Liron Sinvani, MD

We read with interest the article by Maxwell and Mirza.¹ We appreciate using the large National Surgical Quality Improvement Project (NSQIP) database to assess comanagement outcomes, although we have concerns about the study design. Propensity score–matching (PSM) studies are limited; PSMs generate an average effect that neither establishes whether a treatment is optimal for a given patient nor control for unmeasured confounders.² Some baseline characteristics suggest that the comanaged and noncomanaged populations are quite different and, therefore, likely had unmeasured confounders that contributed to not detecting true effects. Also, as suggested by the authors, the NSQIP definitions of comanagement and standardized hip fracture program are broad. Recent studies in hip fracture comanagement attribute best outcomes to an organized program, shared decision making, expert comanagers, and each service having full responsibility including writing their own orders.^3-5 As no large database captures this distinction, it is not yet possible to perform a large, multicenter analysis. This type of comanagement cannot be studied in a randomized controlled trial. We recommend caution in overinterpreting the conclusions because there is substantial evidence in favor of optimized comanagement.

We read with interest the article by Maxwell and Mirza.¹ We appreciate using the large National Surgical Quality Improvement Project (NSQIP) database to assess comanagement outcomes, although we have concerns about the study design. Propensity score–matching (PSM) studies are limited; PSMs generate an average effect that neither establishes whether a treatment is optimal for a given patient nor control for unmeasured confounders.² Some baseline characteristics suggest that the comanaged and noncomanaged populations are quite different and, therefore, likely had unmeasured confounders that contributed to not detecting true effects. Also, as suggested by the authors, the NSQIP definitions of comanagement and standardized hip fracture program are broad. Recent studies in hip fracture comanagement attribute best outcomes to an organized program, shared decision making, expert comanagers, and each service having full responsibility including writing their own orders.^3-5 As no large database captures this distinction, it is not yet possible to perform a large, multicenter analysis. This type of comanagement cannot be studied in a randomized controlled trial. We recommend caution in overinterpreting the conclusions because there is substantial evidence in favor of optimized comanagement.

We read with interest the article by Maxwell and Mirza.¹ We appreciate using the large National Surgical Quality Improvement Project (NSQIP) database to assess comanagement outcomes, although we have concerns about the study design. Propensity score–matching (PSM) studies are limited; PSMs generate an average effect that neither establishes whether a treatment is optimal for a given patient nor control for unmeasured confounders.² Some baseline characteristics suggest that the comanaged and noncomanaged populations are quite different and, therefore, likely had unmeasured confounders that contributed to not detecting true effects. Also, as suggested by the authors, the NSQIP definitions of comanagement and standardized hip fracture program are broad. Recent studies in hip fracture comanagement attribute best outcomes to an organized program, shared decision making, expert comanagers, and each service having full responsibility including writing their own orders.^3-5 As no large database captures this distinction, it is not yet possible to perform a large, multicenter analysis. This type of comanagement cannot be studied in a randomized controlled trial. We recommend caution in overinterpreting the conclusions because there is substantial evidence in favor of optimized comanagement.

Aspiration pneumonia refers to an infection of the lung parenchyma in an individual who has inhaled a bolus of endogenous flora that overwhelms the natural defenses of the respiratory system. It primarily affects older adults with almost 80% of cases occurring in those 65 years and older.¹ Compared with nonaspiration pneumonia, aspiration pneumonia (whether community acquired or healthcare associated) results in more ICU stays, mechanical ventilation, increased length of hospital stay, and higher mortality.²

The etiology of aspiration pneumonia comes from aspirated bacteria from the oropharynx or stomach.³ However, aspiration alone is a common occurrence and does not always lead to clinical pneumonia. Indeed, one study demonstrated that 45% of “normal subjects” aspirate in their sleep,⁴ illustrating that our bodies have evolved defense mechanisms to protect us from aspirated bacteria. Thus, it is only when these systems are overwhelmed, after compromise of both glottic closure and the cough reflex in addition to dysphagia,³ that an infection manifests.

Aspiration pneumonitis refers to a significant inflammation of the lung parenchyma that results from inhalation of regurgitated gastric contents.⁵ It can produce fever, cough, wheezing, shortness of breath, hypoxemia, leukocytosis, and a pulmonary infiltrate as well as lead to severe acute respiratory distress syndrome and even death. In the past, the use of antibiotics shortly after aspiration in patients who develop a fever, leukocytosis, or a pulmonary infiltrate was discouraged.⁵ Empiric antibiotics were recommended only for patients who aspirate gastric contents and who have conditions associated with colonization of gastric contents, such as small-bowel obstruction.⁵ Yet, it is difficult to distinguish aspiration pneumonitis from pneumonia⁶ and there are no randomized trials in older adults to help guide their management.

Pneumonia in older adults can present in an atypical fashion. In one study of community-acquired pneumonia (CAP), the combination of cough, fever, and dyspnea is present in only 31% of patients, although separately, they are present in 67%, 64%, and 71% of patients, respectively. The same study also showed that delirium was present in 45% of patients with CAP.⁷ Nonrespiratory symptoms were present during the initial presentation of CAP in 55% of patients, with confusion in 42%, and falls in 16% of cases.⁸ The same is true of aspiration pneumonia where altered mental status is seen in approximately 30% of community-acquired aspiration pneumonia (CAAP) patients and in 19% of continuing care facility patients with aspiration pneumonia.² Another study that compared CAP, CAAP, and healthcare-associated aspiration pneumonia (HCAAP) showed that confusion is present in 5.1%, 12.7%, and 18.6%, respectively.⁹ The absence of fever in older adults is shown in studies where fever, defined as greater than or equal to 37.5°C, is absent in 32% of the very old¹⁰and in 40% of patients 65 years or older when it was defined as greater than 37°C.⁸ The inconsistencies regarding typical symptoms of pneumonia in the older adult population are also confirmed in nursing home residents.¹¹ Ultimately, it is important to remember that any infection in older adults, especially in those residing in long-term care facilities, may present with subtle findings such as an acute change in cognitive and functional status.¹²

Risk Factors for Aspiration Pneumonia

Risk factors for aspiration pneumonia, while not universally agreed upon, are important to recognize as they increase the probability of the diagnosis when present. A 2011 systematic review identified age, male gender, lung disease, dysphagia, and diabetes mellitus (level 2a), as well as severe dementia, angiotensin I-converting enzyme deletion/deletion genotype, and poor oral health (level 2b) as risk factors.¹³ In 2016, a panel of experts reached a consensus (modified Delphi Method) on the following risk factors for the diagnosis of aspiration pneumonia in nursing home residents: history of dysphagia, choking incident, tube feeding, neurologic disease, and cognitive impairment. The presence of one or more of these risk factors in the appropriate clinical setting may suggest a diagnosis of aspiration pneumonia.¹⁴

Radiographic/Ultrasonographic Imaging

In the appropriate scenario, the diagnosis of aspiration pneumonia is supported with an image representative of pneumonia. The pulmonary segment involved in aspiration pneumonia depends on the position of the patient during the aspiration event. If the aspiration event occurs while the patient is in the recumbent position, development of pneumonia is more common in the posterior segments of the upper lobes and the apical segments of the lower lobes; whereas if it occurs while the patient is in an upright position, the location changes to the basal segments of the lower lobes.³

Overall, the sensitivity of a chest X-ray to diagnose pneumonia ranges between 32%-77.7%,^15-17 suggesting that a significant proportion of patients suspected of having pneumonia in past research studies, may have been misdiagnosed. Studies using lung ultrasound to identify pneumonia demonstrate a higher sensitivity, but additional research is needed to validate these findings.^17-19 Noncontrast CT scans of the chest remain the reference standard for diagnosing pneumonia and currently tend to have the largest impact on diagnosis and subsequent treatment decisions.^15,16,20,21 As a result, if radiation exposure risks are not a concern for the patient, we recommend utilizing noncontrast CT imaging whenever the diagnosis is in doubt until future research elucidates the most appropriate approach to imaging.

