Critical Care Medicine
Aspiration syndromes, Aspiration, Abscess, Pulmonary Abscess
- 1. Description of the problem
- 2. Emergency Management
- 3. Diagnosis
- 4. Specific Treatment
- 5. Disease monitoring, follow-up and disposition
Special considerations for nursing and allied health professionals.
What's the evidence?
Aspiration Pneumonia and Lung Abscess
Aspiration, Abscess, Pulmonary Abscess
1. Description of the problem
What every clinician needs to know
Aspiration can lead to any of four distinct syndromes: pneumonitis (which is not discussed further in this chapter); necrotizing pneumonia; lung abscess; or empyema (which almost always overlaps with pneumonia or abscess formation).
Pulmonary aspiration and its infectious complications are important causes of serious illness and death in hospitalized patients and residents of chronic care facilities.
As a rule, aspiration pneumonia is polymicrobial. The role of anaerobes is controversial but likely less important than historically suggested. Regardless, these organisms should be assumed to be present in patients with risk factors or suspicious physical exam findings.
Serious sequelae can be minimized through prompt recognition of infection, timely initiation of appropriate antibiotic therapy, and strategies to avoid recurrent aspiration.
Steroids have no proven benefit in aspiration pneumonia.
Ventilator-associated pneumonia is a select example of aspiration pneumonia and highlights the importance of minimizing aspiration.
Contrary to popular belief, percutaneous endoscopic gastrostomy (PEG) tubes have not been shown to reduce aspiration compared to nasogastric tubes, and post-pyloric placement has similar rates of aspiration as intragastric placement.
Clinical manifestations of an aspiration event fall anywhere along a diverse spectrum, including asymptomatic, dry cough, dysphonia, stridor, vomiting after meals, or ARDS.
Symptoms of true infection (aspiration pneumonia) are extremely variable and depend on the point at which the patient is seen during the evolution of the disease process, the pathogens involved, and multiple host-specific factors. Symptoms are similar to that of any acute pneumonia process but develop more slowly – typically over several days or weeks instead of hours. Manifestations range from mild illness in an ambulatory patient to critical illness with shock and/or respiratory failure.
Pneumonia is suggested by fever (or hypothermia in the elderly), dyspnea, pleuritic chest pain, and cough productive of purulent mucus. These patients are generally toxic with fevers above 39°C, tachycardia, and tachypnea. Note that patients with aspiration pneumonia almost never have rigors.
Physical findings are consistent with other forms of pneumonia and include decreased breath sounds, dullness to percussion, rales, egophony, pectoriloquy, pleural friction rub, altered mental status, hypotension and/or hypoxemia.
Features suggesting the presence of an anaerobic infection include poor dentition, foul-smelling breath and/or sputum, and consolidative findings in gravity-dependent lung zones.
Without timely recognition and appropriate treatment, anaerobic pneumonia cavitates and/or leads to abscess formation.
Abscess symptoms develop insidiously over many weeks and have a predominance of fatigue, low-grade fever, weight loss and productive cough. Half of patients report expectoration of putrid sputum, which may or may not be associated with hemoptysis. These patients appear chronically ill with fevers generally below 39°C. Uncommon but highly suggestive findings include amphoric breath sounds over the abscess cavity and clubbing of the fingers.
Key management points
Ensure a secure airway and adequate oxygenation if the aspiration event is witnessed. Suction any foreign material from the mouth as it represents potential for further aspiration.
Assess for systemic manifestations of infection, including shock and bacteremia.
Collect adequate culture data. Although ideally this should be done before any antibiotic therapy is administered, initiation of antibiotics should not be delayed for completion of the diagnostic evaluation.
Monitor the clinical response to antibiotic therapy and maintain a low threshold for repeat imaging to assess for infection-related complications.
2. Emergency Management
Emergency management steps
Patients with witnessed aspiration of large volumes of material complicated by acute hypoxia require establishment of a secure airway, oxygen supplementation and appropriate monitoring. Endoscopic evaluation for therapeutic purposes (foreign body removal) and/or diagnostic sampling (culture material) should be considered early in the disease process.
Acutely ill patients require adequate IV access, resuscitation fluids if hypotensive, and correction of any electrolyte or acid-base abnormalities.
Bronchial hygiene is critical and subsequent management is dictated by the severity of respiratory compromise.
Bronchospasm is common after an aspiration event and should be managed with aggressive bronchodilator therapy.
