Abstract
Background and aim
Imaging of patients with COVID-19 has provided unique insights into the pathophysiology of the infection. Cysts are a rare manifestation of the disease in the lung. The aim of this research was to compare COVID-19-positive patients with cysts on CT to patients without cysts and propose a mechanism for cyst formation in this patient population based on radiographic observations.
Materials and Methods
Our HIPAA-compliant IRB-approved research project involved a retrospective review of 219 chest CT scans identified in COVID-19-positive inpatients and emergency room patients at Columbia University Irving Medical Center from February 27, 2020 to July 17, 2020. A thoracic radiologist with over 20 years of experience reviewed the images on lung window settings and identified the presence of cysts, their distribution (central or pleural based), and if there was an accompanying pneumothorax. The extent of consolidation of the entire lung on a scale of 0–16 and the presence of fibrosis were also documented.
Results
Cysts were identified in 10 of the 219 patients. CT scans with cysts were obtained on average on day 57 of symptoms (range 16–115 days) compared to CT scans of those without cysts that were obtained on average on day 19 (range 0–89 days). The distribution of cysts was heterogeneous; six patients had multiple cysts while four were isolated. Seven cysts were peripheral in distribution while three were central. Two patients with cysts developed a subsequent pneumothorax. Fifty percent of those with cysts had been intubated.
Conclusions
Patients with COVID-19 develop cystic lung lesions for at least two reasons; pleural-based lesions are more likely areas of infarction and central lesions with surrounding ground glass are more likely related to infection and/or mechanical ventilation.
Introduction
Severe acute respiratory syndrome coronavirus 2 (SARS-COV-2) is a virus that causes substantial respiratory illness in approximately 20% of infected individuals and especially in the earliest phase of the COVID-19 pandemic many of these patients required admission to intensive care units for monitoring and intervention [1]. Chest CT scans obtained during the patient's hospital course often revealed peripheral and/or central ground-glass opacities, atelectasis, and/or consolidation [2–4]. Many patients' imaging findings resolved completely over time however others have lingering lung disease with the development of pulmonary fibrosis [5, 6]. Fibrosis is more likely to occur in older males with more extensive lung involvement [5]. Fibrosis is more common in those who underwent mechanical ventilation but even those without mechanical ventilation developed fibrosis [6]. Longer telomere length has been shown to be protective against the long-term sequela of pulmonary fibrosis from infection [6]. Less typical features of COVID-19 include cyst formation [7–9] which can lead to further complications including pneumothoraces and pneumomediastinum [10, 11].
A cyst is defined as a round or oval parenchymal lucency that is clearly delineated from the adjacent lung parenchyma by a thin wall less than 2 mm in thickness; lesions with thicker walls are defined as cavities and have different implications [12]. The differential diagnosis for cystic lung lesions is broad and includes genetically predisposed and acquired etiologies. The number of cysts, the location of the cyst (intraparenchymal versus subpleural), and the association with ground glass opacities and/or consolidation must be considered by the radiologists to narrow the differential diagnosis [12]. The purpose of our paper is to compare COVID-19-positive patients with cysts on chest CT to COVID-19-positive patients without cysts and evaluate the radiographic characteristics of the cysts in order to propose a rationale for cyst formation in this patient population.
Materials and methods
Our Health Insurance Portability and Accountability Act (HIPAA) - compliant Internal Review Board -approved research project involved a retrospective review of 219 chest CT scans identified in inpatients and emergency room patients at Columbia University Irving Medical Center with COVID-19 infection from February 27, 2020, to July 17, 2020. A fellowship-trained thoracic radiologist with over twenty years of experience reviewed the CT images on lung window settings and identified the presence of cysts, their distribution (central or pleural-based), and if there was an accompanying pneumothorax.
The extent of consolidation of the entire lung was measured on a scale of 0–16 with a score of 0–4 for the four lung quadrants. A grade of 0 meant no ground glass or consolidation was identified on CT, a grade of 1 meant less than 10% ground glass or consolidation of the quadrant of the lung, a grade of 2 meant that 11–25% of the quadrant had ground-glass opacities or consolidation, a grade of 3 meant that 26–50% of the quadrant had ground glass opacities or consolidation and a grade of 4 meant that greater than 50% of the quadrant had ground-glass opacities or consolidation. The presence of fibrosis was also documented; traction bronchiectasis, architectural distortion, and reticulations were considered evidence of fibrosis. Contrast studies were evaluated for the presence of pulmonary embolism. Additional information including age, gender, days of symptoms at the time of chest CT scan, and history of intubation were also acquired.
