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(Chest. 2004;125:541-547.)
© 2004 American College of Chest Physicians

The Diagnosis of Pneumonia in Renal Transplant Recipients Using Invasive and Noninvasive Procedures*

Gee-Chen Chang, MD; Chieh-Liang Wu, MD; Shin-Hung Pan, MD; Tsung-Ying Yang, MD; Chung-Shih Chin, MD; Yun-Chiu Yang, MD and Chi-Der Chiang, MD

* From the Division of Pulmonary and Critical Care Medicine (Drs. Chang, Wu, Pan, T-Y. Yang, Chin, Y-C. Yang, and Chiang), Department of Internal Medicine, Taichung Veterans General Hospital; and Institute of Toxicology (Dr. Chang), Chung Shan Medical University, Taichung, Taiwan, ROC.

Correspondence to: Gee-Chen Chang, MD, Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Taichung Veterans General Hospital, 160 Chung-Kang Rd. Sec. 3, Taichung, Taiwan, ROC; e-mail: august{at}vghtc.vghtc.gov.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: We used invasive and noninvasive procedures to determine the causes of pneumonia in renal transplant recipients.

Subjects and methods: We retrospectively surveyed 565 renal transplant recipients (transplants received March 1984 to August 2001) to find those with pneumonia. Noninvasive diagnostic methods included serologic testing, and blood and sputum cultures with stains. Invasive procedures included fiberoptic bronchoscopy and percutaneous transthoracic procedures.

Results: A total of 92 patients were enrolled. Of these, 71 patients had a definite etiologic diagnosis of pneumonia. The major infectious pathogens were bacterial (n = 21) and mixed bacterial infection (n = 10), Mycobacterium tuberculosis (TB) [n = 18], and fungi (n = 8). Noninvasive and invasive procedures led to the diagnosis of pneumonia in 31.5% (n = 29) and 45.6% (n = 42) of patients, respectively. Bronchoscopy was used in 64 patients, with a diagnostic yield of 38 cases (59.3%). Patients were 3.62 times more likely to contract pneumonia within 12 months of renal transplantation than they were >= 12 months thereafter (95% confidence interval, 1.33 to 9.84). Twenty-seven of the 92 patients (29.3%) died. The pneumonia mortality rate has dropped significantly since 1996 (41.8% vs 10.8%, p = 0.002).

Conclusion: Both invasive and noninvasive procedures are useful in the diagnosis of pneumonia, with declining mortality, in renal transplant recipients. Bacterial and mixed bacterial infection, TB, and fungal infection are the most common pathogens; cases are most likely to occur within 1 year after renal transplantation.

Key Words: bronchoscopy • diagnosis • pneumonia • renal transplantation


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Renal transplantation is the most common type of organ transplantation. Much progress in the survival of the grafted kidney has been made in the previous 2 decades, especially since the introduction of immunosuppression agents.1 However, infection is a major complication among renal transplant recipients, including pneumonia, one of the most frequent life-threatening complications of long-term immunosuppression. A broad range of potential pathogens is involved, of which the most common are bacterial and opportunistic infections.2 3 4 Early diagnosis and accurate treatment are important in curing such an infection. In this study, both invasive and noninvasive diagnostic techniques were used in renal transplant recipients with pneumonia.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
All 565 renal transplant recipients (transplants received between March 1984 and August 2001) at Taichung Veterans General Hospital, a teaching hospital and tertiary referral center at Taichung, Taiwan, were surveyed. We retroactively studied all episodes of fever, cough, and new pulmonary infiltrates in these patients from the beginning of transplantation to the day of graft failure or patient mortality. All of the patients received prophylactic antibiotics with trimethoprim-sulfamethoxazole (80 to 400 mg/d) for 6 to 9 months after transplantation. Within 1 day after the identification of the pulmonary infiltrates, all patients were surveyed immediately for intensive diagnosis and treatment.

