American Journal of Respiratory and Critical Care Medicine

We sought to investigate prospectively the microbial etiology and prognostic indicators of 95 institutionalized elders with severe aspiration pneumonia, and to investigate its relation to oral hygiene in using quantitative bronchial sampling. Data collection included demographic information, Activity of Daily Living, Plaque Index, antimicrobial therapy, and outcome. Out of the 67 pathogens identified, Gram-negative enteric bacilli were the predominant organisms isolated (49%), followed by anaerobic bacteria (16%), and Staphylococcus aureus (12%). The most commonly encountered anaerobes were Prevotella and Fusobacterium species. Aerobic Gram-negative bacilli were recovered in conjunction with 55% of anaerobic isolates. The Plaque Index did not differ significantly between the aerobic (2.2 ± 0.4) and the anaerobic group (2.3 ± 0.3). Functional status was the only determinant of the presence of anaerobic bacteria. Although seven cases with anaerobic isolates received initially inadequate antimicrobial therapy, six had effective clinical response. The crude mortality was 33% for the aerobic and 36% for the anaerobic group (p = 0.9). Stepwise multivariate analysis identified hypoalbuminemia (p < 0.001) and the burden of comorbid diseases (p < 0.001) as independent risk factors of poor outcome. In view of the rising resistance to antimicrobial agents, the importance of adding anaerobic coverage for aspiration pneumonia in institutionalized elders needs to be reexamined.

Aspiration pneumonia has been reported to be the second most frequent principal diagnosis among hospitalizations of Medicare patients (1). The discharges of patients hospitalized for aspiration pneumonia has doubled over the period from 1991 to 1998, whereas the number of elderly Medicare beneficiaries has increased by only 11.1% (2). The yearly increases in the number of hospitalizations for aspiration pneumonia per 100,000 persons are mostly reported in the very old, and are expected to rise even more with the decades to come.

Risk factors for the development of aspiration pneumonia in older people are broadly classified into those that alter host defenses and others that increase exposure to bacteria. Impairment in clearance, weak cough, and difficulty managing oropharyngeal secretions are among the best predictors of aspiration in older adults (3). Interventions to improve mechanical airway clearance, implementation of infection control strategies, and innovative pharmacologic approaches have shown promise in reducing aspiration events, but their efficacy remains to be established in large randomized trials. The only proven antimicrobial therapy rests largely on earlier studies from the 1970s, when transtracheal aspirates were used for collection of respiratory secretions. The preponderance of anaerobic bacteria in these aspirates led to the widespread practice of using antibiotic treatment with anaerobic coverage for all suspected aspiration. Only recently did the risk of such a strategy become apparent (4).

The Infectious Diseases Society of America and the recent American Thoracic Society guidelines have recommended anaerobic coverage for patients with pneumonia with poor dentition who are at risk for aspiration, or those living in a nursing home (5, 6). These recommendations were based on observational studies and case series, and were not to our knowledge validated prospectively. Moreover, these guidelines did not address the clinical and therapeutic aspects of aspiration pneumonia requiring intensive care due to the paucity of information about the precise microbial etiology and prognostic factors affecting patients with aspiration pneumonia. Previous studies of severe pneumonia have either excluded aspiration pneumonia or have not clearly defined it (7, 8). In others, the diagnosis of aspiration pneumonia was invoked at a late stage of the disease, when necrotizing pneumonia or lung abscess has developed (9, 10). This study was designed to determine the association between oral hygiene, etiology, and prognostic factors influencing mortality of institutionalized elders with aspiration pneumonia.

Study Population

We studied prospectively all patients resident of long-term care facilities, aged 65 years and older, admitted from the emergency department to our intensive care unit between January 2000 and October 2002 with suspected severe pneumonia. The study was approved by the Institutional Review Board of the University at Buffalo. An informed consent was obtained from all participants or their health care proxy.

