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Prognostic analysis of destroyed-lung patients with preoperative massive hemoptysis: a 20-year retrospective study

BMC Pulmonary Medicine volume 24, Article number: 402 (2024) Cite this article

Abstract

Background

Surgery is the main treatment option for destroyed-lung (DL) patients with life-threatening massive hemoptysis. However, short-term and long-term surgical safety and efficacy are unclear, prompting this study.

Methods

Data from 124 DL patients undergoing surgery between November 2001 and January 2022 at Beijing Chest Hospital were retrospectively analyzed. Data of the DL group (82 cases) and DL + massive hemoptysis group (42 cases) were compared with regard to clinical characteristics, long-term postoperative residual lung reinfection.

Results

As compared with DL group rates, The DL + massive hemoptysis group had greater incidence rates of postoperative complications, invasive postoperative respiratory support, long-term postoperative residual lung reinfection, and postoperative tuberculosis recurrence. Revealed risk factors for postoperative complications (Extent of lung lesion resection), postoperative invasive respiratory therapy (preoperative Hb < 9 g/L, severe intraoperative hemoptysis), and postoperative long-term residual lung reinfection (DL with massive hemoptysis).

Conclusions

DL patients with massive hemoptysis had greater rate of invasive respiratory support therapy and postoperative complications. Extensive lesion removal, preoperative anaemia, severe intraoperative bleeding associated with recent postoperative complications for the patient.

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Introduction

Destructive lung (DL), which involves the irreversible loss of lung function in one or more lobes, is most frequently caused by chronic lung infection with Mycobacterium tuberculosis [1,2,3]. The progression can result in massive haemoptysis for three common reasons that tuberculous lesion invasion of adjacent blood vessels, promotion of bronchodilation and the ruptured aneurysm which located in the cavity or the wall of the cavity [2, 4]. Death rate of massive hemoptysis patients of over 50% [5,6,7]. Emergency treatment is necessary for any patient presenting with life-threatening massive hemoptysis to ensure airway patency. Currently, some massive hemoptysis patients undergo arterial embolization, one study demonstrated an unacceptably high massive hemoptysis recurrence rate of 20.4% that was attributed to postoperative establishment of collateral circulation [8]. Surgical resection can effectively eradicate pulmonary lesions to thereby cure patients afflicted with both DL and massive hemoptysis.

Studies showed the DL postoperative complications ranging from 5 to 33.3% and mortality rates ranging from 9 to 38% [9,10,11,12,13,14,15,16]. No analysis of DL patient subgroups has yet been reported, due to limited numbers of patients undergoing surgical treatment for DL. Resulting that it is unclear whether short-term and long-term safety of surgical treatment of DL is equivalent between DL patients with massive hemoptysis and those without massive hemoptysis. Moreover, there are no reported differences in the long-term outcome of both lately, such acute clinical conditions are of concern, even if, as we acknowledge the long-term impact of surgery gradually diminishes over time.

To investigating above clinical questions, we conducted this observational retrospective cohort study of 124 patients who underwent DL pneumonectomy at Beijing Chest Hospital of Capital Medical University during the past 20 years. By analyzing differences in short-term and long-term outcomes between DL patients with and without massive hemoptysis, aim to identify associated risk factor, scientific basis for improving the safety of surgery in patients with DL with massive haemoptysis and for maximising long-term prognosis.

Materials and methods

Study subjects

A total of 124 patients who underwent pneumonectomy for DL from November 2001 to January 2022 at Beijing Chest Hospital were enrolled; including 42 (33.8%) cases of these patients had preoperative massive hemoptysis.

Indications for surgical treatment for DL included: (i) resectable nidus in one side of lung; (ii) massive hemoptysis; (iii) history of DL-related recurrent infections; (iv) multidrug-resistant TB; (v) patient inability to tolerate anti-TB treatment; and (vi) intermittent recurrent positive sputum cultures and/or sputum smears for Mycobacterium tuberculosis infection. (i is mandatory regardless of ii-vi indications).

Inclusion criteria for pneumonectomy included: ≥18 to < 75 years of age and postoperative pathomorphology consistent with TB or another pulmonary inflammatory disease. DL patients who met these criteria underwent pneumonectomy.

Exclusion criteria for pneumonectomy included: respiratory failure, bronchial asthma, chronic obstructive pulmonary disease, interstitial lung disease, malignancy, chronic cardiac insufficiency, and/or chronic renal insufficiency.

The study design complied with the Helsinki Research Ethics Statement. The requirement for patient written informed consent for participation in the study was waived by the Ethics Committee of the Institutional Review Board of Beijing Chest Hospital, an affiliate of Capital Medical University (Ethics number: Clinical Research 2018 (43)).

