Open Access

Trans‑bronchoscopy with implantation of 125I radioactive seeds in patients with pulmonary atelectasis induced by lung cancer

  • Authors:
    • Mingjian Lu
    • Deli Pu
    • Weidong Zhang
    • Jiangrong Liao
    • Tao Zhang
    • Guang Yang
    • Zhenyin Liu
    • Sristi Singh
    • Fei Gao
    • Fujun Zhang
  • View Affiliations

  • Published online on: May 13, 2015     https://doi.org/10.3892/ol.2015.3204
  • Pages: 216-222
  • Copyright: © Lu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

To evaluate the role of low‑dose‑rate interstitial brachytherapy using trans‑bronchoscope 125I radioactive seeds implantation in patients with pulmonary atelectasis induced by lung cancer, in terms of feasibility, safety, quality of life (QOL), and survival time. Between April 2008 and June 2011, 15 patients from two medical institutions that had obstructive pulmonary atelectasis caused by inoperable lung cancer were assigned to receive 125I implantation endoluminal brachytherapy by bronchoscopy. Subsequent to the implantation of 125I seeds, the outcomes were measured in terms of procedure success rate, reopening of atelectasis, complications associated with the procedure, Karnofsky performance status (KPS) scores and survival time. The surgical procedure was successfully performed in all 15 patients. No procedure‑associated mortality occurred and the complications were mild and considered acceptable. Irritable cough and temporary increase of hemoptysis occurred in 11 (73.3%) and 10 (66.7%) patients respectively, and were the most common complications. The pulmonary atelectasis reopening rate subsequent to the procedure was 86.7, 76.9, 80.0, 75.0 and 50.0% at 2, 6, 12, 18 and 24 months, respectively. The KPS score significantly improved following the implantation of 125I seeds and the duration of improvement ranged between 3 and 27 months. The median and mean survival times were 15.6 and 16 months, respectively. Actuarial survival rates at 6, 12 and 24 months after the procedure were 86.7, 66.7 and 13.3%, respectively. In patients with advanced lung cancer and those presenting with obstructive pulmonary atelectasis, treatment with intraluminal implantation of 125I seeds is a safe and effective therapy option with easy accessibility.

Introduction

Lung cancer is one of the most frequently diagnosed types of cancer and is the leading cause of cancer-associated mortality worldwide (1). In China, the incidence and mortality rate of lung cancer have been increasing dramatically in the previous three decades and lung cancer is becoming a notable medical problem (2). Pulmonary atelectasis is a common complication in patients with lung cancer, particularly central type lung cancer. It has been reported that 30% of lung cancer patients present with obstruction of the central airway, such as the trachea or main bronchi, which manifests as symptoms of respiratory distress, bleeding or infection (3). Pulmonary atelectasis decreases quality of life (QOL) and may impair anti-tumor therapy. Due to a low possibility for resection, palliative therapy plays an important role in this condition. Currently, a variety of interventional modalities, including neodymium-doped yttrium aluminium garnet laser therapy, stenting, photo-dynamic therapy and endoluminal brachytherapy, are utilized to relieve airway obstruction, owing to the development of the flexible bronchoscope. Therapy choice depends on the presence of comorbidities, pulmonary function of the patient, previous treatment administered and life expectancy of the patient. High-dose-rate (HDR) endoluminal brachytherapy, with or without additional combined therapy, has been demonstrated to be an effective treatment modality in this condition (4,5). However, due to the high expenses of HDR endoluminal brachytherapy, the application of this technology has been tremendously restricted. As a type of novel therapy technology, 125I radioactive seed implantation has been revealed as efficient in numerous types of malignant tumors (6,7).

The present study aimed to evaluate the feasibility, safety and efficacy of low-dose-rate (LDR) interstitial brachytherapy trans-bronchoscopy with 125I radioactive seed implantation in patients with pulmonary atelectasis induced by lung cancer. To the best of our knowledge, the present study is the first to evaluate the feasibility, safety and efficacy of LDR 125I seed implantation as a palliative therapy in patients with malignant obstructive pulmonary atelectasis induced by lung cancer.

