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Stress and Fear

Clinical Implications for Providers and Patients (in the Time of COVID-19 and Beyond)

      Abstract

      In light of the coronavirus disease 2019 pandemic, we explore the role of stress, fear, and the impact of positive and negative emotions on health and disease. We then introduce strategies to help mitigate stress within the health care team, and provide a rationale for their efficacy. Additionally, we identify strategies to optimize patient care and explain their heightened importance in today’s environment.

      Abbreviations and Acronyms:

      COVID-19 (corona virus disease), HPA (hypothalamic–pituitary–adrenal axis), IL (interleukin), PPE (personal protective equipment), PTSD (post-traumatic stress disorder)
      “With that many sick people, what are we supposed to do? ...if we stop working, we’re classified as traitors. Right now we’re just waiting to die….working like this, we’re tired to exhaustion.… infection is much more horrible than it’s reported on TV…. we have 10 doctors here, and each doctor has treated more than 100 infected patients in just one day.…the patients were begging us desperately, but we couldn’t do anything. They’re dying right in front of our eyes.”Staff at Wuhan Hospital, Wuhan, China
      Leaked Videos From China Reveal What's Really Happening in Hospitals. The Epoch Times.
      “There have been so many deaths, and this is destroying us because we think we aren’t able to do what we are here for. The reality is, we see them dying, and we die inside, too…. I go home for a few hours at night and just collapse on the sofa. I am sleeping but not sleeping because I wake up every hour with nightmares. My husband and daughter wait for me at home. They try to talk to me, but I can’t even hear them. They ask me if I’m listening to them…but I can’t.”Carla Maestrini, Intensive Care Coordinator, Cremona, Italy
      Inside intensive care unit: Italy fights coronavirus outbreak Channel 4 news.
      “A medical war zone…. Every day I come, what I see on a daily basis, is pain, despair, suffering and health care disparities…. We need gowns, we need gloves we need masks we need more vents…. We need psychological support as well. It's not easy coming here when you know what you're getting ready to face.… Certainly no physician wants to be put in a position where they have to triage treatments based on resource availability…. I don't really sleep that well at night…. I’m worried about my family, I worry about my safety. I worry about my colleagues. I worry about how the shift is going to be the next time I come. I worry about if a family member is going to come and be patient as well.”Arabia Mollette, Emergency Physician at Brookdale University Hospital, New York City
      • Marquez M.
      • Moghe M.
      Inside a Brooklyn hospital that is overwhelmed with COVID-19 patients and deaths. CNN.
      The worldwide coronavirus disease 2019 (COVID-19) pandemic has presented extraordinary challenges. The sheer volume of admissions has placed unprecedented strain on provider teams working in underprepared health systems. Inadequate supplies, including mechanical ventilators and personal protective equipment (PPE)
      • Ranney M.L.
      • Griffeth V.
      • Jha A.K.
      Critical supply shortages — the need for ventilators and personal protective equipment during the COVID-19 pandemic.
      coupled with insufficient staff create a Sisyphean task for these teams. These challenges have profound physical and psychological health implications. Providers have died from COVID-19 in the face of inadequate PPE, and have had to confront the ethical dilemma of rationing resources.
      • Rosenbaum L.
      Facing COVID-19 in Italy — ethics, logistics, and therapeutics on the epidemic's front line.
      Unique stressors include fear of infecting others
      • Rose C.
      Am I part of the cure or am I part of the disease? Keeping coronavirus out when a doctor comes home.
      ,
      • Chen Q.
      • Liang M.
      • Li Y.
      • et al.
      Mental health care for medical staff in China during the COVID-19 outbreak.
      eviction by landlords for fear of contamination
      • Mays H.
      NHS paramedic evicted from home for fear he would spread Covid-19. The Guardian.
      ,
      • Yeung J.
      • Gupta S.
      Doctors evicted from their homes in India as fear spreads amid coronavirus lockdown. CNN.
      ; and workplace disruptions.
      • Luhby T.
      • Moghe S.
      • Chen N.
      • Wright J.
      Some ER doctors are losing pay and hours even as coronavirus rages. CNN.
      Post-traumatic stress disorder (PTSD) was reported in 72% of COVID-19 health care workers in China.
      • Lai J.
      • Ma S.
      • Wang Y.
      • et al.
      Factors associated with mental health outcomes among health care workers exposed to coronavirus disease 2019.
      This is occurring within a profession where providers are encouraged to “choke down emotions”
      • Salles A.
      • Gold J.
      Health care workers aren’t just “heroes.” We’re also scared and exposed. Vox.
      ; and where nearly half report burnout manifested as compassion fatigue and decreased quality of care.
      • Mikkelsen M.E.
      • Anderson B.J.
      • Bellini L.
      • Schweickert W.D.
      • Fuchs B.D.
      • Kerlin M.P.
      Burnout, and fulfillment, in the profession of critical care medicine.
      Both acute and chronic stress has measurable physiologic effects, and greater awareness of this relationship is critically important in the current pandemic. The importance of the relationship between stress and health is magnified during critical illness when many patients are already terrified
      B.C. couple in South Korea say country is paralyzed by fear of new coronavirus. Vancouver Sun.
      and vulnerable.
      • Cheek D.B.
      Communication with the critically ill.
      Patient isolation, although necessary, may further exacerbate this distress. Advancing our understanding of the psychologic and physiologic effects of stress and identifying effective mitigating strategies are critically important as we confront this challenge. This paper identifies strategies to maximize performance and resilience while retaining focus on the psychological and emotional needs of our patients.