The 124 patients included in the analysis were assigned to two groups according to severity of preoperative hemoptysis: one group without preoperative massive hemoptysis (DL group) and the other group with both DL and massive hemoptysis (DL + massive hemoptysis group). The definition of massive hemoptysis used in this work, which was based on the definition provided by the guidance document Expert Recommendations for the Diagnosis and Treatment of Massive Hemoptysis in China, aligns with other definitions reported in the international literature [17]. Massive hemoptysis is defined as the expectoration of no less than 300 ml of blood per hemoptysis episode or no less than 500 ml of blood during a 24-h period. In addition, the occurrence of any life-threatening hemoptysis episode or any hemoptysis episode leading to airway obstruction and asphyxia provided further support for a diagnosis of massive hemoptysis [18, 19].

General clinical information was collected from patients at baseline, including gender, age, body mass index, smoking status, preoperative TB history, chronic pulmonary aspergillosis (CPA), bacterial lung infection, common non-pulmonary comorbidities (hypertension, coronary artery disease, diabetes), site of lesion (left or right), secondary or primary multidrug-resistant TB (MDR/XDR), cavities detected on chest computed tomography scans, presence of contralateral lung infection, preoperative pulmonary function, routine laboratory test results, operation time, intraoperative hemoptysis, and extent of pneumonectomy. Recent postoperative observations included death during hospitalization, death within 30 days of discharge, postoperative comorbidities (postoperative infection, respiratory failure, cardiac failure), postoperative drainage intervention measures, invasive respiratory support therapy, and postoperative hospital days.

Long-term post-operative observations included (as of 30 January 2022) follow-up of patients for residual lung reinfection, TB recurrence, residual pulmonary bronchiectasis, recurrence of massive hemoptysis, detection of bronchopleural fistula (BPF), empyema, and mortality.

Spirometry instruments used in this work included Master Screen-IOS and Master Screen-PFT instruments purchased from Jäger (Germany), which measure lung diffusion using the one-breath method. Pulmonary function indicators included forced expiratory volume in one second of predicted (FEV1%pred), maximal minute ventilation of predicted (MVV %pred), and lung diffusion capacity for carbon monoxide of predicted (DLCO %pred). Pulmonary function indicator values were judged to be declining when they were < 80% of expected values. Expected values were determined using the spirometer manufacturer’s default values (i.e., expected values for Europeans as endorsed by the European Respiratory Society)(20). Preoperative pulmonary function measurements were performed for those whose condition permitted, and all indicators of pre-operative test data were completed within 1 week prior to surgery.

Follow-up

DL patients were followed up by trained healthcare practitioners from December 2001 to January 2022 through face-to-face interviews or telephone surveys. During the post-operative follow-up period, readmissions and complications associated with DL surgery (TB recurrence, bacterial reinfection, secondary BPF, and chest abscess) were confirmed by 2 senior chief physicians then were recorded.

Quality control

The overall aim of this study was to adopt a standardized follow-up program, training program, and follow-up methodology. The follow-up program design and questionnaires were reviewed and validated by senior respiratory medicine and thoracic surgery clinicians then the follow-up program was implemented under supervision of highly trained general practitioners (GPs). GPs also conducted face-to-face or telephone follow-up interviews to collect patient after hospital discharge.

Statistical analysis

Measurement data expressed as mean ± standard deviation were compared between groups via t-test. Non-normally distributed measurement data expressed as median percentage value (25%, 75%) were compared between groups via Z-test. Counting-based data expressed as composition ratio or rate (%) were compared between groups via χ2 test. Variables were carefully selected based on clinical relevance and on statistical significance of intergroup differences with regard to univariate terms related to short-term and long-term outcomes. Consequently, 11 relevant factors related to short-term and long-term outcomes were identified: gender, age > 60 years, preoperative massive hemoptysis, TB history, BMI < 18.5, blood Hb level, blood CRP level, intraoperative hemoptysis, extent of pneumonectomy, blood fibrinogen level, and postoperative complications. These factors were analyzed for associations with short-term and long-term outcomes using binary logistic regression analysis. Differences with P < 0.05 were considered statistically significant [15, 21]. The SPSS 26.0 statistical package was used for data analysis.