The inclusion criteria for severe aspiration pneumonia included: (1) the development of new radiographic infiltrate compatible with pneumonia; (2) the presence of symptoms or signs suggestive of lower respiratory tract infection (one major criteria of either cough, sputum production, or fever above 38°C or below 35.5°C, plus two minor criteria of pleuritic chest pain, dyspnea, delirium, increased alveolar arterial gradient, or white blood cell count > 12,000/mm3, and/or left shift or leukopenia < 3,000/mm3) necessitating mechanical ventilation; and (3) the presence of risk factors for oropharyngeal aspiration (documented swallowing abnormality secondary to neurologic dysphagia, disruption of the gastroesophageal junction, or anatomic abnormalities of the upper aerodigestive tract) (11). Patients with severe immunosuppression (solid organ transplantation, steroid therapy of 20 mg/day or more for more than 2 weeks, known HIV, or AIDS-defining criteria), or who had received antimicrobial therapy or were hospitalized within the last 30 days were excluded.

Data Collection

Demographic data collected included age, sex, Activity of Daily Living score (12), comorbid illnesses, the Charlson Index (13), and prior antimicrobial therapy. In addition, the following parameters were recorded at the time of enrollment: clinical symptoms, vital signs, laboratory and radiographic data, the Acute Physiology and Chronic Health Evaluation (APACHE II) score (14), and antibiotic coverage after the initial sampling was performed. Oral examination included the Plaque Index (15) and enumeration of the number of remaining teeth. In addition, the following parameters were recorded during the patients' daily follow up: vital signs, radiographic progression, and organ failure. At the clinical endpoints of hospital discharge or death, the length of mechanical ventilation and ICU stay were recorded.

Microbiology

Two serial blood cultures were performed in all patients at the time of enrollment. Urinary samples were assayed for Legionella pneumophila and pneumococcus antigens. Respiratory samples were obtained within the first 4 hours of presentation to the emergency department via protected bronchoalveolar lavage and processed as previously reported (16, 17).

Definitions

Septic shock was defined according to Bone and colleagues (18). The etiology of pneumonia was considered verified if one of the following criteria is met: (1) positive urinary antigen for Legionella or pneumococcus; (2) bacterial growth in protected bronchoalveolar lavage ⩾ 103 cfu/ml; or (3) positive respiratory assay for influenza A and B antigens. According to bacteriologic results, three groups were identified: an aerobic group corresponding to patients with pneumonia attributed to aerobic microorganisms, an anaerobic group involving patients with pneumonia who had a protected bronchoalveolar lavage specimen containing at least one anaerobic microorganism, and a group of patients with unverified pneumonia in whom the diagnostic workup did not reveal the presence of a microbial pathogen.

Antimicrobial therapy was considered adequate if the causative pathogen(s) was/were susceptible to the prescribed antibiotic(s) therapy on enrollment. The initial therapy was considered effective if the clinical situation remained stable, fever decreased, and leukocytosis improved after 72 hours of treatment. In all other cases, the initial therapy was considered a failure.

Statistics

Data were analyzed using the NCSS 2000 statistical software (NCSS Statistical Analysis System, Kaysville, UT). Results were expressed as means ± SD. Among patients with verified pneumonia, aerobic and anaerobic groups were compared at baseline for epidemiologic and clinical data. Continuous variables were compared using Student's t test for normally distributed variables and the Mann-Whitney test for non-normally distributed variables. Proportions were compared using the chi-square test with Yates correction or Fisher's exact test when necessary. In the same way, such data were compared between patients exhibiting verified and unverified pneumonia. A stepwise logistic regression was performed using those variables found significant in univariate analysis with in-hospital mortality as the dependent variable. All reported p values are two-tailed. The level of significance was set at 5%.

