Prognostic Factors for Discharge Directly Home in Patients With Thoracoscopic Surgery for Empyema: A Multicenter Retrospective Cohort Study

Abstract

Background:

Video-assisted thoracoscopic surgery is a widely recommended treatment for empyema in advanced stages. However, only a few studies have evaluated prognostic factors among patients with empyema who underwent video-assisted thoracoscopic surgery. Furthermore, no studies have evaluated predictors of direct discharge home.

Patients and Methods:

This multicenter retrospective cohort study included 161 patients with empyema who underwent video-assisted thoracoscopic surgery in five acute-care hospitals. The primary outcome was the probability of direct discharge home. The secondary outcome was the length of hospital stay after surgery. We broadly assessed pre-operative factors and performed univariable logistic regression for the direct discharge home and univariable gamma regression for the length of hospital stay after surgery.

Results:

Of the 161 included patients, 74.5% were directly discharged home. Age (>70 years; −24.3%); altered mental status (−33.4%); blood urea nitrogen (>22.4 mg/dL; −19.4%); and pleural pH (<7.2; −17.6%) were associated with high probabilities of not being directly discharged home. Fever (15.2%) and albumin (> 2.7 g/dL; 20.2%) were associated with high probabilities of being directly discharged home. The median length of stay after surgery was 19 days. Age (>70 years; 6.2 days); altered mental status (5.6 days); purulence (2.7 days); pleural thickness (>2 cm; 5.1 days); bronchial fistula (14.6 days); albumin (>2.7 g/dL; 3.1 days); and C-reactive protein (>20 mg/dL; 3.6 days) were associated with a longer post-operation hospital stay.

Conclusions:

Physicians should consider using these prognostic factors to predict non-direct discharge to the home for patients with empyema.

Video-assisted thoracoscopic surgery (VATS) is the recommended treatment for empyema in advanced stages.¹ Because the mortality rate of empyema has improved^2,3 because of the widespread use of antibiotic agents and VATS, more physicians and patients are taking interest in improving the quality of life (QOL) as well. One aspect of QOL is the likelihood of returning directly home.^4,5 Identifying risk factors for not being directly discharged home can lead to better-shared decision-making for treatment modalities. To date, no studies have evaluated the risk factors of not being directly discharged home in patients with empyema.

Furthermore, only two single-centered retrospective cohort studies evaluated prognostic factors among patients with empyema who underwent VATS.^6,7 These studies did not include information on pleural effusion analyses and computed tomography (CT) scan findings, despite these factors being potential prognostic variables for empyema.^1,8–11 Therefore, we conducted this retrospective cohort study to explore risk factors for not being directly discharged home in patients with empyema who underwent VATS.

Patients and Methods

Study design and ethical approval

This multicentered retrospective cohort study included five acute general hospitals in Japan (Kobe City Medical Center General Hospital, Tokyo hospital, Saiseikai Kumamoto Hospital, Ichinomiyanishi Hospital, and Saiseikai Yokohamashi Tobu Hospital). The study protocol was approved by the Institutional Review Board of Kobe City Medical Center General Hospital (approval number: zn220404). We followed the Strengthening the Reporting of Observational Studies in Epidemiology statement (Supplementary Table S1) in reporting this study.¹²

Study participants

Patients from each hospital were enrolled at different time points between January 2006 and September 2021 because the hospitals had different data storage terms. First, we extracted patient data of individuals diagnosed with empyema based on the International Statistical Classification of Diseases and Related Health Problems, 10th Revision, code J86. Thereafter, a pulmonologist or thoracic surgeon confirmed the clinical diagnosis of empyema based on each physician's discretion, instead of using the diagnostic criteria according to the previous randomized controlled trial (RCT),¹³ because this can cause false-negative diagnosis.¹⁴ Finally, we included patients who underwent thoracoscopic surgery during hospitalization. In our hospitals, physicians consider antibiotic agents and tube drainage as initial treatments. Surgical interventions are used if initial treatments fail.

Exposure and outcome

We extracted outcome variables from the electronic medical records. We selected potential prognostic factors and the cutoff points in advance based on previous studies^11,15–19: duration from the day of the diagnosis to the day of the surgery (>20 days), community-acquired empyema, fever, age (>70 years), Charlson comorbidity index (>2 points), altered mental status at admission, purulent pleural effusion, pH of pleural effusion (<7.2), positive/negative pleural effusion culture, loculation, pleural thickness (>2 cm), bronchial fistula on chest CT at admission, albumin (>2.7 g/dL), blood urea nitrogen (>22.4 mg/dL), C-reactive protein (>20 mg/dL) within seven days before the surgery.