Management points not to be missed
Maintain a patent airway and initiate continuous pulse oximetry to ensure adequate oxygenation.
Take appropriate steps to avoid further aspiration.
Although antibiotics are the cornerstone of management for aspiration pneumonia, start antimicrobial therapy only if infection is likely.
Antibiotic therapy for aspiration pneumonia is typically empiric and must include a patient-specific assessment of risk factors to determine the need for coverage of anaerobes and/or pathogens associated with drug resistance (i.e., Pseudomonas aeruginosa, MRSA).
Aspiration pneumonia is most frequently established clinically when pneumonia is diagnosed in a patient with a history of aspiration or with risk factors for aspiration.
The bacteriology of aspiration pneumonia is controversial and is likely influenced by whether the aspiration event was community-acquired or hospital-acquired. The key pathogens are those found in the microbial flora of gastric juice and/or oropharynx. Up to one third of patients have only anaerobes. The remainder have mixed infections with anaerobes, aerobes and facultative organisms.
In hospital-acquired aspirations the clinician must give strong consideration to resistant Gram-negative rods and MRSA.
The diagnostic utility of sputum cultures has been criticized as anaerobes are difficult to reliably isolate using routine culture methods. Accurate results require anaerobic processing and transport to preserve anaerobes and fastidious strains.
Definitive diagnosis of an anaerobic infection typically requires an invasive procedure.
Transtracheal aspiration - once believed to be the gold standard for diagnosis - is rarely pursued given concerns that recovered organisms represent oropharyngeal flora aspirated during the procedure or colonizers of the trachea.
Endoscopic visualization of foreign material below the cords establishes the diagnosis of aspiration, but not pneumonia.
Percutaneous lung biopsy is reliable but invasive.
Transbronchial protected specimen brush sampling avoids oral contamination but requires conscious sedation, which is an established risk factor for further aspiration.
Clinicians are generally hesitant to subject acutely ill patients to the majority of these procedures. Accordingly, the diagnosis is typically based on clinical features.
Because bacteremia is extremely uncommon with anaerobes, blood cultures have diminished predictive value.
Laboratory and radiographic evaluation
Routine studies include a complete blood count (to assess the degree of leukocytosis), a basic metabolic panel (to look for electrolyte disorders and to estimate kidney function for antibiotic dosing), arterial blood gases (to assess the pH and oxygenation), and sputum for Gram stain, culture and microbiology.
Routine blood cultures are not recommended given their low yield in uncomplicated cases (no evidence of sepsis or shock).
Key features of aspiration pneumonia:
White blood cell counts are elevated, often exceeding 20,000 cells/μL.
Radiographic findings are variable, but dense infiltrates typically develop in the pulmonary segments that were dependent when the aspiration occurred. Classically this is seen as posterior upper lobe and superior lower lobe segments when supine and basilar segments of the lower lobes when upright. Lucency within the infiltrate suggests a necrotizing pneumonia.
Costophrenic angle blunting and the presence of a meniscus are signs of parapneumonic pleural effusion. Pleural effusions and/or progression to necrosis with cavitation are common with anaerobic infection. Empyema is reported to develop in up to one third of cases.
Key features of lung abscess:
Leukocytosis is variable but generally is less impressive than with pneumonia.
Anemia of chronic disease is a common finding.
The most common radiographic finding is a single lung abscess, typically >2 cm in diameter, in a dependent segment of the lung. Classic findings include air-fluid levels within a circumscribed infiltrate/density.
How do I know this is what the patient has?
The diagnosis is suspected based on the basis of the clinical presentation and the presence of key features, including aspiration risk factors; periodontal disease; foul-smelling secretions; involvement of dependent lung segments; and the presence of cavitation.
The diagnosis is confirmed if invasive respiratory secretions show numerous polymorphonuclear leukocytes and an abundance of organisms with varying morphologies and Gram stain characteristics.
What else could it be?
Noninfectious aspiration pneumonitis (Mendelson's syndrome) is the major consideration.
The possibility of a retained aspirated foreign body should also be entertained.
Cavitation of a bronchogenic carcinoma can be assessed with bronchoscopy.
Mycoses, hypersensitivity pneumonitis and vasculitis can appear similar radiographically with cavitations that mimic abscess formation.