Cultures and Diagnostic Tests
Samples of blood were drawn for blood cultures and serologic tests, including IgM antibody detection by enzyme-linked immunosorbent assay of cytomegalovirus (CMV) [monoclonal antibody to purified and inactivated CMV], Chlamydia (in vitro assay against Chlamydia trachomatis antigens), and mycoplasma (specific antibody to Mycoplasma pneumoniae). Legionella antibody was detected by indirect fluorescent antibody against heat-killed Legionella bacterium. A sample of spontaneous sputum or induction sputum was obtained before the treatment for Gram stain and Ziehl-Neelsen stain. After the sample was assessed for adequacy (epithelial cells < 10 per lower power fields, polymorphonuclear neutrophils > 25 per lower power fields), it was sent for bacterial, Mycobacterium tuberculosis (TB), and fungal cultures. If the patient was receiving mechanical ventilation, had toxic signs, diffuse lung infiltrates or hypoxemia, or had no sputum production, fiberoptic bronchoscopy was performed only once with bronchoscopic protected specimen brush (PSB), biopsy, or BAL, because of great concern for the safety of this population. BAL was performed with 120 mL of sterile saline solution in six 20-mL aliquots. In patients with localized pulmonary infiltrates, lavage was performed in the affected lobe; in patients with diffuse pulmonary infiltrates, lavage was done in the middle lobe or lingular segment. BAL fluid was centrifuged. The cell pellet was stained with Gram stain, the direct immunofluorescent staining method for Legionella pneumophila, Wright Giemsa stain, Gomori silver stain for Pneumocystis carinii, and Papanicolau stain. PSB and BAL samples were cultured for bacterial pathogens, fungi, virus, and Mycobacteria. Sonography-guided percutaneous transthoracic lung aspiration or thoracentesis with pleural biopsy was performed on patients with peripheral pulmonary lesions or pleural effusion.

Diagnostic Criteria for the Pathogens of Bacterial Pneumonia
The pathogens of pneumonia were determined by the results of the diagnostic tests performed, the patients’ response to specific treatment, and histologic evaluation of the biopsy samples. Bacterial pneumonia was diagnosed whenever blood or sputum samples isolated pathogenic bacteria. Similarly, when the PSB or BAL specimens grew > 103 cfu or 104 cfu per milliliter of fluid, bacterial pneumonia was diagnosed. Prior to January 1998, semiquantitative cultures were performed; after January 1998, quantitative cultures were performed. Semiquantitative cultures were performed by means of a quantitative loop, in which 0.01 mL of BAL fluid was plated to agars including sheep blood agar, MacConkey agar, and chocolate blood agar. Estimates of the number of bacteria in the BAL fluid were expressed in colony forming units per milliliter. The quantitative cultures were performed via serial dilutions.5

Chlamydia, Mycoplasma, and Legionella were also considered to be pathogens whenever elevated titers of antibody were discovered with clinical response to treatment. Pneumonia due to CMV and other viruses were considered if they were isolated by cell culture from BAL fluid and inclusion bodies were present on cytopathologic evaluation. Viral infection was confirmed by immunofluorescent stain with monoclonal antibodies.

P carinii pneumonia (PCP) was considered pathogenic by a positive Gomori methenamine silver stain result. Identification of Legionella and Mycobacteria was accepted as a definite diagnosis. Fungal pneumonia was diagnosed in the presence of fungal hyphae identified by cytopathologic or histopathologic evaluation through the use of bronchoscopic transbronchial lung biopsies or sonoguided percutaneous lung aspiration with positive culture findings from BAL fluid, lung tissue, or blood and compatible clinical and radiographic patterns.

Empiric Treatment
The most common combination of empirical antibiotics was a third-generation cephalosporin with amikacin if no pathogens could be identified after all invasive procedures. Alternative antibiotics were piperacillin with or without tazobactam and amikacin, or ciprofloxacin. If no defervescence occurred for 3 days or staphylococcal infection was suspected, vancomycin was also administered. Amphotericin B was added if no clinical improvement was observed after 1 week of antibiotic treatment in patients without an etiologic diagnosis. Antibiotic changes were based on positive results from either study.