Results
Cysts were identified in 10 of the 219 patients with COVID-19 infection. CT scans from before the infection are not available and so we cannot determine if the cysts are new. The average age of those with cysts was 55 years old (range 26–71 years), and the average age of those without cysts was older at 62 years (range 23–97 years). Cysts were identified on average on day 57 of symptoms (range 16–115) compared to CT scans of those without cysts that were obtained on average on day 19 (range 0–89). The extent of consolidation in those with cysts was on average more than in those without cysts (10 vs 13). Men were more likely to develop cysts than women. 70% of those with cysts had fibrotic changes of the lungs but only 17% of those without cysts had fibrotic lung disease (Table 1).
Comparison of those with and without cysts on chest CT
| Cyst | No cyst | |
| # of patients | 10 (4.5%) | 209 (95.5%) |
| Male | 7/10 (70%) | 116/209 (56%) |
| Average age | 55 years (26–71) | 62 years (23–97) |
| Average CT scan day | Day 57 (16–115) | Day 19 (0–89) |
| Extent of consolidation | 13 (10–16) | 10 (0–16) |
| Intubated | 5/10 (50%) | 18/209 (9%) |
| PE | 1/5 (20%) | 33/155 (21%) |
| Fibrosis | 7/10 (70%) | 36/209 (17%) |
| Pneumothorax | 2/10 (20%) | 2/209 (1%) |
| Peripheral cyst | 7/10 (70%) | NA |
| Central cyst | 3/10 (30%) | NA |
| Multiple cysts | 7/10 (70%) | NA |
| Solitary cyst | 3/10 (30%) | NA |
The distribution of cysts was heterogeneous; six patients had multiple cysts while four were isolated. Seven cysts were subpleural in distribution while three cysts were central (Table 2). Two patients out of ten patients with cysts developed a subsequent pneumothorax but only 2 of 209 patients without cysts developed a pneumothorax. Five of those with cysts were intubated, however, 9% of patients without cysts were also intubated. Representative images from the ten CT scans of patients with cysts are included in Image 1.
Characteristics of patients and their cysts
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Discussion
Pulmonary cysts related to aging
Pulmonary cysts are by definition, thin-walled lung parenchymal lucencies which are roughly round in shape with a well-delineated interface with the remaining lung. Isolated pulmonary cysts are not infrequent and have been attributed to the normal aging process. Araki identified that 7.6% of patients in the Framingham Heart Study had cysts and they were related to the increased age of the patients [12]. Winter et al. found cysts more commonly in an older population greater than 65 years [13]. Some of our patients could have had cysts related to advanced age, however, we found that on average, younger patients had COVID-19-related cysts. McGuiness et al. identified barotrauma in 15% of patients with COVID-19 infection requiring invasive mechanical ventilation with younger people more frequently involved [14]. Cysts must be differentiated from radiologic mimickers that include emphysema and mosaic attenuation secondary to the bronchial obstruction which causes focal geographic decreased attenuation [15]. The key distinguishing feature of a cyst is the absence of a central pulmonary artery which is present in both emphysema and mosaic attenuation.
Cysts in COVID 19
Cysts are a relatively uncommon finding in patients with COVID-19 infection, affecting less than 5% of our study population. We found that males were more likely to develop cysts than females which is expected given their predisposition to worse outcomes from the infection [16]. Cysts were more frequently identified in patients with CT scans obtained later in the course of their disease. Perhaps if we had more CT scans from later dates we would have identified more cysts. Cysts were identified in the lung parenchyma from as early as Day 16 which is not surprising given the rapid evolution of the COVID-19 Acute Respiratory Distress Syndrome (ARDS) into a more fibrotic type pattern after Day 12. Patients with a larger disease burden were more likely to develop cysts which is also expected given their increased likelihood for a prolonged disease course. Similarly, intubated patients were also found to have more cysts. The presence of radiographic pulmonary emboli was not associated with increased cyst formation but does not exclude the possibility of occult thrombotic disease. Not all patients who develop cysts have had mechanical ventilation-supporting etiologies in addition to barotrauma [17]. The appearance of fibrosis frequently accompanied cyst formation [18] however findings of fibrosis could improve on follow up imaging and thus would have been overdiagnoses [19]. Interestingly, cysts are not regularly seen in association with non-COVID-19 fibrosis such as usual interstitial pneumonia, hypersensitivity pneumonitis, and nonspecific interstitial pneumonitis. Pneumothoraces occurred in 20% of those with cysts and rarely occurred when there were no cysts. Pneumomediastinum is another complication of barotrauma and has been reported in patients with COVID-19 infection [20].