      Physiological Effects of Stress on Health and Disease

      Acute and chronic stress can have marked effects on cognition, decision-making, memory, technical performance, and teamwork, leading to impaired judgment and an increase in medical errors.
      • Kent J.
      • Thornton M.
      • Fong A.
      • Hall E.
      • Fitzgibbons S.
      • Sava J.
      Acute provider stress in high stakes medical care: implications for trauma surgeons.
      It is vital to recognize that “healthcare workers, unlike ventilators, cannot run at 100% function for prolonged periods.”
      Editorial. COVID-19: protecting health-care workers.
      The autonomic nervous system is under the control of the limbic system. Persistent stress leads to the activation of the hypothalamic-pituitary-adrenal axis (HPA) and cortisol release.
      Increased glucocorticoid levels inhibit salivary lysozyme secretion
      • Perera S.
      • Uddin M.
      • Hayes J.A.
      Salivary lysozyme: a noninvasive marker for the study of the effects of stress of natural immunity.
      and immunoglobulin A antibody production,
      • Staley M.
      • Conners M.G.
      • Hall K.
      • Miller L.J.
      Linking stress and immunity: Immunoglobulin A as a non-invasive physiological biomarker in animal welfare studies.
      which increases risk for acute infectious respiratory illness including those caused by coronavirus.
      • Cohen S.
      • Tyrrell D.A.
      • Smith A.P.
      Psychological stress and susceptibility to the common cold.
      Stress-mediated suppression of pulmonary interleukin (IL)–1 alpha may also contribute to increased viral pathogenesis.
      • Konstantinos A.P.
      • Sheridan J.F.
      Stress and influenza viral infection: modulation of proinflammatory cytokine responses in the lung.
      Chronic stress attenuates the immune response to influenza vaccination
      • Kiecolt-Glaser J.K.
      • Glaser R.
      • Gravenstein S.
      • Malarkey W.B.
      • Sheridan J.
      Chronic stress alters the immune response to influenza virus vaccine in older adults.
      and inhibits the immunoglobulin G antibody response to pneumococcal antigen following vaccination.
      • Glaser R.
      • Sheridan J.
      • Malarkey W.B.
      • MacCallum R.C.
      • Kiecolt-Glaser J.K.
      Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine.
      Elevated stress and norepinephrine levels correlate with decreased effectiveness of antiretroviral drugs and more rapid disease progression in HIV-infected individuals,
      • Nolan R.
      • Gaskill P.J.
      The role of catecholamines in HIV neuropathogenesis.
      with serum cortisol exerting an independent effect.
      • Leserman J.
      • Petitto J.M.
      • Gu H.
      • et al.
      Progression to AIDS, a clinical AIDS condition and mortality: psychosocial and physiological predictors.
      Stress is known to induce reactivation of latent herpes simplex virus,
      • Huang W.
      • Xie P.
      • Xu M.
      • Li P.
      • Zao G.
      The influence of stress factors on the reactivation of latent herpes simplex virus type 1 in infected mice.
      and to decrease cytomegalovirus antibody titers.
      • Rector J.L.
      • Dowd J.B.
      • Loerbroks A.
      • et al.
      Consistent associations between measures of psychological stress and CMV antibody levels in a large occupational sample.
      Individuals with PTSD show a higher rate of a variety of infections.
      • Jiang T.
      • Farkas D.K.
      • Ahern T.P.
      • Lash T.L.
      • Sorensen H.T.
      • Gradus J.L.
      Posttraumatic stress disorder and incident infections: a nationwide cohort study.
      The term "brain-gut axis” has been coined to acknowledge the role of stress in the pathogenesis of many chronic gastrointestinal diseases.
      • Konturek P.C.
      • Brzozowski T.
      • Konturek S.J.
      Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options.
      Cortisol is inversely correlated with melatonin levels, potentially impeding restorative sleep.
      • Hirotsu C.
      • Tufik S.
      • Andersen M.L.
      Interactions between sleep, stress, and metabolism: From physiological to pathological conditions.
      Chronic stress may also lead to changes in the prefrontal cortex, hippocampus, and amygdala which diminish cognition, decision-making, and memory, and increase emotional responses. For example, high levels of norepinephrine release during stress impair prefrontal abilities that are needed for higher cognition and regulation of a positive mental state, while strengthening the emotional responses of the amygdala.
      • Arnsten A.F.
      Stress signalling pathways that impair prefrontal cortex structure and function.
      The relationship between stress and immune function potentially heightens the risk to health care teams in prolonged close contact with COVID-19 patients.
      • Joynt G.M.
      • Wu W.K.
      Understanding COVID-19: what does viral RNA load really mean?.
      For patients, stress can increase susceptibility to a viral infection and impede recovery through slower wound healing.
      • Marucha P.T.
      • Kiecolt-Glaser J.K.
      • Favagehi M.
      Mucosal wound healing is impaired by examination stress.
      ,
      • Kiecolt-Glaser J.K.
      • Marucha P.T.
      • Malarkey W.B.
      • Mercado A.M.
      • Glaser R.
      Slowing of wound healing by psychological stress.
      These observations suggest the stress of our current environment is deleterious to both caregivers and patients.

