Viral Respiratory Infections in the Morbidity and Mortality of Airway Diseases and Immunocompromised States Acute and Chronic Bronchitis, COPD, Asthma, Cystic Fibrosis, and Immunocompromised Cancer Patients Frequency, Seasonality, and Characteristics of Viral Respiratory Infections (VRIs) Impact of VRIs • Recognized for the last century as the most common infectious illness in humans • Terminology has varied – Common respiratory infection – Common cold – Rhinosinusitis • Rhinoviruses (RVs) cause a majority of these infections Monto AS et al. Clin Ther. 2001;1615. Economic and Societal Burden of VRIs • Adults average ~2 to 4 colds1,2 and children average 3 to 8 colds3 per year • In 1996, colds were associated with ~148 million days restricted activity, 20 million days missed work, 22 million days missed school, 45 million days bedridden4 • In 1998, 25 million office visits to primary care providers for upper respiratory infections (URIs)5 • Costs associated with VRIs estimated at ~$25 billion annually6 1. Turner RB. Pediatr Ann. 1998;27:790. 2. Monto AS et al. Clin Ther. 2001;23:1615. 3. Rosenstein N et al. Pediatrics. 1998;101:181 4. Adams PF et al. Vital Health Stat. 1999;10 (200). 5. Gonzales R et al. Clin Infect Dis. 2001;33:757. 6. Fendrick AM et al. Value in Health. 2001;4:412. Mean Annual Incidence of Respiratory Illnesses per Person-Year, Tecumseh, Michigan, 1965–1971 7 Females Mean annual illness incidence 6 Males 5 4 3 2 1 0 1 1–2 3–4 5–9 10–14 15–19 20–24 Age group (yr) Reprinted from Monto AS, Ullman BM. JAMA. 1974;227:164. 25–29 30–39 40–49 50–59 60 Seasonality of Respiratory Agents: Proportion Isolated in Each Calendar Month During 6 Years of Tecumseh, Michigan, Study 30 RV Parainfluenza viruses Respiratory syncytial virus (RSV) Influenza virus Percent 25 20 15 10 5 0 30 Percent 25 20 15 10 5 0 Jan Apr Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jan Apr Sep Oct Nov Dec Jan Feb Mar Apr May Jun Reprinted from Br J Prev Soc Med, 1977;31:101-108, with permission from the BMJ Publishing Group. Transmission of Respiratory Viruses • Transmission of viruses differs • Influenza – Airborne transmission1 – Widespread outbreaks • RVs – Closer contact required – Aerosol and direct2,3 – Households and schools are sites of transmission4 1. Goldman DA. Pediatr Infect Dis J. 2000;19(10 suppl):S97. 2. Gwaltney JM Jr, Hendley JO. Am J Epidemiol. 1982;116:828. 3. Dick EC et al. J Infect Dis. 1987;156:442. 4. Gwaltney JM Jr. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. 5th ed. Philadelphia: Churchill Livingstone; 2000:1940. Characteristics of VRIs of Known Etiology Coryza Sore throat Headache 100 Cough Activity restriction Lower respiratory symptoms Percent 80 60 40 20 0 RV RSV Parainfluenza virus Hemolytic streptococci Influenza A Influenza B Reprinted from Br J Prev Soc Med, 1977;31:101-108, with permission from the BMJ Publishing Group. Characteristics of RV-Associated Illnesses Illness with indicated syndrome (%) Percent with Median duration Activity Age group No. of Lower Upper LaryngoPhysician (years) isolates respiratory respiratory pharyngeal Other (days) restriction consultation 0–4 61 14.8 83.6 1.6 — 12 0 16.4 5–19 39 5.1 74.4 15.4 5.1 7 56.4 15.4 20–39 59 33.9 59.3 6.8 — 13 11.9 15.3 40 17 64.7 29.4 5.9 — 20 35.3 35.3 176 23.8 68.2 6.8 1.2 12 19.9 17.6 Total Reprinted with permission from Monto AS et al. J Infect Dis. 1987;156:43. ©1987 by The University of Chicago. All rights reserved. Clinical Features and Duration of Illness in Adults with RV Colds (n=276, RV confirmed by PCR or culture) Clinical feature RV % positive First symptom (% of subjects) Sore throat Stuffy nose Runny nose Sneezing 39 17 17 8 Most bothersome symptom (% of subjects) Runny nose Stuffy nose Sore throat Malaise 36 20 19 10 Median duration of symptoms (days) Cold episode Sleep disturbance Interference with daily activities 11 4 7 Adapted with permission from Arruda E et al. J Clin Microbiol. 