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(Chest. 2002;122:1709-1714.)
© 2002 American College of Chest Physicians

Correlates of Prolonged Hospitalization in Inner-city ICU Patients Receiving Noninvasive and Invasive Positive Pressure Ventilation for Status Asthmaticus*

Brian Gehlbach, MD; John P. Kress, MD, FCCP; Jeremy Kahn, MD; Cynthia DeRuiter, MD; Anne Pohlman, RN and Jesse Hall, MD, FCCP

* From the University of Chicago (Drs. Gehlbach, Kress, Kahn, and Hall, and Ms. Pohlman), Chicago, IL; and Johns Hopkins University (Dr. DeRuiter), Baltimore, MD.

Correspondence to: Brian Gehlbach, MD, University of Chicago Hospitals, Section of Pulmonary and Critical Care, 5841 S Maryland Ave, MC 6026, Chicago, IL 60637; e-mail: bgehlbac{at}medicine.bsd.uchicago.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To describe the outcome of patients with status asthmaticus (SA) treated in a medical ICU with positive pressure ventilation (PPV), and to identify those factors associated with increased length of hospital stay.

Design: Retrospective chart review.

Setting: University-based hospital in Chicago, IL.

Patients: All patients admitted with SA and treated with PPV over a 5-year period.

Results: The first ICU admission for each of 78 patients was analyzed. Fifty-six patients underwent endotracheal intubation (ETI) during the hospitalization, while 22 patients were treated with noninvasive PPV alone. Three patients died. The median hospital length of stay was 5.5 days. Cox regression analysis revealed the following factors to be independently associated with increased length of hospital stay: female gender (p < 0.01), ETI (p < 0.01), the administration of neuromuscular blockers for > 24 h (p < 0.01), inhaled corticosteroid use prior to ICU admission (p = 0.01), and increasing APACHE (acute physiology and chronic health evaluation) II score (p < 0.01).

Conclusions: This study suggests that while the mortality associated with SA treated with contemporary methods of PPV is low, certain factors, including female gender, ETI, and the prolonged use of neuromuscular blockade, are associated with an increased length of hospital stay. The development of respiratory failure despite preadmission use of inhaled corticosteroids is also associated with prolonged hospitalization.

Key Words: asthma • female • length of stay • neuromuscular blocking agents • respiratory insufficiency • sex factors • status asthmaticus • ventilators, mechanical


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Controlled hypoventilation is effective at limiting dynamic hyperinflation and barotrauma in patients with status asthmaticus (SA) receiving mechanical ventilation.1 2 Studies3 4 5 6 7 8 9 10 in which patients were treated with this approach have shown a decrease in mortality relative to historical control subjects. Still, we have noticed that a minority of our patients undergo prolonged hospitalization. While previous investigators11 12 13 14 15 have identified risk factors for severe asthma attacks, the factors influencing duration of hospitalization after presenting with respiratory failure are not known. We analyzed the demographics, complications, and clinical outcomes of patients with SA treated with positive pressure ventilation (PPV) in our medical ICU during the past 5 years in order to determine those factors associated with prolonged hospitalization.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
This study was approved by the Institutional Review Board at the University of Chicago Hospitals. Eligible subjects included all patients with SA who were treated in the medical ICU at the University of Chicago Hospitals between May 1995 and May 2000 with either endotracheal intubation (ETI) and mechanical ventilation, or a minimum of 2 consecutive h of noninvasive PPV (NIPPV). Subjects were identified after analyzing the medical records of patients admitted to the ICU and billed with International Classification of Diseases, Ninth Revision codes associated with asthma. Asthma was diagnosed on the basis of the presence of lower-airway obstruction without evidence of COPD. Therefore, patients with evidence of COPD by chest radiography or pulmonary function tests were excluded, as were patients > 40 years old with a smoking history of >= 20 pack-years.