1. If a swallowing disorder is suspected, a variety of confirmatory tests exist, including tracheal pH probes, dye visualization tests, radioactive tracer administration, respiratory cytology analysis, video fluoroscopy, and endoscopy. None of these studies is sufficiently reliable and/or reproducible to be the uniformly accepted standard.
2. Simple bedside assessment of cough and gag reflexes has low positive and negative predictive value. A comprehensive swallow evaluation in consultation with a speech pathologist is most frequently recommended for the evaluation of aspiration.
3. Confirmation of aspiration does not definitively establish that the observed pneumonia resulted directly from the aspirated material, as 45% of healthy adults aspirate during sleep without clinical sequelae. These events are believed to be asymptomatic given the small volumes aspirated, the low pathogen burden in the aspirated material, the presence of efficient clearance mechanisms, and intact immunity. Although many entities have been evaluated (pepsin, lipid-laden macrophages, soluble triggering receptor expressed on myeloid cells 1, C-reactive protein, procalcitonin, various cytokines, exhaled breath condensate), there are no reliable biomarkers to definitively diagnose aspiration pneumonia.
4. Specific Treatment
Antibiotics are always indicated for microbiology-confirmed aspiration pneumonia.
Although penicillin G was historically the drug of choice for aspiration pneumonia, more recent data suggest its role is limited given a reduced focus on anaerobes as causative pathogens and the increasing frequency of beta-lactamase-producing species.
Empiric aspiration pneumonia therapy should have activity against beta-lactamase-producing strains.
Two studies demonstrated that clinical cure rates were superior for clindamycin when compared to penicillin. Clindamycin has also been shown to be as effective as ampicillin-sulbactam and imipenem: clindamycin was also significantly less expensive and led to fewer MRSA superinfections.
Recommendations for “optimal” therapy are challenging given the lack of consensus on the pathogens of most concern and limited prospective comparisons of clinical outcomes with various antibiotic regimens.
When anaerobic bacteria are likely pathogens in aspiration pneumonia, clindamycin is typically used as first-line therapy. Alternative regimens include amoxicillin-clavulanate monotherapy or combination therapy consisting of either amoxicillin or penicillin G PLUS metronidazole.
For nosocomial and nursing home-acquired aspiration pneumonia, companion aerobic organisms are increasingly important. In these patients consider piperacillin-tazobactam or imipenem monotherapy or combination therapy with levofloxacin, ciprofloxacin or ceftazidime PLUS clindamycin or metronidazole.
Metronidazole monotherapy should not be used as it is associated with a failure rate approaching 50%, presumably due to its lack of effect on microaerophilic and aerobic streptococci.
Convincing data are lacking for the use of moxifloxacin, macrolides, cefotaxime and tigecycline in aspiration pneumonia and lung abscess.
Trimethoprim-sulfamethoxazole shows poor in vitro activity against several pathogens of concern and should be avoided.
Regardless of the regimen, therapy is usually given intravenously until the white blood cell count and fever curve show sustained improvement.
Patients with documented swallowing dysfunction require efforts to prevent repeat aspiration events. Prophylactic strategies should combine behavioral, dietary and medical interventions.
Tube feedings are recommended for patients who continue to aspirate despite these interventions.
Corticosteroid therapy is not associated with improved clinical outcomes and should not be routinely used.
Drugs and dosages
The choice of agents prescribed, doses and duration of therapy must be individualized based on patient-specific factors. The doses listed here assume normal renal function.
Amoxicillin 500 mg every 8 hours
Amoxicillin-clavulanate 875 mg every 12 hours
Ceftazidime 2 grams every 8 hours
Ciprofloxacin 400 mg every 8 hours
Clindamycin 600 mg IV twice daily, then 300 mg orally four times daily
Imipenem 500 mg every 8 hours to 1 gram every 6 hours
Levofloxacin 750 mg daily
Metronidazole 500 mg every 8 hours
Penicillin G 1-2 million units every 4-6 hours
Piperacillin-tazobactam 4.5 grams every 6 hours
The duration of therapy is arbitrary as there are no prospective studies on the optimal length of treatment.
Normalization of fever, resolution of leukocytosis, and return of sputum production to baseline suggest resolution of pneumonia.
Antibiotic courses of 7-10 days are often used for an uncomplicated pneumonia (no cavitation, abscess or empyema) that demonstrates prompt clinical improvement. Shorter courses of therapy are likely to be effective but have not been adequately studied.
Patients with antibiotic-resistant pathogens, multi-lobar disease, malnutrition or necrotizing infection are typically treated for 14 or more days.