1997;35:2864. Detection of Viruses by RT-PCR in Middle Ear Fluid and Nasopharyngeal Aspirates from 92 Children with Acute Otitis Media Middle ear fluid, *No. (%) Nasopharyngeal aspirate, †No. (%) Infected children, No. (%) RV 22 (24%) 28 (30%) 32 (35%) RSV 17 (18%) 21 (23%) 26 (28%) HCV 7 (8%) 14 (15%) 16 (17%) 44 (48%) 57 (62%) 69 (75%) Virus Total positive *2 samples had both HRV and RSV RNA; †2 aspirates had both HRV and RSV RNA, and 1 had both RSV and HCV RNA. RV=rhinovirus; RSV=respiratory syncytial virus; HCV=human coronavirus. Reproduced with permission from Pediatrics, Vol. 102, Pages 291-295, Table 2. Copyright 1998. RV in Acute Sinusitis • Sinusitis is an extremely common part of the common cold syndrome • RV has been detected in 50% of adult patients with sinusitis by RT-PCR of maxillary sinus brushings or nasal swabs1 • Frequency of association of RV infection with sinusitis suggests the common cold could be considered a rhinosinusitis2 1. Pitkäranta A et al. J Clin Microbial. 1997;35:1791. 2. Gwaltney JM Jr. Clin Infect Dis. 1996;23:1209. VRIs and Acute Bronchitis • Respiratory viruses are common pathogens in acute bronchitis1 • Respiratory virus infection associated with cough1 – – – – Influenza virus: 75%–93% of cases Adenovirus: 45%–90% RVs: 32%–60% Coronavirus: 10%–50% • 40% of nonasthmatic patients with acute bronchitis had FEV1 80% of predicted2 • Bronchial reactivity remained increased up to 5 weeks after episode of acute bronchitis2,3 1. Gwaltney JM Jr. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. 5th ed. Philadelphia: Churchill Livingstone; 2000:703. 2. Williamson HA Jr. J Fam Pract. 1987;25:251. 3. Hallett JS, Jacobs RL. Ann Allergy. 1985;55:568. RV Infection in the Elderly • In persons 60–90 years of age with RV infection, median duration of illness was 16 days • 19% were confined to bed; 26% had restriction of daily activities • 63% had lower respiratory tract symptoms; 43% consulted their physician • Burden of RV infection in the elderly appears to exceed that of influenza Nicholson KG et al. BMJ. 1996;313:1119. Symptoms of RV Infection in 35 Culture-Documented Illnesses in a Long-Term Care Facility Symptom Upper respiratory Cough Coryza Nasal or sinus congestion Sore throat Total Lower respiratory Productive cough Dyspnea Hoarseness Total Gastrointestinal Anorexia Nausea, vomiting, or diarrhea Total Systemic Malaise or fatigue Myalgia Sweating or chills Total Reprinted from Wald TG et al. Ann Intern Med. 1995;123:588. No. of patients (%) 34 (97) 31 (89) 21 (60) 18 (51) 35 (100) 19 (54) 8 (23) 5 (14) 23 (66) 11 (31) 4 (11) 12 (34) 23 (66) 8 (23) 5 (14) 25 (71) Summary • VRIs are the most common infectious diseases worldwide • RVs are predominant cause of VRIs in all age groups • Transmission requires relatively close contact • Family and school major sites of transmission • RV infections peak in autumn, with minor spring peaks • RVs cause AOM, sinusitis, and bronchitis in otherwise healthy people Role of VRIs in Asthma Exacerbations Causes of Asthma Exacerbations • Poor underlying control • Environmental factors – – – – – – – VRIs Allergen exposure Air pollution Bacterial infections Stress Exercise/cold air