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(Chest. 2005;127:2064-2071.)
© 2005 American College of Chest Physicians

Zinc Chloride (Smoke Bomb) Inhalation Lung Injury*

Clinical Presentations, High-Resolution CT Findings, and Pulmonary Function Test Results

Hsian-He Hsu, MD; Ching Tzao, MD, PhD; Wei-Chou Chang, MD; Chin-Pyng Wu, MD, PhD; Ho-Jui Tung, PhD; Cheng-Yu Chen, MD and Wann-Cherng Perng, MD

* From the Department of Radiology (Drs. Hsu, Chang, and Chen), the Department of Surgery (Dr. Tzao), Division of Thoracic Surgery, the Department of Internal Medicine (Drs. Wu and Perng), Division of Pulmonary and Critical Care Medicine, and the Department of Humanity and Social Studies (Dr. Tung), Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China.

Correspondence to: Wann-Cherng Perng, MD, Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, Tri-Service General Hospital, 325, Section 2, Nei Hu, Cheng Kung Rd, Taipei, Taiwan 114, ROC; e-mail: wperng{at}ms27.hinet.net


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Zinc chloride smoke inhalation injury (ZCSII) is uncommon and has been rarely described in previous studies. We hypothesized that structural changes of the lung might correlate with pulmonary function. To answer this question, we correlated findings from high-resolution CT (HRCT) scan and the results of pulmonary function tests (PFTs) in patients with ZCSII.

Design: Retrospective cohort study.

Setting: University hospital.

Patients: Twenty patients who had been hospitalized with ZCSII-related conditions.

Measurements: The study included HRCT scan scores (0 to 100), static and dynamic lung volumes, and diffusing capacity of the lung for carbon monoxide (DLCO).

Results: HRCT scans and PFTs were performed initially after injury (range, 3 to 21 days) in all patients and during the follow-up period (range, 27 to 66 days) in 10 patients. The predominant CT scan findings were patchy or diffuse ground-glass opacities with or without consolidation. The majority of patients showed a significant reduction of FVC, FEV1, total lung capacity, and DLCO, but normal FEV1/FVC ratio values. Changes of functional parameters correlated well with HRCT scan scores. Substantial improvements in CT scan abnormalities and pulmonary function were observed at follow-up.

Conclusions: The majority of our patients with ZCSII presented with a predominant parenchymal injury of the lung that was consistent with a restrictive type of functional impairment and a reduction in DLCO rather than with obstructive disease. Our results suggest that HRCT scanning and pulmonary function testing may reliably predict the severity of ZCSII.

Key Words: ARDS • high-resolution CT • pulmonary function tests • zinc chloride smoke inhalation injury


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Zinc chloride (smoke bomb) fumes have been widely used as an obscurant in both military training and on the battlefield. A common method of generating this smoke is by the production of zinc chloride aerosol from a pyrotechnic mixture containing zinc oxide and a chlorine donor such as hexachloroethane.123456789 Lung injury after exposure is primarily attributed to the inhalation of zinc chloride fumes, which is the main toxic factor and can rapidly cause respiratory mucosal damage. Substantial inhalation results in cough, hoarseness, chest tightness, tachypnea, dyspnea, and fever.1234567 Exposure to high concentrations, especially in a confined space, may produce ARDS and possibly death.12345 The pathologic changes include pulmonary edema, pneumonitis, alveolar obliteration, diffuse alveolar damage, and pulmonary fibrosis.1234

The clinical, radiographic, pathologic, and other investigative findings in victims exposed to this smoke have been described previously in anecdotal reports.12345678910 To date, the description of chest radiographic findings has been limited to a small number of cases.234567910 There has been only one case report5 describing CT scan findings in a severe case of zinc chloride smoke inhalation injury (ZCSII), which showed diffuse pulmonary infiltrates, subcutaneous emphysema, and pneumomediastinum. To our knowledge, the spectrum of CT scan abnormalities in ZCSII, and the relationship between functional impairment and CT scan findings have not yet been reported. Moreover, there is a lack of description of the CT scan changes during the initial stage of injury and at the follow-up. We performed a retrospective investigation to determine whether the CT scan findings may correlate with the results of pulmonary function tests (PFTs) in a relatively large number of patients with ZCSII.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
Twenty soldiers who had been exposed to zinc chloride smoke following an accidental smoke bomb explosion during a combat exercise on December 2, 2003, were the subject of this retrospective study. They were exposed for 5 to 10 min to dense fumes without mask protection in the confined space of a tunnel. Supplemental oxygen was given through a nasal cannula when hypoxemia was noted. Six patients were admitted to the ICU when respiratory failure developed for 1 to 3 days (mean [± SD] duration, 2.17 ± 0.75 days). As part of their initial evaluation, high-resolution CT (HRCT) scans and PFTs were performed. Follow-up was provided primarily in an outpatient setting. Among them, 10 patients underwent repeat HRCT scans and PFTs due to varying degrees of residual respiratory symptoms.