Treatment Protocol
IV methylprednisolone, 60 to 125 mg q6h, is administered to all patients admitted to the ICU with SA. All patients receive nebulized albuterol, with ipratropium bromide also administered to selected patients at the discretion of the treating physician. Theophylline is used infrequently. NIPPV is administered to patients with high work of breathing as assessed by clinical criteria (tachypnea, accessory muscle use, pulsus paradoxus, and, if obtained, arterial blood gas abnormalities). The decision to institute NIPPV is made by the ICU physician caring for each patient. Patients with contraindications to the use of NIPPV (eg, severely depressed mental status, craniofacial abnormalities, etc.), who present to the emergency department in respiratory arrest, or who progress to respiratory arrest despite NIPPV, undergo ETI and conventional mechanical ventilation. These patients are typically treated with volume-cycled ventilation using low respiratory rates (8 to 15 breaths/min), low tidal volumes (5 to 7 mL/kg), and high flow rates (60 to 90 L/min), with the goal of maintaining intrinsic positive end-expiratory pressure (PEEP) < 15 cm H2O and plateau pressure (obtained through an end-inspiratory hold maneuver) < 30 cm H2O.

Data Collection and Definition of Variables
All charts were reviewed by authors experienced in data abstraction. One of us (B.G.) reviewed all data collection sheets for accuracy and completeness prior to entry into a computer database. To ensure independence of observations, only the first ICU admission for each patient was analyzed. Patients were considered to have received PPV if they received NIPPV for at least 2 consecutive h, or mechanical ventilation via an endotracheal tube at any time after arriving in the ICU. Those patients who received NIPPV only in the emergency department were excluded. The charts of 104 of 105 subjects were available for analysis. For the purpose of missing data points (< 1% of all data), mean or median values for the study population were used.

The following demographic data were collected: age, sex, race, APACHE (acute physiology and chronic health evaluation) II score, tobacco use, illicit drug use, inhaled corticosteroid use, and systemic steroid use for > 24 h at the time of ICU admission. Illicit drug use was recorded if the patient reported current drug use, or if the toxicology screen result was positive. Since opiates and benzodiazepines are commonly used by emergency department staff when managing intubated patients with SA, toxicology screen findings reporting only these substances were considered negative if obtained after these medications were administered in the hospital. Treatment variables analyzed included the duration of mechanical ventilation and the use of neuromuscular blockers. Mortality, duration of hospitalization, and discharge destination were recorded for all patients.

Complications were recorded, and included the following: (1) barotrauma requiring a chest tube, (2) anoxic encephalopathy, and (3) hospital-acquired infection. Hospital-acquired infection required either of the following to occur >= 48 h after ICU admission: (1) the isolation of a typical pathogen from a normally sterile body fluid, or (2) clinical evidence of sepsis with a suspected source of infection and at least two of the following: temperature > 38.5°C or < 35.5°C; leukocyte count > 10,000/µL or < 3,500/µL; heart rate > 100 beats/min; respiratory rate > 24 breaths/min; systolic BP < 90 mm Hg despite sufficient fluid replacement or the need for vasoactive agents to maintain systolic BP >= 90 mm Hg; elevated serum lactate levels or metabolic acidosis not secondary to respiratory alkalosis; and oliguria with urine output < 20 mL/h despite sufficient fluid replacement.16 Organ failures were also recorded, and defined as follows: renal failure, creatinine level > 3.4 mg/dL; hepatic failure, bilirubin level > 3.5 mg/dL, alkaline phosphatase > 350 U/L, and/or international normalized ratio > 2 in the absence of anticoagulants; cardiovascular failure, need for dobutamine, norepinephrine, or epinephrine at any dose, or dopamine at > 5 µg/kg/min; and hematologic failure, WBC < 2.0/µL and/or platelet count < 40,000/µL.17

A separate analysis of sedative strategies was performed on those patients intubated for > 24 h. Sedative and analgesic use were recorded from the first 7 AM following endotracheal intubation until 48 h elapsed, sedatives were discontinued, or extubation occurred. During this period, the arterial blood gas level with the lowest pH and its associated PCO2 was recorded for each patient.

Statistical Analysis
Nominal data were analyzed by {chi}2 or the Fisher exact test, where appropriate. Parametric interval data were analyzed using a two-tailed Student t test, and are reported as mean ± SD. Nonparametric data were analyzed using the Mann-Whitney U test, and are reported as median (interquartile range [IQR]).