      Physiologic and Clinical Impact of Emotions

      The role of the limbic system on our health extends beyond the HPA axis. Individuals with greater positive self-perceptions of aging lived 7.5 years longer than a matched group
      • Levy B.R.
      • Slade M.D.
      • Kunkel S.R.
      • Kasl S.V.
      Longevity increased by positive self-perceptions of aging.
      and tended to practice more preventive health behaviors.
      • Levy B.R.
      • Myers L.M.
      Preventive health behaviors influenced by self-perceptions of aging.
      Markers of positive psychological well- being, such as optimism, are prospectively associated with metrics of cardiovascular health and improved cardiovascular and rheumatologic outcomes.
      • Kubzansky L.D.
      • Huffman J.C.
      • Boehm J.K.
      • et al.
      Positive psychological well-being and cardiovascular disease: JACC Health Promotion Series.
      Laughing therapy, operationalized by viewing humorous films, upregulated natural killer cell activity and decreased IL-4 and IL- 6 levels.
      • Takahashi K.
      • Iwase M.
      • Yamashita K.
      • et al.
      The elevation of natural killer cell activity induced by laughter in a crossover designed study.
      ,
      • Matsuzaki T.
      • Nakajima A.
      • Ishigami S.
      • Tanno M.
      • Yoshino S.
      Mirthful laughter differentially affects serum pro- and anti-inflammatory cytokine levels depending on the level of disease activity in patients with rheumatoid arthritis.
      Non-noxious stimuli, integrated by oxytocin, activate a psycho-physiological pattern opposite to the fight-or-flight response and are associated with relaxation and growth. Oxytocin has a known anti-stress effect and may explain why relationships, social contact, and touch may have health promoting and disease preventing effects.
      • Uvnas-Moberg K.
      Oxytocin linked antistress effects—the relaxation and growth response.
      Use of relaxation, hypnosis, and guided imagery techniques has been associated with increased oxytocin levels and fewer viral infections, increase in natural killer cell activity to herpes simplex virus, and decreased white blood cell count and cortisol.
      • Gruzelier J.H.
      A review of the impact of hypnosis, relaxation, guided imagery and individual differences on aspects of immunity and health.
      • Trakhtenberg E.C.
      The effects of guided imagery on the immune system: a critical review.
      • Varga K.
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      Oxytocin and cortisol in the hypnotic interaction.
      • Kasos E.
      • Kasos K.
      • Pusztai F.
      • Polyak A.
      • Kovacs K.J.
      • Varga K.
      Changes in oxytocin and cortisol in active-alert hypnosis: hormonal changes benefiting low hypnotizable participants.
      Massage therapy and tai chi have been associated with improved immune function, enhanced vaccination response, and increased circulating myeloid dendritic cells.
      • Ho R.T.
      • Wang C.W.
      • Ng S.M.
      • et al.
      The effect of t'ai chi exercise on immunity and infections: a systematic review of controlled trials.
      • Yang Y.
      • Verkuilen J.
      • Rosengren K.S.
      • et al.
      Effects of a Taiji and Qigong intervention on the antibody response to influenza vaccine in older adults.
      • Chiang J.
      • Chen Y.Y.
      • Akiko T.
      • et al.
      Tai Chi Chuan increases circulating myeloid dendritic cells.
      • Toups D.M.
      A healing touch: massage therapy and HIV/AIDS.
      • Major B.
      • Rattazzi L.
      • Brod S.
      • Pilipovic I.
      • Leposavic G.
      • D'Acquisto F.
      Massage-like stroking boosts the immune system in mice.
      Compelling evidence in the emerging field of affective immunology suggests a multitude of pathways linking emotion and immune function.
      • D'Acquisto F.
      Affective immunology: where emotions and the immune response converge.
      Excessive cognitive load can increase our propensity to form negative thoughts.
      • Dispenza J.
      You Are the Placebo.
      The term “moral injury” has been suggested to describe the distress that health care workers experience from unachievable demands on one’s energy, strength, and resources needed for their patients.
      • Talbot S.
      • Dean W.
      Physicians aren’t ‘burning out.’ They’re suffering from moral injury. STAT.
      Moral distress can manifest as malaise, fatigue, frustration, and cynicism. Although often viewed as signs of “burnout,” this term fails to capture the similarities of this syndrome with PTSD and its associated psychological morbidity.
      • Freudenberger H.
      The Staff Burnout Syndrome in Alternative Institutions.
      The impact of medical errors or untoward outcomes on providers is just beginning to be explored. Negative ruminations and perseveration are common after these events, and providers are now recognized to be at risk for becoming “second victims” as they struggle with subsequent feelings of anxiety, fear, guilt, or anger, leading to social withdrawal, troubling memories, depression, and insomnia.
      • Ozeke O.
      • Ozeke V.
      • Coskun O.
      • Budakoglu II,
      Second victims in health care: current perspectives.
      The basis for negative auto-suggestion that accelerates and prolongs stress in these circumstances is uncertain. However, it is conceivable that the hostility of the historical medical training environment
      • Olasoji H.O.
      Broadening conceptions of medical student mistreatment during clinical teaching: message from a study of "toxic" phenomenon during bedside teaching.
      • Markman J.D.
      • Soeprono T.M.
      • Combs H.L.
      • Cosgrove E.M.
      Medical student mistreatment: understanding “public humiliation.
      • Peng J.
      • Clarkin C.
      • Doja A.
      Uncovering cynicism in medical training: a qualitative analysis of medical online discussion forums.
      perpetuates a negative self-assessment which is exacerbated in times of stress.
      Although a negative bias may have conferred protective evolutionary benefits, there are detrimental physiologic consequences. Higher prefrontal cortical regions regulate the activity of the subgenual cingulate “visceral-motor output center” that regulates our autonomic nervous system
      • Wallis C.U.
      • Cardinal R.N.
      • Alexander L.
      • Roberts A.C.
      • Clarke H.F.
      Opposing roles of primate areas 25 and 32 and their putative rodent homologs in the regulation of negative emotion.
      and is activated during rumination and depression.
      • Cooney R.E.
      • Joormann J.
      • Eugène F.
      • Dennis E.L.
      • Gotlib I.H.
      Neural correlates of rumination in depression.
      ,
      • Mayberg H.S.
      • Lozano A.M.
      • Voon V.
      • et al.
      Deep brain stimulation for treatment-resistant depression.
      Repetitive negative thinking was recently linked to subsequent cognitive decline, as well as the deposition of harmful brain proteins linked to Alzheimer disease.
      • Marchant N.L.
      • Lovland L.R.
      • Jones R.
      • et al.
      Repetitive negative thinking is associated with amyloid, tau, and cognitive decline.
      A 30-year longitudinal follow-up of a cohort of 839 general medical patients showed a 19% increase in mortality risk among those with a pessimistic outlook.
      • Maruta T.
      • Colligan R.C.
      • Malinchoc M.
      • Offord K.P.
      Optimists vs pessimists: survival rate among medical patients over a 30-year period.
      Negative emotions such as anger and depression, via activation of pro-inflammatory response, have been implicated in the pathophysiology of many chronic conditions.
      • Suarez E.C.
      • Boyle S.H.
      • Lewis J.G.
      • Hall R.P.
      • Young K.H.
      Increases in stimulated secretion of proinflammatory cytokines by blood monocytes following arousal of negative affect: the role of insulin resistance as moderator.
      ,
      • Barlow M.A.
      • Wrosch C.
      • Gouin J.P.
      • Kunzmann U.
      Is anger, but not sadness, associated with chronic inflammation and illness in older adulthood?.
      Depression is linked with impaired T cell function,
      • Lehto S.M.
      • Huotari A.
      • Niskanen L.
      • et al.
      Serum IL-7 and G-CSF in major depressive disorder.
      chronic graft rejection, and increased mortality among solid organ transplant recipients.
      • Pennington K.M.
      • Benzo R.P.
      • Schneekloth T.D.
      • et al.
      Impact of affect on lung transplant candidate outcomes.
      ,
      • Smith P.J.
      • Blumenthal J.A.
      • Trulock E.P.
      • et al.
      Psychosocial predictors of mortality following lung transplantation.