CT Scan Evaluation
As part of the evaluation for the extent of lung injury, an HRCT scan (Somatom Plus 4 CT scanner; Siemens; Erlangen, Germany) of the chest was performed in all patients. The scans were obtained at 10-mm intervals throughout the chest using 2-mm collimation and were reconstructed with a high-spatial-frequency algorithm. The images were photographed at window settings appropriate for the assessment of the lung parenchyma (window level, –600 to –700 Hounsfield units; window width, 950 to 1,500 Hounsfield units). The HRCT scans were obtained with the patients in the supine position. Where necessary, a limited number of sections was obtained with the patient in the prone position to clarify the effects of gravity on areas of increased attenuation in the dependent parts of the lung.

HRCT Scan Evaluation and Scoring
The HRCT scans were retrospectively reviewed by two independent observers (H.H.H. and W.C.C.) who were not aware of clinical information or the results of PFTs. Each individual section on the HRCT scan images was assessed for the patterns, distribution, and extent of the following pulmonary abnormalities: (1) ground-glass opacity (GGO), which was defined as areas of hazy increased attenuation without obscuration of the underlying vascular and bronchial markings; (2) airspace consolidation, which was defined as a homogeneous increase in lung attenuation that obscured the underlying vessels and bronchial walls; and (3) areas of linear opacity, which included interlobular septal lines and intralobular interstitial thickening. Other associated findings, in particular the presence of pleural effusion, pneumothorax, and pneumomediastinum, were also assessed. The distribution of each finding was classified as follows: predominantly in the upper, middle, or lower lung zone, or random; and patchy, diffuse, or random.

Employing a scoring system similar to the one described by Hsu et al,11 the extent of pulmonary abnormalities was assessed for each of the three lung zones that corresponded to approximately one third of the images from the lung apex to 1 cm below the domes of the diaphragm. The HRCT scan score in the upper, middle, and lower lung zones was determined by visually estimating the extent of injury in each zone. The score represented the percentage of lung parenchyma that showed evidence of abnormalities and was estimated to the nearest 5% of parenchymal involvement. The overall percentage of involvement was calculated by averaging the six lung zones by each individual observer. The reproducibility or intraobserver variability of HRCT scan scoring was determined by correlating readings for the same images on two occasions 1 week apart by each individual observer. Final scores were determined by an average of scores assessed by two observers with a difference within 5%. Reading was repeated when the differences of scores between two observers exceeded 5% until a consensus was reached.

Pulmonary Function Testing
PFTs were undertaken to determine the degree of functional impairment and were performed in our pulmonary function laboratory using standard procedures.12 Spirometry and lung volumes were measured with a spirometer (Bodyscreen II-Bodybox; Jaeger; Wurzburg, Germany) using specific software (MasterLab ML3 software; Jaeger). All spirometric values were expressed as a percentage of the predicted values, and the predicted values for all parameters were obtained from the prediction equation for the Chinese population.13 The diffusing capacity of the lung for carbon monoxide (DLCO) was determined by the single-breath carbon monoxide technique using an infrared analyzer (model 66200; SensorMedics; Yorba Linda, CA). The results of PFTs are represented as the mean ± SD.

