How to cite this article: Ramírez-García LE, Juárez-Hernández F, Tanus-Hajj J, Avelar-Garnica FJ. [Assessment of pulmonary complications in renal transplantation through the use of radiography]. Rev Med Inst Mex Seguro Soc. 2016;54 Suppl 2:S168-74.
Received: November 2nd 2015
Judged: May 2nd 2015
Laura Elena Ramírez-García,a Fortunato Juárez-Hernández,a Janet Tanus-Hajj,a Francisco José Avelar-Garnicaa
aDepartamento de Radiología, Hospital de Especialidades, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Ciudad de México, México
Communication with: Laura Elena Ramírez García
Telephone: (55) 5627 6900, extension 21316
Background: Lower respiratory tract infections are the most common complications in kidney transplant patients in the first six months and they are associated with high mortality. Other complications include pulmonary edema, pulmonary embolism, and pulmonary hemorrhage. The aim of this study was to evaluate pulmonary complications in kidney transplant patients by using chest radiography.
Methods: We analyzed a total of 516 chest X-rays of 150 patients who received a kidney transplant in 2014. Chest radiographs were performed in the preoperative and in the postoperative assessments, as well as within the next 48 hours after the surgery, and from 3 to 7, 8-15, 16-30, 31-90, 91-180 and 180 days. For the radiographic study of the lung parenchyma, chest was divided into four quadrants by assigning a value of 1 to each radiographic pattern: reticular, nodular alveolar occupation; lobar or segmental; atelectasis; and ground-glass. Lung parenchyma obtained a minimum value of 0 and a maximum value of 16 points. Also, we assessed variables such as gender, age, associated comorbidity, and type of renal transplantation.
Results: we obtained data from a total of 150 patients; 19 patients had pulmonary complications in the first 24 to 48 hours and 15 patients between 90 and 180 days after the kidney transplantation. The most frequent complications were acute pulmonary edema in early stage and infections in late stage.
Conclusion: the prevalence of complications diagnosed by chest radiograph was low and it was observed more often in early and late stages.
Keywords: Thoracic radiography; Kidney transplantation; Lung diseases
The first successful kidney transplant was performed in Mexico in 1963, with a 20-year survival. Currently about 1,500 transplants are performed annually, most from living donors.1-3
One of the most serious and frequent complications in kidney transplant patients are pulmonary infections.4-7 Risk factors for infections in these patients include immunosuppressive therapy, comorbidity, ventilatory support, pulmonary hypertension, catheters and urinary probes, as well as prolonged operative time, blood transfusion, and the experience of the surgical team.8,9
Bacterial and viral infections are the most common subsequent to transplantation. The reactivation of previously acquired infections such as that caused by Mycobacterium tuberculosis is another mechanism of infection.9,10
Because of its low cost and accessibility, plain chest radiography is useful as a first-line screening in the presence or absence of pulmonary symptoms; also comparison can be made with previous studies, as well as monitoring to find pulmonary complications in patients with renal transplantation.11
Patterns that occur in the chest x-ray are as follows:12-16
Alveolar disease pattern in the airspace: This pattern is spread through intra-alveolar connections. Initially it is limited to a lobe or segment, and the most common pathogen is Streptococcous pneumoniae. In the chest radiograph it is presented as airway consolidation with the presence of air bronchograms.
Bronchopneumonia pattern: This is an airway infection that subsequently spreads and blocks adjacent airspaces. Its most common pathogens are Staphylococcus aureus, Legionella pneumoniae, and certain gram-negative bacteria. In the chest x-ray it is presented as a mild peribronchial thickening and ill-defined air opacities; in late stages, it is presented in non-homogeneous areas of consolidation, typically involving several lobes. It can also occur as a series of consolidations affecting the terminal respiratory bronchioles and adjacent alveoli, which results in ill-defined nodular opacities that are 4 to 10 mm in diameter (airspace nodules), or involving the entire lobe.