Patients and methods

Patient eligibility and characteristics

Between April 2008 and June 2011, 15 patients with central type lung cancer and secondary obstructive pulmonary atelectasis underwent interventional bronchoscopy with 125I implantation for symptomatic palliation of pulmonary atelectasis at either the Department of Oncology, Guizhou Astronautics Hospital (Zunyi, Guizhou, China) or the Department of Imaging and Intervention Radiology, Cancer Center of Sun Yat-sen University (Guangzhou, Guangdong, China). All patients were diagnosed with primary lung cancer involving the central airway, which was confirmed by biopsy, and were not candidates for surgical resection. All patients had previously received chemotherapy at least four times, with a poor response rate (RR). Three patients had received prior radiation therapy at a dose between 40 and 50 Gy, at a conventional fractionation. The other patients did not undergo external beam radiation therapy due to numerous causes. Pre-operative evaluation and treatment decision making was based on the health of the patients, previous bronchoscopy exam, computed tomography (CT) scan, previous therapy and the willingness of patients. The patients consisted of 15 patients with airway obstructive atelectasis that presented with various symptoms, such as respiratory distress, cough, hemoptysis and pneumonia. All patients presented with a cough and respiratory distress, and 9 patients (60%) presented with hemoptysis. Squamous cell carcinoma was the most common histological diagnosis in 11 patients. The patient characteristics are reported in Table I. Symptoms of acute obstruction and medium to severe hemoptysis were considered unsuitable for the present study and patients exhibiting these symptoms were excluded from the study.

Table I.

Background characteristics of patients before 125I seed implantation (n=15).

Table I.

Background characteristics of patients before 125I seed implantation (n=15).

Patient characteristicValue
Gender, n (%)
  Male11 (73.3)
  Female4 (26.7)
Age, years
  Median62.1
  Range43-80
Pathology type, n
  Squamous cell cancer12
  Adenocarcinoma cell cancer3
Main clinical presentation, n
  Respiratory distress15
  Cough15
  Bleeding9
  Infection5
  Other11
Obstructive location, n
  Right bronchus10
  Left bronchus5
Clinical stage, n
  IIIA2
  IIIB5
  IV8
Previous therapy, n
  Chemotherapy15
  External beam radiotherapy3
Pre-operative preparation and surgical procedure

The present study used 0.7 mCi 125I radioactive seeds (catalog no., CIAE-6711; Chinese Atomic Energy Science Institution, Beijing, China). The dose of the radioactive seeds was determined according to the following empirical formula: Total dose (mCi) = (length + width + height) / 3 × 5. The number of seeds was calculated as follows: Number of seeds = total dose / 0.7. The prescription dose determined from this formula was expected to reach 100–130 Gy. The endoscope was obtained from Olympus (BF-IT40; Olympus Corporation, Tokyo, Japan).

Implantation of 125I seeds

The technique for this therapy was, overall, the same as regular bronchoscope examination (8). All procedures were performed under airway topical anesthesia with monitoring of electrocardiogram, pulse, blood pressure and blood oxygen saturation. A unilateral nasal catheter was placed prior to the procedure for the purpose of oxygen supply. Using a specialized instrument (Endoscope with particle pusher; Innovative Medical Device Technology Co., Ltd. Jinan, Shandong, China; Fig. 1), a channel was created to implant the radioactive seeds into the tumor.

Monitoring of patients

All 15 patients that underwent this therapy were followed up clinically or by telephone, and surveillance bronchoscopy and CT scans were performed two months subsequent to the first procedure and every subsequent two months. At each follow-up, the patients were clinically evaluated through a thorough history and physical examination, and the patients were assessed to determine their Karnofsky performance status (KPS) score. Additional bronchoscopies and CT scans were performed based upon the symptoms of the patients.

Assessment of the efficacy of pulmonary atelectasis reopening

Assessment of pulmonary reopening was based on the follow-up CT scan, and the CT image was evaluated by two independent radiologists. The efficacy was defined as follows: Complete reopening (CR), lung expansion had returned to the normal size and there was no atelectasis residue; partial reopening (PR), lung expansion was partial and the maximum diameter of pulmonary atelectasis was reduced by >50%; and no reopening (NR), lung expansion was not evident, or the maximum diameter of pulmonary atelectasis reduced <50% and progressed <20%. Progressive disease (PD) was defined as the maximum diameter of pulmonary atelectasis increasing by >20%.

Assessment of QOL

Data from the assessment of the QOL of all patients was obtained using the KPS score. KPS measurements range between 0 and 100. A high score represents a high QOL. The KPS scores were determined by clinicians prior to trans-bronchoscopy with implantation of 125I radioactive seeds, and again at each subsequent follow-up.

