|Year : 2017 | Volume
| Issue : 1 | Page : 7-16
Ultrasound assessment of antibiotic-induced pulmonary reaeration in ventilator-associated pneumonia
Amer A El-Moursi1, Bassem N Beshey1, Noha M Abdel Rahman MSc 2
1 Department of Critical Care Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt
2 Department of Critical Care Medicine, Faculty of Medicine, Alexandria University; Department of Critical Care Medicine, Ministry of Health Hospitals, Alexandria, Egypt
|Date of Submission||18-Jan-2016|
|Date of Acceptance||24-May-2016|
|Date of Web Publication||22-Mar-2017|
Noha M Abdel Rahman
Department of Critical Care Medicine, Faculty of Medicine, Alexandria University, Alexandria, PC 21500
Source of Support: None, Conflict of Interest: None
In this study we assessed lung reaeration by means of bedside chest radiography, lung computed tomography (CT), and lung ultrasound (LUS) in patients with ventilator-associated pneumonia (VAP) treated by antibiotics.
VAP is a subtype of hospital-acquired pneumonia that occurs in patients under mechanical ventilation for at least 48 h and is characterized by the presence of a new or progressive infiltrate, signs of systemic infection (temperature, blood cell count), changes in sputum characteristics, and detection of the causative agent. Ultrasound examination is increasingly being used as a valuable bedside method for the diagnosis of various thoracic conditions in ICUs, including pleural or pericardial effusion, empyema, pneumothorax, pulmonary embolism, and pneumonia. To date, only a few studies have investigated the use of LUS in the diagnosis of pneumonia in the emergency department or in the ICU. In critically ill patients with acute lung injury, pulmonary aeration may be reliably assessed using bedside LUS.
This is a randomized prospective comparative trial.
The study was conducted in the Critical Care Department of Alexandria Main University Hospital.
Patients and methods
This study was carried out on 60 patients with a preliminary diagnosis of VAP who matched the inclusion and exclusion criteria in the Critical Care Medicine Department in Alexandria University. In all patients chest ultrasound (US),chest radiography, and chest CT (the gold standard) were performed in sequence at day 0 and day 7 after antibiotic administration. Thereafter, all patients were categorized on the basis of the radiological findings and finally the effectiveness of each method was calculated and statistical comparisons were made.
In our study, we compared lung reaeration by bedside chest radiography, lung CT, and LUS in patients with VAP treated with antibiotics. We included 60 patients with a preliminary diagnosis of VAP (33.3% were male and 16.7% were female); their ages ranged between 31 and 70 years (mean±SD: 48.3±11.063 years). In our study, we found a highly significant correlation between LUS score and CT reaeration findings (P<0.001). US scores showed that 40 (95.2%) patients were truly reaerated, compared with two (4.8%) cases that were missed as their scores ranged between −10 and 5 (region of interest of no changes), with US scores ranging between 3 and 25 (mean±SD: 15.90±5.86 and median: 16). Moreover, 12 (66.7%) patients were accurately diagnosed by US as lost aeration compared with six (33.3%) cases that were missed as their scores ranged between −10 and 5 (region of interest of no changes) with US scores ranging between −20.0 and 1.0 (mean±SD: −10.89±7.53 and median: −12). Among those who showed no progression (i.e. improvement or no change) on chest radiography, 18 patients had LUS score above 5, one patient had LUS score between −10 and 5, and three patients had LUS score less than −10. Thus, there was no significant correlation between LUS score and chest radiographic progression.
This study can affirm the superiority of chest US over chest radiographs for quantifying lung reaeration in patients with VAP who are successfully treated with antibiotics. LUS is a reliable, dynamic, rapid, noninvasive, bedside technique. Thus, considering the benefits of chest US versus the multiple drawbacks of chest CT, such as the requirement for a special request, the dose of radiation, and the major problem of patient transfer, chest US can be reported to be a reasonable substitute, allowing the early detection of antibiotic-induced lung reaeration or the extension of lung infection in cases of antimicrobial therapy failure. Ultrasound can be considered a reasonable bedside ‘gold standard’ in the critically ill.