Diagnosis

Diagnosing aspiration pneumonia is difficult, in part because there is no universal definition or set of diagnostic criteria. The diagnosis of aspiration pneumonia is supported by the fulfillment of three criteria. First, appropriate risk factors for aspiration, as documented above, should be present. Second, there should be evidence of clinical signs and symptoms of pneumonia (typical or atypical). Third, radiographic representation of pneumonia in a dependent pulmonary segment confirms the diagnosis. Once these criteria are met, it is important to distinguish between CAAP and HCAAP with particular attention to risk factors for multidrug-resistant (MDR) organisms and Pseudomonas aeruginosa (PA).

Many studies have tried to determine the exact bacterial etiology of aspiration pneumonia as documented in the Table.

Even when an ideal method is used to obtain a good sample, however, the results are limited by other variables in the study. For example, in studies that use protected brush specimens and protected bronchoalveolar lavage to acquire samples for culture, many patients received antibiotics prior to sampling, and the studies are small (Table). Although anaerobes have traditionally been implicated in aspiration pneumonia, only El-Solh et al.²² were able to culture a significant proportion of anaerobes. The study, however, was limited to institutionalized older adults requiring mechanical ventilation and it did not require the typical radiographic location for aspiration pneumonia. Even under the best circumstances, it is difficult to determine causality because the antibiotics used to treat these cases of aspiration pneumonia cover a broad range of organisms. Based on the studies in the Table, causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods in addition to traditional organisms classically thought to cause aspiration pneumonia-anaerobes. Microbiologic etiology, however, may also be insinuated from the studies discussed in the therapeutic strategies section below as some include antibiotics with limited antimicrobial activity.

Therapeutic Strategies

The management of aspiration pneumonia has evolved significantly since it was first studied in the 1970s because of the development of antibiotic resistance patterns, newer antibiotics, and increasing information on the diversity of pathogens involved in each subset of aspiration syndromes. The antimicrobial treatment of aspiration pneumonia was classically directed against anaerobic pathogens; treatment of these infections, however, was extrapolated from studies of pulmonary abscesses and other anaerobic pulmonary infections.

A randomized controlled trial in the mid-1980s comparing penicillin and clindamycin demonstrated a significantly improved cure rate in the clindamycin group.²³ A follow-up study in 1990 implicated a significant number of penicillin-resistant Bacteroides infections—the majority of these infections were subsequently reclassified as Prevotella melaninogenica—as the cause for high rates of penicillin resistance in lung abscesses and necrotizing pneumonias, further supporting clindamycin as the treatment of choice for these infections.²⁴ Amoxicillin-clavulanic acid (IV and PO regimens), studied in the treatment of community-acquired necrotizing pneumonia/lung abscess, shows good efficacy as well.²⁵ This study also attempted to elucidate the underlying causative organisms in these patients. Organisms associated with CAP as well as anaerobic organisms were isolated, giving more credence to the idea of broader coverage for aspiration pneumonia.

Community-Acquired Aspiration Pneumonia/Healthcare-Associated Aspiration Pneumonia

The importance of making a diagnostic distinction between CAAP versus HCAAP is critical for management strategies. A prospective population-based study demonstrated that ICU length of stay and 30-day mortality is highest for HCAAP, followed by CAAP, and lastly for those with CAP.⁹ Although some studies use different nomenclature for identifying aspiration pneumonia patients at risk for a wider array of microorganisms, we attempt to standardize the language by using HCAAP. The literature on nonaspiration pneumonia is changing from terms such as CAP and healthcare-associated pneumonia (HCAP) to pneumonia with the risk of MDR organisms. One study proposed a new treatment algorithm for CAP based on the presence or absence of the following six risk factors: prior hospitalization of greater than or equal to two days in the preceding 90 days, immunosuppression, previous antibiotic use within the preceding 90 days, use of gastric acid-suppressive agents, tube feeding, and nonambulatory status.²⁶ A similar approach proposed years earlier for HCAP patients found the following to be risk factors for MDR organisms: hospitalization in the past 90 days, antibiotic therapy in the past six months, poor functional status as defined by activities of daily living score, and immune suppression.²⁷ Other factors, such as structural lung disease, that increase the risk of organisms resistant to standard antibiotic treatment regimens^28-31 should be considered in aspiration pneumonia as well. Aspiration pneumonia is following a similar trajectory where the risk of MDR organisms is taking precedence over the environment of acquisition. The final nomenclature will allow the healthcare provider to understand the organisms that need to be targeted when choosing an appropriate antibiotic treatment regimen.

There is evidence supporting the premise that CAAP and nursing home patients with no risk factors for MDR organisms can be treated with standard regimens used for patients with CAP. A prospective cohort study in 2014 did not show any statistically significant differences in clinical outcomes in nursing and healthcare-associated aspiration pneumonia patients (with no risks of MDR organisms) treated with azithromycin versus ampicillin/sulbactam. However, only 36 patients were included in the azithromycin arm, and the therapeutic choices were made by the treating physician.³²

A prospective study of 95 long-term care residents reported that of those patients admitted to the ICU with severe aspiration pneumonia, the causative organisms are gram-negative enteric bacilli in 49% of isolates, anaerobes in 16%, and Staphylococcus aureus in 12%.²² This study mentioned that six of seven anaerobic pneumonia cases had inadequate anaerobic coverage yet were effectively treated; based on the organisms represented, however, the antibiotics administered did provide some coverage.²² Prevotella was one of the common anaerobic organisms that could be treated by levofloxacin or ceftriaxone/azithromycin, possibly explaining the success of azithromycin in the study quoted previously.^22,32 Therefore, although anaerobic organisms still need to be considered, some may be treated by traditional CAP coverage.²²

In a 2005 randomized prospective study of 100 patients aged 71 to 94 years, clindamycin was found to have clinical efficacy equivalent to ampicillin-sulbactam and panipenem in the treatment of mild-to-moderate aspiration pneumonia.³³ Most patients in this study are nursing home residents, and 53% of sputum cultures in the clindamycin arm grew gram-negative rods. In contrast to the previous study, the significance of gram-negative rod infections in this population of patients, with less severe infections, is called into question, as clindamycin has no coverage against these organisms. This premise is supported by a more recent study using azithromycin in nursing and healthcare-associated aspiration pneumonia patients, mentioned previously.³² Taken together, these three studies suggest that the severity of aspiration pneumonia may be a risk factor that needs to be taken into account when considering broad-spectrum antimicrobial coverage.