An algorithmic approach
We set out to determine the most likely etiology of cysts in COVID-19-positive patients using imaging patterns described in the existing published literature. We applied the algorithmic approach provided by Raoof et al [21]. in their article entitled Cystic Lung Diseases: Algorithmic Approach to attempt to narrow down the differential diagnosis. The first branch point in the algorithm was to determine if the lesion qualifies as a cyst by confirming that the wall thickness was less than 2 mm. Our 10 patients met this criterion and had cysts by definition. The second branch point was to determine if the cysts were subpleural (adjacent to the pleural surface) or intraparenchymal (not in direct contact with the pleural surface). In the majority of our COVID-19 patients, the cysts were subpleural. The variable distribution supports the possibility that two types of cysts might occur in patients with COVID-19 infection.
Pulmonary infarcts
Raoof provided a differential diagnosis for peripheral cysts that included honeycombing that occurs in end-stage fibrosis, paraseptal emphysema that occurs with stiff lungs, and bulla. As per the algorithm, bulla remained the last differential consideration. Bulla classically occur when two or more terminal bronchi become confluent which can be secondary to atelectasis and/or consolidation however because single bulla are rare this is a less likely consideration [22].
Given the appearance of the lesions, lung infarctions may be a reasonable explanation for the pleural-based cysts [23–25]. There is increasing evidence including our own experience supporting the microthrombotic nature of COVID-19 infections as a driving force behind many widespread deadly phenomena of patients who contract the disease [26]. Given the extensive microthrombotic burden in these patients and the lack of convincing etiology from the aforementioned algorithm, it is reasonable to postulate that these subpleural cysts are the sequela of extensive microthrombi resulting in lung infarctions [27]. Patients with COVID-19 often have peripheral opacities or discrete Hampton's humps representing infarcted lung tissue. Pulmonary infarctions are histologically well-defined areas of ‘coagulative necrosis’ of the lung within an area of hemorrhage adjacent to the pleura. There is relatively preserved tissue architecture following the death of tissue [25]. The coagulative necrosis could result in a residual cystic space in contact with the pleura just as the Hampton's Hump contacted the pleura. We would expect that over time these areas of the infarcted lung would heal and the cyst would shrink in size. Further support is provided by the younger age of patients with subpleural cysts (25–66 years old) compared to those with central cysts (66–72 years old); infarcts of the lung are more common in younger patients who do not have established collateral circulation from the bronchial arteries which can compensate for ischemia.
Pneumatocele
Referring back to the algorithm, we looked to classify the more centrally located cysts. Step 3 gives a differential for multiple non-subpleural cysts, which includes Birt Hogg Dube, lymphocytic interstitial pneumonitis (LIP), Langerhans cell histiocytosis (LCH), and Lymphangioleiomyomatosis (LAM). If the cysts are fewer in number the differential includes pneumatocele and bronchogenic cysts. Bronchogenic cysts are unlikely given their propensity for the subcarinal and right paratracheal regions. Of the listed causes for central cysts, pneumatocele is most likely in patients with COVID-19 infection. Pneumatoceles are thin-walled gas-filled spaces within the lung parenchyma, which are most often transient. Pneumatoceles are thought to be secondary to an infectious insult with subsequent lung necrosis. It is postulated that local drainage of necrotic tissue causes the initial pneumatocele. There is subsequently enlargement secondary to inflammatory debris that obstructs the surrounding bronchioles and bronchi and exhibits a one-way valve effect on adjacent bronchi [28]. Pneumatoceles have been reported in association with continuous positive airway pressure (CPAP) [29, 30].
Pneumatoceles are pseudocysts because they do not have an epithelial lining. They vary in size but are of uniform thickness. They are most frequently associated with the infection including Staphylococcus Aureus with 60% of patients developing pneumatoceles. They can be caused by trauma and usually occur within 1–2 days of the injury [31]. In our study intubation was more commonly associated with cysts however not all people who were intubated developed cysts and some people who were not intubated did develop cysts. Given the extreme pro-inflammatory state of the infected patient and/or frequent use of continuous positive airway pressure (CPAP) in patients with COVID-19 infection, it is likely that these cysts represent pneumatoceles [31]. In addition, low surfactant levels which are known to be a complication of COVID-19 [32] may be a risk factor for pneumatocele development in the same way that premature babies who have low surfactant develop pneumatoceles [33, 34].