Interstitial pattern: this pattern mainly affects the lung interstitium and is produced by an initial bronchopneumonic focus. The most common pathogens are viruses, such as Mycoplasma pneumoniae and Chlamydia pneumoniae. In the chest radiograph it is presented as a linear pattern and increased radiopacity normal for the lung parenchyma, known as "ground glass pattern". Tuberculosis can be due to Mycobacterium tuberculosis, M. bovis, M. africanum, or M. microti. In primary TB disease the Ranke complex, lymphadenopathy, and pleural disease are identified; in post-primary disease, the parenchymal condition is associated with cavitation in 80%, finding endobronchial dissemination and pleural involvement. In the chest radiograph we can identify focal areas of consolidation and nodular opacities preferably located in the upper lobes, hilar mediastinal lymphadenopathy, and pleural effusion; 20% have associated cavitation and 10% mediastinal lymphadenopathy. The miliary pattern, generally present in patients with immunosuppressive states, is diffuse and bilateral.16 High-resolution tomography has acquired great diagnostic significance compared with chest radiography in the usual interstitial pneumonia, as it detects earlier disease more reliably, better estimates the extent of disease, and can sometimes predict disease activity. Reticular opacities predominate by thickening of the partitions, and perivascular interstitial thickening is common, producing irregular interfaces between the lung and the pulmonary vessels in the early stages; honeycombing occurs subsequently, which is a thick network of irregular fibrosis with architectural distortion around cystic spaces 2 to 20 mm in diameter, often associated with traction bronchiectasis, in approximately 80% of patients. It is more severe in the lower lobes and in the subpleural and dorsal regions.
In this case the chest radiograph is normal in a great percentage. The most common findings are decreased lung volume associated with patchy airway consolidation, atelectasis, pleural effusion, and increased unilateral or bilateral pulmonary artery caliber.17 Chronic pulmonary embolism shows increased caliber of both pulmonary arteries and the right chambers of the heart.
Pulmonary angiography is used as an initial radiological study and is often unique for diagnosis. Sensitivities close to 95% are shown for the detection of pulmonary emboli in a multidetector tomography matrix.18,19
The most reliable sign of acute pulmonary embolism in computed tomography is the demonstration of a relatively central defect in intraluminal pulmonary artery repletion surrounded by contrast medium. These vessels occluded in the axial plane can resemble train tracks. Sometimes one can see an expansion associated with the affected artery. Emboli can occur in multiple locations, both centrally and peripherally. The diagnosis of pulmonary embolism should not be made if a non-opacified artery is only seen at one cutoff; this may be due to vascular pulsation and an artefact of flow.20
The accumulation of fluid in the lung interstitium that has exceeded the capacity of lymphatic drainage of the lung, as the amount of extravascular fluid increases, accumulates in the margins of the alveolar spaces; if retention continues, the fluid passes into the alveolar spaces.
The chest radiograph shows perihilar ground glass images, Kerley lines A and B, diffuse vascular contours, unilateral or bilateral pleural effusion, and increased azygos vein. The presence of bilateral symmetric confluent consolidations and predominant airspace in the middle and lower lung zones occurs when the liquid has passed the interstitial space to the alveoli; we can see these consolidations in in what is typically called a "butterfly" distribution.20,21
In high resolution tomography, findings include a smooth thickening of the intralobular partitions up to 5 mm, peribronchial thickening, dependent ground glass opacities, pleural effusion, and thickening of fissures.22,23
Chest radiography shows rapid onset of airspace consolidations with a drop in hematocrit and hemoptysis, suggesting the diagnosis. One may also find loss of definition of intrapulmonary vascular paths, perihilar ground glass images, and thickening of the interlobular fissures.23
Radiological records were reviewed for renal transplant patients from January 1 to December 31, 2014 at the Hospital de Especialidades “Dr. Bernardo Sepúlveda” of the Centro Médico Nacional Siglo XXI of the Instituto Mexicano del Seguro Social. Patients of either gender were included who were adults with a history of renal transplantation with x-rays in the established period.