      Unintended Nocebo Effect

      There is another major negative emotion that pervades our current reality: fear. The WHO appropriately observed “The 2019-nCoV2 outbreak and response has been accompanied by a massive ‘infodemic’ — an over-abundance of information — some accurate and some not.”
      Novel coronavirus (2019-nCoV): situation report-13. World Health Organization.
      This is particularly relevant today, as negative expectations can impact outcomes. The nocebo effect describes heightened negative consequences of a treatment when a patient holds negative expectations.
      • Bryan H.
      • Dubljevic V.
      To disclose or not to disclose: when fear of nocebo effects infringes upon autonomy.
      Overwhelming media coverage emphasizing the lack of proven efficacious therapy for COVID-19 and the potential harm of other interventions places patients at risk of the nocebo effect. An example of this phenomenon is the enthusiastic advocacy for treatment with hydroxychloroquine and azithromycin, despite only a single publication suggesting benefit.
      • Gautret P.
      • Lagier J.C.
      • Parola P.
      • et al.
      Hydroxychloroquine and azithromycin as a treatment of COVID-19: results of an open-label non-randomized clinical trial.
      This article was subsequently retracted,
      Hydroxychloroquine-COVID-19 study did not meet publishing society’s “expected standard”. Retraction Watch.
      but not before overdoses with chloroquine and the fatal ingestion of a chloroquine-containing pool cleaning substance.
      • Johnson J.
      Nigeria Reports Chloroquine Overdoses After Trump—Without Evidence—Touted Drug as Possible Coronavirus Treatment. Common Dreams.
      ,
      • Edwards E.
      • Hillyard V.
      Man dies after taking chloroquine in an attempt to prevent coronavirus NBC news.
      Robert Hyzy, a COVID-19–team intensive care unit director at the University of Michigan, discussed the role of fear: “Doctors have a fear of exposing nurses and ourselves to the virus. This is driving a willingness to deviate from established practices. It is easier to induce a medical coma with propofol than to do what is right, turning off the sedation every day with A2Fs (ie, ABCDEF bundle). Ultimately, it backfires because nurses end up getting more exposure because of longer patient stays.”
      • Ely E.W.
      Doctors fear the coronavirus. Is that affecting their medical decisions? The Washington Post.
      This fear can cross from health care providers to patients, creating untoward emotional stress in both groups. Darin Portnoy, a physician with COVID-19 teams at Montefiore and past-president of Médecins Sans Frontières said, “What I’m seeing in the Bronx is eerily similar to Ebola in West Africa [in 2014]. Both diseases have had confusing and dissonant public health messaging at the start, growing levels of community mistrust, and patients separated from their families when they seek care. Patients see us dressed in unfamiliar and threatening gear and they struggle to hear our muffled voices through masks. They sense our uncertainty when we can’t tell them exactly what to expect with their illness, and we have no cure to offer. At death in both diseases, families are unable to be with patients at their bedside or come together to mourn their death later.”
      • Ely E.W.
      Doctors fear the coronavirus. Is that affecting their medical decisions? The Washington Post.
      Fear is not merely an emotion or state of mind. In 1942, Cannon’s research into “Voodoo death” — a sudden, unexplained death resulting from a Voodoo curse — formed the basis for much of our modern understanding of the physiological response fight-or-flight systems linking emotions, such as fear, with illness.
      • Sternberg E.M.
      Walter B. Cannon and " 'Voodoo' Death": a perspective from 60 years on.
      Sympathetic activation and the subsequent catecholamine release brought on by emotional distress is implicated in the pathophysiology of the “broken heart syndrome.”
      • Wang X.
      • Pei J.
      • Hu X.
      The brain-heart connection in takotsubo syndrome: the central nervous system, sympathetic nervous system, and catecholamine overload.
      Thus, a state of fear and panic can potentially worsen clinical outcomes through sympathetic activation, the HPA axis, or other, yet unexplained mechanisms.