Diagnosis
Chest x-ray has been the primary imaging tool for patients with COVID-19. In the beginning, when nasal swab testing was limited, they provided a means for not only diagnosis but also for triaging patients based on the extent of pulmonary infiltrates [35]. They are used routinely in the ICU setting to assess line placement, and disease progression and identify clinically occult complications of illness. As such, chest X-rays provide the first opportunity to identify a pulmonary cyst if it is large enough. If the majority of the lung contains consolidation, a cyst will stand out more because of the contrast in density. In addition to identifying a cyst, chest x-rays can alert the clinician to the development of a pneumothorax or pneumomediastinum which could be life-threatening. Chest x-rays are not as useful in determining the location of a cyst (peripheral vs central) especially if the exam is obtained portably without the benefit of a lateral projection.
The three-dimensional capability of a chest CT allows localization of the cyst to a central or peripheral location. Chest CT scans can be performed without intravenous contrast for this purpose. New lower-dose techniques are ideal especially if the patient will require multiple follow-up exams. Additional findings on chest CT allow characterization of the extent of the disease and the acuity of the infiltrates, complications of pneumothorax and pneumomediastinum are readily diagnosed. The use of contrast is indicated if there is a suspicion of pulmonary embolism however much of the thrombotic disease may affect the smaller vessels and not be seen on chest CT and require a VQ scan for diagnosis. We did not observe an increase in cysts in patients with pulmonary embolism. Chest CT is readily available but there is the challenge of transportation to the scanner which can provide an obstacle for critically ill patients.
Treatment
Imaging allows the differentiation of cysts from abscesses which require additional treatment. Pneumatoceles usually spontaneously resolve and so treatment of the underlying condition is most appropriate as was done in the case of COVID-19. If the pneumatocele increases in size patient positioning techniques could be employed but are usually not necessary. Rarely would surgery be indicated unless the cyst continued to enlarge. Treatment of complications caused by the cyst includes chest tube placement and adjustment of respirator settings if indicated [28]. The goal of treatment is to avoid any potential complications which could potentially include lung abscess, pyothorax, and hemothorax [28]. Assessing for pulmonary emboli and the risk for recurrent infarction may be indicated as well.
Limitations
There are many limitations to this study caused by the seriousness of the pandemic with high patient mortality and staffing challenges due to employee illness. Chest CT scans were not performed on all patients and when performed they were at variable times during their illness and used a variety of protocols. Dual energy CT had not been used at our hospital prior to pandemic and was instituted later during its course. Many patients had been well prior to the onset of their illness and as such did not have prior exams to determine if the cysts had been present. The patients were seen at the onset of the pandemic and risk factor information was limited.
Conclusion
It is likely that patients with COVID-19 develop cystic lung lesions for at least two reasons and that the location of the lesions may point to the etiology. Pleural-based lesions are more likely to represent areas of infarcted lung and central lesions with surrounding ground glass opacities are more likely pneumatoceles related to infection or diminished surfactant or barotrauma related to mechanical ventilation. Time will tell the role of heredity in cyst development [36]. Understanding the possibility that multiple etiologies may account for cyst development can help us develop the best treatment strategies [37, 38].
Authors' contribution
The study’s inception and design involved input from all authors. M Salvatore contributed to the background research. M. Salvatore collected the data. All writers provided feedback on earlier drafts of the paper after M. Salvatore wrote the original draft. All authors assisted with manuscript editing. The final manuscript was read and approved by all writers.
Funding sources
No funding was obtained for this specific study. M Salvatore received funding from the companies listed below for other studies.
Conflict of interests
K Capaccione has served as an advisor for Cardinal Health.
Disclosures
Mary Salvatore, MD, MBA-Consultant: Genentech, Boehringer Ingelheim.
Speaker
France Foundation, Peer View, Genentech, Boehringer Ingelheim.
Research
Bioclinica, AbbVie, Lunglife AI.
Grant funding
Genentech, Boehringer Ingelheim.
Ethical statement
Research was approved by IRB. This retrospective study was HIPAA compliant and the need for informed consent was waived due to retrospective nature.
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