While further research is needed to validate treatment approaches, based on the current literature we propose the following:

CAAP requiring hospitalization but without any of the following-risk for PA or MDR organisms, septic shock, the need for ICU admission, or mechanical ventilation-can be treated with standard CAP therapy that covers anaerobes.^26,32-34 Patients with CAAP and either of the following—risk factors for MDR organisms, septic shock, need for ICU admission, or mechanical ventilation—should be considered for broader coverage with vancomycin or linezolid, antipseudomonal antibiotics, and anaerobic coverage. CAAP with specific risk for a PA infection should be considered for two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic, and one has anaerobic coverage).

Severe HCAAP without risk for MDR organisms or PA but with any of the following-septic shock, ICU admission, or mechanical ventilation-can be treated based on the 2016 Infectious Diseases Society of America guideline recommendation for hospital-acquired pneumonia, with a regimen that also provides adequate anaerobic coverage.³⁵ If patients have HCAAP with one or more risk factors for MDR organisms, no septic shock, and no need for ICU admission or mechanical ventilation, provide coverage with a similar regimen. In contrast, HCAAP with risk factors for PA or severe HCAAP causing septic shock, requiring ICU admission, or needing mechanical ventilation, which occurs in the setting of one or more risk factors for MDR organisms, or structural lung disease, should receive two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic and one has anaerobic coverage) in addition to vancomycin or linezolid.

A recent systematic review demonstrates the paucity of studies of ideal methodologic design which complicates the ability to recommend, with confidence, one guideline-based antimicrobial regimen over another.³⁶ Future studies may determine that despite the severity of the infection, if patients do not carry any risk for MDR pathogens or PA, they may only require CAAP coverage. When a patient presents with an acute infection, it is prudent to review previous cultures, and although it may be necessary to treat with broad-spectrum antibiotics initially, it is always important to narrow the spectrum based on reliable culture results. If future studies support the results of many studies cited in this article, we may be using fewer antibiotics with narrower spectrums in the near future.

Prevention

Although the healthcare system has practices in place to prevent aspiration pneumonia, the evidence supporting them are either inconclusive or not of ideal methodological design. Two systematic reviews failed to show statistically significant decreases in rates of aspiration pneumonia or mortality using the standard of care positioning strategies or thickened fluids in patients with chronic dysphagia.^37,38 One study showed a decreased incidence of all pneumonia in dysphasic patients with dementia or Parkinson disease when a chin-down posture (with thin liquids) or thickened fluids in a head-neutral position was used. The study, however, has significant limitations, including a lack of a “no treatment” group for comparison, which did not allow investigators to conclude that the decreased incidence was from their interventions.³⁹

There are preventive strategies that show a decreased risk of aspiration pneumonia. Poor oral hygiene seems to be a modifiable risk factor to establish better control of oral flora and decrease aspiration pneumonia. A systematic review of five studies, evaluating the effects of oral healthcare on the incidence of aspiration pneumonia in frail older people, found that tooth brushing after each meal along with cleaning dentures once a day and professional oral healthcare once a week decreases febrile days, pneumonia, and dying from pneumonia.⁴⁰A two-year historical cohort study using aromatherapy with black pepper oil, followed by application of capsaicin troches, and finally menthol gel, as the first meal, leads to a decreased incidence of pneumonia and febrile days in older adults with dysphagia.⁴¹ Well-designed validation studies may establish these practices as the new standard of care for preventing pneumonia in patients with dysphagia.

Feeding Tubes

Multiple studies show that in older adults with advanced dementia there is no survival benefit from percutaneous endoscopic gastrostomy (PEG) tube placement^42-44 and more recent systematic reviews also conclude that there is currently no evidence to support the use of PEG tubes in this specific population.^45,46 In February 2013, as part of the American Board of Internal Medicine Foundation Choosing Wisely^® campaign, the American Geriatrics Society advised providers not to recommend percutaneous feeding tubes in patients with advanced dementia, rather, “offer assisted oral feeding.”⁴⁷ It is worth noting, however, that none of the studies reviewed were of ideal methodological design, so opinions may change with future studies.

A more recent study compared liquid feeds versus semisolid feeds in patients with PEG tubes. The study shows a 22.2% incidence of aspiration pneumonia in the liquid feed group, which is comparable to prior studies, but the incidence of aspiration pneumonia is only 2.2% in the semisolid feed group (P < .005).⁴⁸ A benefit of this size warrants future studies for validation.

Aspiration pneumonia leads to increased mortality when compared with CAP and HCAP.² Until future studies validate or refute the current understanding surrounding its management, the following should provide some guidance: aspiration pneumonia should be suspected in any individual with risk factors of aspiration who presents with typical or atypical symptoms of pneumonia. Confirmation of the diagnosis requires an image representative of pneumonia in the typical dependent lung segment on chest X-ray, lung ultrasound, or noncontrast CT scan of the chest. Treatment of aspiration pneumonia should take into account the site of acquisition, severity of illness, and risk for MDR organisms as the causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods, in addition to the traditional organisms classically thought to cause aspiration pneumonia-anaerobes.

Disclosures

The authors have nothing to disclose.

Aspiration pneumonia refers to an infection of the lung parenchyma in an individual who has inhaled a bolus of endogenous flora that overwhelms the natural defenses of the respiratory system. It primarily affects older adults with almost 80% of cases occurring in those 65 years and older.¹ Compared with nonaspiration pneumonia, aspiration pneumonia (whether community acquired or healthcare associated) results in more ICU stays, mechanical ventilation, increased length of hospital stay, and higher mortality.²

The etiology of aspiration pneumonia comes from aspirated bacteria from the oropharynx or stomach.³ However, aspiration alone is a common occurrence and does not always lead to clinical pneumonia. Indeed, one study demonstrated that 45% of “normal subjects” aspirate in their sleep,⁴ illustrating that our bodies have evolved defense mechanisms to protect us from aspirated bacteria. Thus, it is only when these systems are overwhelmed, after compromise of both glottic closure and the cough reflex in addition to dysphagia,³ that an infection manifests.

Aspiration pneumonitis refers to a significant inflammation of the lung parenchyma that results from inhalation of regurgitated gastric contents.⁵ It can produce fever, cough, wheezing, shortness of breath, hypoxemia, leukocytosis, and a pulmonary infiltrate as well as lead to severe acute respiratory distress syndrome and even death. In the past, the use of antibiotics shortly after aspiration in patients who develop a fever, leukocytosis, or a pulmonary infiltrate was discouraged.⁵ Empiric antibiotics were recommended only for patients who aspirate gastric contents and who have conditions associated with colonization of gastric contents, such as small-bowel obstruction.⁵ Yet, it is difficult to distinguish aspiration pneumonitis from pneumonia⁶ and there are no randomized trials in older adults to help guide their management.