      Implications of Psychological Milieu for Critically Ill Patients and Their Providers

      Awareness of the nocebo effect is particularly relevant in the intensive care unit. During critical illness, cognitive processes change, becoming literal and overly sensitive to both direct and covert meanings of communicated messages.
      • Cheek D.B.
      Communication with the critically ill.
      ,
      • Papathanassoglou E.D.
      • Patiraki E.I.
      Transformations of self: a phenomenological investigation into the lived experience of survivors of critical illness.
      In such altered states, people may accept suggestions with minimal critical appraisal of the content.
      • Cheek D.B.
      Communication with the critically ill.
      Although rarely appreciated, provider expectations of an intervention may be non-verbally communicated to the patients and impact outcome.
      • Gracely R.H.
      • Dubner R.
      • Deeter W.R.
      • Wolskee P.J.
      Clinicians' expectations influence placebo analgesia.
      ,
      • Chen P.A.
      • Cheong J.H.
      • Jolly E.
      • Elhence H.
      • Wager T.D.
      • Chang L.J.
      Socially transmitted placebo effects.
      Semantic processing continues in an altered state of consciousness,
      • Rama P.
      • Relander-Syrjanen K.
      • Ohman J.
      • Laakso A.
      • Naatanen R.
      • Kujala T.
      Semantic processing in comatose patients with intact temporal lobes as reflected by the N400 event-related potential.
      ,
      • Davis M.H.
      • Coleman M.R.
      • Absalom A.R.
      • et al.
      Dissociating speech perception and comprehension at reduced levels of awareness.
      with some patients later recalling things said to them while comatose
      • Szilágyi A.
      Suggestive communication at the intensive care unit.
      that may lead to an unintended potential for harm. Although a call for the mindful choice of words with the critically ill dates back to 1969,
      • Cheek D.B.
      Communication with the critically ill.
      clinical adoption has been limited. Patients may perceive staff performing painful interventions as hostile adversaries, which can further complicate care and outcomes.
      • Szilágyi A.
      Suggestive communication at the intensive care unit.
      • Misak C.J.
      The critical care experience: a patient's view.
      • Alonso-Ovies A.
      • Heras La Calle G.
      ICU: a branch of hell?.
      Personal protective equipment requirements, combined with fatigue, fear, and isolation from family
      • Rosa R.G.
      • Tonietto T.F.
      • da Silva D.B.
      • et al.
      Effectiveness and safety of an extended ICU visitation model for delirium prevention: a before and after study.
      may further limit healing human interactions and exacerbate patient vulnerability to negative suggestion. Given patients’ heightened suggestibility, Varga et al
      • Varga K.
      • Varga Z.
      • Frituz G.
      Psychological support based on positive suggestions in the treatment of a critically ill ICU patient — a case report.
      have developed a therapeutic system of psychological support based on positive suggestions which hastened ventilator weaning and decreased the need for sedatives and analgesics.
      • Szilágyi AKDCBL
      • Varga K.
      Effectiveness of psychological support based on positive suggestions with the ventilated patient.
      • Szilágyi A.
      • Diószeghy C.
      • Fritúz G.
      • Gál J.
      • Varga K.
      Shortening the length of stay and mechanical ventilation time by using positive suggestions via MP3 players for ventilated patients.
      • Schlanger J.
      • Fritúz G.
      • Varga K.
      Therapeutic suggestion helps to cut back on drug intake for mechanically ventilated patients in intensive care unit.
      Given the sustained and uncertain nature of the ongoing pandemic, how can health care providers best prepare themselves to stay human?
      Editorial. COVID-19: protecting health-care workers.
      How can we preserve human-patient interaction and make it mindful and positive? Without life support, our critically ill would die, but without humanity they may die in different ways. This is why it is so important to us all to remain human, now more than ever. Effective strategies to prevent moral injury include workplace modifications to streamline workflow and minimize clerical work, mindset training, and fostering resilience through restorative scheduling practices, structured opportunities to debrief after critical events, and ongoing opportunities to promote community, connectedness, and meaning.
      • West C.P.
      • Dyrbye L.N.
      • Shanafelt T.D.
      Physician burnout: contributors, consequences and solutions.
      The suggestions presented in Tables 1 and 2 offer a structured approach for health care teams based on available evidence.
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      The effect of diaphragmatic breathing on attention, negative affect and stress in healthy adults.
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      Breathing control center neurons that promote arousal in mice.
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      • Lange T.
      • Haack M.
      The sleep-immune crosstalk in health and disease.
      • Colonna M.
      The immune system and nutrition: homing in on complex interactions.
      • Kao S.
      • Drollette E.
      • Ritondale J.
      • Khan N.
      • Hillman C.
      The acute effects of high-intensity interval training and moderate-intensity continuous exercise on declarative memory and inhibitory control.
      • Loprinzi P.D.
      • Kane C.J.
      Exercise and cognitive function: a randomized controlled trial examining acute exercise and free-living physical activity and sedentary effects.
      • Simpson R.J.
      • Campbell J.P.
      • Gleeson M.
      • et al.
      Can exercise affect immune function to increase susceptibility to infection?.
      • Ohly H.
      • White M.P.
      • Wheeler B.W.
      • et al.
      Attention restoration theory: a systematic review of the attention restoration potential of exposure to natural environments.
      APPLE
      A mindful response to thoughts.
      • Pai H.C.
      The effect of a self-reflection and insight program on the nursing competence of nursing students: a longitudinal study.
      • Malin K.
      • Littlejohn G.O.
      Rumination modulates stress and other psychological processes in fibromyalgia.
      • Creswell J.D.
      • Dutcher J.M.
      • Klein W.M.
      • Harris P.R.
      • Levine J.M.
      Self-affirmation improves problem- solving under stress.
      • Uvnas-Moberg K.
      • Oxytocin Petersson M.
      a mediator of anti-stress, well-being, social interaction, growth and healing. [In German.].
      • Nietzsche F.
      Twilight of the Idols.