Occupational exposure Viruses Detected During Asthma Exacerbations in Children Method of detection Virus PCR Culture Picornaviruses 146 47 17 14 Coronavirus Influenza viruses Immunofluorescence Antibody rise by ELISA Total 147 * 21 38 14 10 20 21 Parainfluenza viruses 1, 2, and 3 6 6 18 21 RSV 6 6 12 12 Other 2 1 2 3 *84 identified as RV on further testing. ELISA=enzyme-linked immunosorbent assay. Reprinted from BMJ. 1995;310:1225-1229, with permission from the BMJ Publishing Group. VRIs and Hospitalizations for Asthma Hospital admissions for asthma correlate with virus isolation peaks and school terms. URIs 20 Total pediatric and adult hospitalizations 15 School holidays 10 5 0 Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Adapted with permission from Johnston SL et al. Am J Respir Crit Care Med. 1996;154:654. Official Journal of the American Thoracic Society. ©American Lung Association. Children with Wheezing Presenting to the ER • Comparison of wheezing and nonwheezing (control) children – Age, atopic status, eosinophil markers • In wheezing children <2 years old – Respiratory viruses detected in 82% (18/22) – RSV predominant, 68% (15/22) • In wheezing children 2 years old – Respiratory viruses detected in 83% (40/48) – RV predominant, 71% (34/48) – +PCR for RV and nasal eosinophilia or elevated nasal ECP, 48% (23/48) Rakes GP et al. Am J Respir Crit Care Med. 1999;159:785. Viruses Detected in 229 Symptomatic Asthma Episodes in Adults Pathogen RV HCV OC43 HCV 229E Influenza B Parainfluenza RSV Chlamydia psittaci Dual infection Number Percent of all episodes 76 21 15 2 5 2 3 5 33.2 9.2 6.6 0.9 2.2 0.9 1.3 2.2 RV=rhinovirus; HCV=human coronavirus; RSV=respiratory syncytial virus. Nicholson KG et al. BMJ. 1993;307:982. Viruses Detected in Adult Patients Hospitalized with Asthma 3% Influenza A Influenza B RV Adenovirus RSV Herpes 3% 6.1% 27.3% 54.5% 6.1% 33 organisms isolated; 5 subjects had >1 virus detected and some viruses were detected by >1 test. Data from Teichtahl H et al. Chest. 1997;112:591. Respiratory Infections in Infancy May Protect Against Development of Asthma • 2 episodes of “common cold” before age 1 yr decrease risk of asthma by age 7 by ~50% • Other viral infections—eg, herpes, varicella, measles—also protective • Reported LRI with wheeze in the first 3 years of life increases risk of asthma Illi S et al. BMJ. 2001;322:390. Effect of Day Care in Infancy and Number of Older Siblings on Asthma Risk Children who had 2 older siblings or attended day care during first 6 mo of life had increased risk of wheeze early in life but decreased risk later. Adjusted relative risk of frequent wheezing 2.7 P=0.01 P=0.03 1.0 P=0.001 P<0.001 P<0.001 0.4 0.1 1 2 3 4 5 6 7 8 Age (yr) 9 10 11 12 Reprinted with permission from Ball TM et al. N Engl J Med. 2000;343:538. Copyright ©2000 Massachusetts Medical Society. All rights reserved. 13 14 Immunologic Mechanisms of VRIInduced Asthma Exacerbations • Viral infections (esp. RV) frequently cause exacerbations of asthma • Possible mechanisms – Extension into the lower airway1-3 – Inflammation2,3 1. Gern JE et al. Am J Respir Crit Care Med. 1997;155:1159. 2. Gern JE, Busse WW. J Allergy Clin Immunol. 2000;106:201. 3. Fraenkel DJ et al. Am J Respir Crit Care Med. 1995;151:879. RV-Induced Airway Inflammation Plasma leakage Inflammatory cell recruitment and activation Mucus hypersecretion Virus-infected epithelium Airway Hyperresponsiveness Neural activation Adapted from Gern JE, Busse WW. J Allergy Clin Immunol. 