Following univariate analysis, those variables found significant at p < 0.10 were subjected to Cox regression to determine those variables independently associated with length of hospital stay. Morbidity odds ratios with 95% confidence intervals are presented. A p value of < 0.05 was considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Seventy-nine patients were admitted a total of 105 times to the University of Chicago Hospitals Medical ICU and treated with PPV. Seventy-eight charts were available for review.

Characteristics of the study population are shown in Table 1 . Nearly all (96%) of the patients were African American, and 72% were female. Fewer than half (47%) were receiving inhaled corticosteroids on presentation, while 33% had been receiving systemic steroids for > 24 h. Thirty-one percent used tobacco, and at least 19% were using illicit drugs. A toxicology screen was not performed in 53% of the patients. Seventy-two percent underwent ETI during the hospitalization, while the remaining 22 patients were treated with NIPPV alone. Except for APACHE II scores (ETI median score, 12 [IQR, 10 to 15] vs NIPPV median score, 9.5 [IQR, 7 to 15]), patient characteristics did not differ between patients treated with NIPPV only and patients who underwent ETI.


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  		Table 1. Patient Characteristics*

 
ICU admission outcomes are summarized in Table 2 . Mortality was low, with three deaths (4%), none attributable to barotrauma. An 18-year-old male patient with numerous prior hospital admissions for asthma succumbed to the ARDS and multiple organ failure after presenting with SA and community-acquired pneumonia. A 51-year-old woman with inactive systemic lupus erythematosus and a history of moderate persistent asthma had prolonged SA followed by acute tubular necrosis, abdominal distension, ARDS, and septic shock. A 55-year-old woman had both SA and disseminated intravascular coagulation develop in the setting of influenza pneumonia. Her course was complicated by upper- and lower-extremity deep venous thromboses, multiple infectious complications, GI bleeding, seizures, and shock. One patient, who had anoxic encephalopathy develop after presenting to the emergency department in full cardiac arrest, was transferred to a long-term care facility after undergoing tracheostomy and gastrostomy tube placement.


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  		Table 2. Patient Outcomes

 
Complications (Table 3 ) occurred almost exclusively in the patients who underwent ETI. Only one patient received a chest tube for barotrauma. One patient suffered an anoxic encephalopathy (described above). Eight patients required acute rehabilitation for newly acquired weakness. Eight patients had a total of 15 organ failures: renal (n = 3), liver (n = 2), GI (n = 1), cardiovascular (n = 6), and hematologic (n = 3). Only one patient required dialysis. Ten patients received a diagnosis of at least one hospital-acquired infection: ventilator-associated pneumonia (n = 4), sinusitis (n = 4), line sepsis (n = 2) Clostridium difficile colitis (n = 1), urinary tract infection (n = 3), and occult sepsis (n = 1).


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  		Table 3. Complications*

 
Thirty-five patients received NIPPV on at least one occasion in the ICU. Twenty-nine patients received NIPPV as initial therapy, with 7 patients in this group (24%) progressing to intubation. One patient in whom NIPPV was unsuccessful as initial therapy received it successfully following extubation. Six patients who underwent ETI as initial therapy were later treated with NIPPV following extubation; none of these patients required reintubation.

The median length of hospital stay was 5.5 days (IQR, 3.8 to 11.1 days). Associated with increased length of hospital stay by univariate analysis (p < 0.10) were the following independent variables: ETI, female gender, use of inhaled corticosteroids on ICU admission, systemic steroid use for > 24 h on admission to the ICU, absence of illicit drug use on ICU admission, and administration of neuromuscular blockers for > 24 h. These variables were subjected to Cox regression analysis along with age and APACHE II scores to determine those variables independently associated with increased length of hospital stay. Table 4 summarizes these results. Duration of hospitalization was significantly associated with female gender (p < 0.01; Fig 1 ), ETI (p < 0.01), the administration of neuromuscular blockers for > 24 h (p < 0.01; Fig 2 ), inhaled corticosteroid use on ICU admission (p = 0.01), and increasing APACHE II score (p < 0.01). Illicit drug use, age, and systemic steroid use at ICU admission were not independently associated with duration of hospitalization.


