Lesson 11, Volume 15—Pediatric Community-Acquired Pneumonia

By Glenda Hsiao, MD; Cindy Black-Payne, MD; and G. Douglas Campbell, MD, FCCP

Objectives

1. Understand the significance of pediatric community-acquired pneumonia (PCAP).
2. Identify the common bacterial etiologies of PCAP based on age.
3. Identify the signs and symptoms of PCAP.
4. Appropriately use the common diagnostic tests in the evaluation of PCAP.
5. Choose appropriate antibiotics for the treatment of PCAP.

Key words

diagnosis; etiology; pediatric, pneumonia; Streptococcus pneumoniae; treatment

Abbreviations

MIC = minimum inhibitory concentration; PCAP = pediatric community-acquired pneumonia; RSV = respiratory syncytial virus

The American Thoracic Society, the Infectious Disease Society of America, and the Canadian Thoracic Society have published evaluation and treatment guidelines for community-acquired pneumonia in adults.^1-3 Extrapolation of these guidelines to children is worrisome because of the difference in the clinical presentation, the spectrum of etiologic agents, complications, and available antibiotic therapy. Many pulmonary physicians trained to care for adults, however, are asked to care for young children and adolescents. In 1997, prior to the widespread use of the newer macrolide antibiotics, a consensus of Canadian experts published recommendations for the diagnosis and treatment of pediatric community-acquired pneumonia (PCAP).⁴ At present, no US consensus exists for the treatment of PCAP.

Challenges remain in the diagnosis and treatment of PCAP in previously healthy children and adolescents. Numerous pathogens cause PCAP, and at best, the etiology is determined in only half of the cases.⁵ Practical diagnostic methods to identify the etiology of PCAP are not widely available. Additionally, interobserver variability occurs in the clinical assessment of children with respiratory illnesses. These factors confound attempts to formulate a workable case definition that would allow central data collection to advance understanding of the disease.

Because the etiology of PCAP is rarely identified in a timely manner and because of the associated morbidity, treatment of PCAP is usually empirical. A patient’s age, the time of year, and the patient’s vaccination status all affect the incidence, etiology, and thus treatment of PCAP (Table 1).⁶ Complicating empirical antibiotic selection is the increase in drug-resistant organisms, especially Streptococcus pneumoniae.

Table 1—Common Agents Causing PCAP and Months During Which They Are Usually Seen

The objective of this review is to provide an approach to the diagnosis and management of PCAP for pulmonary physicians. This review is limited to previously healthy, postneonatal, immunocompetent children.

Significance

PCAP accounts for 37% of the community-acquired pneumonia cases, or 1.5 million cases, in the United States each year.⁷ The incidence peaks between 1 and 5 years of age, and declines in older children. PCAP remains a major cause of pediatric morbidity and health-care costs, accounting for numerous emergency room visits, office visits, and hospitalizations. In 1996, 178,000 hospital admissions with an average length of stay of 3.6 days⁸ were attributed to PCAP. It is the most frequent diagnosis of patients admitted to the pediatric ICUs, where the average cost per stay is estimated to be $12,342.⁹

Only 1,000 deaths from PCAP occurred in 1995.⁸ Mortality in the United States tends to be associated with S pneumoniae bacteremia and sepsis, but in developing countries, mortality is associated with malnutrition and poor access to medical care.

Etiology

There is a spectrum of pathogens that commonly cause PCAP, including both bacterial and viral agents. The exact incidence of each agent is unknown because an exact etiology is only rarely determined. The most commonly reported bacterial pathogens include S pneumoniae, Moraxella catarrhalis, Haemophilus influenzae (usually nontypable if the patient has received the H influenzae serotype B vaccine), Mycoplasma pneumoniae, and Chlamydia pneumoniae.¹⁰ In addition, numerous respiratory viruses are reported to cause PCAP, with respiratory syncytial virus (RSV), influenza A and B, and adenovirus accounting for the majority.