Statistical Analysis
The Pearson correlation was used to correlate HRCT scores and measured functional parameters. Comparison between the results of the initial and follow-up PFTs was made by one-way analysis of variance with significant difference considered when the p value was < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Clinical information and initial HRCT scan findings in the 20 patients with ZCSII are summarized in Table 1 . Briefly, all patients presented to our emergency department with nausea, sore throat, paroxysmal cough, varying degrees of shortness of breath, and chest tightness when admitted. Their pulse rates ranged from 80 to 130 beats/min with the majority being > 100 beats/min. Respiratory rates rose from 24 to 30 breaths/min in almost all patients. Body temperatures were essentially normal, except that two patients had fevers with temperatures up to 38.4°C and 40.3°C. The majority of our patients showed bilateral areas of diffuse or patchy GGO with or without consolidations on chest radiographs initially after injury. In general, these radiographic abnormalities resolved substantially with supportive treatment within 1 month after hospital admission except for those patients who developed ARDS. The total number of hospital days ranged from 12 to 178 days (mean [± SD], 61.8 ± 35.2 days). The median time between exposure to this smoke and the initial CT scans and PFTs was 4 days (range, 3 to 21 days). The results of follow-up CT scans and PFTs were available in 10 patients, with an interval of 27 to 66 days (mean, 43 days) after the initial studies had been performed.


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  		Table 1. Clinical Data and Information of Initial HRCT of 20 Patients With Zinc Chloride Smoke Inhalation Injury*

 
Initial and Follow-up CT Scan Findings
Bilateral areas of GGO were the most extensive abnormality found on initial CT scans and were observed in all patients (Fig 1 ). Bilateral patchy areas of airspace consolidation, which were always present in combination with areas of GGO, were observed in 11 patients (55%). Patchy areas of consolidation were more common in the posterior regions. Other findings included thickening of interlobular septa (n = 4; 20%) and intralobular interstitium (n = 6; 30%), small bilateral pleural effusions (n = 5; 25%), bilateral or unilateral pneumothorax (n = 2; 10%), and pneumomediastinum (n = 3; 15%). Among all 20 patients, 10 patients had subsequent CT scan evaluation over a mean follow-up period of 43 ± 16 (range, 27 to 66 days) after the initial scan. The initial and follow-up results of PFTs and CT scan scores are summarized in Table 2 . Five patients had initial scans showing < 50% involvement with increased opacities, and their follow-up scans showed substantial decreases in the extent of GGO and complete resolution of consolidation (Fig 2 ). Among those patients, one patient had complete resolution of abnormal opacities. In the remaining five patients with more extensive areas of GGO and consolidation (overall extent of increased opacities, > 70%) during the acute phase, the follow-up HRCT scans demonstrated complete or nearly complete resolution of consolidation and persistence of GGO associated with reticulation and traction bronchiectasis (Fig 3 ). When consolidation improved, it evolved into GGO mixed with a variable degree of fibrosis. Changes in total HRCT scan scores and scores for each individual abnormality are indicated in Figure 4 . At follow-up, there was a general decrease in total HRCT scan scores (n = 10) [Fig 4, top, A], and five patients had lower initial scores for GGO [Fig 4, middle, B] and scores for consolidation (n = 10) [Fig 4, bottom, C]. In contrast, GGO scores for patients with higher initial scores for GGO (n = 5) were increased at the follow-up, as some areas of GGO evolved from consolidation to GGO (Fig 4, middle, B).



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  		Figure 1. HRCT scan obtained 3 days after smoke inhalation in a patient (case 6) with ZCSII shows symmetric extensive areas of GGO (white arrowheads) anteriorly and airspace consolidation (black arrowheads) posteriorly. Also note the presence of a small pneumomediastinum (arrow).

 

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  		Table 2. Initial and Follow-up PFT Results and HRCT Scores*

 


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  		Figure 2. HRCT scan at the level of the aortic arch in a patient (case 9) with ZCSII. Top: the initial scan obtained 3 days after exposure shows patchy areas of GGO, with thickened interlobular septa giving a crazy-paving appearance. Bottom: the follow-up HRCT scan obtained 66 days after the initial scan shows an almost complete resolution of the abnormalities. Small patches of residual GGO are still observed (arrowhead).