To avoid cognitive bias, one radiologist read a plain chest CT scan within seven days after the diagnosis without any clinical information. Empyema lacks clear diagnostic criteria and is typically diagnosed based on clinical judgment by physicians. Therefore, we also relied on clinical assessment for the diagnosis of empyema in our study. As part of sensitivity analysis, we categorized patients diagnosed using the diagnostic criteria used in the previous retrospective study as “definite empyema” and conducted additional analyses for this subgroup of patients (Supplementary Fig. S2). Based on the previous study, the staging of empyema was determined as follows: stage 1 encompasses empyema cases with a pleural pH of 7.2 or above; stage 2 includes empyema cases with a pleural pH below 7.2 and without pleural thickening; and stage 3 consists of empyema cases exhibiting pleural thickening.

The primary outcome was the probability of direct discharge to home and the secondary outcome was length of hospital stay after surgery. Direct discharge home was defined as the patient's capacity to return directly to their own residence with the ability to resume their activities of daily living (ADL) fully after the completion of acute treatment for empyema. In contrast, “inability to be directly discharged home” was defined as the necessity for transferring the patient to a rehabilitation or another type of long-term care facility when they cannot maintain ADL suitable for home life after completing the acute treatment for empyema.

Statistical analysis

Participants' baseline characteristics were summarized using proportions for categorical variables and as medians and interquartile range for continuous variables. Missing values were imputed using multiple imputation by chained equations under missing at random assumption creating 100 multiply imputed datasets.²⁰ The difference in the probabilities of direct discharge home based on each exposure was calculated using univariable logistic regression. The probabilities of direct discharge to home are the average of the absolute differences between two predicted outcomes for every single patient based on each explanatory variable. If physicians find each prognostic factor, they can expect a difference in the probability of direct discharge home and length of hospital stay after surgery. These analyses were conducted within each imputed dataset, and the estimated were combined using Rubin's combining rule.²¹

For the secondary outcome, univariate gamma regression was used to calculate the estimated difference in the length of hospital stay after surgery. As sensitivity analyses, complete case analyses were conducted and imputed models only including patients with a definite diagnosis of empyema.¹³ Diagnosis criteria of definite empyema were a positive gram stain or culture from pleural fluid or a pleural pH <7.2 or purulence of pleural fluid according to the previous randomized control study.¹³ All analyses were conducted using the R statistical software (version 4.0.1).

Results

Participant characteristics

Based on the International Statistical Classification of Diseases and Related Health Problems, 10th Revision, code 897, hospitalized patients with empyema were selected (Fig. 1). After excluding 264 patients with incorrect diagnoses and 472 patients who did not undergo VATS, we included 161 patients with empyema who underwent VATS for empyema. Among them, 100 of 161 (62%) patients met a definite diagnosis of empyema according to the previous RCT.¹³ The patient characteristics are summarized in Table 1 and Supplementary Table S2. Among 161 patients, 40 patients (24.8%) were transferred to other hospitals, one patient (0.6%) died during the hospitalization, and 120 patients (74.5%) were directly discharged home. A total of 130 patients were followed up 30 days after VATS. However, 11 patients failed to attend an outpatient visit, nine were transferred to other hospitals, and 11 were not available for follow-up. Among 130 patients, 12 (9.2%) patients died. The median length of hospital stay was 25 days (interquartile range, 15–35 days).

FIG. 1.

Patient flow.

Table 1.