Two recent studies attempted to determine the incidence of each pathogen as a cause for PCAP (Fig 1). An etiology was identified in only half of the cases and often was based on serologic testing. Together, these studies indicated that S pneumoniae was the most common pathogen across all age groups, and that while the incidence of viral pathogens decreased among older children, the incidence of M pneumoniae and C pneumoniae increases with age.^5,10

	Figure 1. A, incidence of etiologic agents in three age groups as reported by Wubble et al.5 B, incidence of etiologic agents in three age groups as reported by Heiskanen-Kosma et al.10

Diagnosis

Although adolescents may demonstrate the classic adult presentation of pneumonia, including the abrupt onset of symptoms, high fever, productive cough, pleuritic chest pain, and possible toxic appearance, the presentation of the younger child with PCAP is often subtle. It may include any combination of fever, lethargy, tachypnea, irritability, vomiting, diarrhea, and poor feeding. Physical findings are variable based on age, size of the child, easy transmission of breath sounds, absence of crackles, and skill of the examiner.¹¹

Studies evaluating the use of physical exam findings to diagnose PCAP have shown that such findings are limited. No one finding can be used to diagnose or exclude pneumonia, but the absence of all the findings of tachypnea, crackles, fever, and decreased breath sounds excludes the diagnosis of PCAP with 100% specificity. The findings most sensitive for predicting infiltrate on the chest radiograph were tachypnea, cough, and toxic appearance. Grunting, flaring, and pallor were the most specific predictors for pulmonary infiltrate (Table 2).^12-14 Because the clinical presentation of PCAP may be subtle, radiographic and laboratory studies aid in the diagnosis of PCAP and allow identification of its etiology.

Chest Radiographs

A chest radiograph is generally regarded as the gold standard for confirming the presence of PCAP. The routine use of a screening chest radiograph for every child with a cough or fever is not appropriate. In one study of 121 febrile children without respiratory symptoms, chest radiography failed to identify a single case of PCAP.¹⁵ In another study, however, 18% of children with S pneumoniae pneumonia had no respiratory symptoms.¹⁶ In children younger than 3 years old in whom abnormal clinical signs and symptoms are absent, a chest radiograph identified pneumonia in up to 25% of patients with a fever > 39.6°C and a WBC count > 15,000 cells/mm³.^17,18 A chest radiograph should be obtained in toxic-appearing children without an identifiable source of infection, children younger than 36 months of age with fever > 39.6°C and WBC > 15,000 cells/mm³, and children with the classical presentation of PCAP.

Infiltrate patterns are not sensitive to determine the etiology of PCAP. S pneumoniae is as likely to cause alveolar infiltrates as interstitial infiltrates. While there is some modest predictive value of alveolar infiltrates for bacterial pneumonia, both bacterial and viral etiologies must be considered in the presence of either type of infiltrate. Several studies have confirmed these findings.^19-21

When a child's clinical course is deteriorating or failing to improve, an additional radiograph may be helpful to identify complications. These may include pleural effusion, lung abscess, or the presence of an obstructing foreign body.¹⁶ In uncomplicated pneumonia, a follow-up chest radiograph is unlikely to alter management.

CT of the Chest

Children with PCAP who respond poorly to treatment rarely require CT of the chest to direct management. CT scans may reveal abnormalities in complicated pneumonia that are not obvious by a chest radiograph. These may include parenchymal and pleural complications and pericardial effusions. CT should be considered in this very select population.²²

Laboratory Studies

WBC count cannot differentiate viral from bacterial pneumonia. In a study of 121 patients with PCAP, no statistically significant differences in leukocyte count among children with viral, bacterial, or mixed pneumonias were noted. Additionally, C-reactive protein and erythrocyte sedimentation rates have been studied, and the results are similar to those for leukocyte count. These studies suggest they are of little value in determining an etiology of the PCAP.^23-25 Antigen tests for Influenza A and B and RSV are readily available. Their sensitivity for detection is > 70% with a specificity approaching 100%.^26-28

Although some clinicians commonly collect blood cultures when PCAP is suspected, the necessity of doing so is controversial. In the outpatient setting, blood cultures dramatically increase the expense of treatment without greatly influencing management decisions. Antibiotic decisions in outpatients and the need for re-evaluation of therapy are primarily based on clinical judgment.¹⁸ In inpatients, the incidence of bacteremia associated with pneumonia is higher in children than adults.²⁹ In hospitalized patients, blood cultures may help direct the antibiotic coverage and even narrow it if an organism is isolated. The sensitivity for detecting bacteremia increases with increasing number of sets collected, approaching 99% with three sets.²⁹ The risk of bacteremia with PCAP is greatest among the very young and increases with fever and high leukocyte counts.¹⁸

Pulse Oximetry

The presence of hypoxemia associated with PCAP is an indication for admission. In children, the sensitivity of physicians detecting hypoxemia clinically is less than 40%. Accordingly, it is appropriate to use pulse oximetry in the routine assessment of PCAP.³⁰