 


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  		Figure 3. HRCT scan at the lower lobes in a patient (case 1) with ZCSII. Top: the initial scan obtained 15 days after exposure demonstrates diffuse GGO and patchy consolidation. There are also a pneumomediastinum (arrowhead) and bilateral pneumothoraces. Bottom: the follow-up HRCT scan obtained 34 days later demonstrates extensive evidence of fibrosis with irregular reticulation, irregular interfaces, traction bronchiectasis (arrowheads), and architectural distortion. The persistent unilateral pneumothorax is still present.

 


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  		Figure 4. Changes in total HRCT scan scores (top, A), and in scores for GGO (middle, B) and consolidation at the initial ZCSII and follow-up (bottom, C) of 10 patients are shown. A general reduction in total HRCT scan scores in 10 patients was demonstrated (top, A), in 5 patients with lower GGO scores (middle, B) and in scores for consolidation in 10 patients (bottom, C). The scores of five patients with higher GGO scores were increased at the follow-up, as some areas of GGO evolved from consolidation to GGO (middle, B).

 
Pulmonary Function Testing
Of all 20 patients who were examined, 13 underwent PFTs 3 to 5 days after the accident, whereas the other 7 patients underwent PFTs 10 to 21 days after the accident because of initially severe lung injury. The results of the initial PFTs are summarized in Table 3 . The PFTs showed restrictive lung disease in 18 patients (90%). Of these 18 patients, 15 had mild volume restriction (ie, total lung capacity [TLC] between 60% and 79%) and 3 had moderate volume restriction (ie, TLC between 40% and 59%). The DLCO was reduced in 16 of these patients (75%). Obstructive lung disease was seen in only two patients, who had a mixed obstructive-restrictive pattern. The FEV1 was reduced in 18 of 20 patients (90%), while the FVC was abnormally low in all patients. Follow-up PFTs were performed in 10 of these 20 patients between days 27 and 66 after injury, but it should be noted that all 20 PFTs were scheduled within 3 days of the CT scan examinations. Initial and follow-up PFT results for each of the 20 patients are summarized in Table 2. A comparison of the initial and follow-up PFT results in 10 of the 20 patients is shown in Figure 5 . Although they were not statistically significant (p = 0.051), substantial improvements were noted in FEV1 (p = 0.024), FVC (p = 0.021), TLC (p = 0.047), and DLCO at the follow-up (Fig 5).


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  		Table 3. Initial Pulmonary Function in 20 Patients With ZCSII*

 


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  		Figure 5. Comparison of the results of the initial and follow-up PFTs shows a significant improvement in FEV1, FVC, and TLC.

 
Correlation of HRCT Scan Findings With PFT Results and Length of Hospital Stay
Correlation between selected pulmonary function parameters, and scores of different CT scan patterns and total increased opacity of the 20 patients is shown in Table 4 . FVC, FEV1, TLC, and DLCO correlated well with the scores of consolidation (r = –0.63, –0.48, –0.72, and –0.53, respectively) and GGO (r = –0.55, –0.52, –0.53, and –0.60, respectively), with a consistency in total CT scan scores (r = –0.69, –0.65, –0.71, and –0.71, respectively). A significant correlation was observed between initial HRCT scan scores and length of hospital stay in days (r = 0.85). Over the follow-up period, changes in HRCT scan scores correlated well only with FVC (r = –0.68) [Fig 6 ]. Despite high CT scan scores, PFTs did not appear to identify a solitary obstructive lung disease in these patients.


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  		Table 4. Correlation Between Initial PFT Results and Different CT Scan Findings Among the 20 Patients*

 


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  		Figure 6. Changes in HRCT scan scores correlates well with changes in FVC from the time of the initial injury to the follow-up.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
HRCT scanning was used to evaluate the structural changes caused in the lung by smoke inhalation injury because it has become a major imaging method in the assessment of infiltrative lung disease.1415 GGO usually reflects a variety of pathologic processes such as mild airspace disease, interstitial lung disease, or both.1516 In patients with ZCSII, the histologic features include pulmonary edema, alveolitis, interstitial and intraalveolar fibrosis, and diffuse alveolar damage,1234 which may be detected as GGOs on HRCT scans.