Patient Characteristics

During the study period, a total of 138 patients were eligible for enrollment. Forty-three patients could not be enrolled because of the lack of informed consent. Out of the 95 who underwent bronchial samplings, 54 participants had at least one microorganism isolated. Anaerobic bacteria were recovered from 11 (20%) of the 54 subjects. Characteristics of the study population are shown in Table 1

TABLE 1. Demographic and clinical characteristics of the study population




Aerobic
 (n = 43)

Anaerobic
 (n = 11)

Unverified
 (n = 41)
Age, mean ± SD80.2 ± 6.577.1 ± 6.180.6 ± 5.2
Sex (M/F), n26/434/1119/41
Clinical presentation
Cough13 (30)2 (18)5 (12)
Fever29 (67)7 (63)33 (80)
Dyspnea37 (86)10 (91)36 (88)
Delirium20 (47)7 (64)18 (44)
Comorbidities
Cardiac23 (53)6 (55)17 (41)
Pulmonary14 (33)4 (36)18 (44)
Renal7 (16)2 (18)5 (12)
Hepatic cirrhosis1 (2)0 1 (2)
Central nervous system36 (84)8 (73)32 (78)
Diabetes Mellitus8 (19)4 (36)5 (12)
Neoplastic
2 (5)
0
2 (5)
. All 95 participants had at least one comorbid illness, with 87% having two or more comorbidities. Stroke (78%) was the most prevalent comorbidity, followed by ischemic heart disease (51%) and chronic obstructive pulmonary disease (35%). The majority of patients presented with dyspnea, fever, and delirium. On physical examination, crepitations were the main auscultatory findings (n = 62), followed by rhonchi (n = 23) and wheezing (n = 5). A “silent” chest was present only in five subjects (5%).

Clinical and radiographic presentations are summarized in Table 2

TABLE 2. Clinical and radiographic presentation




Aerobic (n = 43)

Anaerobic (n = 11)

Unverified (n = 41)
APACHE II score20.5 ± 6.521.8 ± 5.121.5 ± 6.1
PaO2/FIO2, mmHg284.0 ± 47.5270.3 ± 49.2254.2 ± 18.6
Shock8 (19)2 (18)8 (20)
Oral examination
Number of teeth, mean ± SD13.2 ± 8.214.1 ± 7.917.4 ± 8.6
Number of teeth, range0–260–230–28
Edentulous18 (42)3 (27)11 (27)
Plaque Index, mean ± SD2.2 ± 0.42.3 ± 0.32.3 ± 0.6
Radiographic patterns, n (%)
Multilobar12 (28)4 (36)19 (46)
Bilateral10 (23)2 (18)16 (39)
Pleural effusion1 (2)0 4 (10)
Progression of infiltrate in the first 48 hours
14 (33)
4 (36)
17 (41)
. The severity of illness and the degree of hypoxemia were not significantly different between those with aerobic and anaerobic bacteria, or between those with verified and those with unverified pneumonia. Similarly, the distribution of radiographic infiltrates was similar among the groups identified. The involvement of the right lower lobe was no more frequent in the anaerobic group than in the aerobic one. No patient with an anaerobic strain had necrotizing pneumonia with an abscess formation or empyema. A computed tomography of the chest was performed on 18 of the 95 subjects. None showed evidence of lymphadenopathy or cavitation.

The mean number of teeth present and the Plaque Index were comparable across the various groups (Table 2). The percentage of patients who were edentates was more frequent, however, in those with aerobic compared with anaerobic isolates, although the difference did not attain statistical significance (18 of 43 versus 3 of 11; p = 0.5). Seven of those 18 edentates with aerobic bacteria had dentures, compared with 2 of 3 with anaerobic strains, and 7 of the 11 with unverified pneumonia.

Microbial Etiology

Positive blood cultures were positive in three (3%) patients, and consisted of Staphylococcus aureus, Klebsiella pneumoniae, and Streptococcus pneumoniae. No anaerobic bacterium was isolated from blood cultures. Thoracocentesis was performed in six cases. In all six instances, the fluid analysis revealed an exudative effusion suggestive of parapneumonic process; however, no bacterial pathogen (whether aerobic or anaerobic) was recovered from cultures of the pleural fluid.