Pneumonia in older adults can present in an atypical fashion. In one study of community-acquired pneumonia (CAP), the combination of cough, fever, and dyspnea is present in only 31% of patients, although separately, they are present in 67%, 64%, and 71% of patients, respectively. The same study also showed that delirium was present in 45% of patients with CAP.⁷ Nonrespiratory symptoms were present during the initial presentation of CAP in 55% of patients, with confusion in 42%, and falls in 16% of cases.⁸ The same is true of aspiration pneumonia where altered mental status is seen in approximately 30% of community-acquired aspiration pneumonia (CAAP) patients and in 19% of continuing care facility patients with aspiration pneumonia.² Another study that compared CAP, CAAP, and healthcare-associated aspiration pneumonia (HCAAP) showed that confusion is present in 5.1%, 12.7%, and 18.6%, respectively.⁹ The absence of fever in older adults is shown in studies where fever, defined as greater than or equal to 37.5°C, is absent in 32% of the very old¹⁰and in 40% of patients 65 years or older when it was defined as greater than 37°C.⁸ The inconsistencies regarding typical symptoms of pneumonia in the older adult population are also confirmed in nursing home residents.¹¹ Ultimately, it is important to remember that any infection in older adults, especially in those residing in long-term care facilities, may present with subtle findings such as an acute change in cognitive and functional status.¹²

Risk Factors for Aspiration Pneumonia

Risk factors for aspiration pneumonia, while not universally agreed upon, are important to recognize as they increase the probability of the diagnosis when present. A 2011 systematic review identified age, male gender, lung disease, dysphagia, and diabetes mellitus (level 2a), as well as severe dementia, angiotensin I-converting enzyme deletion/deletion genotype, and poor oral health (level 2b) as risk factors.¹³ In 2016, a panel of experts reached a consensus (modified Delphi Method) on the following risk factors for the diagnosis of aspiration pneumonia in nursing home residents: history of dysphagia, choking incident, tube feeding, neurologic disease, and cognitive impairment. The presence of one or more of these risk factors in the appropriate clinical setting may suggest a diagnosis of aspiration pneumonia.¹⁴

Radiographic/Ultrasonographic Imaging

In the appropriate scenario, the diagnosis of aspiration pneumonia is supported with an image representative of pneumonia. The pulmonary segment involved in aspiration pneumonia depends on the position of the patient during the aspiration event. If the aspiration event occurs while the patient is in the recumbent position, development of pneumonia is more common in the posterior segments of the upper lobes and the apical segments of the lower lobes; whereas if it occurs while the patient is in an upright position, the location changes to the basal segments of the lower lobes.³

Overall, the sensitivity of a chest X-ray to diagnose pneumonia ranges between 32%-77.7%,^15-17 suggesting that a significant proportion of patients suspected of having pneumonia in past research studies, may have been misdiagnosed. Studies using lung ultrasound to identify pneumonia demonstrate a higher sensitivity, but additional research is needed to validate these findings.^17-19 Noncontrast CT scans of the chest remain the reference standard for diagnosing pneumonia and currently tend to have the largest impact on diagnosis and subsequent treatment decisions.^15,16,20,21 As a result, if radiation exposure risks are not a concern for the patient, we recommend utilizing noncontrast CT imaging whenever the diagnosis is in doubt until future research elucidates the most appropriate approach to imaging.

Diagnosis

Diagnosing aspiration pneumonia is difficult, in part because there is no universal definition or set of diagnostic criteria. The diagnosis of aspiration pneumonia is supported by the fulfillment of three criteria. First, appropriate risk factors for aspiration, as documented above, should be present. Second, there should be evidence of clinical signs and symptoms of pneumonia (typical or atypical). Third, radiographic representation of pneumonia in a dependent pulmonary segment confirms the diagnosis. Once these criteria are met, it is important to distinguish between CAAP and HCAAP with particular attention to risk factors for multidrug-resistant (MDR) organisms and Pseudomonas aeruginosa (PA).

Many studies have tried to determine the exact bacterial etiology of aspiration pneumonia as documented in the Table.

Even when an ideal method is used to obtain a good sample, however, the results are limited by other variables in the study. For example, in studies that use protected brush specimens and protected bronchoalveolar lavage to acquire samples for culture, many patients received antibiotics prior to sampling, and the studies are small (Table). Although anaerobes have traditionally been implicated in aspiration pneumonia, only El-Solh et al.²² were able to culture a significant proportion of anaerobes. The study, however, was limited to institutionalized older adults requiring mechanical ventilation and it did not require the typical radiographic location for aspiration pneumonia. Even under the best circumstances, it is difficult to determine causality because the antibiotics used to treat these cases of aspiration pneumonia cover a broad range of organisms. Based on the studies in the Table, causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods in addition to traditional organisms classically thought to cause aspiration pneumonia-anaerobes. Microbiologic etiology, however, may also be insinuated from the studies discussed in the therapeutic strategies section below as some include antibiotics with limited antimicrobial activity.

Therapeutic Strategies

The management of aspiration pneumonia has evolved significantly since it was first studied in the 1970s because of the development of antibiotic resistance patterns, newer antibiotics, and increasing information on the diversity of pathogens involved in each subset of aspiration syndromes. The antimicrobial treatment of aspiration pneumonia was classically directed against anaerobic pathogens; treatment of these infections, however, was extrapolated from studies of pulmonary abscesses and other anaerobic pulmonary infections.

A randomized controlled trial in the mid-1980s comparing penicillin and clindamycin demonstrated a significantly improved cure rate in the clindamycin group.²³ A follow-up study in 1990 implicated a significant number of penicillin-resistant Bacteroides infections—the majority of these infections were subsequently reclassified as Prevotella melaninogenica—as the cause for high rates of penicillin resistance in lung abscesses and necrotizing pneumonias, further supporting clindamycin as the treatment of choice for these infections.²⁴ Amoxicillin-clavulanic acid (IV and PO regimens), studied in the treatment of community-acquired necrotizing pneumonia/lung abscess, shows good efficacy as well.²⁵ This study also attempted to elucidate the underlying causative organisms in these patients. Organisms associated with CAP as well as anaerobic organisms were isolated, giving more credence to the idea of broader coverage for aspiration pneumonia.

Community-Acquired Aspiration Pneumonia/Healthcare-Associated Aspiration Pneumonia

The importance of making a diagnostic distinction between CAAP versus HCAAP is critical for management strategies. A prospective population-based study demonstrated that ICU length of stay and 30-day mortality is highest for HCAAP, followed by CAAP, and lastly for those with CAP.⁹ Although some studies use different nomenclature for identifying aspiration pneumonia patients at risk for a wider array of microorganisms, we attempt to standardize the language by using HCAAP. The literature on nonaspiration pneumonia is changing from terms such as CAP and healthcare-associated pneumonia (HCAP) to pneumonia with the risk of MDR organisms. One study proposed a new treatment algorithm for CAP based on the presence or absence of the following six risk factors: prior hospitalization of greater than or equal to two days in the preceding 90 days, immunosuppression, previous antibiotic use within the preceding 90 days, use of gastric acid-suppressive agents, tube feeding, and nonambulatory status.²⁶ A similar approach proposed years earlier for HCAP patients found the following to be risk factors for MDR organisms: hospitalization in the past 90 days, antibiotic therapy in the past six months, poor functional status as defined by activities of daily living score, and immune suppression.²⁷ Other factors, such as structural lung disease, that increase the risk of organisms resistant to standard antibiotic treatment regimens^28-31 should be considered in aspiration pneumonia as well. Aspiration pneumonia is following a similar trajectory where the risk of MDR organisms is taking precedence over the environment of acquisition. The final nomenclature will allow the healthcare provider to understand the organisms that need to be targeted when choosing an appropriate antibiotic treatment regimen.