Chest radiographs were performed with CMR fixed equipment GMX-AF console MRF90T table, EMERALD 125 KV tube, Bucky VERT SBV-1, serial number 27626, and portable equipment AMX-4; they were taken in anterior-posterior position in supine patients, with 75 to 80 kV factors and 2 to 4 mA intensity at 1 m distance, with minimal exposure and proper collimation of the beam. Patients who could stand or sit underwent posterior-anterior projection at 1.80 m distance. If the patient was cooperative, the study was conducted in inspiratory apnea, with 75 to 80 kV and 2 to 4 mA intensity. Each x-ray was analyzed and the most important findings were noted. For lung parenchyma, the chest was divided into four quadrants by assigning a value of 1 to each radiographic pattern found: reticulonodular or alveolar occupation, lobar or segmental, and atelectasis or ground glass; the lung parenchyma obtained a minimum value of 0 and a maximum of 16 points. Chest X-rays were taken during follow-up time, as needed: postoperative (within 48 hours after the operation), at 3 to 7 days, 8 to 15 days, 16 to 30 days, 31 to 90 days, 91 to 180 days, and more than 180 days.
The presence of unilateral or bilateral, free or loculated pleural effusion was assessed in pleura. As for items of life support, the central venous catheter with entry into internal jugular or right or left subclavian was assessed, along with the associated complications; we found a higher prevalence in right internal jugular catheter, and the complications found were kinking in the unnamed segment and cephalization of the catheter.
In addition, variables were evaluated such as gender, age, associated comorbidities, and type of renal transplantation.
High-resolution computed tomography has a complementary role in the evaluation of pulmonary disease and is generally used for additional findings or to establish the pulmonary pattern with greater specificity; CT scans were also made for patients who needed them. The studies were made with the 64-detector CT scanner MD Aquilion, Toshiba brand that we have at the Hospital de Especialidades.
Information was obtained from a total of 150 patients between January 1 and December 31, 2014. The mean age was 36 years, ranging from 18 to 71 years. Patients were 66 women and 84 men, 53 of whom (35%) showed a cardiothoracic index > 0.5. Eighty-six patients (57%) came from Mexico City and 64 patients (43%) were from the interior of Mexico. As for the type of transplant, it was from living donors in 100 patients and deceased donors in 50 patients.
We reviewed a total of 516 chest X-rays, 216 of which were performed using AMX-4 portable instruments, and the rest with table-top equipment, as well as five high-resolution thorax scans. 100% of the chest X-rays within the first 48 hours were performed using portable instruments.
Within the first 48 hours after kidney transplantation, 17% of patients presented some findings from chest radiography; in the range of 3 to 7 days and 91 to 180 days, 10% of patients had findings. In the first hours 42% presented a value of 1, 27% presented 2 and 4. 58% of patients presented atelectasis, 10% pleural effusion, and 22% bilateral effusion. At 3 and 7 days 34% had a value of 4, 53% had multisegmental consolidation, and 47% had atelectasis. Between 91 and 180 days, 60% had a value of 4, 73% had multisegmental consolidation, 20% had atelectasis, and 6% of patients had ventilatory support. Table I shows the findings from the other days of follow-up.
|Table I Chest x-ray findings in the pulmonary parenchyma taken after renal transplantation in patients|
|Time periods to assess x-rays|
|24-48 hours||3-7 days||8-15 days||16-30 days||31-90 days||91-180 days||> 180 days|
|Findings in the pulmonary parenchyma||17||10||3||4||3||10||3|
|Paving with ground glass||0||0||0||0||0||0||25|
|Unilateral pleural effusion||10||3||1||0.7||0.7||5||1|
|Free bilateral pleural effusion||22||7||5||7||1.4||3||1|
|Central venous catheter||94||74||3||30||4||9||3|
|Ventilatory support with endotracheal tube||3||0.6||0||0.7||0||6||0|
Regarding ventilatory support, in one of the patients the endotracheal tube was located in the right bronchus with consequent complete atelectasis of the contralateral hemithorax; the endotracheal tube was repositioned with resolution at 12 hours. Three days after the transplant, another patient required ventilatory support with endotracheal tube; evaluation of the lung parenchyma was 4 for a multisegmental consolidation in relation to pulmonary edema and bilateral pleural effusion; the patient died on the fourth day after renal transplantation. Another patient required ventilatory support with endotracheal tube at 20 days of renal transplantation; they had a lung parenchyma score of 5 with lobar lung consolidation and bilateral pleural effusion with left passive atelectasis (Figure 1).
Figure 1 Poster-anterior chest x-ray showing left lobar pneumonia, with silhouette sign and air bronchograms
Complementary study with chest tomography was necessary in five patients (3%) in the period between 91 and 180 days.