Overall, 67 pathogens were isolated from bronchial samplings (Table 3)

TABLE 3. Microbial etiology of pulmonary aspiration




Aerobic Group
 (n = 43)

Anaerobic Group
 (n = 11)
Gram-positive aerobic cocci
Streptococcus pneumoniae5
Streptococcus spp.6
Staphylococcus aureus8
Gram-negative aerobic bacilli
Haemophilus influenzae2
Escherichia coli112
Klebsiella pneumoniae82
Serratia spp.71
Proteus mirabilis61
Enterobacter cloacae1
Pseudomonas aeruginosa2
Anaerobic
Prevotella spp.6
Fusobacterium spp.3
Bacteroides spp.1
Peptostreptococcus spp.

1
; 42 had one pathogen, 11 had two, and 1 had three pathogens. Gram-negative enteric bacilli were the predominant organisms isolated (49%), followed by anaerobic bacteria (16%) and S. aureus (12%). The majority of S. aureus (six of eight) was methicillin-sensitive. Atypical infections were identified in none of the participants. Table 4

TABLE 4. Antimicrobial susceptibility of anaerobic isolates




Penicillin

Metronidazole

Clindamycin
Prevotella, S/R4/25/16/0
Fusobacterium, S/R3/03/03/0
Peptostreptococcus, S/R1/01/01/0
Bacteroides, S/R
0/1
1/0
1/0

Definition of abbreviation: S/R = Sensitive/resistant.

depicts the antimicrobial susceptibility patterns of anaerobic isolates. Resistance to penicillin was detected in 27%. One isolate of Prevotella spp. was resistant to both penicillin and metronidazole.

Compared with the aerobic group, the burden of comorbidities was not found to be a determinant for the isolation of anaerobic bacteria (the median Charlson Index for aerobic and anaerobic infection was 3 and 3, respectively; p = 1.0). Similarly, the presence of percutaneous gastrotomy tube or prior pneumonia episodes was not indicative of an anaerobic aspiration. However, anaerobic pathogens were more likely to be recovered from patients with impaired functional status (p < 0.04) (Figure 1)

.

Polymicrobial infection was present in 12 (22%) of the 54 patients in whom a microbial etiology was determined (Table 5)

TABLE 5. Etiology of polymicrobial cases




n
Double infection
S. pneumoniae + E. coli1
S. aureus + Proteus spp.1
Streptococcus spp. + Serratia spp.2
Streptococcus spp+ E. coli1
Peptostreptococcus spp. + Serratia spp.1
Prevotella spp. + E. coli1
Prevotella spp. + Serratia spp.1
Bacteroides spp. + Proteus spp.1
Fusobacterium spp + E. coli1
Fusobacterium spp. + K. pneumoniae1
Triple infection
   S. aureus + K. pneumoniae + E. cloacae
1
. Aerobic Gram-negative bacteria were associated with six anaerobic isolates. No clinical or radiographic patterns characterized mixed anaerobic from mixed aerobic cases.

Antimicrobial Therapy

In patients with verified pneumonia, initial empiric antimicrobial treatment consisted of either monotherapy (n = 22) or dual combination (n = 32). As a single agent, the administered drugs were levofloxacin (n = 10), ampicillin/sulbactam (n = 6), piperacillin/tazobactam (n = 5), and carbapenem (n = 1). The main drugs prescribed in combination included ceftriaxone plus azithromycin (n = 11), ampicillin/sulbactam plus azithromycin (n = 6), levofloxacin plus clindamycin or metronidazole (n = 5), piperacillin/tazobactam plus levofloxacin or azithromycin (n = 3), and vancomycin plus ciprofloxacin (n = 2). The initial antimicrobial coverage of anaerobic isolates is shown in Table 6

TABLE 6. Initial antimicrobial coverage of anaerobic isolates


Organisms

Antimicrobial Therapy
Prevotella spp.Ampicillin/sulbactam + azythromycin
Prevotella spp.Ceftriaxone + azythromycin*
Prevotella spp.Levofloxacin*
Prevotella spp.Levofloxacin + clindamycin
Prevotella spp. + E. coliCeftriaxone + azythromycin*
Prevotella spp. + Serratia spp.Levofloxacin + metronidazole
Fusobacterium spp.Ceftriaxone + azythromycin*
Fusobacterium spp + E. coliLevofloxacin*
Fusobacterium spp. + K. pneumoniaeAmpicillin/sulbactam + azythromycin*
Bacteroides spp. + Proteus spp.Ceftriaxone + azythromycin*
Peptostreptococcus spp. + Serratia spp.
Levofloxacin + metronidazole

*Inadequate initial antimicrobial therapy.