There is evidence supporting the premise that CAAP and nursing home patients with no risk factors for MDR organisms can be treated with standard regimens used for patients with CAP. A prospective cohort study in 2014 did not show any statistically significant differences in clinical outcomes in nursing and healthcare-associated aspiration pneumonia patients (with no risks of MDR organisms) treated with azithromycin versus ampicillin/sulbactam. However, only 36 patients were included in the azithromycin arm, and the therapeutic choices were made by the treating physician.³²

A prospective study of 95 long-term care residents reported that of those patients admitted to the ICU with severe aspiration pneumonia, the causative organisms are gram-negative enteric bacilli in 49% of isolates, anaerobes in 16%, and Staphylococcus aureus in 12%.²² This study mentioned that six of seven anaerobic pneumonia cases had inadequate anaerobic coverage yet were effectively treated; based on the organisms represented, however, the antibiotics administered did provide some coverage.²² Prevotella was one of the common anaerobic organisms that could be treated by levofloxacin or ceftriaxone/azithromycin, possibly explaining the success of azithromycin in the study quoted previously.^22,32 Therefore, although anaerobic organisms still need to be considered, some may be treated by traditional CAP coverage.²²

In a 2005 randomized prospective study of 100 patients aged 71 to 94 years, clindamycin was found to have clinical efficacy equivalent to ampicillin-sulbactam and panipenem in the treatment of mild-to-moderate aspiration pneumonia.³³ Most patients in this study are nursing home residents, and 53% of sputum cultures in the clindamycin arm grew gram-negative rods. In contrast to the previous study, the significance of gram-negative rod infections in this population of patients, with less severe infections, is called into question, as clindamycin has no coverage against these organisms. This premise is supported by a more recent study using azithromycin in nursing and healthcare-associated aspiration pneumonia patients, mentioned previously.³² Taken together, these three studies suggest that the severity of aspiration pneumonia may be a risk factor that needs to be taken into account when considering broad-spectrum antimicrobial coverage.

While further research is needed to validate treatment approaches, based on the current literature we propose the following:

CAAP requiring hospitalization but without any of the following-risk for PA or MDR organisms, septic shock, the need for ICU admission, or mechanical ventilation-can be treated with standard CAP therapy that covers anaerobes.^26,32-34 Patients with CAAP and either of the following—risk factors for MDR organisms, septic shock, need for ICU admission, or mechanical ventilation—should be considered for broader coverage with vancomycin or linezolid, antipseudomonal antibiotics, and anaerobic coverage. CAAP with specific risk for a PA infection should be considered for two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic, and one has anaerobic coverage).

Severe HCAAP without risk for MDR organisms or PA but with any of the following-septic shock, ICU admission, or mechanical ventilation-can be treated based on the 2016 Infectious Diseases Society of America guideline recommendation for hospital-acquired pneumonia, with a regimen that also provides adequate anaerobic coverage.³⁵ If patients have HCAAP with one or more risk factors for MDR organisms, no septic shock, and no need for ICU admission or mechanical ventilation, provide coverage with a similar regimen. In contrast, HCAAP with risk factors for PA or severe HCAAP causing septic shock, requiring ICU admission, or needing mechanical ventilation, which occurs in the setting of one or more risk factors for MDR organisms, or structural lung disease, should receive two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic and one has anaerobic coverage) in addition to vancomycin or linezolid.

A recent systematic review demonstrates the paucity of studies of ideal methodologic design which complicates the ability to recommend, with confidence, one guideline-based antimicrobial regimen over another.³⁶ Future studies may determine that despite the severity of the infection, if patients do not carry any risk for MDR pathogens or PA, they may only require CAAP coverage. When a patient presents with an acute infection, it is prudent to review previous cultures, and although it may be necessary to treat with broad-spectrum antibiotics initially, it is always important to narrow the spectrum based on reliable culture results. If future studies support the results of many studies cited in this article, we may be using fewer antibiotics with narrower spectrums in the near future.

Prevention

Although the healthcare system has practices in place to prevent aspiration pneumonia, the evidence supporting them are either inconclusive or not of ideal methodological design. Two systematic reviews failed to show statistically significant decreases in rates of aspiration pneumonia or mortality using the standard of care positioning strategies or thickened fluids in patients with chronic dysphagia.^37,38 One study showed a decreased incidence of all pneumonia in dysphasic patients with dementia or Parkinson disease when a chin-down posture (with thin liquids) or thickened fluids in a head-neutral position was used. The study, however, has significant limitations, including a lack of a “no treatment” group for comparison, which did not allow investigators to conclude that the decreased incidence was from their interventions.³⁹

There are preventive strategies that show a decreased risk of aspiration pneumonia. Poor oral hygiene seems to be a modifiable risk factor to establish better control of oral flora and decrease aspiration pneumonia. A systematic review of five studies, evaluating the effects of oral healthcare on the incidence of aspiration pneumonia in frail older people, found that tooth brushing after each meal along with cleaning dentures once a day and professional oral healthcare once a week decreases febrile days, pneumonia, and dying from pneumonia.⁴⁰A two-year historical cohort study using aromatherapy with black pepper oil, followed by application of capsaicin troches, and finally menthol gel, as the first meal, leads to a decreased incidence of pneumonia and febrile days in older adults with dysphagia.⁴¹ Well-designed validation studies may establish these practices as the new standard of care for preventing pneumonia in patients with dysphagia.

Feeding Tubes

Multiple studies show that in older adults with advanced dementia there is no survival benefit from percutaneous endoscopic gastrostomy (PEG) tube placement^42-44 and more recent systematic reviews also conclude that there is currently no evidence to support the use of PEG tubes in this specific population.^45,46 In February 2013, as part of the American Board of Internal Medicine Foundation Choosing Wisely^® campaign, the American Geriatrics Society advised providers not to recommend percutaneous feeding tubes in patients with advanced dementia, rather, “offer assisted oral feeding.”⁴⁷ It is worth noting, however, that none of the studies reviewed were of ideal methodological design, so opinions may change with future studies.

A more recent study compared liquid feeds versus semisolid feeds in patients with PEG tubes. The study shows a 22.2% incidence of aspiration pneumonia in the liquid feed group, which is comparable to prior studies, but the incidence of aspiration pneumonia is only 2.2% in the semisolid feed group (P < .005).⁴⁸ A benefit of this size warrants future studies for validation.