Results

A total of 124 DL patients who received surgical treatment were enrolled in the study, including 53 (42.7%) males and 71 (57.3%) females, average age was 39.3 ± 13.7 years. Study subjects included 42 patients (21 males and 21 females, aged 44.5 ± 14.2 years) who were also afflicted with massive hemoptysis, of whom 6 patients who underwent bronchial artery embolization for massive hemoptysis experienced recurrences of massive hemoptysis within 6 to 36 months of surgery, among them, 2 patients underwent 3 BAE treatments, 3 patients underwent 2 BAE treatments, and 1 patient underwent 1 BAE treatment Fig. 1. Pathological examination of all 124 patients confirmed rates of TB-damaged lung of 61.2% (76/124), inflammation-damaged lung of 38.8% (48/124), and preoperative comorbid CPA of 23.4% (29/124). All patients underwent surgery through thoracotomy. No one uses VATS. 29 cases (23.4%) underwent lobectomy, and 95 cases (76.6%) underwent pneumonectomy.

Fig. 1
figure 1

Flowchart of patients underwent pulmonary resection for damaged lung

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As compared to the DL group, the DL + massive hemoptysis group had a higher rate of comorbid CPA (P = 0.020), a longer history prior to admission of bacterial lung infection (P = 0.007), a higher rate of comorbid diabetes (P = 0.001), longer operative time (P = 0.034), more severe intraoperative hemoptysis (P = 0.004), and more extensive lung lesion resection (P = 0.020). As compared to the DL + massive hemoptysis group, patients in the DL group had a higher rate of preoperative TB history (P = 0.012), higher mean preoperative hemoglobin level (P < 0.001), and preoperative lower lung diffusion capacity of carbon monoxide percent predicted value (DLCO %pred, P = 0.034) (Table 1).

Table 1 Baseline characteristics of DL patients with or without massive hemoptysis
Full size table

No statistical differences in mortality rates were observed between DL and DL + massive hemoptysis patient groups within 30 days of discharge and at the end of follow-up (P values of 0.214 and 0.158, respectively). The incidence rate of postoperative complications was greater for the DL + massive hemoptysis group than for the DL group (45.2% vs. 24.4%, respectively; P = 0.018), as was the incidence rate of invasive respiratory support therapy (21.4% vs. 4.9%, respectively, P = 0.004). Moreover, the DL + massive hemoptysis group exhibited greater incidence of residual lung reinfection than the DL group (20.5% vs. 2.5%, respectively; P = 0.002) and the DL + massive hemoptysis group exhibited greater incidence of postoperative TB recurrence as compared to that of the DL group (15.4% vs. 3c 0.8%, respectively; P = 0.033), (Table 2) and Figs. 2 and 3).

Table 2 Outcomes of DL patients with or without massive hemoptysis
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Fig. 2
figure 2

Short-term postoperative efficiency of DL group and DL + Massive Hemoptysis group

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Fig. 3
figure 3

Long-term postoperative efficiency of DL group and DL + Massive Hemoptysis group

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Extent of lung lesion resection was an independent risk factor for postoperative complications, while independent risk factors for postoperative invasive respiratory support therapy included preoperative Hb < 9 g/L and massive intraoperative hemoptysis. Furthermore, DL combined with massive hemoptysis was an independent risk factor for postoperative long-term residual lung reinfection (Tables 3 and 4; Fig. 4).

Table 3 The binary logistic regression analysis for risk factors of severe postoperative complications and invasive ventilation support in patients with DL
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Table 4 The binary logistic regression analysis for risk factors of pulmonary infection of the remaining lung and recurrence of TB in patients with DL
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Fig. 4
figure 4

Preoperative and postoperative chest CT of patient with DL

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Discussion

Patients with DL are prone to haemoptysis. Small amounts of haemoptysis are often self-limiting or can be controlled with medication. In the case of life-threatening haemoptysis, bronchial artery embolisation or surgical intervention is often required [20,21,22]. Some patients with massive hemoptysis are treated with pulmonary embolization, the hemoptysis recurrence rate in such patients can be unacceptably high (5-20.4%) [8, 23]. By contrast, surgical excision of DL lesions can completely prevent hemoptysis and this is potentially a superior treatment option, although use of this DL treatment method has rarely been reported in the literature. Our results revealed rates of postoperative complications, invasive respiratory support, residual lung reinfection, and TB recurrence in the DL + massive hemoptysis group of 45.2%, 21.4%, 20.5%, and 15.4%, respectively. Our study also suggests that patients with extensive surgical resection have a high incidence of postoperative complications, that anaemia and intraoperative bleeding are risk factors for the need for invasive ventilatory support in the postoperative period, and that patients with DL combined with massive haemoptysis have a high rate of long-term residual lung infection.

