Anaesth
. 2020; 25:447–9.
16. US Food and Drug Administration. N95 Respirators, Surgical Masks, and Face Masks. FDA [Internet]. [cited 2020 December 30]. Available from: https://www.fda.gov/medical-devices/personal-protective-equipment-infection-control/n95-respirators-surgical-masks-and-face-masks
17. Guo ZD, Wang ZY, Zhang SF, et al. Aerosol and surface distribution of severe acute respiratory syndrome coronavirus 2 in hospital wards, Wuhan, China, 2020. Emerg. Infect. Dis
. 2020; 26:1583–91.
18. Christopherson DA, Yao WC, Lu M, et al. High-efficiency particulate air filters in the era of COVID-19: function and efficacy. Otolaryngol. Head Neck Surg
. 2020; 14:194599820941838.
19. Nazarenko Y. Air filtration and SARS-CoV-2. Epidemiol Health
. 2020; 42:e2020049.
20. Kormuth KA, Lin K, Prussin AJ 2nd, et al. Influenza virus infectivity is retained in aerosols and droplets independent of relative humidity. J. Infect. Dis
. 2018; 218:739–47.
21. Kucirka LM, Lauer SA, Laeyendecker O, et al. Variation in false-negative rate of reverse transcriptase polymerase chain reaction-based SARS-CoV-2 tests by time since exposure. Ann. Intern. Med
. 2020; 173:262–7.
22. CDC. Increased risk for COVID-19 [Internet]. Centers for Disease Control and Prevention. 2020. [cited 2021 January 4]. Available from: https://www.cdc.gov/screening/index.html
23. Phelan D, Kim JH, Chung EH. A game plan for the resumption of sport and exercise after coronavirus disease 2019 (COVID-19) infection. JAMA Cardiol
. 2020; 5(10):1085–6.
24. Emery MS, Phelan DMJ, Martinez MW. Exercise and athletics in the COVID-19 pandemic era. American College of Cardiology online
. [cited 2021 January 4]. Available from: https://www.acc.org/latest-in-cardiology/articles/2020/05/13/12/53/exercise-and-athletics-in-the-covid-19-pandemic-era
25. Bhatia RT, Marwaha S, Malhotra A, et al. Exercise in the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) era: a question and answer session with the experts endorsed by the section of sports cardiology & exercise of the European Association of Preventive Cardiology (EAPC). Eur. J. Prev. Cardiol
. 2020; 27:1242–51.
26. Bahl P, Doolan C, de Silva C, et al. Airborne or droplet precautions for health workers treating COVID-19? J. Infect. Dis
. 2020; jiaa189. doi:10.1093/infdis/jiaa189.