Statistical analysis

Statistical analysis was performed using SPSS software, version 13.0 (SPSS Inc., Chicago, IL, USA). The survival time was calculated from the time between the date of the procedure and time of mortality. Survival was calculated using the Kaplan-Meier method, and KPS data were analyzed using a paired-samples t-test. P<0.05 was considered to indicate a statistically significant difference.

Ethical approval and patient consent

Ethical approval was obtained prior to the commencement of the study from the Ethical Committee of the Sun Yat-sen University Cancer Center and the Ethical Committee of Guizhou Astronautics Hospital. The present study was performed in accordance with national law and the Helsinki Declaration of 1975, in its current, revised form (9). Written informed consent was obtained from all patients prior to the commencement of the treatment procedure.

Results

Technical feasibility

The present study enrolled 15 patients, 11 male and 4 female, with a median age of 62.1 years. A total of 15 interventional bronchoscopies were performed. The procedure time ranged between 20 and 50 min, with an overall average duration of 35 min. The present study was easily performed and was well tolerated by all patients. No procedure-associated mortalities occurred and no patient required a prompt discontinuation of the surgical procedure.

Complications

No patient succumbed to disease within 30 days of the initial procedure. An irritable cough and temporary increase of hemoptysis occurred in 11 (73.3%) and 10 (66.7%) patients, respectively, and were the most common complications. Other complications, including chest pain and fever, were mild and considered acceptable. No patients required additional emergency bronchoscopic treatment subsequent to the initial intervention.

Pulmonary atelectasis control

Overall, lung reopening was observed in the majority of patients between the procedure and the last follow-up. The reopening rate, calculated as the sum of the CR and PR, was 86.7, 76.9, 80.0, 75.0 and 50.0% in patients at 2, 6, 12, 18 and 24 months, respectively. The pulmonary atelectasis control rate is reported in Table II. A typical case is illustrated in Fig. 2.

Table II.

The effect of trans-bronchoscope 125I radioactive seeds implantation for the treatment of atelectasis in 15 patients with central type lung cancer.

Table II.

The effect of trans-bronchoscope 125I radioactive seeds implantation for the treatment of atelectasis in 15 patients with central type lung cancer.

Reopening of atelectasis

Follow-up time, monthsPatients, nCRPRNRPDReopening rate, %
215582086.7
613372176.9
1210261180.0
188241175.0
244112050.0

[i] Reopening rate was calculated from the sum of the CR and PR. CR, complete reopening; PR, partial reopening; NR, no reopening.

QOL response

The majority of the patients demonstrated an improvement in KPS scores subsequent to the surgery, particularly in those with a lower KPS score prior to the procedure. The improvement in symptoms and feeling of well-being was observed 2–3 weeks subsequent to the procedure and was maintained until the final follow-up in the majority of patients. In addition, there was a significant improvement in the pre- and post-operative KPS scores. The mean KPS score was 72.3±5.6 prior to the procedure and was improved to 84.7±4.8 one month later (P=0.004; Table III).

Table III.

KPS scores for the 15 patients pre- and post-implantation of 125I radioactive seeds.

Table III.

KPS scores for the 15 patients pre- and post-implantation of 125I radioactive seeds.

KPS score

Patient numberGenderAge, years Pre-implantation1-month follow-up2-month follow-up6-month follow-up1-year follow-up2-year follow-up
1M6565758080
2M647080808580
3M60608585858085
4M637080808075
5M467585808080
6M72809090
7M697590908580
8M80759085
9M6070808580
10M437085908080
11F577085909080
12F63758585858580
13F678090858580
14F5480909080
15F687080858080
Mean ± SD 62.1±9.572.3±5.684.7±4.885.4±4.082.7±4.380.0±2.482.5±3.5

[i] KPS, Karnofsky performance status; SD, standard deviation.

Survival analysis

The median follow-up time was 20.8 months (range, 5–27). The median survival time was 15.6 months, and the survival rate was 86.7% at 6 months, 66.7% at 12 months and 13.3 at 24 months subsequent to the procedure (Fig. 3).