Lung abscesses are often treated with IV therapy for 4-8 weeks followed by extended courses of oral therapy (up to 1 year). The decision to stop therapy is generally driven by radiographic findings. These patients are often treated until there is complete clearance of radiographic findings or only a small and stable residual lesion.
What do I do about particularly refractory cases
Ensure ongoing aspiration has been excluded.
Assess the adequacy of antibiotics, appropriateness of dosing, and patient compliance with therapy.
Search for infection-related complications such as metastatic abscess (including brain abscess), bronchopleural fistula with empyema, and secondary amyloidosis. Any associated pleural effusion should be sampled to exclude empyema.
Consider consultation from a pulmonologist (for bronchoscopic inspection, invasive cultures and possible biopsy), thoracic surgeon (chest tube drainage, decortication, surgical resection) or infectious disease specialist.
Persistent or enlarging abscess cavities may rarely require percutaneous drainage or surgical resection.
Similarly, life-threatening hemoptysis is a surgical emergency.
Institutionalized individuals with refractory, life-threatening infections who do not phonate may be candidates for laryngo-tracheal separation (the Lindeman procedure).
5. Disease monitoring, follow-up and disposition
Expected response to treatment
The time course for improvement is variable and appears to be directly related to the extent of infection, the causative pathogen(s) and the timeliness and adequacy of prescribed antibiotic therapy.
Case series suggest that fevers should resolve in 1-3 weeks.
It may take many months for abscess cavities to close.
Reported fatality rates are variable but generally low. The presence of necrotizing pneumonia is the exception, with mortality approaching 20%.
When should I suspect I've made the wrong diagnosis?
Persistent fever should prompt an evaluation for an alternate diagnosis and/or an aspiration pneumonia-related complication.
What follow-up should this patient receive?
Ongoing monitoring is generally targeted at assessment of clinical features of active infection.
Serial radiographs have limited value in aspiration pneumonia as radiographic findings typically lag clinical cure by weeks to months.
Patients with abscess require serial imaging as the ultimate duration of therapy is heavily influenced by resolution of the abscess cavity.
Aspiration is defined as entry of particulate or liquid matter below the level of the true vocal cords. Aspirated substances can be endogenous (oropharyngeal secretions, gastric juice) or exogenous (food, water).
There are two forms of aspiration syndrome: (1) large-volume aspiration, which is acutely symptomatic, and (2) chronic, small-volume aspiration with slowly progressive complaints.
The bulk of aspiration events cause chemical pneumonitis – not infection (pneumonia) – and are not discussed further. Note that indiscriminate use of antibiotics in aspiration pneumonitis selects resistant pathogens and predisposes to bacterial superinfection.
Aspiration causes direct loss of ciliated cells and non-ciliated cells. This injury takes up to a week for recovery and predisposes to establishment of active infection.
Aspirated gastric contents can also introduce viable endogenous flora into the lower airways.
Conditions that increase the volume of aspirated material and/or the bacterial burden of secretions in a person with impaired defenses promote aspiration pneumonia.
Widespread use of proton pump inhibitors (PPIs) – particularly common in the population at risk for aspiration – alters pH and increases the risk for colonization. These patients are more likely to have pathogens other than anaerobes identified.
It is increasingly clear that the majority of aspiration pneumonia cases are polymicrobial. In one classic series, patients averaged 3.2 isolates, of which 2.6 were anaerobes and 0.6 were non-anaerobes.
Early bacteriology studies routinely implicated anaerobic species (Bacteroides, Prevotella, Fusobacterium, Peptostreptococcus) in community-acquired aspiration pneumonia. Subsequent evaluations have suggested that admixed aerobic Gram negatives (particularly Pseudomonas aeruginosa, Klebsiella pneumoniaeand Escherichia coli) and Gram positives (particularly Staphylococcus aureus and Streptococcus pneumoniae) are increasingly important. Two more recent and rigorously designed trials using protected specimen brush samples and anaerobic culturing in patients with acute, witnessed aspiration failed to recover any anaerobes. These studies imply that anaerobes have a more limited role than traditionally believed.
Oral flora changes in institutionalized elderly (attributable to poor oral hygiene and malnutrition) promote colonization with anaerobic and aerobic Gram-negative organisms. A study using bronchial sampling in cases of severe aspiration pneumonia in this population suggested that ~50% had Gram-negative bacilli, with anaerobic bacteria in only ~15%.