Keywords: air bronchogram, chest radiograph, computed tomography, lung reaeration, lung ultrasound, lung ultrasound score, ventilator-associated pneumonia
|How to cite this article:|
El-Moursi AA, Beshey BN, Abdel Rahman NM. Ultrasound assessment of antibiotic-induced pulmonary reaeration in ventilator-associated pneumonia. Res Opin Anesth Intensive Care 2017;4:7-16
|How to cite this URL:|
El-Moursi AA, Beshey BN, Abdel Rahman NM. Ultrasound assessment of antibiotic-induced pulmonary reaeration in ventilator-associated pneumonia. Res Opin Anesth Intensive Care [serial online] 2017 [cited 2020 May 31];4:7-16. Available from: http://www.roaic.eg.net/text.asp?2017/4/1/7/202699
| Introduction|| |
Pneumonia can be generally defined as inflammation of the lung parenchyma, in which consolidation of the affected part and a filling of the alveolar air spaces with exudate, inflammatory cells, and fibrin is characteristic. Infection by bacteria or viruses is the most common cause, although inhalation of chemicals, trauma to the chest wall, or infection by other infectious agents such as Rickettsiae, fungi, and yeasts may occur. In adults, bacteria are the most common cause of pneumonia ,,.
Pneumonia is generally classified as:
- Community-acquired pneumonia (CAP): defined as pneumonia that develops in the outpatient setting or within 48 h of admission to a hospital .
- Healthcare-associated pneumonia (HCAP): defined as pneumonia that develops in the outpatient setting or within 48 h of admission to a hospital in patients with increased risk for exposure to multidrug-resistant (MDR) bacteria as a cause of infection. Risk factors for HCAP include the following :
- Hospitalization for 2 or more days in an acute care facility within 90 days of current illness.
- Exposure to antibiotics, chemotherapy, or wound care within 30 days of current illness.
- Residence in a nursing home or long-term care facility.
- Hemodialysis at a hospital or clinic (chronic dialysis).
- Home nursing care (infusion therapy, wound care) contact.
- Hospital-acquired pneumonia (HAP): defined as pneumonia that develops at least 48 h after admission to a hospital and, as in HCAP, is characterized by an increased risk of exposure to MDR organisms as well as Gram-negative organisms . Risk factors for exposure to such organisms in HAP include the following :
- Antibiotic therapy within 90 days of the hospital-acquired infection.
- Current length of hospitalization of 5 days or more.
- High frequency of antibiotic resistance in the local community or within the specific hospital unit.
- Immunosuppressive disease or therapy.
- Presence of HCAP risk factors for exposure to MDR bacteria.
- Aspiration pneumonia develops after the inhalation of oropharyngeal secretions and colonized organisms .
- Nosocomial pneumonia is generally described as that acquired in the hospital setting. The term nosocomial pneumonia has evolved into the more succinct clinical entities of HAP and ventilator-associated pneumonia (VAP) .
Eighty-six percent of nosocomial pneumonias are associated with mechanical ventilation and are termed VAP. Between 250 000 and 300 000 cases per year occur in the USA alone, which is an incidence rate of 5–10 cases per 1000 hospital admissions ,.
A diagnosis of VAP is made when the patient has a new diagnosis of pneumonia after initiation of mechanical ventilation. VAP should be suspected in any person on mechanical ventilation exhibiting increasing numbers of white blood cells on blood testing, and new shadows (infiltrates) on a chest radiograph indicative of pneumonia. Blood cultures may reveal the microorganisms causing VAP. Thus, the diagnosis of VAP is established on the basis of two criteria:
- A clinical pulmonary infection score of 6 :
This is a score developed to establish a numerical value for clinical, radiographic, and laboratory markers of pneumonia. Scores above 6 suggest pneumonia [Table 1] .
- A positive lower respiratory tract specimen obtain from a unprotected bronchoalveolar lavage (BAL) or a protected mini-bronchoalveolar lavage (mini-BAL) . A positive sample is defined as 104 colony-forming units/ml for unprotected BAL and 103 colony-forming units/ml for protected mini-BAL ,,.