At the time of analysis, 13 patients had succumbed. Nine patients had succumbed to progressive disease, including locoregional progression and brain metastasis, two patients had succumbed to a brain-vascular accident, one of which possessed a history of hypertension, one patient with a history of coronary artery disease succumbed to sudden cardiac arrest, and one patient with a history of COPD experienced heart failure. The characteristics of the 125I seed implantation and outcome of the treatment with 125I seed implantation is reported in Table IV.

Table IV.

Characteristics of the patients that underwent 125I seed implantation and the outcome of the treatment.

Table IV.

Characteristics of the patients that underwent 125I seed implantation and the outcome of the treatment.

Treatment and follow-up result

Patient numberGenderAge, yearsPathologyClinical stageSeeds, nAliveSurvival time, monthsCause of mortalityMedical history
1M65SCIV10No9Heart failureCOPD
2M64SCIV9No16Brain metastasesDiabetes
3M60SCIIIA6Yes>26
4M63SCIV8No13CVDCoronary disease
5M46SCIIIB8No21Tumor progression
6M72SCIV8No6Brain metastasesCOPD
7M69SCIV10No15Brain metastasesDiabetes
8M80SCIV10No5AMICOPD, diabetes
9M60SCIIIB9No15Tumor progression
10M43SCIV12No11Brain metastases
11F57SCIIIA10No20Tumor progressionDiabetes
12F63ACIIIB7Yes>27
13F67ACIIIB11No17Tumor progressionHypertension
14F54SCIV13No12Brain metastases
15F68ACIIIB14No20Tumor progression

[i] SC, squamous cancer; AC, adenocarcinoma; COPD, chronic obstructive pulmonary disease; CVD, cerebrovascular disease; AMI, acute myocardial infarction.

Discussion

Lung cancer remains the leading cause of cancer mortality worldwide, and only 25–30% of patients with non-small cell lung cancer present with locally-advanced disease on initial diagnosis, whereas 40–50% present with metastatic disease (1,10). Although the majority of the patients with inoperable lesions experience clinical benefit subsequent to receiving chemotherapy, radiotherapy and even targeted therapy, the overall survival (OS) rate remains suboptimal, with a five-year survival rate of <1% (11). The overall survival time was 8–10 months and the one-year survival rate was 30–35% (12). The majority of patients with lung cancer eventually require palliative treatment (13). Obstruction of the central airway is frequently encountered in patients with inoperable lung cancer, and may be caused by an intraluminal tumor growth, extrinsic compression or weakness of the bronchial wall. A variety of bronchoscopic techniques are currently available for the management of malignant obstruction of the central airway (14). For all these bronchoscopic techniques, several studies have reported excellent palliation with varying rates of complications in patients treated with endobronchial brachytherapy (15,16).

For locally advanced lung cancer, there are several studies (1719) that have demonstrated the effectiveness of 125I radioactive seeds implantation in the local control and improvement of OS time and rate. However, for central type lung cancer, the technique of percutaneous puncture means great risk of hemorrhage and pneumothorax. However, the development of the technology used in interventional bronchoscopy makes the trans-bronchoscopy procedure with 125I radioactive seed implantation possible and flexible. In the present study, all 15 patients completed this therapy safely. The procedure time was 20–50 min, with an average duration of 35 min in all patients, and there was no procedure-associated mortality. The present result revealed that this technique is safe and flexible.

Complications of HDR intraluminal brachytherapy are mild and infrequently reported in the majority of previous studies, while severe complications, such as fatal hemoptysis and broncho-esophageal fistula, were occasionally observed (15,20,21). Therefore, the adverse effects of HDR brachytherapy on the airways are more thoroughly considered. Compared with HDR, LDR demonstrates an improved relative biological effect (RBE) (22,23). The present results revealed that the treatment complications were mild and acceptable, mainly presenting as a transient increase in hemoptysis, chest pain and fever. However, the duration of the complications was short and the majority of patients did not require additional therapy. There were no severe complications compared with those reported for HDR intraluminal brachytherapy. Probable explanations include that LDR has more excellent radiation biology characteristics compared with that of HDR. LDR brachytherapy is a type of continuous therapy with reduced peak dose. In addition, HDR intracavitary therapy requires several surgical procedures, and this increases the risk of complications. Notably, in the current study, one patient expelled two radioactive seeds two weeks subsequent to the procedure. This case resulted in certain requirements for radiological safety. Therefore, a small lead bottle was prepared for each patient in the present study to store any seeds that were coughed out so that the radioactive seeds would not harm the environment or other individuals.