. Thirty-nine of the 43 patients with aerobic isolates received adequate antimicrobial therapy, compared with 4 of the 11 with anaerobic species (p < 0.001). Only one of the aerobic cases who received inadequate therapy had effective initial therapy. Vancomycin was added in two cases because of methicillin-resistant S. aureus infection, and one had a change of antimicrobial therapy to cover for Pseudomonas aeruginosa. In contrast, the initial therapy was considered effective in six of the seven anaerobic cases with inadequate anaerobic antimicrobial coverage. The only case identified as showing signs of ineffective therapy had an ampicillin-resistant K. pneumoniae isolated along with Fusobacterium spp. Imipenem was substituted for the initial antimicrobial regimen.

Outcome and Prognostic Factors

When adjusted for severity of illness and underlying comorbidities, there was no significant difference in the length of mechanical ventilation or ICU stay between the aerobic and the anaerobic group (6.3 ± 3.4 days and 9.5 ± 4.4 days for the aerobic group versus 7.6 ± 4.3 and 10.9 ± 4.5 for the anaerobic group, p = 0.7 and p = 0.6; respectively). Compared with patients with verified pneumonia, those with unverified pneumonia were ventilated for longer period of time (8.6 ± 4.8 versus 6.5 ± 3.6; p = 0.01) and had a prolonged ICU stay (11.7 ± 5.1 versus 9.8 ± 4.4; p = 0.06). Fourteen patients had a “do not resuscitate” order written on admission. Overall, 35 patients died during their hospitalization (14 in the aerobic group, 4 in the anaerobic group, and 17 of those with unverified pneumonia). The cause of mortality was attributed to progressive pneumonia in 24 patients and multiorgan failure in 11. Survivors were less likely to be functionally impaired (p = 0.01), nutritionally depleted (p < 0.001), or have significant comorbidities (p = 0.002). By multivariate analysis, only the Charlson Index (β coefficient 0.92 ± 0.22; p < 0.001) and serum albumin (β coefficient 2.22 ± 0.5; p < 0.001) were found to be independently associated with poor outcome.

The etiology of severe aspiration pneumonia in institutionalized elderly has rarely been well defined in prospective studies because this population has never been analyzed as an independent group. The present study establishes a rigorous and precise classification of the etiology of long-term care facility–acquired aspiration pneumonia so as to allow comparison with future studies. The comparison of current microbial patterns of patients with severe aspiration pneumonia with previous findings (8, 19) must, however, be interpreted with caution, because several diagnostic techniques were not applied in the latter series. These include either invasive bronchial samplings or anaerobic cultures.

In our study, Gram-negative enteric bacilli were by far the most common etiologic agents in nursing home–acquired aspiration pneumonia. These findings are consistent with Leroy and colleagues' investigation (19) of 116 patients who met the criteria for community-acquired aspiration pneumonia. Out of the 94 aerobic organisms isolated, Gram-negative enteric bacilli accounted for 27% of all isolates. However, the study lacked data about anaerobic causes of aspiration. Although an association of advanced age with Gram-negative pathogens has been postulated (20), the plausible mechanism remains the aspiration of endogenous flora.

The contribution of anaerobic bacteria to the pathogenesis of aspiration pneumonia continues to be the subject of debate because of the tedious and delicate techniques required for the transport media and culture of these organisms. For the purpose of this study, we have made every effort to hand-deliver all bronchial specimens within 30 minutes of sampling and maintain strict anaerobic transport media. In most of our cases, anaerobes were found in combination with enteric Gram negative bacilli. Bartlett and coworkers (9) found similar results with transtracheal aspirates in patients with suspected aspiration pneumonia. Whether the virulence of these microbes is enhanced by their coexistence with Gram-negative bacteria, or whether they are simple coinhabitants, remains to be determined. Nonetheless, the resolution of clinical signs of infection within 72 hours in those with anaerobic isolates despite initial inadequate antimicrobial coverage implies that anaerobic coverage may not always be necessary for cases of aspiration. Future clinical trials are needed to examine the utility of providing an anaerobic coverage to the standard antimicrobial regimens prescribed for patients with aspiration pneumonia.