Inpatient vs Outpatient Treatment

Criteria for the admission of children with PCAP are similar to those for adults. In addition to considering severity of illness, ability to maintain hydration and take oral medication, and opportunity for follow-up, the physician must also consider the family support structure and seek to identify the primary caregiver. Children, especially young children, are often dependent on their caregivers to administer the medication. If the ability or motivation of the caregiver(s) to administer the medication is in doubt, admission should be considered (Table 3).²⁹

Treatment

The treatment of PCAP is almost always empirical, as it is extremely rare that a causative organism is identified before antibiotics are selected (Table 4). Because it is difficult to distinguish between bacterial, viral, and mixed infections, most children with PCAP are treated with antibiotics. When selecting empirical therapy, it is important to consider the spectrum of likely pathogens and risk for resistant organisms. Goals of timely therapy include expediting clinical improvement and preventing complications.³¹

S pneumoniae is the most common bacterial cause of PCAP in all ages.³² Elevated minimum inhibitory concentrations (MICs) to penicillin are being identified in S pneumoniae (0.1 to 1.0 mg/mL, intermediate; 1.0 to 2.0 mg/mL, resistant) and are increasingly more common among children younger than 6 years and those attending day-care centers. Fortunately, at this time, S pneumoniae isolates with an MIC > 4.0 mg/mL are rare. Current studies suggest that in the absence of meningitis, beta-lactam antibiotics are effective treatment against S pneumoniae with MIC to penicillin < 4.0 mg/mL.^33,34

The newer macrolides continue to be effective against a broad range of pulmonary pathogens, including most S pneumoniae. Azithromycin offers improved activity over clarithromycin against H influenzae.³⁵ Vancomycin should be reserved for very ill patients in whom there is a suspicion of methicillin-resistant Staphylococcus aureus or S pneumoniae with an MIC to penicillin > 4.0 mg/mL.³⁶ Fluoroquinolones, widely used to treat community-acquired pneumonia in adults, are not approved for use in children. Tetracycline may be used in children whose permanent front teeth have erupted, usually around age 8 years. Linezolid has not been approved for pediatric use.

Antibiotic Selection

Outpatient. Empiric therapy for PCAP in children aged 3 months to 5 years is predominately directed at S pneumoniae (Table 4). Amoxicillin with or without clavulanate is usually the drug of choice in otherwise healthy children. In penicillin-allergic patients, a macrolide can be used. Erythromycin is the only one approved for children younger than 6 months. After age 5 years, empirical therapy should include coverage for M pneumoniae and C pneumoniae, necessitating the use of a macrolide. Newer macrolides are preferred over erythromycin because of increased activity against S pneumoniae.³⁷

Empirical therapy for PCAP in hospitalized patients aged 3 to 6 months may include ceftriaxone or cefotaxime. These specific third-generation cephalosporins cover the pathogens likely to cause PCAP, and will treat meningeal infection that may be subtle in this age group. Ceftriaxone, cefotaxime, or cefuroxime are appropriate in the 6 months to 5 years age group. In children older than 5 years, a macrolide may be added for coverage of atypical bacterial pathogens. In critically ill children, vancomycin may be considered as additive therapy to ceftriaxone or cefotaxime. Again, it is prudent to treat children in this group with antibiotics that also treat meningeal infection, as the clinician may be unable to adequately assess the presence of meningitis in a critically ill child.⁴

The administration of an initial parenteral dose (IV or IM) of antibiotic to outpatients with PCAP who are moderately ill is common practice.^38,39 Reasons offered to justify this practice include timely initiation of therapy and a desire to attain high tissue concentrations rapidly. Additionally, concerns over the patient's compliance and tolerance of oral medications are addressed. Reports regarding empirical outpatient ceftriaxone therapy are usually in the context of preventing complications.⁴⁰ Evidential support for outpatient empirical parenteral cephalosporin therapy for pneumonia is limited. A recent retrospective review of children with S pneumoniae bacteremia treated as outpatients supports it. Children who were initially administered a parenteral antibiotic were more likely to have an improved condition at a follow-up visit. They were also less likely to require subsequent hospitalization. Notably, children treated with oral agents alone also did well.⁴1 Siegel et al⁴² conducted a study in adult inpatients with community-acquired pneumonia who received ceftriaxone initially, followed by oral antibiotics. This group did equally as well as the group who received a longer course of parenteral antibiotics. Empirical parenteral outpatient therapy in PCAP likely has an important role, but it remains to be defined.