Prior antibiotic exposure is also relevant, as nearly half of culture-positive pneumonia patients who had received a single dose of antibiotics before microbiological sampling had Pseudomonas aeruginosa, Staphylococcus aureus and/or Gram-negative bacilli as causative pathogens.
Anaerobic pathogens are particularly prone to induce a fibrosing response, which limits extension of the infectious process. This confines the infection to a single lung segment and leads to abscess formation.
The true incidence of aspiration pneumonia is unknown but generally accepted as low (5-15% of all community-acquired pneumonia cases). The variability in reported rates in the literature stems from a lack of standardized diagnostic criteria, inherent difficulties in diagnosis, and inability to distinguish pneumonitis from pneumonia.
Medicare data suggest a cost of $10,000-$12,000 per case.
Aspiration pneumonia is seen with increased frequency in elderly patients, particularly residents of nursing homes. One study of cases with nursing home-acquired pneumonia and controls with community-acquired pneumonia suggested the prevalence of aspiration pneumonia was 18% in nursing home residents compared to 5% in CAP patients. A more recent study with similar design suggested that aspiration pneumonia represented 30% of all nursing home-acquired pneumonia cases, whereas it is 10% of true CAP.
Incidence has been reported in 10% of patients admitted to the hospital with drug overdose and in 0.003% of surgical cases where general anesthesia is administered.
Risk factors for aspiration and aspiration pneumonia include advanced age, neurologic disorders (stroke, dementia), altered level of consciousness (coma, seizure, alcohol or sedative/hypnotic use), neuromuscular disease, functional dependence with activities of daily living, and various gastrointestinal conditions (gastroesophageal reflux, esophageal dysmotility, swallowing disorder, delayed gastric emptying).
Obesity is increasingly recognized as a risk factor given increased intra-abdominal pressures, high residual gastric volumes, low pH, delayed gastric emptying and increased rates of reflux.
Periodontal disease is also a major risk factor for development of anaerobic pleuropulmonary infections. Bacterial counts in gingival crevices are markedly elevated in patients with a variety of periodontal diseases, and the risk of aspiration pneumonia is lower in edentulous patients.
Pulmonary aspiration and its infectious complications are important causes of serious illness and death in hospitalized patients and in residents of chronic care facilities.
Reported mortality rates are 19.4% for community-acquired aspiration pneumonia and 28.4% for nursing-home-acquired aspiration pneumonia.
Prognosis is heavily determined by underlying comorbid disease, complications of infection, and the overall functional status of the host.
Some populations are particularly at risk for poor outcomes. For example, aspiration pneumonia is the most common cause of death in patients with dysphagia due to neurologic disorders.
Special considerations for nursing and allied health professionals.
What's the evidence?
Bartlett, JG. "Diagnostic accuracy of transtracheal aspiration bacteriologic studies". Am Rev Respir Dis. vol. 115. 1977. pp. 777-82.(A critical evaluation of the utility - and limitations - of transtracheal aspiration to obtain microbiologic samples.)
Henriquez, AH, Mendozza, J, Gonzalez, PC. "Quantitative culture of bronchoalveolar lavage from patients with anaerobic lung abscesses". J Infect Dis. vol. 164. 1991. pp. 414-7.
Huxley, E, Viroslav, J, Gray, W. "Pharyngeal aspiration in normal adults and patients with depressed consciousness". Am J Med. vol. 64. 1978. pp. 564-8.An older – but critically important – study that reminds us that not all aspiration is clinically relevant.
Wimberley, NW, Bass, JB, Boyd, BW. "Use of a bronchoscopic protected catheter brush for the diagnosis of pulmonary infections". Chest. vol. 81. 1982. pp. 556-62.
El Sohl, AA, Saliba, R. "Pharmacologic prevention of aspiration pneumonia: a systematic review". Am J Geriatr Pharmacother. vol. 5. 2001. pp. 352-62.(A systematic review of various strategies available to minimize aspiration.)
Finegold, SM. "Increasing resistance in anaerobes". Infect Surg. vol. 3. 1984. pp. 332-8.(Description of the increasing relevance of antimicrobial resistance among anaerobic pathogens.)
Gudiol, F, Manressa, F, Pallares, R. "Clindamycin vs. penicillin for anaerobic lung infections. High rate of penicillin failures associated with penicillin-resistant Bacteroides malaninogenicus". Arch Intern Med. vol. 150. 1990. pp. 2525-9.(Relatively uncommon head-to-head study that delineated the increasingly limited role of penicillin in anaerobic infections.)