There have been reports12345 describing ARDS soon after a significant exposure to zinc chloride (smoke bomb) fumes. In contrast, others have reported34 some type of delayed ARDS with a slowly progressive clinical course over the ensuing 2 weeks. A discrepancy in the progression to ARDS over time or severity among different investigations may be attributed to the amount of smoke inhalation, to the duration of exposure, and to whether exposure occurred in an open or confined space.24 In this study, ARDS developed in five of our patients (25%) within 72 h after inhalation. In general, these patients had higher HRCT scan scores, suggesting that they had more severe lung injury soon after inhalation. The exact mechanism by which ARDS is triggered remains unclear, although there is evidence of involvement of the release of proinflammatory cytokines.4

Pneumomediastinum and/or pneumothorax have been reported in patients with ZCSII.345617 These conditions may follow severe strain or cough induced by exposure to a variety of toxic agents such as chlorine gas18 and oxides of nitrogen.19 The mechanism involved in pneumothorax or pneumomediastinum is probably the result of alveolar rupture caused by the direct injury of the alveoli or secondarily by barotrauma from mechanical ventilation.1820 In our 20 patients, 2 patients had pneumothorax, and pneumomediastinum developed in 3 patients, with 1 and 2 patients, respectively, who required mechanical ventilation because of ARDS. Our observations therefore support previously proposed possible mechanisms, as described above. Five patients had minimal pleural effusions initially after injury, all of which resolved spontaneously as clinical conditions improved. We speculated that the effusion was reactive secondary to the inhalation injury, as none of the patients presented with clinical signs of infection.

In general, follow-up HRCT scans of our patients showed a considerable improvement in lung abnormalities over a relatively short period of time in less severely injured patients as compared with those in whom ARDS developed (Table 2). Consistent with observations from previous reports,234 severe ZCSII may cause extensive interstitial and intraalveolar fibrosis. Similarly, it was noted that our five severely injured patients presented with reticular opacities and traction bronchiectasis consistent with lung fibrosis at follow-up,1521 thus supporting the view that fibrosis is more likely to develop in patients with more severe injury.12345

To our best knowledge, this is the first report of initial and follow-up studies of pulmonary function and CT scan changes in a relatively large series of patients with ZCSII. Significant declines were observed in FVC, FEV1, TLC, and DLCO, but not in FEV1/FVC ratio, early after smoke inhalation, with a good correlation noted between HRCT scan scores and functional parameters, suggesting that this combined modality may predict reliably the severity of the ZCSII. Although remaining lower than normal, all functional parameters improved significantly in a follow-up period ranging from 1 to 2 months after exposure. Similarly, Zerahn et al9 also showed a decrease in TLC and DLCO that was observed during a short-term follow-up (4 weeks after exposure) in 13 patients who had experienced a modest exposure to zinc chloride smoke. Both studies suggested that flow conduction appeared to be fairly preserved with damage confined to the lung parenchyma. Of these 20 patients, obstructive ventilatory impairment was identified in only 2 patients with the highest HRCT scan scores who had abnormal FEV1 values and reduced FEV1/FVC ratios. Taken together, these results further suggest that, in general, ZCSII causes insignificant airway injury except in the context of a more severe alveolar injury that might be associated airway obstruction. A significant correlation between the initial HRCT scan scores and lengths of hospital stay that were observed in this study suggested that the HRCT scan score might reflect reliably the severity of the inhalation injury. Intriguingly, changes in HRCT scan scores correlated well only with changes in FVC in the follow-up period, suggesting that FVC may be the only significant functional predictor of long-term outcome for patients with ZCSII. However, this assumption needs to be tested in a larger number of patients.

In conclusion, the CT scan features of ZCSII are predominantly GGOs with or without associated consolidation, no zonal predominance, and both central and peripheral distribution. A good correlation was observed between HRCT scan findings and pulmonary function in our study, and our results suggest that ZCSII causes predominantly parenchymal damage of the lung and a restrictive type of functional impairment in general.


   Acknowledgements
 
The authors thank Dr. Mark Ferguson at the University of Chicago for his review of this manuscript.


   Footnotes
 
Abbreviations: DLCO = diffusing capacity of the lung for carbon monoxide; GGO = ground-glass opacity; HRCT = high-resolution CT; PFT = pulmonary function test; TLC = total lung capacity; ZCSII = zinc chloride smoke inhalation injury

Received for publication September 3, 2004. Accepted for publication November 30, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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