Aspiration pneumonia leads to increased mortality when compared with CAP and HCAP.² Until future studies validate or refute the current understanding surrounding its management, the following should provide some guidance: aspiration pneumonia should be suspected in any individual with risk factors of aspiration who presents with typical or atypical symptoms of pneumonia. Confirmation of the diagnosis requires an image representative of pneumonia in the typical dependent lung segment on chest X-ray, lung ultrasound, or noncontrast CT scan of the chest. Treatment of aspiration pneumonia should take into account the site of acquisition, severity of illness, and risk for MDR organisms as the causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods, in addition to the traditional organisms classically thought to cause aspiration pneumonia-anaerobes.

Disclosures

The authors have nothing to disclose.

Aspiration pneumonia refers to an infection of the lung parenchyma in an individual who has inhaled a bolus of endogenous flora that overwhelms the natural defenses of the respiratory system. It primarily affects older adults with almost 80% of cases occurring in those 65 years and older.¹ Compared with nonaspiration pneumonia, aspiration pneumonia (whether community acquired or healthcare associated) results in more ICU stays, mechanical ventilation, increased length of hospital stay, and higher mortality.²

The etiology of aspiration pneumonia comes from aspirated bacteria from the oropharynx or stomach.³ However, aspiration alone is a common occurrence and does not always lead to clinical pneumonia. Indeed, one study demonstrated that 45% of “normal subjects” aspirate in their sleep,⁴ illustrating that our bodies have evolved defense mechanisms to protect us from aspirated bacteria. Thus, it is only when these systems are overwhelmed, after compromise of both glottic closure and the cough reflex in addition to dysphagia,³ that an infection manifests.

Aspiration pneumonitis refers to a significant inflammation of the lung parenchyma that results from inhalation of regurgitated gastric contents.⁵ It can produce fever, cough, wheezing, shortness of breath, hypoxemia, leukocytosis, and a pulmonary infiltrate as well as lead to severe acute respiratory distress syndrome and even death. In the past, the use of antibiotics shortly after aspiration in patients who develop a fever, leukocytosis, or a pulmonary infiltrate was discouraged.⁵ Empiric antibiotics were recommended only for patients who aspirate gastric contents and who have conditions associated with colonization of gastric contents, such as small-bowel obstruction.⁵ Yet, it is difficult to distinguish aspiration pneumonitis from pneumonia⁶ and there are no randomized trials in older adults to help guide their management.

Pneumonia in older adults can present in an atypical fashion. In one study of community-acquired pneumonia (CAP), the combination of cough, fever, and dyspnea is present in only 31% of patients, although separately, they are present in 67%, 64%, and 71% of patients, respectively. The same study also showed that delirium was present in 45% of patients with CAP.⁷ Nonrespiratory symptoms were present during the initial presentation of CAP in 55% of patients, with confusion in 42%, and falls in 16% of cases.⁸ The same is true of aspiration pneumonia where altered mental status is seen in approximately 30% of community-acquired aspiration pneumonia (CAAP) patients and in 19% of continuing care facility patients with aspiration pneumonia.² Another study that compared CAP, CAAP, and healthcare-associated aspiration pneumonia (HCAAP) showed that confusion is present in 5.1%, 12.7%, and 18.6%, respectively.⁹ The absence of fever in older adults is shown in studies where fever, defined as greater than or equal to 37.5°C, is absent in 32% of the very old¹⁰and in 40% of patients 65 years or older when it was defined as greater than 37°C.⁸ The inconsistencies regarding typical symptoms of pneumonia in the older adult population are also confirmed in nursing home residents.¹¹ Ultimately, it is important to remember that any infection in older adults, especially in those residing in long-term care facilities, may present with subtle findings such as an acute change in cognitive and functional status.¹²

Risk Factors for Aspiration Pneumonia

Risk factors for aspiration pneumonia, while not universally agreed upon, are important to recognize as they increase the probability of the diagnosis when present. A 2011 systematic review identified age, male gender, lung disease, dysphagia, and diabetes mellitus (level 2a), as well as severe dementia, angiotensin I-converting enzyme deletion/deletion genotype, and poor oral health (level 2b) as risk factors.¹³ In 2016, a panel of experts reached a consensus (modified Delphi Method) on the following risk factors for the diagnosis of aspiration pneumonia in nursing home residents: history of dysphagia, choking incident, tube feeding, neurologic disease, and cognitive impairment. The presence of one or more of these risk factors in the appropriate clinical setting may suggest a diagnosis of aspiration pneumonia.¹⁴

Radiographic/Ultrasonographic Imaging

In the appropriate scenario, the diagnosis of aspiration pneumonia is supported with an image representative of pneumonia. The pulmonary segment involved in aspiration pneumonia depends on the position of the patient during the aspiration event. If the aspiration event occurs while the patient is in the recumbent position, development of pneumonia is more common in the posterior segments of the upper lobes and the apical segments of the lower lobes; whereas if it occurs while the patient is in an upright position, the location changes to the basal segments of the lower lobes.³

Overall, the sensitivity of a chest X-ray to diagnose pneumonia ranges between 32%-77.7%,^15-17 suggesting that a significant proportion of patients suspected of having pneumonia in past research studies, may have been misdiagnosed. Studies using lung ultrasound to identify pneumonia demonstrate a higher sensitivity, but additional research is needed to validate these findings.^17-19 Noncontrast CT scans of the chest remain the reference standard for diagnosing pneumonia and currently tend to have the largest impact on diagnosis and subsequent treatment decisions.^15,16,20,21 As a result, if radiation exposure risks are not a concern for the patient, we recommend utilizing noncontrast CT imaging whenever the diagnosis is in doubt until future research elucidates the most appropriate approach to imaging.

Diagnosis

Diagnosing aspiration pneumonia is difficult, in part because there is no universal definition or set of diagnostic criteria. The diagnosis of aspiration pneumonia is supported by the fulfillment of three criteria. First, appropriate risk factors for aspiration, as documented above, should be present. Second, there should be evidence of clinical signs and symptoms of pneumonia (typical or atypical). Third, radiographic representation of pneumonia in a dependent pulmonary segment confirms the diagnosis. Once these criteria are met, it is important to distinguish between CAAP and HCAAP with particular attention to risk factors for multidrug-resistant (MDR) organisms and Pseudomonas aeruginosa (PA).

Many studies have tried to determine the exact bacterial etiology of aspiration pneumonia as documented in the Table.

Even when an ideal method is used to obtain a good sample, however, the results are limited by other variables in the study. For example, in studies that use protected brush specimens and protected bronchoalveolar lavage to acquire samples for culture, many patients received antibiotics prior to sampling, and the studies are small (Table). Although anaerobes have traditionally been implicated in aspiration pneumonia, only El-Solh et al.²² were able to culture a significant proportion of anaerobes. The study, however, was limited to institutionalized older adults requiring mechanical ventilation and it did not require the typical radiographic location for aspiration pneumonia. Even under the best circumstances, it is difficult to determine causality because the antibiotics used to treat these cases of aspiration pneumonia cover a broad range of organisms. Based on the studies in the Table, causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods in addition to traditional organisms classically thought to cause aspiration pneumonia-anaerobes. Microbiologic etiology, however, may also be insinuated from the studies discussed in the therapeutic strategies section below as some include antibiotics with limited antimicrobial activity.