In the same period, three patients died; the first died five months after renal transplant, which showed lung parenchyma values 4 due to multisegmental consolidation and bilateral pleural effusion. The second patient died five months after renal transplantation; they had lung parenchyma values of 5 due to reticular pattern with diffuse distribution, along with ground glass, without pleural effusion. The third patient died six months after kidney transplant with lung parenchyma values of 5 due to multisegmental consolidation and ground glass; this patient did not have pleural effusion either, and they had a right pneumothorax of 50% due to right subclavian catheter complication (Figures 2 and 3).
Figure 2 Poster-anterior chest x-ray and high-resolution tomography of the lung: the characteristic radiological pattern of multisegmental interstitial involvement (or "ground glass") is seen with a trend towards consolidation, with thickening of interlobular and intralobular septa. Note the absence of pleural effusion, 90 days after renal transplantation.
Figure 3 Right pneumothorax with complications associated with central venous catheter placement. Note the increased attenuation and tomographic pattern of involvement of the pulmonary interstitium
Within the period of more than 180 days after transplantation, one patient presented a ground glass paving pattern; they had to have a complementary study with chest tomography (Figure 4).
Figure 4 Multisegmental affectation, consolidations of airspace in more than one segment, with air bronchograms, "ground glass", and areas of architectural distortion and minimal bilateral pleural effusion. Image taken five months after renal transplantation
Pulmonary complications are common in kidney transplant patients. Chest radiography is a study that is available in most hospitals; it is a low-cost resource that allows the diagnosis of pulmonary complications. While there are studies involving more technology such as computed tomography and magnetic resonance imaging, chest radiography is a useful test for diagnosis. Kidney transplant patients have special situations related to conditions of transplant surgery and immunosuppressive therapy. The number of kidney transplants at the Hospital de Especialidades has increased in response to the high demand for these transplants in the country. The present study analyzed chest radiographs of patients who received a kidney transplant during 2014. Patients were monitored for 180 days. During that period pulmonary complications were observed more often between 24 and 48 hours and between 91 and 180 days after transplantation (Figure 5). The disorders were related to fluid overload in the early hours and pneumonia after 90 days. The findings are consistent with the work of Webb et al.,9 who evaluated 416 patients who had kidney transplants from September 1972 to March 1976. This study evaluated subsequent complications within two weeks; among their findings, Webb et al. found that opportunistic lung infections from Pneumocystis jiroveci, gram-positive bacteria (Staphylococcus aureus) and gram-negative bacteria (Pseudomonas, Escherichia coli) were the most common. As in our study, one patient had a crazy paving pattern, characteristic of Pneumocystis carinii. As for the relationship between time and presentation of pulmonary patterns, between 2007 and 2010 Kupeli et al.6 evaluated demographic data, chest radiography and lung function, C-reactive protein, albumin and leukocyte cell count after renal transplantation in 136 patients. Fifteen of them developed lung complications within the first year (respiratory infections were pneumonia from Streptococcus pneumoniae and Acinetobacter baumannii, and tuberculosis).
Figure 5 Pulmonary complications in chest x-ray in relation to the time after kidney transplantation
During the first 15 days multisegmental consolidation predominated in connection with parenchymal edema, inherent complications of fluid overload during and after the surgery, which was resolved in the following 24 to 48 hours. In the later stages (180 days), infections suggesting the presence of opportunistic pathogens predominated, probably related to immunosuppressive therapy.
Lung infection is a common cause of morbidity and mortality in transplant recipients, as up to 30% die in the first three months.24 In this study, mortality was low, given that three patients died in the period from 91 to 180 days with imaging related to pneumonia.
Pulmonary complications from chest x-ray imaging was rare; pulmonary edema was found in acute postoperative x-rays in the early hours of transplantation; in late stage images were suggestive of atypical pneumonia, caused by various viral infections.
We give our thanks to the Renal Transplant Unit of the Unidad Médica de Alta Especialidad Hospital de Especialidades “Dr. Bernardo Sepúlveda” of the Centro Médico Nacional Siglo XXI.
Conflict of interest statement: The authors have completed and submitted the form translated into Spanish for the declaration of potential conflicts of interest of the International Committee of Medical Journal Editors, and none were reported in relation to this article.