Patients' Baseline Characteristics

Characteristic	Overall	Patients who were not directly discharged home	Patients who were directly discharged home
Number of patients	161	41 (25.4%)	120 (74.5%)
Death, no.	1 (0.6%)	1 (2.4%)	0 (0%)
30-day death, no. 130/161 patients followed at 30 d after VATS.	12/130 (9.2%)	5/29 (17%)	7/101 (6.9%)
Duration from admission to operation, d	4.0 (2.0–8.0)	4.0 (2.0–7.0)	4.0 (2.0–9.0)
Missing data	8	3	5
Duration from operation to discharge, d	19 (10, 29)	16 (6, 28)	20 (11, 30)
Missing data	8	3	5
Length of stay, day.	25 (15–35)	20 (8–36)	26 (17–35)
Age, y	69 (57, 76)	75 (69, 80)	66 (55, 75)
Male, no.	136 (84%)	34 (83%)	102 (85%)
BMI	22.0 (19.6, 25.5)	21.0 (17.9, 23.4)	22.5 (20.2, 25.8)
Missing data	19	12	7
Actives of daily living at admission
Full support	153 (98%)	37 (97%)	116 (98%)
Independent	1 (0.6%)	0 (0%)	1 (0.8%)
Partial support	2 (1.3%)	1 (2.6%)	1 (0.8%)
Missing data	5	3	2
Charlson comorbidity index
Very high (> 4 points)	11 (7.0%)	3 (7.9%)	8 (6.7%)
High (3, 4 points)	19 (12%)	5 (13%)	14 (12%)
Medium (1, 2 points)	50 (32%)	13 (34%)	37 (31%)
Low (0 point)	77 (49%)	17 (45%)	60 (50%)
Missing data	4	3	1
COPD	11 (7.0%)	2 (5.3%)	9 (7.6%)
Missing data	4	3	1
Diabetes mellitus	21 (13%)	5 (13%)	16 (13%)
Missing data	4	3	1
Chronic kidney disease	2 (1.3%)	2 (5.3%)	0 (0%)
Missing data	4	3	1
Malignancy	17 (11%)	3 (7.9%)	14 (12%)
Missing data	4	3	1
Hugh-Jones classification
0	31 (20%)	16 (42%)	15 (13%)
1	51 (32%)	4 (11%)	47 (39%)
2	24 (15%)	3 (7.9%)	21 (18%)
3	25 (16%)	3 (7.9%)	22 (18%)
4	20 (13%)	9 (24%)	11 (9.2%)
5	6 (3.8%)	3 (7.9%)	3 (2.5%)
Missing data	4	3	1
Altered mental status	15 (9.4%)	8 (21%)	7 (5.8%)
Missing data	4	3	1
Fever	101 (63%)	20 (49%)	81 (68%)
Community-acquired empyema	156 (96.9%)	38 (92.3%)	118 (98.3%)
Purulent pleural effusion	78 (59%)	23 (62%)	55 (57%)
Missing data	28	4	24
Pleural pH	7.54 (7.14–8.00)	7.41 (7.00–8.00)	7.58 (7.36–8.00)
Missing data	38	8	30
Positive culture	47 (38%)	14 (40%)	33 (37%)
Missing data	36	6	30
Albumin within 7 d before operation, g/dL	2.50 (2.10–2.90)	2.10 (1.90–2.50)	2.50 (2.28–3.00)
Missing data	34	10	24
BUN within 7 d before operation, mg/dL	14 (10–19)	16 (11–35)	13 (10–17)
Missing data	25	8	17
C-reactive protein within 7 d before operation, mg/L	20 (10–29)	21 (13–27)	19 (10–29)
Missing data	25	8	17
Pleural thickness of chest CT at admission, cm.	1.58 (0.00–2.23)	1.79 (0.00–2.14)	1.55 (0.00–2.29)
Missing data	6	3	3
Loculation of chest CT at admission	78 (50%)	21 (55%)	57 (49%)
Missing data	6	3	3
Bronchial fistula of chest CT at admission, no.	4 (2.9%)	1 (3.0%)	3 (2.8%)
Missing data	22	8	14
Empyema stage
1	89 (72%)	18 (55%)	71 (79%)
2	52 (4.1%)	3 (9.1%)	2 (2.2%)
3	29 (24%)	12 (36%)	17 (19%)
Missing data	38	8	30

IQR = interquartile range; COPD = chronic obstructive pulmonary disease; CT = computed tomography; BUN = blood urea nitrogen.

Results of statistical analyses

Figure 2 shows the estimated difference in probabilities of direct discharge to home. In our primary analysis, age (>70 years), altered mental status, blood urea nitrogen (BUN; >22.4 mg/dL), and pleural pH (<7.2) were associated with low probabilities of direct discharge to home (age: −24.7%, 95% confidence interval [CI], −37.9% to −11.5%; altered mental status: −32.9%, 95% CI, −59.0% to −6.9%; BUN: −19.4%, 95% CI, −38.9 to −0.02; pleural pH: −17.6%, 95% CI, −35.2 to −0.05). Fever and albumin (>2.7 g/dL) were associated with high probabilities of direct discharge home (fever: 15.2%, 95% CI, 0.8–30.0; albumin: 20.2%, 95% CI, 7.1–32.3). These statistically significant results were consistent with those of the complete case analysis and those of patients with a definite diagnosis of empyema (Fig. 3, Supplementary Figure S1, and Supplementary Figure S2).

FIG. 2.

Difference in predicted probabilities of directly discharge home in main analysis.

FIG. 3.

Difference in predicted probabilities of directly discharge home in sensitivity analysis of complete case analysis.