      • Poulin M.J.
      Volunteering predicts health among those who value others: two national studies.
      • Gangestad S.W.
      • Grebe N.M.
      Hormonal systems, human social bonding, and affiliation.
      • Pohl T.T.
      • Young L.J.
      • Bosch O.J.
      Lost connections: Oxytocin and the neural, physiological, and behavioral consequences of disrupted relationships.
      • Bhui K.
      • Dinos S.
      • Galant-Miecznikowska M.
      • de Jongh B.
      • Stansfeld S.
      Perceptions of work stress causes and effective interventions in employees working in public, private and non- governmental organisations: a qualitative study.
      • Bergin A.J.
      • Jimmieson N.L.
      The importance of supervisor emotion recognition for praise and recognition for employees with psychological strain.
      • Messner R.L.
      Gratitude: a stress buster.
      • Sansone R.A.
      • Sansone L.A.
      Gratitude and well being: the benefits of appreciation.
      • Worthington Jr., E.L.
      • Witvliet C.V.
      • Pietrini P.
      • Miller A.J.
      Forgiveness, health, and well-being: a review of evidence for emotional versus decisional forgiveness, dispositional forgivingness, and reduced unforgiveness.
      • Toms J.
      Mind the gap: MIND, the mental hygiene movement and the trapdoor in measurements of intellect.
      • Billings J.A.
      • Keeley A.
      • Bauman J.
      • et al.
      Merging cultures: palliative care specialists in the medical intensive care unit.
      • Brown S.M.
      • Azoulay E.
      • Benoit D.
      • et al.
      The Practice of Respect in the ICU.
      • Sokol-Hessner L.
      • Folcarelli P.H.
      • Sands K.E.
      Emotional harm from disrespect: the neglected preventable harm.
      • Wahlberg K.
      • Lambirth S.
      • Gardner Z.
      Improving patients' ability to identify their physicians through the use of physician facecards and whiteboards.
      • Pun B.T.
      • Balas M.C.
      • Barnes-Daly M.A.
      • et al.
      Caring for critically ill patients with the ABCDEF bundle: results of the ICU Liberation Collaborative in over 15,000 adults.
      • Jahangir K.
      “I Am Not Touching That Coronavirus Patient!”.
      Table 1Strategies for Staff
      Resilience techniquesTake advantage of diaphragmatic breathing between patient interactions. Diaphragmatic breathing involves contraction of the diaphragm, expansion of the belly, and deepening of inhalation and exhalation, which decreases the respiration frequency.
      • Ma X.
      • Yue Z.Q.
      • Gong Z.Q.
      • et al.
      The effect of diaphragmatic breathing on attention, negative affect and stress in healthy adults.
      Breathe this way until your stress level can come down to 4/10 on a 1-10 scale with 10 being the highest.
      • Lauria M.J.
      • Gallo I.A.
      • Rush S.
      • Brooks J.
      • Spiegel R.
      • Weingart S.D.
      Psychological Skills to Improve Emergency Care Providers' Performance Under Stress.
      Diaphragmatic breathing triggers body relaxation by reversing the frontal lobes when in deep HPA activation, and normalizing noradrenergic activity in the locus coeruleus, which is increased during stress.
      • Yackle K.
      • Schwarz L.A.
      • Kam K.
      • et al.
      Breathing control center neurons that promote arousal in mice.
      Meditate to improve sleep quality,
      • Black D.S.
      • O'Reilly G.A.
      • Olmstead R.
      • Breen E.C.
      • Irwin M.R.
      Mindfulness meditation and improvement in sleep quality and daytime impairment among older adults with sleep disturbances: a randomized clinical trial.
      mediate physiological markers of stress,
      • Pascoe M.C.
      • Thompson D.R.
      • Jenkins Z.M.
      • Ski C.F.
      Mindfulness mediates the physiological markers of stress: systematic review and meta-analysis.
      improve a sense of well-being,
      • Allen R.
      • Robinson A.
      • Allen S.
      • Nathan E.
      • Coghlan E.
      • Leung Y.
      Designing meditation for doctor well- being: can 'Om' help obstetrics and gynaecology doctors?.
      and reduce anxiety, depression,
      • Gonzalez-Valero G.
      • Zurita-Ortega F.
      • Ubago-Jimenez J.L.
      • Puertas-Molero P.
      Use of meditation and cognitive behavioral therapies for the treatment of stress, depression and anxiety in students. a systematic review and meta-analysis.
      and negative affectivity.
      • Schumer M.C.
      • Lindsay E.K.
      • Creswell J.D.
      Brief mindfulness training for negative affectivity: a systematic review and meta-analysis.
      There are many readily available public resources to help you start your own journey in this area.
      Practice self-care: Little steps are more important than “fixing” everything at once. Adequate sleep restores immune system function and can reduce infection risk/improve infection outcome.
      • Besedovsky L.
      • Lange T.
      • Haack M.
      The sleep-immune crosstalk in health and disease.
      Nutrition also plays a key role in multiple immune system pathways.
      • Colonna M.
      The immune system and nutrition: homing in on complex interactions.
      Exercise improves cognitive function and memory, psychological functioning, and benefits the immune system.
      • Kao S.
      • Drollette E.
      • Ritondale J.
      • Khan N.
      • Hillman C.
      The acute effects of high-intensity interval training and moderate-intensity continuous exercise on declarative memory and inhibitory control.
      • Loprinzi P.D.
      • Kane C.J.
      Exercise and cognitive function: a randomized controlled trial examining acute exercise and free-living physical activity and sedentary effects.
      • Simpson R.J.
      • Campbell J.P.
      • Gleeson M.
      • et al.
      Can exercise affect immune function to increase susceptibility to infection?.
      Look at green plants. It helps to restore cognitive skills, especially attention. Nature and green for most of us — especially those who are working in highly technical environment —means being away from work stress and reminds us of pleasant, relaxed times.
      • Ohly H.
      • White M.P.
      • Wheeler B.W.
      • et al.
      Attention restoration theory: a systematic review of the attention restoration potential of exposure to natural environments.
      Use the APPLE technique to manage uncertainty. Healthy coping approaches involve “leaning into”, rather than “running from” anxiety. The APPLE technique stands for:
      • Acknowledge — Notice the uncertainty as it comes to mind.
      • Pause — Don't react as you normally do. Don't react at all. Just pause, and breathe.
      • Pull back — Tell yourself this is just the anxiety or depression talking, and
      • this thought or feeling is only a thought or feeling. Don't believe everything you think! Thoughts are not statements of fact.