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  		Table 4. Length of Hospital Stay, Cox Regression Analysis*

 


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  		Figure 1. Duration of hospitalization by gender. After adjustment for baseline characteristics (age, APACHE II score, illicit drug use, inhaled corticosteroid use prior to ICU admission and systemic steroid use > 24 h prior to ICU admission) and treatment characteristics (mode of mechanical ventilation, neuromuscular blockade > 24 h), women had longer hospitalizations than men (relative risk of prolonged hospitalization, 4.1; 95% confidence interval, 2.1 to 7.9; p < 0.01).

 


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  		Figure 2. Duration of hospitalization by administration of neuromuscular blockers (NMB) for > 24 h or < 24 h. After adjustment for baseline characteristics (age, sex, APACHE II score, illicit drug use, inhaled corticosteroid use prior to ICU admission, systemic steroid use > 24 h prior to ICU admission) and mode of PPV, patients who received neuromuscular blockers for > 24 h had longer hospitalizations than those who did not (relative risk of prolonged hospitalization, 2.9; 95% confidence interval 1.4 to 5.8; p < 0.01).

 
Forty-two patients were intubated for > 24 h, and were thus eligible for analysis of sedative practice. Sixty-nine percent (29 patients) received propofol as the primary sedative during the data collection period, at a mean dose of 51.7 ± 18.3 µg/kg/min. Seven percent (three patients) received midazolam as the primary sedative at a dose of 0.073 ± 0.041 mg/kg/h. Twenty-one percent (nine patients) received a combination of propofol (56.7 ± 15 µg/kg/min) and low-dose midazolam (0.05 mg/kg/24 h; IQR, 0.02 to 0.17 mg/kg/24 h). Sedative data were incomplete for one patient. All patients received morphine at 0.072 ± 0.05 mg/kg/h. Fourteen of the patients who received propofol also received lorazepam at 0.05 mg/kg/24 h (IQR, 0.02 to 0.07 mg/kg/24 h). The lowest pH for the group during the data collection period averaged 7.22 ± 0.11, and the associated PCO2 was 52.5 mm Hg (IQR, 43 to 63 IQR). Neuromuscular blockers were administered for > 24 h to 17 patients (40.5%).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In a mostly African-American population of patients receiving PPV for SA, we found an association between increased length of hospital stay and female gender, as well as with preadmission use of inhaled corticosteroids. Both ETI and the administration of neuromuscular blockers for > 24 h were also associated with longer hospitalizations.

One of the major findings of our study is the significantly longer length of stay for women compared with men (7.1 days vs 4.8 days), even after adjusting for other baseline variables. Conceivably, the relatively small number of male patients in our study may have influenced the results. However, our findings are consistent with other work suggesting that women are disproportionately affected by asthma. Previous investigators have reported a 2.5-fold to threefold increase in asthma ICU admission rates for women relative to men.13 Women also report more symptoms and worse quality of life than men with similar airflow obstruction, suggesting differences in the perception, impact, or reporting of this disease.18 Both biological and social factors may contribute to the greater expression of asthma in women.19 20 A hormonal influence on asthma expression is supported by a shift from excess male to excess female risk after puberty,13 and by increased rates of asthma among users of hormone replacement therapy.21 Bronchial responsiveness is also increased in women relative to men following puberty, even after controlling for baseline lung function.22 Although traditional gender roles are changing, women historically have been exposed to a different spectrum of environmental antigens than men.19 20 It is also possible that unidentified differences in the preadmission or inpatient management of women in our study exist. This would not be surprising, given the evidence for gender disparities in how physicians manage other diseases.23 Still, our findings are similar to those of Afessa et al,24 who analyzed outcomes of SA in a similar inner-city, predominantly African-American population, and found deaths in 10 of 70 women and none of 19 men.

Patients receiving inhaled corticosteroids at ICU admission stayed longer than patients not receiving these medications. This negative association likely serves as a marker of severity of illness: patients who have respiratory failure develop when receiving optimal medication may have more severe disease.

Tobacco use was not correlated with duration of hospitalization in our study. Although patients using illicit drugs had a significantly shorter length of hospital stay after univariate analysis, this difference did not persist after adjustment for other baseline and treatment variables. Given the absence of a toxicology screen in 53% of our group, the influence of this practice on duration of hospitalization is difficult to determine.