Response to Therapy

Children treated for PCAP as outpatients should be reassessed 24 to 48 h after the initial visit. If the child's condition has deteriorated further, the clinician should consider inpatient treatment of the child. Within 48 to 72 h of appropriate treatment initiation, a clinical response should be noted in children with bacterial PCAP. The clinical response time in atypical pneumonias is less clear, and in cases of viral pneumonias, 7 to 10 days may be needed for acute symptoms to resolve. In any case, if some improvement is not noted within 72 h, repeat laboratory studies and chest radiograph should be obtained and therapy re-examined.^43,44

When treating inpatients for PCAP, a switch from IV to oral antibiotics is appropriate when the fever has abated and the patient can tolerate oral medication and is otherwise clinically improving. Patients may be discharged when the criteria for outpatient management of PCAP are met.³⁶

Patients with bacterial PCAP occasionally develop complications, either acutely or subacutely. These complications are most commonly associated with S pneumoniae in children younger than 2 years and include meningitis, purpura fulminans, arthritis, parapneumonic effusions, empyema, abscess formation, endocarditis, and pericarditis. Mortality, although rare, is usually related to the development of meningitis. There is no increased risk of morbidity or mortality associated with the presence of penicillin-resistant S pneumoniae.⁴⁵

Complications of viral PCAP, including focal necrosis and airway plugging, may lead to atelectasis, bronchospasm, apnea spells, and respiratory failure. Rarely, ARDS occurs. Long-term sequelae of viral pneumonia include recurrent reactive airway disease, bronchiectasis, bronchiolitis obliterans, and rarely pulmonary fibrosis.²⁹ Irreversible reduced lung function has been noted to occur in adults with histories of PCAP.^46,47

Special Concerns

Antiviral agents have been used in the treatment of PCAP, but their role is controversial. The efficacy of ribavirin for RSV has been variable in clinical trials. Its use is considered in hospitalized patients who are at risk for or already have developed severe disease from RSV infection. Several antiviral agents have activity against influenza A, and one against influenza B. It is unclear whether or not they prevent complications or can treat influenza pneumonia. Aspirin should be avoided because of the increased risk of Reye's syndrome in children with influenza infections.

If concurrent otitis media is present and amoxicillin is used, the Centers for Disease Control and Prevention recommend high-dose amoxicillin in children at risk for drug-resistant S pneumoniae infections. When concurrent bacterial meningitis is suspected, vancomycin and ceftriaxone or cefotaxime should be used until sensitivities are obtained and coverage can be narrowed.

Summary

Although the diagnosis of pneumonia in adults is recognized based on history and examination findings, in children, signs and symptoms of PCAP may be subtle. Tachypnea, cough, and toxic appearance are relatively sensitive but not specific for the diagnosis. Grunting, flaring, pallor, retractions, and crackles are fairly specific but not sensitive. When combined with fever > 39°C, both the sensitivity and specificity of these signs and symptoms increase. Pulse oximetry should be obtained in all patients in whom pneumonia is suspected. A chest radiograph should be obtained if (1) the diagnosis is questionable; (2) this is a repeated episode; (3) the patient is ill enough to be admitted; (4) the child is younger than 3 years and has a fever > 39°C without a source and leukocytosis > 15,000 mm³; or (5) a complicated pneumonia is suspected. Blood culture may be reserved for inpatients as it is unlikely to alter the outpatient management in a pediatric setting. During RSV and influenza seasons, it may be useful to check antigen tests for these viruses; however, it must be remembered that mixed bacterial and viral infections are not uncommon.

Children who are very young, hypoxic, toxic-appearing, lethargic, hyperirritable, or in respiratory distress should be admitted and empirical treatment should be initiated as soon as possible. For outpatient treatment of PCAP, a newer macrolide or amoxicillin with clavulanate may be used for patients younger than 5 years, and a macrolide for older children. Children who are ill enough to be admitted should be treated with parenteral therapy. Older infants and children should be treated with a second- or third-generation cephalosporin (ceftriaxone or cefotaxime). In children 5 years and older, a macrolide may be added. When an inpatient with PCAP improves enough to meet criteria for outpatient therapy, the treatment may be changed to comparable oral antibiotics. Total therapy should continue for 7 to 10 days in an uncomplicated pneumonia. S aureus pneumonia and complicated pneumonias may require more extensive intervention and length of therapy. Finally, an initial IM injection of ceftriaxone has limited evidential support but is a widely accepted and utilized practice.