Therapeutic Strategies

The management of aspiration pneumonia has evolved significantly since it was first studied in the 1970s because of the development of antibiotic resistance patterns, newer antibiotics, and increasing information on the diversity of pathogens involved in each subset of aspiration syndromes. The antimicrobial treatment of aspiration pneumonia was classically directed against anaerobic pathogens; treatment of these infections, however, was extrapolated from studies of pulmonary abscesses and other anaerobic pulmonary infections.

A randomized controlled trial in the mid-1980s comparing penicillin and clindamycin demonstrated a significantly improved cure rate in the clindamycin group.²³ A follow-up study in 1990 implicated a significant number of penicillin-resistant Bacteroides infections—the majority of these infections were subsequently reclassified as Prevotella melaninogenica—as the cause for high rates of penicillin resistance in lung abscesses and necrotizing pneumonias, further supporting clindamycin as the treatment of choice for these infections.²⁴ Amoxicillin-clavulanic acid (IV and PO regimens), studied in the treatment of community-acquired necrotizing pneumonia/lung abscess, shows good efficacy as well.²⁵ This study also attempted to elucidate the underlying causative organisms in these patients. Organisms associated with CAP as well as anaerobic organisms were isolated, giving more credence to the idea of broader coverage for aspiration pneumonia.

Community-Acquired Aspiration Pneumonia/Healthcare-Associated Aspiration Pneumonia

The importance of making a diagnostic distinction between CAAP versus HCAAP is critical for management strategies. A prospective population-based study demonstrated that ICU length of stay and 30-day mortality is highest for HCAAP, followed by CAAP, and lastly for those with CAP.⁹ Although some studies use different nomenclature for identifying aspiration pneumonia patients at risk for a wider array of microorganisms, we attempt to standardize the language by using HCAAP. The literature on nonaspiration pneumonia is changing from terms such as CAP and healthcare-associated pneumonia (HCAP) to pneumonia with the risk of MDR organisms. One study proposed a new treatment algorithm for CAP based on the presence or absence of the following six risk factors: prior hospitalization of greater than or equal to two days in the preceding 90 days, immunosuppression, previous antibiotic use within the preceding 90 days, use of gastric acid-suppressive agents, tube feeding, and nonambulatory status.²⁶ A similar approach proposed years earlier for HCAP patients found the following to be risk factors for MDR organisms: hospitalization in the past 90 days, antibiotic therapy in the past six months, poor functional status as defined by activities of daily living score, and immune suppression.²⁷ Other factors, such as structural lung disease, that increase the risk of organisms resistant to standard antibiotic treatment regimens^28-31 should be considered in aspiration pneumonia as well. Aspiration pneumonia is following a similar trajectory where the risk of MDR organisms is taking precedence over the environment of acquisition. The final nomenclature will allow the healthcare provider to understand the organisms that need to be targeted when choosing an appropriate antibiotic treatment regimen.

There is evidence supporting the premise that CAAP and nursing home patients with no risk factors for MDR organisms can be treated with standard regimens used for patients with CAP. A prospective cohort study in 2014 did not show any statistically significant differences in clinical outcomes in nursing and healthcare-associated aspiration pneumonia patients (with no risks of MDR organisms) treated with azithromycin versus ampicillin/sulbactam. However, only 36 patients were included in the azithromycin arm, and the therapeutic choices were made by the treating physician.³²

A prospective study of 95 long-term care residents reported that of those patients admitted to the ICU with severe aspiration pneumonia, the causative organisms are gram-negative enteric bacilli in 49% of isolates, anaerobes in 16%, and Staphylococcus aureus in 12%.²² This study mentioned that six of seven anaerobic pneumonia cases had inadequate anaerobic coverage yet were effectively treated; based on the organisms represented, however, the antibiotics administered did provide some coverage.²² Prevotella was one of the common anaerobic organisms that could be treated by levofloxacin or ceftriaxone/azithromycin, possibly explaining the success of azithromycin in the study quoted previously.^22,32 Therefore, although anaerobic organisms still need to be considered, some may be treated by traditional CAP coverage.²²

In a 2005 randomized prospective study of 100 patients aged 71 to 94 years, clindamycin was found to have clinical efficacy equivalent to ampicillin-sulbactam and panipenem in the treatment of mild-to-moderate aspiration pneumonia.³³ Most patients in this study are nursing home residents, and 53% of sputum cultures in the clindamycin arm grew gram-negative rods. In contrast to the previous study, the significance of gram-negative rod infections in this population of patients, with less severe infections, is called into question, as clindamycin has no coverage against these organisms. This premise is supported by a more recent study using azithromycin in nursing and healthcare-associated aspiration pneumonia patients, mentioned previously.³² Taken together, these three studies suggest that the severity of aspiration pneumonia may be a risk factor that needs to be taken into account when considering broad-spectrum antimicrobial coverage.

While further research is needed to validate treatment approaches, based on the current literature we propose the following:

CAAP requiring hospitalization but without any of the following-risk for PA or MDR organisms, septic shock, the need for ICU admission, or mechanical ventilation-can be treated with standard CAP therapy that covers anaerobes.^26,32-34 Patients with CAAP and either of the following—risk factors for MDR organisms, septic shock, need for ICU admission, or mechanical ventilation—should be considered for broader coverage with vancomycin or linezolid, antipseudomonal antibiotics, and anaerobic coverage. CAAP with specific risk for a PA infection should be considered for two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic, and one has anaerobic coverage).

Severe HCAAP without risk for MDR organisms or PA but with any of the following-septic shock, ICU admission, or mechanical ventilation-can be treated based on the 2016 Infectious Diseases Society of America guideline recommendation for hospital-acquired pneumonia, with a regimen that also provides adequate anaerobic coverage.³⁵ If patients have HCAAP with one or more risk factors for MDR organisms, no septic shock, and no need for ICU admission or mechanical ventilation, provide coverage with a similar regimen. In contrast, HCAAP with risk factors for PA or severe HCAAP causing septic shock, requiring ICU admission, or needing mechanical ventilation, which occurs in the setting of one or more risk factors for MDR organisms, or structural lung disease, should receive two antipseudomonal antibiotics (where only one can be a beta-lactam antibiotic and one has anaerobic coverage) in addition to vancomycin or linezolid.

A recent systematic review demonstrates the paucity of studies of ideal methodologic design which complicates the ability to recommend, with confidence, one guideline-based antimicrobial regimen over another.³⁶ Future studies may determine that despite the severity of the infection, if patients do not carry any risk for MDR pathogens or PA, they may only require CAAP coverage. When a patient presents with an acute infection, it is prudent to review previous cultures, and although it may be necessary to treat with broad-spectrum antibiotics initially, it is always important to narrow the spectrum based on reliable culture results. If future studies support the results of many studies cited in this article, we may be using fewer antibiotics with narrower spectrums in the near future.