Ultrasound(US) results depend on the operator’s training and experience. The period of training is shorter when the operator aims at mastering limited and focused studies .
US has been used in a wide variety of specialties and has increased in use in the last decade as US machines have become more compact and portable . Chest US has only recently been appreciated by the greater medical community , because for a long time US was considered to be unfit for assessing the pulmonary parenchyma .
In critically ill patients with acute lung injury, pulmonary aeration may be reliably assessed using bedside lung ultrasound (LUS) .
Normal aeration is detected as the visualization of the pleural line with its characteristic lung sliding and artifactual horizontal A-lines . Pulmonary interstitial syndrome, which induces a moderate decrease in lung aeration caused by the thickening of the interlobular septa, is detected as multiple and regularly spaced vertical B-lines (comet tails), at least 7 mm apart . Alveolar interstitial edema resulting from the eruption of liquid within the alveolar space corresponds to the computed tomography (CT) entity of ground glass and is detected as abutting comet tails 3 mm apart . Lung consolidation appears as a tissue structure whose dimensions do not vary with respiratory movements and which contains white points characterized by an inspiratory reinforcement, corresponding to persisting aeration of distal bronchioles .
CT is the reference method for measuring lung aeration and its variations ,. CT requires the transportation of the patient outside the ICU  and exposes the patient to high radiation exposure , two limitations that preclude the routine use of CT in clinical practice. In addition, quantitative analysis of lung aeration is time-consuming and requires much training. As different US patterns correspond to different degrees of aeration loss, therapeutic interventions aimed at increasing lung aeration, such as positive end-expiratory pressure or antimicrobial therapy for treating VAP, should result in LUS changes. If the whole lung is examined, LUS might be accurate enough to quantify lung reaeration.
| Aim|| |
The aim of this work is to compare lung reaeration by bedside chest radiography, lung CT, and LUS in patients with VAP treated with antibiotics.
| Patients and methods|| |
This study was carried on 60 patients with a preliminary diagnosis of VAP who matched the inclusion and exclusion criteria in the Critical Care Medicine Department in Alexandria University. In all patients chest US,chest radiography, and chest CT (the gold standard) were performed in sequence on day 0 and day 7 after antibiotic administration. Thereafter, all patients were categorized on the basis of the radiological findings and finally the effectiveness of each method was calculated and statistical comparisons were made. Informed consent was taken from first degree relative of every patient included in the study. This study was approved from the Ethical Committee of Alexandria faculty of medicine.
Lung parenchyma was divided into 12 regions by cephalocaudal midclavicular and transversal hilar lines. Lung aeration was assessed by comparing the extension of consolidation and alveolar interstitial syndrome on days 0 and 7. An US lung reaeration score was calculated from changes in the US pattern of each region (12 regions) of interest between day 0 and day 7 either by two different investigators blinded to each other’s evaluations and to CT and chest radiography or by the same investigator twice at different time intervals.
Four US patterns were defined:
- Normal aeration (no bronchopneumonia): presence of lung sliding with A-lines and, occasionally, an isolated B-line 
- Loss of lung aeration resulting from scattered foci of bronchopneumonia or interstitial pneumonia: presence of multiple well-defined and irregularly spaced US lung ‘comets’ issued from the pleural line or a small subpleural consolidation.
- Loss of lung aeration resulting from confluent bronchopneumonia: multiple abutting US lung comets issued from the pleural line or a small subpleural consolidation.
- Lung consolidation characterizing extensive bronchopneumonia: presence of a tissue pattern  containing hyperechoic punctiform images representative of air bronchograms  ([Table 2]).
|Table 2 Lung ultrasound reaeration score aimed at evaluating the effects of antibiotics on lung aeration|
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An USscore of more than 5 was associated with a successful antimicrobial therapy to treat lung infection. An US score of less than −10 was associated with a failure of antibiotics to treat lung infection. A highly significant correlation was found between CT and US lung reaeration. LUS score was less effective in detecting smaller changes in lung aeration; chest radiography was also inaccurate in predicting lung reaeration.