The association between oral health and respiratory disease has been suggested by a number of recent microbiologic and epidemiologic studies (21, 22). Our study indicates a potential link between functional status and anaerobic pulmonary aspiration in the elderly. Many old institutionalized patients have deterioration in their activity of daily living, and it is quite plausible that poor oral health because of difficulty to access professional dental care and insufficient poor oral hygiene leads to colonization of dental plaques by these bacteria (23). Furthermore, neither nursing home staff nor physicians appear to give high priority to the resident's oral care (24). The lack of attention to oral hygiene results in an increase in the dental plaque, which may foster an environment that promotes colonization by anaerobic and Gram-negative organisms. Once aspirated, it is not uncommon for cultures of bronchial specimens to recover mixed aerobic and anaerobic bacteria. What remains unclear, however, are the underlying conditions that would predispose anaerobic bacteria to acquire virulence leading to necrotizing pneumonia and abscess formation.

Reported mortality from aspiration pneumonia has ranged from 0 to 85% (25). Our study demonstrates that mortality associated with aspiration pneumonia in the elderly is still high. One of the difficulties in comparing mortality between published studies is the variability of criteria used in establishing aspiration. The diagnosis is usually based on the presence of new radiographic infiltrates on chest X-ray, hypoxemia, or leukocytosis along with an underlying risk factor for aspiration such as altered mental status or drug overdose. In many patients, however, the episode of aspiration is not observed, and the presenting clinical symptoms are mere reflections of the pneumonic process.

Our results show that the burden of comorbidities and poor nutritional status are independent risk factors for poor outcome. Malnutrition has been correlated with increased incidence of sepsis, prolonged ventilator dependence (26), and increased mortality (27). Given that nutritional deficits have been reported in 35% of the elderly population (28), it is not surprising that nutritional modulation of immune function acting in concert with coexistent chronic diseases predispose for worse prognosis.

Potential limitations should be considered in interpreting the results of this study. The size of the study population is relatively small due to the strict inclusion criteria in defining aspiration pneumonia and due to the selective group of participants. The use of invasive bronchial sampling in our investigation, however, represents a more rigorous approach than previously published studies in this age group. The selection of 103 threshold may have underestimated the presence of anaerobic pathogens at the expense of aerobic Gram-negative bacteria. However, by lowering the threshold to 500 cfu/ml, we were not able to demonstrate any improved sensitivity of detecting anaerobic infection. Second, although there is no clinical gold standard to distinguish aspiration pneumonia from aspiration pneumonitis, we have adopted the definition proposed by Marik (11) because it represents the less imprecise definition available to study aspiration pneumonia. Third, it could be argued that a comparator group of community residents is needed to obtain a comprehensive understanding of the data presented. We have previously established that pneumonia of elders residing in a long term-care facility exhibits a different spectrum of microbial pathogens (29), thus making any comparison unsuited for the objectives delineated. Fourth, we could not rule out the possibility that the newer generation of antibiotics provides some anaerobic coverage, though inadequate by the current microbiological standards.

In summary, the results of our study suggest that although anaerobes represent a significant proportion of the oral flora, these commensals may have been overemphasized as pulmonary pathogens in aspiration pneumonia of elders residing in long-term care facilities. Instead, the bacteriology of aspiration pneumonia may represent the aerobic microorganisms that are likely to colonize dental plaques or oropharyngeal cavity at the time of aspiration.

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Correspondence and requests for reprints should be addressed to Ali El-Solh, M.D., M.P.H., Division of Pulmonary, Critical Care, and Sleep Medicine, Erie County Medical Center, 462 Grider Street, Buffalo, NY 14215. E-mail:

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