The atelectasis reopening rate, calculated from the sum of the CR and PR, was revealed to be 86.7, 76.9, 80.0, 75.0 and 50.0% in patients at 2, 6, 12, 18 and 24 months subsequent to the procedure, respectively. Compared with a previous study (20), the atelectasis recanalization effect was good, and the effect was similar between the two studies, but demonstrated a longer duration in the present study. A possible reason is that the implantation of 125I radioactive seeds by intraluminal brachytherapy has a longer therapeutic effect compared with HDR intraluminal brachytherapy. The majority of patients in the present study demonstrated an improved KPS score subsequent to the surgical procedure. The mean KPS score was 72.3±5.6 prior to the procedure and improved to 84.7±4.8 one month later (P=0.004). Intraluminal brachytherapy with 125I radioactive seed implantation has a longer therapeutic effect, which may be an explanation for the comparatively long duration of the improvement in KPS.

In the present study, the long-term survival of lung cancer was the ultimate treatment goal. The median survival was 15.6 and the survival rate was 86.7% at 6 months subsequent to the procedure, 66.7% at 12 months and 13.3% at 24 months. The two-year survival rate was lower in the current study compared with certain studies of HDR intraluminal brachytherapy (5,24). This difference may be a result of patient selection or additional therapy, as numerous intraluminal brachytherapy procedures were combined with external radiation treatment. In the present study, eight patients presented with stage IV disease. Therefore, a two-year survival rate of 13.3% is a favorable outcome. However, the present study also demonstrated certain limitations. Firstly, accurate measurement of the dosimetry of the irradiation was not possible due to the lack of sophisticated measuring techniques dedicated to this condition. Therefore, no quantitative data associated with radiation therapy could be provided. Secondly, pulmonary atelectasis is occasionally challenging to differentiate from the tumor, so the present study cannot supply accurate data for local tumor control. Thirdly the current study was not a randomized trial and, as a pilot study, only 15 patients were approved to receive the therapy.

Management of malignant tumor complicated with pulmonary atelectasis is a challenging issue. Interventional bronchoscopy with a multimodality approach may improve symptom control and survival. This study demonstrated that trans-bronchoscopy with 125I radioactive seed implantation is a feasible procedure that demonstrates good symptom control, minimal complications and improvement in survival and QOL. Physicians treating such patients should recognize the limitation of single modality therapy and become skilled in utilizing alternative complementary treatment approaches in order to achieve optimal outcome.

Acknowledgements

This study was supported by the Provincial & Ministry of Education Research Project of Guangdong (grant no., 2012B091100458), Major Project of Science and Technology of Guangzhou (grant no., 132400027) and National Natural Science Foundation of China (grant no., 81371654). The authors thank Dr. Marcin Bednarz and Dr. Zou Fang for their kind help with the English language.

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Lu M, Pu D, Zhang W, Liao J, Zhang T, Yang G, Liu Z, Singh S, Gao F, Zhang F, Zhang F, et al: Trans‑bronchoscopy with implantation of 125I radioactive seeds in patients with pulmonary atelectasis induced by lung cancer. Oncol Lett 10: 216-222, 2015.
APA
Lu, M., Pu, D., Zhang, W., Liao, J., Zhang, T., Yang, G. ... Zhang, F. (2015). Trans‑bronchoscopy with implantation of 125I radioactive seeds in patients with pulmonary atelectasis induced by lung cancer. Oncology Letters, 10, 216-222. https://doi.org/10.3892/ol.2015.3204
MLA
Lu, M., Pu, D., Zhang, W., Liao, J., Zhang, T., Yang, G., Liu, Z., Singh, S., Gao, F., Zhang, F."Trans‑bronchoscopy with implantation of 125I radioactive seeds in patients with pulmonary atelectasis induced by lung cancer". Oncology Letters 10.1 (2015): 216-222.
Chicago
Lu, M., Pu, D., Zhang, W., Liao, J., Zhang, T., Yang, G., Liu, Z., Singh, S., Gao, F., Zhang, F."Trans‑bronchoscopy with implantation of 125I radioactive seeds in patients with pulmonary atelectasis induced by lung cancer". Oncology Letters 10, no. 1 (2015): 216-222. https://doi.org/10.3892/ol.2015.3204