The data were analyzed statistically using statistical package for the social sciences (SPSS, version 17; SPSS Inc., Chicago, Illinois, USA). Means and SDs were used to describe data distribution. ANOVA or F-test was performed for comparison of more than 2 means. Least significant difference was basically a t-test, used only when the F value was significant to detect the presence of significance between two groups. The test was considered significant if the P value was less than 0.05.
| Results|| |
Air bronchogram by chest ultrasound
[Table 3] shows the results of the chest US for air bronchogram before and after antibiotic administration. Before antibiotic administration 31 (51.7%) patients had a dynamic air bronchogram and 29 (48.3%) patients had a static air bronchogram. After treatment, in 19 (31.7%) patients the air bronchogram disappeared and resolved (totally reaerated); in 23 (38.3%) patients the air bronchogram became dynamic after being static (partially reaerated); and in 18 (30%) patients the air bronchogram was static: in the latter case, in 12 patients the dynamic air bronchogram became static and in six patients the static air bronchogram remained static. The P value was less than 0.001, which means that the air bronchogram was significant for assessing lung reaeration by US before and after antibiotic administration ([Table 3] and [Figure 1]).
|Table 3 Comparison of air bronchogram results on chest ultrasound before and after antibiotic administration|
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|Figure 1 Comparison of air bronchogram results on ultrasound before and after antibiotic administration.|
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[Table 4] and [Figure 2] show the correlation between chest reaeration CT and progression of chest radiography findings, using CT as the gold standard in the assessment of lung reaeration after antibiotic administration. Radiographic findings showed that 18 (42.9%) patients were truly reaerated and their condition improved compared with 24 (57.1%) patients who were missed and who showed progression and deterioration. Moreover, four (22.3%) patients were wrongly considered on radiograph as having improved, whereas 14 (77.7%) patients were accurately diagnosed as having deteriorated. These results had a P value of 0.129. Thus, these differences showed that there was no significant correlation between progression of chest radiography findings and chest CT findings.
|Table 4 Distribution of lung reaeration diagnosed using progression of chest radiography findings in relation to results revealed by computed tomography|
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|Figure 2 Distribution of lung reaeration on progression of chest radiography in relation to computed tomography.|
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[Table 5] and [Figure 3] show the correlation between LUS score and CT reaeration findings, using CT as the gold standard for assessment of lung reaeration. US scores showed that 40 (95.2%) patients were truly reaerated compared with two (4.8%) patients who were missed as their scores ranged between −10 and 5 (region of interest of no changes) with US scores ranging between 3 and 25 (mean±SD: 15.90±5.86 and median: 16). Moreover, 12 (66.7%) patients were accurately diagnosed by US as having lost aeration compared with six (33.3%) patients who were missed as their scores ranged between −10 and 5 (region of interest of no changes) with US scores ranging between −20.0 and 1.0 (mean±SD: −10.89±7.53 and median: −12). This is accompanied by a P value of less than 0.001. These differences showed that there is a highly significant correlation between LUS score and CT reaeration findings.
|Table 5 Distribution of lug reaeration using lung ultrasound score findings in relation to results revealed by computed tomography|
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|Figure 3 Distribution of lung reaeration on lung ultrasound in relation to computed tomography.|
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[Table 6] shows the relation between air bronchogram and chest CT findings by US. Nineteen (45.2%) patients had a resolved air bronchogram (totally reaerated) and 23 (54.8%) patients had a dynamic air bronchogram (partially reaerated) out of 42 patients who showed reaeration on CT. Eighteen (100%) patients had a static air bronchogram, similar to that of CT cases with no reaeration. The P value was less than 0.001, which indicated significant correlation between air bronchogram and CT for assessment of lung reaeration ([Figure 4]).