      • Let go — Let go of the thought or feeling. It will pass. You don't have to respond to them. You might imagine them floating away in a bubble or cloud.
      • Explore — Explore the present moment, because right now, in this moment, all is well. Notice your breathing, and the sensations of breathing. Notice the ground beneath you. Look around and notice what you see, what you hear, what you can touch, what you can smell. Right now. Then, shift your focus of attention to something else — on what you need to do, on what you were doing before you noticed the worry, or do something else — mindfully, with your full attention.”
        APPLE
        A mindful response to thoughts.
      Recognize that it is likely that at some point we will transition from an acute to chronic crisis mentality. This can be a difficult transition because it can feel like defeat. It’s not.
      Remind yourself daily that you are the one who is the best trained to deal with this situation, even if the challenge sometimes seems bigger than your coping potential.
      Schedule “worry time” — write down all the things you worry about. Then decide on when you’re going to address each of the items. If you notice yourself worrying, remind yourself that you will address it at that time. Recognize that many of these anxieties are chronic in nature and will still exist after the current pandemic is over — they can be addressed again then.
      Stay connected with your loved ones, including digital methods if necessary. Turn to your colleagues, friends, or team leader for social support — your colleagues may be having similar experiences to you. If you need help and support from others, be very clear and specific about what your needs are.
      Zentensivism — Focus on what is relevant and important. Born in social media as a parody opposite for the professional role of the intensivist, #zentensivist has touted a voice of reason highlighting multiple iatrogenic threats that have emerged due to fear during the pandemic, and advocating for a measured, compassionate, best supportive care. In the absence of clearly effective treatments, delivery of best evidence-based resuscitation, supportive critical care practices with early de-escalation, prevention of iatrogenic complications, and appropriate palliative care approaches remain the key tools to achieve best possible outcome.
      Brush up now on the skills you consider outside, but proximal to, your normal scope of practice. You don’t know where you may be needed.
      Remember your bandwidth — Our working memory is only able to hold in mind 7±2 pieces of information, and so much right now is preoccupied with COVID-19. Take your time with big decisions. It might take longer to think things through if you are feeling overwhelmed. Also, consider your psychological energy levels — you will need to “fill up” with rest, rewards, and positive experiences after “emptying the tank” at work.
      Seek information updates at specific times during the day once or twice. The sudden and near-constant stream of news reports can cause anyone to feel worried. Get the facts.
      Maintain a positive mindsetReflect on positive aspects of what you experienced — Actively find positive moments (teamwork, collegiality, patient not dying, supportive tweets, etc). Positive self-reflection can reduce stress,
      • Pai H.C.
      The effect of a self-reflection and insight program on the nursing competence of nursing students: a longitudinal study.
      whereas negative rumination (repetitive focus on symptoms of distress and the causes and consequences of one’s predicament without improving the ability to solve the problem at hand) exacerbates feelings of distress.
      • Malin K.
      • Littlejohn G.O.
      Rumination modulates stress and other psychological processes in fibromyalgia.
      Use positive self-suggestions such as “I am able and will manage it,” “I have strong reserves,” ”I am strong and quiet deep inside,” — this can increase problem solving under stress.
      • Creswell J.D.
      • Dutcher J.M.
      • Klein W.M.
      • Harris P.R.
      • Levine J.M.
      Self-affirmation improves problem- solving under stress.
      Do this particularly when you feel like being critical of yourself.
      Have a positive future image that represents what the future holds when we are over this difficult time. Recall this image in moments of especially high tension (eg, when you are back home, sitting in an armchair, drinking wine/whisky, etc).
      Recall moments of “love” and “being loved” and treasure the times of human connection throughout the day. This may lead to an increase in central oxytocin, which reduces stress, tension, pain, and anxiety.
      • Uvnas-Moberg K.
      • Oxytocin Petersson M.
      a mediator of anti-stress, well-being, social interaction, growth and healing. [In German.].
      “Hearty laughter is a good way to jog internally without having to go outdoors” — Norman Cousins.
      • Nietzsche F.
      Twilight of the Idols.
      Be proud of yourself. You are providing very important service for mankind. There is a great meaning in the work you do. As Nietzsche said, if we have our own “why” of life, we shall get along with almost any “how.”
      • Nietzsche F.
      Twilight of the Idols.
      The act of helping and sharing your resources can buffer the effect of stress
      • Poulin M.J.
      Volunteering predicts health among those who value others: two national studies.
      and increase central oxytocin.
      • Gangestad S.W.
      • Grebe N.M.
      Hormonal systems, human social bonding, and affiliation.
      ,
      • Pohl T.T.
      • Young L.J.
      • Bosch O.J.
      Lost connections: Oxytocin and the neural, physiological, and behavioral consequences of disrupted relationships.
      Practice the golden rulePraise your colleagues for their assistance, use the word “thank you” and “please” as frequently as you can. Lack of appreciation exacerbates work-related stress, and feeling recognized decreases psychological strain at work.
      • Bhui K.
      • Dinos S.
      • Galant-Miecznikowska M.
      • de Jongh B.
      • Stansfeld S.
      Perceptions of work stress causes and effective interventions in employees working in public, private and non- governmental organisations: a qualitative study.
      ,
      • Bergin A.J.
      • Jimmieson N.L.
      The importance of supervisor emotion recognition for praise and recognition for employees with psychological strain.
      Feelings of gratitude can also decrease the levels of stress and burnout, improving a sense of well-being.
      • Messner R.L.
      Gratitude: a stress buster.
      ,
      • Sansone R.A.
      • Sansone L.A.
      Gratitude and well being: the benefits of appreciation.