Table 2 summarizes our secondary analysis. Age (>70 years), altered mental status, purulence, pleural thickness (>2 cm), bronchial fistula, albumin, and C-reactive protein (>20 mg/dL) were associated with longer duration from the day of operation to discharge from hospital (age: 6.2 days, 95% CI, 4.0 days to 8.5 days; altered mental status: 5.6 days, 95% CI, 0.9 days to 10.2 days; purulence: 2.7 days, 95% CI, 0.4 days to 5.1 days; pleural thickness: 5.1 days, 95% CI, 2.3 days to 7.9 days; bronchial fistula: 14.6 days, 95% CI, 4.52 days to 24.6 days; albumin: 3.1 days, 95% CI, 0.6 to 5.7; C-reactive protein: 3.6 days, 95% CI, 1.09 days to 6.0 days). These statistically significant results were consistent with those of the complete case analysis.

Table 2.

Estimated Difference in the Length of Hospital Stay After Surgery

	Average marginal effects (days, 95% CI)
	Main analysis	Sensitivity analysis
Age (>70 y)	6.24 (3.96 to 8.51)	6.01 (1.52 to 10.5)
Charlson comorbidity index (>2 points)	1.23 (−1.98 to 4.44)	0.27 (−0.94 to 1.48)
Duration from diagnosis to surgery (>20 d)	4.81 (−2.21 to 11.8)	4.91 (−6.85 to 16.7)
Altered mental status	5.56 (0.92 to 10.2)	5.40 (−2.38 to 13.2)
Fever	0.50 (−1.83 to 2.85)	0.27 (−4.40 to 4.93)
Community-acquired	0.93 (−7.42 to 9.29)	5.91 (−10.4 to 22.3)
Purulence	2.72 (0.36 to 5.07)	2.17 (−3.17 to 7.50)
pH (< 7.2)	−0.05 (−2.74 to 2.62)	0.13 (−3.17 to 6.21)
Positive culture	1.57 (−0.95 to 4.08)	1.49 (−3.92 to 6.90)
Loculation	−2.31 (−4.60 to −0.02)	−2.30 (−6.89 to 2.27)
Pleural thickness (> 2 cm)	5.09 (2.31 to 7.87)	4.70 (−0.50 to 9.99)
Bronchial fistula	14.6 (4.52 to 24.6)	14.1 (0.35 to 27.8)
Albumin (<2.7 g/dL)	3.14 (0.59 to 5.68)	1.68 (−3.67 to 7.03)
BUN (>22.4 mg/dL)	2.31 (−0.99 to 5.61)	0.94 (−5.18 to 7.05)
C-reactive protein (>20 mg/dL)	3.55 (1.09 to 6.00)	3.37 (−1.39 to 8.13)

CI = confidence interval; BUN = blood urea nitrogen.

Discussion

Summary of findings

To our knowledge, this is the first study to assess patient-oriented prognostic factors among patients with empyema who underwent VATS. It is also novel to broadly assess pre-operative factors including the patient's background, blood test, pleural effusion analysis results, and CT findings. We found that age (>70 years), altered mental status, BUN (>22.4 mg/dL), and pleural pH (<7.2) were associated with low probabilities of direct discharge to home, whereas fever and albumin (>2.7 g/dL) were associated with high probabilities of direct discharge to home. Additionally, age (>70 years), altered mental status, purulence, pleural thickness (>2 cm), bronchial fistula, albumin (<2.7 g/dL), and C-reactive protein (>20 mg/dL) were associated with longer length of stay after surgery.

Implications of the findings

We found that combining pre-operative factors could predict probabilities of not being directly discharged to home for patients with empyema treated with VATS. This information can be used by physicians for shared decision-making about surgery, and to manage patients' expectations. In Japan, some patients, including elderly patients, are discharged to other hospitals rather than being directly discharged to their homes because such patients cannot perform their ADLs at home.²² Indeed, it is shown in Supplementary Table S3 that patients who were not directly discharged to their homes exhibited lower ADL scores. Anticipating not being directly discharged to their home may help patients and families prepare for their home-life situation.

Relation to previous studies

No studies have reported the probabilities of direct discharge home among patients with empyema who undergo surgical treatment, although the prognosis was similar to cardiac surgery. As reported in previous studies,^23–26 20% to 50% of the patients could not be discharged directly to home after cardiac surgery, whereas this number was 25.4% in our study. Both patients have similar probabilities of direct discharge to home.