2000;106:201. What Is Different About VRIs in Asthma? • VRIs (especially RV infections in children >2 yr old) and atopy synergistically enhance the risk of wheezing1 – Antigen-specific IgE – Eosinophilic inflammation • Cytokine production pattern is related to outcomes of experimental infection2 • High IFN-/IL-5 ratio=Th1-type (antiviral) response2 • Low IFN-/IL-5 ratio=Th2-type (allergic) response2 1. Rakes GP et al. Am J Respir Crit Care Med. 1999;159:785. 2. Gern JE et al. Am J Respir Crit Care Med. 2000;162:2226. Immunologic Risk Factors for More Severe VRIs • PBMC IFN- secretion • Sputum IFN-/IL-5 mRNA ratio correlates with – Lower symptom scores – More rapid viral clearance IFN/IL-5 ratio (units) – Reduced peak viral shedding 104 Th1 103 102 101 100 Th2 No Yes Virus detected at 14 days? Parry DE et al. J Allergy Clin Immunol. 2000;105:692. Reprinted from Gern JE et al. Am J Respir Crit Care Med. 2000;162:2226. Summary • Viruses cause asthma exacerbations in adults and children • RVs cause ~60% of virus-induced exacerbations of asthma • RVs directly infect the bronchial airways • The response to viral infection is shaped by the host’s antiviral response • VRIs in early childhood may protect against the development of asthma Role of VRI and RV in Acute Exacerbations of Chronic Bronchitis Cost of Acute Exacerbations of Chronic Bronchitis (AECB) • Hospitalization (500,000 episodes) – Total cost, $1.6 billion – Mean LOS, 6 days – Mean cost, $5500/patient • Outpatient office visits – 65 yr: 331,000, cost $24.9 million – <65 yr: 237,000, cost $15.1 million • Indirect costs – Days lost from work – Lost productivity . Niederman MS et al. Clin Ther. 1999;21:576-591 AECB: Etiology • Infectious, 80% – Bacterial pathogens, 40%–50% – Viruses, 30%–40% – Atypical bacteria, 5%–10% • Noninfectious, 20% – Environmental factors – Noncompliance with medical therapy Sethi S. Chest. 2000;117(suppl):380S. Viral AECB: Pathogens 35 Control % of total identified 30 FEV1 50% 25 FEV1 <50% 20 15 10 5 0 Picornaviruses Parainfluenza viruses Coronaviruses Influenza viruses Data from Greenberg SB et al. Am J Respir Crit Care Med. 2000;162:167. RSV Adenoviruses Virus-Associated Illness in Controls and COPD Patients Controls FEV1 50% FEV1 <50% No. patients 55 30 32 No. respiratory illnesses/yr 1.4 1.8 3 No. VRIs/yr 0.54 0.38 0.52 % LRT symptoms alone 0 0 26 LRT = lower respiratory tract. Data from Greenberg SB et al. Am J Respir Crit Care Med. 2000;162:167. Viral AECB: Medical Resource Utilization 100 • FEV1<50% predicted 80 70 60 % VRI – 52 hospitalizations in 12 patients – 82% acute exacerbations, 22% pneumonia – 5 of 6 deaths were COPD related Control FEV1 50% predicted FEV1 <50% predicted 50 40 30 20 10 0 Office ER=emergency room. Data from Greenberg SB et al. Am J Respir Crit Care Med. 2000;162:167. ER Hospital Viral AECB: Clinical Presentation • AECB manifestations – Increased dyspnea, 76% – Increased sputum volume, 62% – Increased sputum purulence, 39% • Anthonisen type – Type 1 (all 3 of above symptoms), 20% – Type 2 (2 of above symptoms), 46% – Type 3 (1 of above symptoms), 34% • 64% of AECB associated with prior cold (18 days) Seemungal T et al. Am J Respir Crit Care Med. 2001;164:1618. AECB: Viral Detection and Symptoms 25 % of reported exacerbations • 39.2% of AECB associated with viral infection • Cold, increased dyspnea with cold, and sore throat associated with viral isolation 20 15 10 5 0 RV Corona Infl A Data from Seemungal T et al. Am J Respir Crit Care Med. 2001;164:1618. Infl B Parainfl Adeno RSV Summary • AECB are associated with considerable morbidity, mortality, and health care costs • VRIs are an important cause of AECB • RVs are frequently detected in the airway secretions of patients with AECB VRIs in Patients with Cystic Fibrosis Cystic Fibrosis (CF): Respiratory Viruses • Cause exacerbations and LRIs • Contribute to long-term pulmonary deterioration, morbidity, mortality • Strongly associated with every measure of CF disease progression1 • Contribute to initial bacterial colonization2 1. Wang EEL et al. N Engl J Med. 1984;311:1653. 