      Say “sorry” if you were rude or aggressive with someone (colleague, patient). Briefly, simply. This way we can prevent the accumulation of tension, resolve any potential interpersonal conflict, and replace negative unforgiving emotions with positive other-oriented emotion.
      • Worthington Jr., E.L.
      • Witvliet C.V.
      • Pietrini P.
      • Miller A.J.
      Forgiveness, health, and well-being: a review of evidence for emotional versus decisional forgiveness, dispositional forgivingness, and reduced unforgiveness.
      aCOVID-19 = coronavirus disease 2019; HPA = hypothalamic-pituitary-adrenal axis.
      Table 2Strategies for Mindful Patient Interactionsa
      Techniques to reduce patient distress1. Practice mental hygiene in parallel with physical one (during hand washing, donning/doffing). The concept of “mental hygiene” is a historically “loaded” term that refers to the mismanagement of patients,
      • Toms J.
      Mind the gap: MIND, the mental hygiene movement and the trapdoor in measurements of intellect.
      but it can have a different application in the context of critical care. Clearing your mind of previous patient interactions before entering a new patient’s room is important, recognizing that a patient’s perception is primarily affect-based
      • Cheek D.B.
      Communication with the critically ill.
      and they may be more in tune to your emotional state than to the medical terms you use to communicate what is happening.
      2. Promote sleep and movement within the constraints of the environment. Physical therapy can and should still happen.
      3. Limit television news reports in patient rooms — Excessive information, and the risk for (mis)information can heighten fear or fight or flight response.
      4. Do not cease the most basic forms of human contact and touch despite PPE.
      5. Ask about how the patient is feeling when you can, and don’t rush to make them feel better — acknowledge the validity of difficult feelings. As Martin Gabel put it, “Don’t just do something; stand there.” And we might add, “…and listen.”
      6. Acknowledge normalcy of their fear — try to understand the drivers of fear/anxiety.
      7. Maintain authentic dialogue with the patient. It is still ok to talk to them, particularly about non-medical topics, their interests, or families.
      8. Thank the patient for bearing with their isolation, honoring their altruism as we express how grateful we are for their helping others remain safe.
      9. Understand that you may become a confidante — in select circumstances, a patient may have no one else in the twilight of life.
      (Positive) communication10. Use “Get to Know Me” board. Adapted from palliative care medicine,
      • Billings J.A.
      • Keeley A.
      • Bauman J.
      • et al.
      Merging cultures: palliative care specialists in the medical intensive care unit.
      it is a poster that introduces information about the patient’s routine life, including hobbies, activities, accomplishments, favorite books, movies, food, and other information (Figure 1). Even without the pandemic, vulnerability of the critically ill to the loss of respect, dignity, and anonymity is heightened
      • Brown S.M.
      • Azoulay E.
      • Benoit D.
      • et al.
      The Practice of Respect in the ICU.
      and can result in erosion of trust in providers, communication breakdown and feeling violated.
      • Sokol-Hessner L.
      • Folcarelli P.H.
      • Sands K.E.
      Emotional harm from disrespect: the neglected preventable harm.
      This simple tool can aid providers in seeing the human in the patient, someone valuable, unique, and an individual.
      11. Tell one thing about the patient as a person on rounds daily.
      12. Positive communication and awareness of language — Say “good morning,” “sleep well,” or parting with the words, “have a nice day.” There is a sharp negative connotation if we stop saying these routine phrases to a human being who is alive (even without active contact with their surroundings, such when comatose or sedated). Use the words “please” and “thank you” as frequently as you can (eg, “Open your mouth, please…”).
      13. Reassure when able. For the patient who is feeling lonely or fearful in COVID-19 isolation, provide communication either at necessary interval visits, or at other times via digital devices. Reassure that we are prepared to help and take care of them. Explain, even if the patient is sedated, each time a procedure or intervention is being done to help them, such as performing a nebulizer treatment, bronchoscopy, or even just turning or cleaning them. Reassure that they are safe. Reassure that they are not alone in this process.
      Connect with team, family and friends14. Post printed pictures of the team caring for the patient with descriptions of who they are so patients can see faces, not just the masks, and know who their team members are.
      • Wahlberg K.
      • Lambirth S.
      • Gardner Z.
      Improving patients' ability to identify their physicians through the use of physician facecards and whiteboards.
      15. Communicate messages by families to patients, even if the patient is sedated. It’s a “delirium factory” out there due to isolation, lack of family presence and PPE; do not forget the ABCDEF bundle
      • Pun B.T.
      • Balas M.C.
      • Barnes-Daly M.A.
      • et al.
      Caring for critically ill patients with the ABCDEF bundle: results of the ICU Liberation Collaborative in over 15,000 adults.
      and the importance of environment and family on patient’s mental health outcomes.
      16. Hello, my name is… — Emergency physicians have recently designed a simple poster that can help connect with the patient and their family (Figure 2).
      • Jahangir K.
      “I Am Not Touching That Coronavirus Patient!”.
      aABCDEF bundle = Assess, prevent, and manage pain, Both spontaneous awakening trials and spontaneous breathing trials, Choice of analgesia and sedation, Delirium: assess, prevent, and manage, Early mobility and exercise, and Family engagement and empowerment; COVID-19 = coronavirus disease 2019; PPE = personal protective equipment.

      Conclusion

      The physiological and psychological consequences of the worldwide COVID-19 pandemic on both patients and caregivers are well documented, but the link between physiology, pathophysiology, and psychology in this milieu is underappreciated. We have provided a brief overview of the physiologic consequences of stress and fear; better understanding of these relationships can inform care of both patients and providers. Diligent attention to stress management and human interactions can have a rapid and positive influence on patient outcomes. The approaches recommended in this paper can be implemented immediately to reduce suffering imposed by this pandemic and beyond.

      Supplemental Online Material

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