Prevention

Although the healthcare system has practices in place to prevent aspiration pneumonia, the evidence supporting them are either inconclusive or not of ideal methodological design. Two systematic reviews failed to show statistically significant decreases in rates of aspiration pneumonia or mortality using the standard of care positioning strategies or thickened fluids in patients with chronic dysphagia.^37,38 One study showed a decreased incidence of all pneumonia in dysphasic patients with dementia or Parkinson disease when a chin-down posture (with thin liquids) or thickened fluids in a head-neutral position was used. The study, however, has significant limitations, including a lack of a “no treatment” group for comparison, which did not allow investigators to conclude that the decreased incidence was from their interventions.³⁹

There are preventive strategies that show a decreased risk of aspiration pneumonia. Poor oral hygiene seems to be a modifiable risk factor to establish better control of oral flora and decrease aspiration pneumonia. A systematic review of five studies, evaluating the effects of oral healthcare on the incidence of aspiration pneumonia in frail older people, found that tooth brushing after each meal along with cleaning dentures once a day and professional oral healthcare once a week decreases febrile days, pneumonia, and dying from pneumonia.⁴⁰A two-year historical cohort study using aromatherapy with black pepper oil, followed by application of capsaicin troches, and finally menthol gel, as the first meal, leads to a decreased incidence of pneumonia and febrile days in older adults with dysphagia.⁴¹ Well-designed validation studies may establish these practices as the new standard of care for preventing pneumonia in patients with dysphagia.

Feeding Tubes

Multiple studies show that in older adults with advanced dementia there is no survival benefit from percutaneous endoscopic gastrostomy (PEG) tube placement^42-44 and more recent systematic reviews also conclude that there is currently no evidence to support the use of PEG tubes in this specific population.^45,46 In February 2013, as part of the American Board of Internal Medicine Foundation Choosing Wisely^® campaign, the American Geriatrics Society advised providers not to recommend percutaneous feeding tubes in patients with advanced dementia, rather, “offer assisted oral feeding.”⁴⁷ It is worth noting, however, that none of the studies reviewed were of ideal methodological design, so opinions may change with future studies.

A more recent study compared liquid feeds versus semisolid feeds in patients with PEG tubes. The study shows a 22.2% incidence of aspiration pneumonia in the liquid feed group, which is comparable to prior studies, but the incidence of aspiration pneumonia is only 2.2% in the semisolid feed group (P < .005).⁴⁸ A benefit of this size warrants future studies for validation.

Aspiration pneumonia leads to increased mortality when compared with CAP and HCAP.² Until future studies validate or refute the current understanding surrounding its management, the following should provide some guidance: aspiration pneumonia should be suspected in any individual with risk factors of aspiration who presents with typical or atypical symptoms of pneumonia. Confirmation of the diagnosis requires an image representative of pneumonia in the typical dependent lung segment on chest X-ray, lung ultrasound, or noncontrast CT scan of the chest. Treatment of aspiration pneumonia should take into account the site of acquisition, severity of illness, and risk for MDR organisms as the causative organisms may include Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and gram-negative rods, in addition to the traditional organisms classically thought to cause aspiration pneumonia-anaerobes.

Disclosures

The authors have nothing to disclose.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

BACKGROUND: Medicare patients account for approximately 50% of hospital days. Hospitalization in older adults often results in poor outcomes.

OBJECTIVE: To test the feasibility and impact of using Assessing Care of Vulnerable Elders (ACOVE) quality indicators (QIs) as a therapeutic intervention to improve care of hospitalized older adults.

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For more articles and subscription information, visit www.journalofhospitalmedicine.com.

BACKGROUND: Medicare patients account for approximately 50% of hospital days. Hospitalization in older adults often results in poor outcomes.

OBJECTIVE: To test the feasibility and impact of using Assessing Care of Vulnerable Elders (ACOVE) quality indicators (QIs) as a therapeutic intervention to improve care of hospitalized older adults.

Also in JHM

Use of simulation to assess incoming interns’ recognition of opportunities to choose wisely
AUTHORS: Kathleen M. Wiest, Jeanne M. Farnan, MD, MHPE, Ellen Byrne, Lukas Matern, Melissa Cappaert, MA, Kristen Hirsch, Vineet M. Arora, MD, MAPP

Clinician attitudes regarding ICD deactivation in DNR/DNI patients
AUTHORS: Andrew J. Bradley, MD, Adam D. Marks, MD, MPH

Using standardized patients to assess hospitalist communication skills
AUTHORS: Dennis T. Chang, MD, Micah Mann, MD, Terry Sommer, BFA, Robert Fallar, PhD, Alan Weinberg, MS, Erica Friedman, MD

Techniques and behaviors associated with exemplary inpatient general medicine teaching: An exploratory qualitative study
AUTHORS: Nathan Houchens, MD, Molly Harrod, PhD, Stephanie Moody, PhD, Karen E. Fowler, MPH, Sanjay Saint, MD, MPH

A simple algorithm for predicting bacteremia using food consumption and shaking chills: A prospective observational study
AUTHORS: Takayuki Komatsu, MD, PhD, Erika Takahashi, MD, Kentaro Mishima, MD, Takeo Toyoda, MD, Fumihiro Saitoh, MD, Akari Yasuda, RN, Joe Matsuoka, PhD, Manabu Sugita, MD, PhD, Joel Branch, MD, Makoto Aoki, MD, Lawrence M. Tierney Jr., MD, Kenji Inoue, MD, PhD

For more articles and subscription information, visit www.journalofhospitalmedicine.com.

BACKGROUND: Medicare patients account for approximately 50% of hospital days. Hospitalization in older adults often results in poor outcomes.

OBJECTIVE: To test the feasibility and impact of using Assessing Care of Vulnerable Elders (ACOVE) quality indicators (QIs) as a therapeutic intervention to improve care of hospitalized older adults.

Also in JHM

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AUTHORS: Kathleen M. Wiest, Jeanne M. Farnan, MD, MHPE, Ellen Byrne, Lukas Matern, Melissa Cappaert, MA, Kristen Hirsch, Vineet M. Arora, MD, MAPP

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AUTHORS: Andrew J. Bradley, MD, Adam D. Marks, MD, MPH

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AUTHORS: Dennis T. Chang, MD, Micah Mann, MD, Terry Sommer, BFA, Robert Fallar, PhD, Alan Weinberg, MS, Erica Friedman, MD

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AUTHORS: Nathan Houchens, MD, Molly Harrod, PhD, Stephanie Moody, PhD, Karen E. Fowler, MPH, Sanjay Saint, MD, MPH

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AUTHORS: Takayuki Komatsu, MD, PhD, Erika Takahashi, MD, Kentaro Mishima, MD, Takeo Toyoda, MD, Fumihiro Saitoh, MD, Akari Yasuda, RN, Joe Matsuoka, PhD, Manabu Sugita, MD, PhD, Joel Branch, MD, Makoto Aoki, MD, Lawrence M. Tierney Jr., MD, Kenji Inoue, MD, PhD

For more articles and subscription information, visit www.journalofhospitalmedicine.com.