Numerous studies have investigated prognostic factors for patients with empyema without surgical treatment, and our findings were consistent with them. Age, BUN, and albumin were included in the RAPID (Renal [urea], Age, fluid Purulence, Infection source, Dietary [albumin]) score, which predicted high mortality rates in patients with empyema.¹¹ Pleural fluid pH (<7.2) was also associated with poor outcomes in patients with empyema.²⁷ However, some of our findings contradicted those of previous studies. Although purulence was not a predictor of poor outcomes in the previous study,¹¹ it was not a significant predictor in our study. This might be explained by the differences in the background of patients such as age and surgical intervention. Additionally, in that study, fever was reported as a predictor of poor outcomes¹⁵; in our study it was a predictor of good outcomes. This might be because patients with fever often seek medical treatment earlier than those without fever, as in our study, 61 of 101 patients with fever met the criteria for definite empyema.¹³ Unsurprisingly, elderly age, altered mental status, and BUN were common with the widely used CURB-65 and Pneumonia Severity Score, predictive of mortality of community-acquired pneumonia.^28,29

As for CT findings, bronchial fistula and pleural thickness on CT scans were associated with high probabilities of longer stays after VATS. Bronchopleural fistula and pleural thickness require more invasive VATS surgery, leading to post-operative complications such as prolonged air leaks.³⁰ Computed tomography scans are usually taken before surgery and physicians can make use of these findings to predict the patient's prognosis.

Limitations

Our study has several limitations. First, there might be measurement errors in exposure variables. Second, there was missing data: pleural culture was missing in 23% of the cases, pleural pH missing in 22% of the cases, and albumin on blood test missing in 21% of the cases. We imputed missing values using multiple imputation. We conducted a sensitivity analysis using complete case analysis, which showed robustness of the results. Third, there is a possibility of bias due to the low number of participants with an average inclusion of approximately two patients per year and per facility. Fourth, variations in discharge criteria among participating facilities may have influenced the length of stay. Fifth, some patients were not followed up 30 days after VATS. This could preclude our ability to determine 30-day mortality after VATS. Sixth, we did not have information on tube drainage and intrapleural treatment of fibrinolytics. These treatments encompassed both pre-surgical management, and post-surgical management, including the duration of tube drainage, which might impact the invasiveness of VATS and mobilization after VATS. Additionally, the potential variability in prognostic factors due to differences in treatment methods necessitates to be validated in other studies.

Conclusions

Our study showed that pre-operative factors might predict the probabilities of not being directly discharged home. Physicians may consider using the prognostic factors in our study for predicting non-direct discharge to home for patients with empyema treated with VATS. Further research is needed to validate these prognostic factors.

Footnotes

Authors' Contributions

Shiroshita, Kimura, Shirakawa, Cong, H. Suzuki, Anan, Sato, Nakashima, Takeshita, Okuno, Nitawaki, and Kataoka contributed to the conception and design of the study. Shiroshita, Kimura, Yamada, Shirakawa, Cong, H. Suzuki, Anan, Sato, Nakashima, Takeshita, Okuno, Nitawaki, and J. Suziki collected data. Shiroshita, Kimura, Shirakawa, Cong, H. Suzuki, Anan, Sato, Nakashima, Takeshita, Okuno, Nitawaki, Hiroyuki S, Igei, J. Suziki, Tomii, Ohgiya, and Kataoka contributed to the study interpretation. Shiroshita, Kimura, Shirakawa, and Cong manipulated the database and performed the data analysis. All authors confirmed the validity of the data analysis and contributed to the interpretation. Shiroshita, Kimura, Yamada, Hiroyuki S, and Kataoka drafted the manuscript. All authors critically revised the manuscript and approved the final version of the manuscript. All authors agreed to be accountable for all aspects of the work.

Data Availability

The data underlying this article cannot be shared publicly because of the privacy of individuals that participated in the study. The data will be shared on reasonable request to the corresponding author.

Funding Information

This work was supported by Ichinomiyanishi Hospital and Southern Tohoku Hospital. The English editing and literature ordering fees were supported by Kobe City Medical Center General Hospital (profit organization, funding number: none). Costs for data export and preservation were supported by Southern Tohoku Hospital (profit organization, funding number: none). The funders played no role in the study design, study execution, data analyses, data interpretation, or decision to submit the results.

Author Disclosure Statement

Chigusa Shirakawa received financial support for this study from Kobe City Medical Center General Hospital and Southern Tohoku Hospital. Akihiro Shiroshita received financial support for his doctoral study from Vanderbilt University and Fulbright Association. No other authors have no conflict of interest.

Supplementary Material

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