Statistical Analysis
Analyses were performed with the Statistical Package for Social Sciences statistical software (SPSS standard version 8.0; SPSS; Chicago, IL). We compared mortality rates between patients with pneumonia occurring before or after 1996 with a Fisher exact test; p < 0.05 was considered statistically significant. We also calculated the relative risks of pneumonia developing within 6 months or 12 months after renal transplantation, using logistic regression.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Of the 565 patients (330 men and 235 women; mean age, 40.0 ± 11.7 years [mean ± SD]), 92 patients had episodes of pneumonia (58 men and 34 women; mean age, 42.2 ± 13.6 years). The median follow-up period of these 565 patients was 81.0 ± 46.1 months (range, 1 to 209 months). Initially, 106 patients had pulmonary infiltrates; of these, 14 patients were excluded due to acute pulmonary edema combining with other infections (n = 12) and diffuse pulmonary hemorrhage (n = 2). In the remaining 92 patients enrolled as having pneumonia, 71 patients had a definite etiologic diagnosis. Bacterial and mixed bacterial infections were the most common causes of pneumonia (21 of 92 patients and 10 of 92 patients, respectively), followed by TB (18 of 92 patients) and fungi (8 of 92 patients) [Table 1 ]. Staphylococcus aureus, Streptococcus pneumoniae, and Gram-negative bacilli were the most common bacterial pathogens (Table 2 ). In mixed infections, most of the pathogens were found in the BAL fluid, with or without biopsy. Seven patients had two bacterial pathogens, two patients had bacterial and fungal infection, and one patient had bacterial and nontuberculosis mycobacterial infection. Of the 18 patients with TB infections, 2 patients had miliary TB and 1 patient had TB pleurisy. The distribution of pulmonary lesions on the chest images was similar between the upper and lower lobes (Table 3 ). The prevalence of pulmonary tuberculosis in our patients was 3.2%, and the annual incidence was 0.2%. The response to standard combined antituberculosis therapy for 6 to 9 months was good without recurrence in all but one patient, who did not receive a diagnosis until after death.


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  		Table 1.. Etiology of the 92 Episodes of Pneumonia in Renal Transplant Recipients

 

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  		Table 2.. Bacterial Etiology of Pneumonia (Including Mixed Infection)

 

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  		Table 3.. Chest Radiographic Appearances of Tuberculosis

 
Pneumonia was diagnosed in 29 patients (31.5%) through noninvasive procedures. Seventeen patients showed an adequate Gram stain with positive culture findings for bacteria. One case of Chlamydia pneumoniae, two cases of M pneumoniae, and one case of Legionella pneumoniae were diagnosed through serum analysis. Eight patients had positive mycobacterial tuberculosis culture findings from the sputum; among them, four patients had smear-positive TB.

Pneumonia was diagnosed in 42 patients (45.6%) through invasive procedures. Bronchoscopy was performed in 64 cases, giving a final overall diagnostic yield of 38 patients (59.3%). A transbronchial lesion biopsy was performed on eight selected cases with a diagnosis of fungal and nocardia infections. Nine of the 38 patients also received a bronchoscopic examination. A diagnosis was made and treatment initiated immediately after the invasive procedure, although seven patients had positive blood culture findings and two patients had a positive CMV IgM test results with an inclusion body in the BAL fluid. A diagnosis was not made in 10 patients initially, but positive TB culture findings were found later. Five patients initially received bronchoscopy without diagnosis, but later were shown to have pneumonia by percutaneous transthoracic procedures (n = 4) and blood Legionella testing (n = 1). Three patients received percutaneous transthoracic needle lung aspiration with stains and cultures, revealing pulmonary nocardiasis in one patient, pulmonary aspergillosis in two patients, and one patient had TB pleurisy proved by pleural biopsy.

Twenty-seven of the 92 patients (29.3%) with pneumonia died (Fig 1 ). The pneumonia mortality rate has dropped significantly since 1996 (41.8% vs 10.8%, p = 0.002). Eleven of the 33 patients died of bacterial or mixed bacterial infection. Five of the 6 patients with aspergillosis, 3 of the 4 patients with PCP, 1 of 18 patients with pulmonary TB, and 7 of 21 patients without a specific diagnosis died. Fourteen patients survived after empiric treatment. There was no mortality among patients with CMV infection and atypical pneumonia. Respiratory failure developed in 32 patients with endotracheal intubation and mechanical ventilation use; of these, only 6 patients survived. The relative risk of pneumonia within 6 months or 12 months of renal transplantation vs after 6 months or 12 months of renal transplantation were 2.97 (95% confidence interval [CI], 1.13 to 7.28) and 3.62 (95% CI, 1.33 to 9.84), respectively.



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  		Figure 1.. The distribution of pneumonia of various etiologies vs time after renal transplantation. The dot signifies mortality.