References

1. Neiderman MS, Bass JB, Campbell GD, et al. Guidelines for the initial management of adults with community-acquired pneumonia: diagnosis, assessment of severity, and initial antimicrobial therapy. Am Rev Respir Dis 1993; 148:1418–1426
2. Bartlett JG, Breiman RF, Mandell LA, et al. Community-acquired pneumonia in adults: guidelines for management. Clin Infect Dis 1998; 26:811–838
3. Mandell LA, Marrie TJ, Grossman RF, et al. Canadian guidelines for the initial management of community-acquired pneumonia: an evidence-based update by the Canadian Infectious Diseases Society and the Canadian Thoracic Society. The Canadian Community-Acquired Pneumonia Working Group. Clin Infect Dis 2000; 31:383-421
4. Jadavji T, Law B, Lebel MH, et al. A practical guide for the diagnosis and treatment of pediatric pneumonia. Can Med Assoc J 1997; 156:703–711
5. Wubble L, Muniz L, Ahmed A, et al. Etiology and treatment of community-acquired pneumonia in ambulatory children. Pediatr Infect Dis J 1999; 18:98–104
6. Sinaniotis CA. Community-acquired pneumonia: diagnosis and treatment. Pediatr Pulmonol Suppl 1999; 18:144–145
7. Jokinen C, Heiskanen L, Juvonen H, et al. Incidence of community-acquired pneumonia in the population of four municipalities in eastern Finland. Am J Epidemiol 1993; 137:977–988
8. Vital Statistics of the United States. Hyattsville, MD: National Center for Health Statistics 1998:98–105
9. Chalom R, Raphaely RC, Costarino AT. Hospital costs of pediatric intensive care. Crit Care Med 1999; 27:2079–2085
10. Heiskanen-Kosma T, Korppi M, Jokinen C, et al. Etiology of childhood pneumonia: serologic results of a prospective, population-based study. Pediatr Infect Dis J 1998; 17:986–991
11. Churgay CA. The diagnosis and management of bacterial pneumonias infants and children. Prim Care 1996; 23:821–835
12. Leventhal JM. Clinical predictors of pneumonia as a guide to ordering chest roentgenograms. Clin Pediatr 1982; 21:730–734
13. Taylor JA, Del Beccaro M, Done S, et al. Establishing clinically relevant standards for tachypnea in febrile children younger than 2 years. Arch Pediatr Adolesc Med 1995; 149:283–286
14. Berman S, Simoes EAF, Lanata C. Respiratory rate and pneumonia in infancy. Arch Dis Child 1991; 66:81–84
15. Patterson RJ, Bisset GS, Kirks DR, et al. Chest radiographs in the evaluation of the febrile infant. AJR Am J Roentgenol 1990; 155:833–835
16. Totapally BR, Walsh WT. Pneumococcal bacteremia in childhood. Chest 1998; 113:1207–1214
17. Bachur R, Perry H, Harper MB. Occult pneumonias: empiric chest radiographs in febrile children with leukocytosis. Ann Emerg Med 1999; 33:166–173
18. Baraff LJ, Bass JW, Fleisher GR, et al. Practice guideline for the management of infants and children 0-36 months of age with fever without source. Ann Emerg Med 1993; 22:1198–1210
19. Korppi M, Kiekara O, Heiskanen-Kosma T, et al. Comparison of radiological findings and microbial aetiology of childhood pneumonia. Acta Paediatr 1993; 82:360–363
20. Isaacs D. Problems in determining the etiology of community-acquired childhood pneumonia. Pediatr Infect Dis J 1989; 8:143–148
21. Wahlgren H, Mortenson W, Eriksson M, et al. Radiographic patterns and viral studies in childhood pneumonia at various ages. Pediatr Radiol 1995; 25:627–630
22. Donnelly LF, Klosterman LA. The yield of CT of children who have complicated pneumonia and noncontributory chest radiography. AJR Am J Roentgenol 1998; 170:1627–1631
23. Nohynek H, Valkeila E, Leinonen M, et al. Erythrocyte sedimentation rate, white blood cell count and serum C-reactive protein in assessing etiologic diagnosis of acute lower respiratory infections in children. Pediatr Infect Dis J 1995; 14:484–490
24. Korppi M, Kroger L, Laitinen M. White blood cell and differential counts in acute respiratory viral and bacterial infections in children. Scand J Infect Dis 1993; 25:435–440