|Table 6 Relation between computed tomography chest findings and air bronchogram by ultrasound after antibiotic administration|
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|Figure 4 Relation between chest computed tomography findings and air bronchogram detected by ultrasound after antibiotic administration.|
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[Table 7] and [Figure 5] show the relation between LUS score and progression of chest radiography. LUS scores showed that 18 (81.8%) patients were truly reaerated compared with four (18.2%) patients who were missed, with scores ranging between −15 and 25 (mean±SD: 12.32±11.84 and median: 18). Moreover, the condition of nine (23.7%) patients deteriorated compared with 29 (76.3%) patients who were missed, with scores ranging between −20 and 25 (mean±SD: 5.29±14.51 and median: 11). These differences were negative with no significant correlation between LUS score and progression of chest radiographic findings.
|Table 7 Distribution of lung reaeration diagnosed using lung ultrasound score in relation to results revealed by progression of chest radiography findings|
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|Figure 5 Distribution of lung reaeration on lung ultrasound in relation to progression of chest radiography findings.|
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[Table 8] shows that there was negative but no significant correlation between LUS score and CT and chest radiographic findings and a positive and highly significant correlation between CT and LUS score ([Table 7] and [Figure 6],[Figure 7],[Figure 8]).
|Table 8 Correlation between lung ultrasound, progression of chest radiograph, and computed tomography|
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|Figure 6 Correlation between computed tomography (CT) and lung ultrasound.|
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|Figure 7 Correlation between lung ultrasound and progression of chest radiography.|
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|Figure 8 Correlation between computed tomography (CT) and progression of chest radiography.|
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[Table 9] and [Figure 9] show the agreement (sensitivity, specificity, and accuracy) of US score and progression on chest radiography with chest CT findings in the assessment of pulmonary reaeration in VAP after antibiotic administration. The receiver operating characteristic curve for chest US and chest radiograph with CT was 1.000 for US assessment (P<0.001) and 0.603 for chest radiograph (P=0.208). For US scores, when cutoff points for scores were more than 1 and less than or equal to 1, sensitivity was 100%, specificity was 100%, positive predictive value (PPV) was 100.0%, negative predictive value (NPV) was 100%, and accuracy was 100.0%. In comparison with chest radiographic progression, sensitivity was 42.86%, specificity was 77.78%, PPV was 36.84%, NPV was 81.82%, and accuracy was 53.33%.
|Table 9 Agreement (sensitivity, specificity, and accuracy) for lung ultrasound score and chest radiograph progression with computed tomography reaeration|
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[Table 10] shows the agreement (sensitivity, specificity, and accuracy) of US score and progression on chest radiograph with chest CT in the assessment of pulmonary reaeration in VAP after antibiotic administration. For US scores, when the cutoff point was more than 5 and less than 5, sensitivity was 95.24%, specificity was 100%, PPV was 90.0%, NPV was 100%, and accuracy was 96.67% and when he cutoff point was less than −10 and more than −10, sensitivity was 100%, specificity was 66.67%, PPV was 100.0%, NPV was 87.50%, and accuracy was 90.0%. In comparison with chest radiographic progression, sensitivity was 42.86%, specificity was 77.78%, PPV was 36.84%, NPV was 81.82%, and accuracy was 53.33%.
|Table 10 Agreement (sensitivity, specificity, and accuracy) for lung ultrasound score with computed tomography chest|
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| Discussion|| |
The present study was designed to assess lung reaeration induced by antibiotics using US scores and compare it with CT (gold standard) and chest radiograph.
The sensitivity, specificity, and accuracy of LUS versus CT when the cutoff point was more than 5 and less than 5 were 95.24, 100, and 96.67% and when the cutoff point was less than −10 and more than −10 was 100, 66.67, and 90.0%.
In a recent multicenter research, Reissig et al.  reported that US had 93.4% sensitivity and 97.7% specificity for diagnosis of VAP, and 86.7% of VAP patients had an air bronchogram. Consolidation is a common US finding in VAP, but is not always present. Several reports have demonstrated that an interstitial pattern (B line) on US is indicative of VAP ,, and patients with this change may have diffuse ground glass opacification on CT. The B-line correlated with interstitial edema and may be focal (pneumonia, lung contusion) or diffuse (acute respiratory distress syndrome, cardiogenic pulmonary edema). Cortellaro et al.  reported that 49% of VAP patients could have an interstitial pattern, and most of the interstitial patterns were near the lesion. In this study, focal interstitial pattern and consolidation had 38.4 and 71.4% sensitivity for diagnosis of VAP, respectively. Some VAP cases may be interstitial pneumonia, which shows diffuse ground glass opacification on CT.