Loeb, MB, Becker, M, Eady, A, Walker-Dilks, C. "Interventions to prevent aspiration pneumonia in older adults: a systematic review". J Am Geriatr Soc. vol. 51. 2003. pp. 1018-22.(A systematic review of various strategies used to minimize aspiration.)
Marek, PE. "Aspiration pneumonitis and aspiration pneumonia". N Engl J Med. vol. 344. 2001. pp. 665-71.(A thorough review of the interrelated consequences of aspiration events.)
Mier, L, Dreyfuss, D, Darchy, B. "Is penicillin G an adequate initial treatment for aspiration pneumonia? A prospective evaluation using a protected specimen brush and quantitative cultures". Intensive Care Med. vol. 19. 1993. pp. 279-84.(Microbiologically rigorous study that further highlights the limitations of penicillin therapy for anaerobic infections.)
Baine, WB, Yu, W, Summe, JP. "Epidemiologic trends in the hospitalization of elderly Medicare patients for pneumonia 1991-1998". Am J Public Health . vol. 91. 2001. pp. 1121-3.(An analysis of composite Medicare data to delineate epidemiologic trends and attributable costs of aspiration pneumonia.)
Bartlett, J, Gorbach, S, Finegold, S. "The bacteriology of aspiration pneumonia". Am J Med. vol. 56. 1974. pp. 202-7.(Sentinel work illustrating the importance of anaerobic pathogens in the pathophysiology of pleuropulmonary disease after aspiration.)
Bartlett, J, Gorbach, S, Tally, F. "Bacteriology and treatment of primary lung abscess". Am Rev Respir Dis. vol. 109. 1974. pp. 510-8.(Original work outlining pathogens – including anaerobes – specifically in lung abscess.)
Bartlett, JG, Finegold, SM. "Anaerobic infections of the lung and pleural space". Am Rev Respir Dis. vol. 110. 1980. pp. 56-74.(Large case series delineating the prevalence of anaerobes in aspiration pneumonia.)
Bartlett, JG. "Anaerobic infections of the lung". Chest. vol. 91. 1987. pp. 6901-9.(Observational data describing changes in the prevalence of anaerobic pathogens in aspiration pneumonia.)
El-Solh, AA, Pietrantoni, C, Bhat, A. "Microbiology of severe aspiration pneumonia in institutionalized elderly". Am J Resp Crit Care Med. vol. 167. 2003. pp. 1650-5.(Rigorous evaluation of the microbiology of aspiration pneumonia in a select population of patients.)
Kollef, MH, Fraser, VJ. "Antibiotic resistance in the intensive care unit". Ann Intern Med. vol. 134. 2001. pp. 298-314.(Prospective data demonstrating that unnecessary antibiotic therapy for aspiration pneumonitis leads to resistance and superinfections.)
Sanduleanu, S, Jonkers, D, De Bruine, A, Hameeteman, W, Stockbrügger, RW. "Non-Helicobacter pylori bacterial flora during acid-suppressive therapy: differential findings in gastric juice and gastric mucosa". Aliment Pharmacol Ther. vol. 15. 2001. pp. 379-88.(This report is a rigorous illustration of the effects of altered pH on gastric colonization with pathogens.)
Shariatzadeh, MR, Huang, JQ, Marrie, TJ. "Differences in the features of aspiration pneumonia according to site of acquisition: community or continuing care facility". J Am Geriatr Soc. vol. 54. 2006. pp. 296-302.(This is a prospective population-based study on the prevalence and risk factors of aspiration pneumonia from community and long-term care facilities.)
Vaughan, RW, Bauer, S, Wise, L. "Volume and pH of gastric juice in obese patients". Anesthesiology. vol. 43. 1975. pp. 686-9.(This classic study is of increasing relevance given recent trends in the fitness of the U.S. population.)
Beck-Sague, C, Villarino, E, Giuliano, D. "Infectious diseases and death among nursing home residents: results of surveillance in 13 nursing homes". Infect Control Hosp Epidemiol. vol. 15. 1994. pp. 494-6.(This prospective surveillance study of 1,754 nursing home residents identified pneumonia as a major cause of morbidity. Pneumonia was the only infection specifically associated with increased mortality in this population.)
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