2. Armstrong et al. Pediatr Pulmonol. 1998;26:371. CF: Proposed Mechanisms of Virus-Induced Exacerbation • Infection of epithelial cells – Release of proinflammatory mediators – Attraction and activation of inflammatory cells – Neutrophil release of prostaglandins and oxygen radicals • • • • Altered endothelial permeability Promotion of edema, enhanced cell recruitment Stimulation of mucus secretion Airway smooth muscle contraction Prober CG. Clin Rev Allergy. 1991;9:87. Summary • VRIs are associated with clinical exacerbations of CF with disease progression • Inflammatory response most likely mechanism by which VRIs exacerbate CF • Viruses predispose to bacterial colonization and infection VRIs in Immunosuppressed Cancer Patients Impairments in Viral Immunity in BMT Recipients with Cancer • B lymphocytes – – – Reduced response to stimulatory cytokines (IL-4) Reduced serum immunoglobulins Depressed primary and secondary responses to antigens • T lymphocytes – – – – – Reduced CD4 lymphocyte numbers Reduced helper cell activity Increased suppressor cell activity Reduced proliferative responses Reduced CD8 lymphocyte cytotoxic function • Mucositis • Reduced IgA secretion Couch RB et al. Am J Med. 1997;102(suppl 3A):2. Risk Factors Associated with Serious Morbidity from VRIs in BMT Recipients • Allogeneic transplant • Hematologic malignancy • Graft-vs-host disease • Corticosteroid therapy • ? Conditioning regimen • Lymphopenia (<200/mL) • Age >65 years • <100 days post-transplant Sable CA, Donowitz GR. Clin Infect Dis. 1994;18:273. Important Features of VRIs in Immunocompromised Patients • High potential for nosocomial acquisition1 • Prolonged shedding of virus, even with treatment2 • High frequency of pneumonia and death1 • Viral pneumonia often associated with other infections1 • Outbreaks can occur in absence of community epidemic1 1. Couch RB et al. Am J Med. 1997;102(suppl 3A):2. 2. Bodey GP. Am J Med. 1997;102(suppl 3A):77. Progression of VRIs in Leukemia and BMT No. of infections leading to pneumonia Pneumonia (% of infections) Death (% of those with pneumonia)* 22 33 59 61 32 36 Leukemia BMT 27 20 78 70 33 25 Parainfluenza Leukemia BMT 9 45 67 58 44 22 22 32 100 RSV1 Leukemia BMT Influenza RV2 BMT *Other pulmonary infections often present. 1. Data from Couch RB et al. Am J Med. 1997;102(suppl 3A):2. 2. Data from Ghosh et al. Clin Infect Dis. 1999;29:528. Summary • VRIs are an important cause of morbidity and mortality in immunosuppressed cancer patients • Underlying disease and immunosuppressive therapy contribute to the high mortality rate in BMT patients with VRIs Acute Respiratory Infections and Antibiotic Use: A Primary Care and Health Services Research Perspective Acute Respiratory Infections (ARIs): Primary Care Office Visits, Antibiotic Use, and Bacterial Prevalence in US, 1998 100 25,000 Office visits (1000) Antibiotic prescription 20,000 80 Bacterial prevalence 60 15,000 62% 76% 10,000 30% 40 59% 70% 20 5000 0 0 URI Otitis media Sinusitis Pharyngitis Bronchitis Reprinted from Gonzales R et al. Clin Infect Dis. 2001;33:757. Antibiotic Rx and estimated