Similarly, a study performed by Lichtenstein and Mezière  found the sensitivity of US to detect consolidation to be 90% and specificity to be 98%.
Kakouros and Kakouros  found that air bronchograms are frequently seen in patients with acute respiratory distress syndrome.
Another study by Lichtenstein et al.  indicated that chest US consolidation is a nonspecific sign of VAP because it is also present in lung atelectasis, and differential diagnosis could be difficult. The US sign that differentiates pneumonia from obstructive atelectasis is the presence of a dynamic air bronchogram in the former case (specificity 94% and PPV 97%). The possibility of a dynamic evaluation gives US an advantage over chest radiography, and possibly also over a CT scan, which cannot always clearly differentiate the two conditions ,.
Lichtenstein et al.  documented 74, 77, and 73% concordance for the detection of alveolar interstitial syndrome, alveolar consolidation, and pleural effusion, respectively, between two physicians with similar experience. They stated that bedside chest radiography had a diagnostic accuracy of 47% for pleural effusion, 75% for alveolar consolidation, and 72% for alveolar interstitial syndrome, whereas chest US had a diagnostic accuracy of 93% for pleural effusion, 97% for alveolar consolidation, and 95% for alveolar interstitial syndrome. They eventually concluded that chest US is better than auscultation and bedside chest radiography for diagnosing pleural effusion, alveolar consolidation, and alveolar interstitial syndrome and for assessing the extent of lung injury. Bedsides,chest radiography was a poor predictor of the extent of lung injury compared with chest US.
Vitturi et al.  showed the total concordance of chest US in comparison with chest CT for diagnosing consolidation, pneumothorax, pulmonary edema, and pleural effusion to be 96.7, 98.9, 97.8, and 97.8%, respectively. Thus, considering the benefits of chest US versus the multiple drawbacks of chest CT, such as the need for a special request, the dose of radiation, and the major problem of patient transfer, chest US can be taken as a reasonable substitution.
Recently, Lichtenstein  reported that all of the four major pulmonary pathologies found using CT as the ‘gold standard’ were diagnosed by chest US with sensitivity and specificity ranging from 90 to 100%, allowing US to be considered a reasonable bedside ‘gold standard’ in the critically ill.
Peris et al.  addressed the effectiveness of bedside US in the ICU setting as an alternative to chest radiographs and CT scans. After the introduction of routine chest US in their ICU, they found a significant decrease in the number of chest radiographs (26%) and CT scans (47%) performed, with no significant adverse changes in patient mortality.
Thus, from our study we found a negative but not significant correlation between LUS score and chest radiographic progression and CT. However, there is a positive and highly significant correlation between CT and LUS score.
| Conclusion|| |
The chest US is superior to chest radiographs for quantifying lung reaeration in patients with VAP who are successfully treated with antibiotics as well as in the case of unstable patients for whom CT chest has to be delayed for 1 or 2 days because their transfer poses considerable risk.
For obese patients visualization of lung parenchyma might be difficult. Thoracic US is an operator-dependent technology. Focused, supervised training is needed to ensure that the operator correctly interprets the sonographic findings. Because the same probe serves multiple patients, it can be the vector of or disseminate resistant pathogens in the ICU and imposes special decontamination procedures. These limitations should be balanced against the benefits of LUS, which has a direct diagnostic and therapeutic impact for critically ill patients.
LUS appears to be an accurate diagnostic tool for assessing the respiratory effects of antimicrobial therapy in patients with VAP. As US is noninvasive and easily repeatable at the bedside, it allows the early detection of antibiotic-induced lung reaeration or the extension of lung infection in cases of antimicrobial therapy failure. This study concludes that US can be considered a reasonable bedside ‘gold standard’ in the critically ill.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10]