Previous investigators24 25 26 27 28 29 have demonstrated the feasibility of NIPPV in SA. Patients managed with NIPPV in our study were unlikely to require subsequent intubation, and had shorter hospitalizations than those patients managed with conventional ETI and mechanical ventilation. The design of our study, however, does not allow direct comparison of these two approaches. Patients successfully "treated" with NIPPV may have experienced an improved outcome because they were less ill (APACHE II score, 9.5 vs 12; p < 0.01), because of either earlier presentation or more rapidly reversible airflow obstruction. Still, our results suggest that NIPPV can be used safely in SA in carefully selected patients, and that patients successfully managed with this approach experience very little morbidity.

Patients who received neuromuscular blockers for > 24 h (30% of the intubated patients) experienced longer hospitalizations than those who did not, even after controlling for mode of PPV, APACHE II scores, and baseline characteristics. Conceivably, neuromuscular blockers were administered to patients with more severe airflow obstruction, in whom target airway pressures (plateau pressure and auto-PEEP) were difficult to achieve without the use of these agents. Alternatively, given the risk of myopathy with concomitant high-dose steroid and neuromuscular blockade administration beyond 24 h,30 liberation from the ventilator may have been delayed by the development of weakness. Since our study was retrospective, we did not attempt to identify cases of myopathy, a condition that is often diagnosed on clinical grounds and not always rigorously documented in the medical record. Because the administration of neuromuscular blockers was not controlled, it is impossible to know whether the extremely low rate of barotrauma in our study (2%) could have been achieved without the use of these agents. Nonetheless, the high doses of multiple sedatives and analgesics used in our study illustrate the challenge of enforcing controlled hypoventilation (mean lowest pH 7.22) in patients with SA.

Our treatment protocol was highly effective at limiting death from SA. Notably, all three of the patients who died in our study had significant acute or chronic comorbidities. The complications acquired by our patients are similar to those documented in other studies, infection and weakness being most problematic. Although organ failures occurred in eight patients, only one patient required hemodialysis. A single patient received a discharge diagnosis of anoxic encephalopathy.

There are several important limitations to our study. Because of its retrospective design, we are unable to report clinical data routinely used by clinicians in the bedside assessment of asthma severity (for example, pulsus paradoxus and auto-PEEP), and used by physicians in our study to guide the administration of individual therapies (for example, NIPPV and neuromuscular blockers). Reliable data on the preadmission management of our patients (for example, patient use of peak flow monitors) was also not available to us. Our patient population may also differ from others in important ways. Mortality rates from asthma are disproportionately high in Chicago, for reasons that are speculative but may relate to socioeconomic and/or racial disparities, as well as environmental conditions.31 Variables associated with prolonged hospitalization may be unique to our own patient population, and not representative of patients in other regions. Also, the widespread use of NIPPV in our institution may be dissimilar from the practices of other institutions. Our study population may therefore differ from other study groups comprising only patients treated with ETI. Similarly, direct comparison of the efficacy of NIPPV with conventional mechanical ventilation in our study is problematic, since the allocation of NIPPV was not random.

The following conclusions can be drawn about the treatment of SA in our institution: (1) patients treated with a strategy employing NIPPV and ETI with controlled hypoventilation have low mortality; (2) patients with SA requiring PPV are more likely to be women, and women with SA requiring PPV also experience longer hospitalizations; (3) NIPPV is safe in the management of SA for those patients able to tolerate this intervention, and most patients treated with NIPPV do not require ETI; (4) the administration of neuromuscular blockers for > 24 h is associated with prolonged hospitalization; and (5) the development of respiratory failure despite preadmission use of inhaled corticosteroids is associated with a greater duration of hospitalization. These findings should be useful to clinicians in the management of patient with SA, and to clinical investigators in the design of future studies assessing interventions in these patients.


   Acknowledgements
 
The authors thank Michael Woo, MD, for the identification of subjects in the study.


   Footnotes
 
Abbreviations: APACHE = acute physiology and chronic health evaluation; ETI = endotracheal intubation; IQR = interquartile range; NIPPV = noninvasive positive pressure ventilation; PEEP = positive end-expiratory pressure; PPV = positive pressure ventilation; SA = status asthmaticus

This work was performed at the University of Chicago.

Received for publication September 7, 2001. Accepted for publication February 28, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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