bacterial prevalence (% of visits) Office visits Estimated Annual Cost of Antibiotic Use for ARIs in US, 1998 ARI diagnosis Otitis media Pharyngitis URI Sinusitis Bronchitis Total No. of prescriptions (millions) 9.6 8.7 7.4 7.9 7.8 41.4 Cost estimate (millions) $280 $215 $227 $310 $289 $1322 Estimated 55% of prescriptions (22.6 million) for ARIs are unnecessary, at a cost of $726 million. Adapted from Gonzales R et al. Clin Infect Dis. 2001;33:757. Emergency Department Visits and Antibiotic Use for ARIs in US, 1996 Condition URIs, all Visits (millions) Antibiotic use 2.0 26% URIs only* 1.6 24% Bronchitis, all 2.1 42% 1.2 42% Otitis media 2.7 55% Pharyngitis 1.5 52% Total ARIs 8.1 44.5% Bronchitis only* *Excludes patients with additional diagnoses of asthma, COPD, chronic bronchitis, pneumonia, otitis, pharyngitis, sinusitis, HIV. Adapted from Stone S et al. Ann Emerg Med. 2000;36:320. Use of Antibiotics: Patient Expectations, Physician Perceptions, Public Beliefs • Patients who expect antibiotics receive them more often1-3 • Strongest predictor of receipt of antibiotics for ARI is MD perception of patient expectation1,3 • Patient satisfaction more closely related to quality of communication (explanations, contingency plans) than receipt of antibiotics1,3,4 • Public beliefs about antibiotic effectiveness5 – Useful for VRI: 55% – Useful for bacterial but not viral illness: 21% 1. Hamm RM et al. J Fam Pract. 1996;43:56. 2. Bauchner H et al. Pediatrics. 1999;103:395. 3. Mangione-Smith R et al. Pediatrics. 1999;103:711. 4. Mangione-Smith R et al. Arch Pediatr Adolesc Med. 2001;155:800. 5. Wilson AA et al. J Gen Intern Med. 1999;14:658. Decreasing Antibiotic Overuse Is Hard But Possible • Pre-, post-intervention trial to decrease antibiotic use in acute, uncomplicated bronchitis in HMO sites • Full intervention: household and office-based patient-education materials; clinician education, profiling, and academic detailing • Limited intervention: office-based patient education materials • Antibiotic use declined from 74% to 48% only at site with full intervention • No differences in revisits, other prescriptions, other diagnoses Gonzales R et al. JAMA. 1999;281:1512. Summary • “Just Say No” to unnecessary antibiotics for ARI – Community and patient education – Office-based interventions – Clinician-oriented interventions • Better technology for rapid diagnostic testing to identify bacterial vs viral illness • Possible development of antiviral medications Program Summary • VRIs are an important cause of morbidity and increased health care costs • RVs are the most common cause of VRIs • RVs are also an important cause of morbidity in patients with asthma, COPD, and CF, and in immunocompromised patients • In immunocompromised cancer patients, VRIs increase mortality and morbidity from pneumonia • The mechanism of exacerbation of asthma, chronic bronchitis, and CF is related to the host inflammatory response • Patients with VRIs are often prescribed antibiotics Contributors Homer A. Boushey, Jr., MD, Editor University of California San Francisco Gerald P. Bodey, Sr., MD The University of Texas M. D. Anderson Cancer Center Houston Sebastian L. Johnston, MD Imperial College of Science, Technology and Medicine London, UK James E. Gern, MD University of Wisconsin Madison Arnold S. Monto, MD University of Michigan School of Public Health Ann Arbor Ethan A. Halm, MD, MPH Mount Sinai School of Medicine New York Harley A. Rotbart, MD University of Colorado Health Sciences Center Denver Sanjay Sethi, MD State University of New York Buffalo