 

   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The choice of a diagnostic procedure in immunocompromised patients must be based on the yield for the most likely pathogens and the safety of the procedure. Sputum should be obtained from renal transplant patients with pneumonia because it is easily done, although BAL or biopsy provides a more accurate means of diagnosis. Open lung biopsy (OLB) is considered the "gold standard" for evaluation of lung infiltrates in the immunocompromised host. In the report by White et al,6 OLB in patients with hematologic malignancy has a significant yield in diagnosis and impact on survival at 30 days and 90 days in patients with specific rather than a nonspecific pulmonary diagnosis; in other reports,7 8 there was no proven impact on outcome. The differences in these studies may be related to the type of patients included or the definition accepted for specific diagnosis. In this study, we avoid surgery, as our clinicians considered this procedure carried some risk, while bronchoscopic procedures are very convenient, less invasive, and less time-consuming than OLB by experienced physicians. Bronchoscopy has an excellent yield for diffuse lung diseases, but its yield with fungal infection is lower, in the range of 50%.9 Also, it does not measure the invasiveness of microorganism in tissue. Another problem arises, as the contamination of culture material by upper respiratory tract flora is inevitable most of the time. By discarding the initial part of BAL fluid, BAL with quantitative cultures significantly aids in investigating possible lower respiratory tract infections and may distinguish them from bacterial colonization.10 Using semiquantitative cultures of BAL fluid, the diagnosis of bacterial pneumonia can be enhanced,11 12 13 but the rate of diagnostic error also increases. Furthermore, the BAL fluid was centrifuged with cell pellet for Gram stain in our series, and this could facilitate the identification of possible pathogens rapidly, especially the bacteria phagocytized by polymorphonuclear neutrophils. With the use of both invasive and noninvasive procedures, specific diagnoses were made in 79.3% (noninvasive alone, 31.5%; invasive, 47.8%) of the renal transplant recipients with pneumonia. Bacterial infections are common in transplant patients,14 15 and were the most common type of infection in our survey group. Gram-negative bacilli and methicillin-resistant S aureus were the most common pathogens, and the cause of pneumonia was undetermined in 19 to 31% of patients.16 17 18 In our study, 21 of 92 patients (22.8%) had undetermined causes of pneumonia, similar to the results of a study by Rano et al17 (12.5%), but lower than those of the studies by Sternberg et al18 (31%) and Torres et al16 (34%) [Table 4 ]. We used antipseudomonal antibiotics and vancomycin in patients who lacked a definite diagnosis even after invasive procedures. Amphotericin B was added if fever and lung lesions continued for > 7 days. After this empiric treatment, 7 of the 21 patients died. For these patients, OLB may have a higher yield of diagnosis and possibly result into less mortality.6 Although there was no increase in mortality in patients with empiric treatment, this finding does not mean that specific diagnosis is of no value. On the contrary, it may mean that the patients with specific diagnoses are at higher risk of death without prompt specific therapy. Since empiric therapy would not have covered some of the pathogens recovered, we believe that a specific diagnosis has value because it can allow therapy for organisms not ordinarily treated, and it can allow therapy to be targeted to the identified pathogens, thus avoiding overtreatment.


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  		Table 4.. Comparison of Etiology of Pneumonia in Transplant Recipients in Four Different Studies*

 
Simultaneous occurrence of multiple causes of pneumonia were present in 10 of the 92 patients. This phenomenon had been reported in renal transplant patients by quantitative BAL cultures.18 19 20 21 Ramsey et al19 reported that a superinfection developed in 23 cases (43%) and was significant in 22 of 27 deaths. Caution is needed in interpretation as BAL sampling problems may influence these results. High probability of simultaneous infection had been found in OLB in transplant patients, including renal transplant patients.7 8 22 In the study of Waltzer et al7 by OLB, 22 infections were diagnosed in 16 patients, thereby reflecting the frequency of simultaneous infection (37.5%).

Many immunocompromised patients with atypical pneumonia do not produce sufficient sputum to allow pathogen identification. The assessment of the immunocompromised host with pneumonia with immunoserology is not standardized and doubtful. The potential for alteration of immune response in these patients relegates these tests to a very restricted role. Serology is generally confined to testing for agents for which other methods are not yet available, such as M pneumoniae and C pneumoniae. In our study, in the consideration of pathogens of atypical pneumonia, besides the elevated antibody titers, clinical response to treatment was also evaluated.