25. Korppi M, Heiskanen-Kosma T, Leinonen. White blood cells, C-reactive protein and erythrocyte sedimentation rate in pneumococcal pneumonia in children. Eur Respir J 1997; 10:1125–1129
26. Gibson NA, Hollman AS, Paton JY. Value of radiological follow up of childhood pneumonia. BMJ 1993; 307:1117
27. Darville T, Yamauchi T. Respiratory syncytial virus. Pediatr Rev 1998; 19:55–61
28. Washington JA. Blood cultures: principles and techniques. Mayo Clin Proc 1975; 50:91–98
29. Latham-Sadler BA, Morell VW. Community-acquired respiratory infections in children. Prim Care 1996; 23:837–841
30. Maneker AJ, Emory MP, Krug SE. Contribution of routine pulse oximetry to evaluation and management of patients with respiratory illness in a pediatric emergency department. Ann Emerg Med 1995; 25:36–40
31. Boccazzi A, Tonelli P, Bellosta C, et al. Clinical and pharmacological evaluation of a modified cefotaxime bid regimen versus traditional tid in pediatric lower respiratory tract infections. Diagn Microbiol Infect Dis 1998; 32:265–272
32. Prevention of pneumococcal disease: recommendations of the advisory committee on immunization practices (ACIP). MMWR Morb Mortal Wkly Rep1997; 46:1–24
33. Tan TQ, Mason EO, Barson WJ, et al. Clinical characteristics and outcome of children with pneumonia attributable to penicillin susceptible and penicillin nonsusceptible Streptococcus pneumoniae. Pediatrics 1998; 102:1369–1375
34. Friedland IR, McCracken GH. Drug therapy: management of infections caused by antibiotic-resistant Streptococcus pneumoniae. New Engl J Med 1994; 331:377–382
35. Schaad UB. Antibiotic therapy of childhood pneumonia. Pediatr Pulmonol Suppl 1999; 18:146–149
36. Deeks SL, Palacio R, Ruvinsky R, et al. Risk factors and course of illness among children with invasive penicillin-resistant Streptococcus pneumoniae. Pediatrics 1999; 103:409–413
37. Harris JS, Kolokathis A, Campbell M, et al. Safety and efficacy of azithromycin in the treatment of community-acquired pneumonia in children. Pediatr Infect Dis J 1998; 17:865–871
38. Long SS. Treatment of acute pneumonia in infants and children. Pediatr Clin North Am 1983; 30:297–320
39. Kays MA, Pichichero ME. Outpatient management of pediatric pneumonias. Semin Pediatr Infect Dis 1990; 1:340–348
40. Chumpa A, Bachur RG, Harper MB. Bacteremia-associated pneumococcal pneumonia and the benefit of initial parenteral antimicrobial therapy. Pediatr Infect Dis J 1999; 18:1081–1085
41. Fleisher GR. Intramuscular versus oral antibiotic therapy for the prevention of meningitis and other bacterial sequelae in young, febrile children at risk for occult bacteremia. J Pediatr 1994; 124:504–512
42. Siegel RE, Alicea M, Lee A, et al. The use of one dose of IV therapy prior to oral switch for hospitalized patients with community-acquired pneumonia [abstract]. Am J Respir Crit Care Med 2000; 161:A652
43. Schidlow DV, Callahan CW. Pneumonia. Pediatr Rev 1996; 17:300–309
44. Muhe L. Pattern of resolution of tachypnoea and fever in childhood pneumonia. East Afr Med J 1998; 75:63–67
45. Johnston RB. Pathogenesis of pneumococcal pneumonia. Rev Infect Dis 1991; 13:(suppl 6):S509–S517
46. Johnston ID, Strachan DP, Anderson HR. Effect of pneumonia and whooping cough in childhood on adult lung function. N Engl J Med 1998; 338:581–587
47. Shaheen SO, Sterne JA, Tucker JS, et al. Birth weight, childhood lower respiratory tract infection and adult lung function. Thorax 1998; 53:549–553
48. Hsiao GR, Black-Payne C, Campbell GD. Pneumonia, Part 1: Making the diagnosis. J Respir Dis for Pediatricians 2001; 3:68–77

Copyright ©2001 American College of Chest Physicians

3300 Dundee Road • Northbrook, Illinois 60062-2348 • (847) 498-1400 • (800) 343-2227
Copyright ©1999-2008 American College of Chest Physicians. All Rights Reserved.
ACCP Privacy Policy | ACCP Web Site Terms of Use