Mycobacterial infection is well known as a complication in immunocompromised patients, and pulmonary tuberculosis is an endemic disease throughout Asia. The prevalence of tuberculosis in renal transplant recipients varies from 0.5 to 1% in North America23 24 to 11.5% in India.25 The annual incidence of pulmonary TB of our patients was less than that of patients receiving dialysis, but higher than in the general population (0.49% for dialysis patients, 0.07% for the general population).26 The distributions of pulmonary lesions on the chest images differed from those of nonimmunocompromised patients with upper-lobe predominance; in immunocompromised patients, the lower lobes of the lung were more seriously affected.

Fungal infections, especially Aspergillus, have high mortality rates in immunocompromised patients27 and in renal transplant recipients due to the use of immunosuppressive agents such as corticosteroids.28 It is better to begin the specific treatment for invasive disease if Aspergillus species are present in the sputum or BAL fluid until proven otherwise.29 Two patients had cryptococcal pneumonia with systemic dissemination, including cerebrospinal fluid, skin, and blood. Both patients recovered after treatment with amphotericin B.

Four patients had PCP, which developed in spite of prophylactic treatment with trimethoprim-sulfamethoxazole for 6 to 9 months. One patient who acquired PCP < 6 months after transplantation complied poorly with prophylactic treatment. Diagnoses were made in all our patients using BAL with a silver stain, considered the most accurate method of analysis.30 Fever, hypoxemia, and diffuse interstitial lung infiltrations were present in these patients, and helped the clinicians to make their diagnoses. Three of the four patients died in spite of treatment. Delayed diagnosis or pneumonia superimposed with other infections may have been causes of these deaths.19 31

CMV is the most important viral pathogen affecting transplant recipients. Up to 70% of CMV-seropositive transplant recipients show CMV reactivation following transplantation, but only approximately 20% of these patients have CMV disease. The clinical diagnosis of CMV pneumonia is based on hypoxemia, diffuse infiltrates observed via chest radiograph, and detection of CMV in BAL fluid.32 Two patients had CMV pneumonia, diagnosed by diffuse interstitial infiltrations, serologic tests, and positive cytomegalic cells in the BAL fluid. The incidence (2%) was approximately the same as that in the study by Rano et al,17 but was lower than the incidence found by Tamm et al33 (4 of 49 patients, 8.2%) in patients with renal transplantation and in orthotopic liver transplantation patients (10%).16 One cause of low incidence of CMV pneumonia might be that almost all of our patients had CMV infection prior to renal transplantation, showing positive CMV IgG antibodies. Another possible reason is that the incidence of CMV pneumonia following solid-organ transplantation depends on the type of allograft and immunosuppressive regimen, with lung transplantation having an incidence of 50%.34 Immunostaining with anti-CMV antibodies in the BAL is helpful in diagnosing CMV pneumonia and in differentiation between CMV infection and CMV pneumonia.35

Rubin36 has proposed a timetable of the usual sequence of infections after organ transplantation. Because of sustained immunosuppression, opportunistic infections, including viruses, PCP, and fungi, usually occur within 1 to 6 months after transplantation. Deviations from the timetable suggest the presence of an unusual epidemiologic exposure or excessive immunosuppression. In our survey group, the relative risk of pneumonia occurring within 6 months vs after 6 months of renal transplantation was 2.97 (95% CI, 1.13 to 7.28). However, the relative risk of occurrence within 12 months vs after 12 months of renal transplantation was even higher (relative risk, 3.62; 95% CI, 1.33 to 9.84). Our treatment did not include excessive immunosuppression; unusual epidemiologic exposure might be partially responsible, so we had a high index of suspicion of opportunistic infections for the first year after renal transplantation.

Worldwide, the mortality rate in solid-organ transplant recipients due to infection has decreased gradually since the early to mid-1990s; we observed the same trend in our patients. The decline may be ascribed to the ability to recognize the types of infections after transplant, improvements in prevention and management of infections, and improvements in immunosuppression.37 38 39

This study shows that both invasive and noninvasive procedures are useful in the diagnosis of pneumonia in renal transplant recipients. Bacterial and mixed bacterial infection, pulmonary tuberculosis, and fungal infection are the most common pathogens, especially within 1 year after renal transplantation.


   Acknowledgements
 
We thank Dr. Michael S. Niederman for the review of this manuscript.


   Footnotes
 
Abbreviations: CI = confidence interval; CMV = cytomegalovirus; OLB = open lung biopsy; PCP = Pneumocystis carinii pneumonia; PSB = protected specimen brush; TB = Mycobacterium tuberculosis

Received for publication August 29, 2002. Accepted for publication August 8, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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