Our research suggests that the history of pulmonary tuberculosis in the DL group is higher than that DL + massive hemoptysis group, which may be related to the high proportion of CPA, which is more likely to cause hemoptysis. In the DL + hemoptysis group, the proportion of pulmonary infections is high, and CPA is more prone to recurrent hemoptysis, which may be related to the high proportion of anemia in the DL + hemoptysis group.

In our study, the postoperative complication rate was higher in the DL combined with haemoptysis group than in the DL group, which may be related to the proportion of patients with diabetes and the high rate of preoperative bacterial infection in the haemoptysis group, the large extent of the operation, and the longer duration of the operation. A 1.6–37.7% increase in complication rates after total pneumonectomy compared to lobectomy has been reported [23,24,25,26]. Furthermore, preoperative preparations such as anti-infection, sputum chemotherapy and nutritional therapy may be inadequate for patients with massive haemoptysis. One study reported that emergency surgery may increase postoperative complications by 29.6% [26]. Our study also found that preoperative Hb < 9 g/L and high intraoperative bleeding in patients with DL combined with haemoptysis increased the risk of requiring postoperative respiratory support therapy. The results suggest that in patients with DL combined with haemoptysis, preoperative anaemia should be corrected as far as possible, intraoperative blood transfusion should be given in a timely manner, and postoperative haemoglobin changes should be monitored and blood loss should be replaced in a timely manner to minimise the occurrence of postoperative complications. Wang X et al. showed that regional arterial embolisation combined with surgical treatment can reduce the risk of conventional surgical treatment, shorten the duration of surgery, and reduce postoperative complications, and this finding is also a new treatment modality to reduce postoperative complications in DL patients with preoperative co-morbid haemoptysis [27, 28].

With follow-up, we found that patients with DL combined with haemoptysis had a higher rate of residual lung reinfection in the distant postoperative period than patients in the DL group. It may be related to the high proportion of patients with diabetes in the haemoptysis group, the relatively short preoperative preparation time, the fact that some patients had emergency surgery and the relatively short preoperative anti-infection and anti-tuberculosis treatment time. In our study, more patients in the DL combined with massive haemoptysis group had combined CPA and fewer had a history of TB. Structural damage to the lungs due to TB tended to be more severe than in CPA, possibly related to the lower DLCO in the DL group in our study. CPA is limited to pulmonary cavities and is more prone to massive hemoptysis. CPA is relatively limited, and lung tissue damage may be limited to lung lobes. Long term invasion of pulmonary tissue by Mycobacterium tuberculosis usually leads to more extensive and thorough damage to lung structure. This may be the reason why DLCO is lower in the DL group compared to the DL + hemoptysis group. In our previous study, we also found that TDL combined with CPA increased postoperative complications [15].

This study had several limitations. First, the study was retrospectively designed based on a single-center patient cohort without further stratification of the cohort into subgroups based on high and mild hemoptysis severity. However, all DL patients treated at our center during a period of over 20 years were included in the study as an adequately large sample to provide useful results for improving DL surgical practices. Secondly, the large time span of this study and variable levels of thoracic surgical expertise may have biased our clinical postoperative outcomes-based results. Finally, long-term DL patient outcomes may be influenced by factors that are not easily controlled by clinicians, such as patient lifestyle, environmental factors, patient psychiatric factors, and so on.

Conclusion

Our retrospective study on the surgical treatment of massive haemoptysis in combination with destroyed lung found higher rates of postoperative complications and need for invasive respiratory support in patients with DL combined with massive haemoptysis, but no difference in near or long-term survival. Extensive surgical resection, preoperative anaemia and heavy intraoperative bleeding are associated with recent postoperative complications, and DL with haemoptysis is more likely to result in postoperative residual lung reinfection. Clinicians need to actively address risk factors to reduce postoperative complications and improve the long-term prognosis of patients.

Data availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Abbreviations

TDL:

Tuberculosis-destroyed lung

CPA:

Chronic pulmonary aspergillosis

BPF:

Bronchopleural fistula

MDR-TB:

Multidrug-resistant tuberculosis

XDR-TB:

Extensively drug-resistant tuberculosis

BMI:

Body mass index

FEV1% pred:

Forced expiratory volume in one second of predicted

MMV% pred:

Maximal minute ventilation of predicted

DLCO% pred:

Lung diffusion capacity for carbon monoxide of predicted

CRP:

C-reaction protein

OR:

Odds ratio

CI:

Confidence interval

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Author notes

  1. Jing Zhao, Xiaoman Cao and Yunsong Li contributors and co-first authors.

Authors and Affiliations

  1. Department of Anesthesia, Beijing Chest Hospital, Capital Medical University, Beijing Tuberculosis and Thoracic Tumor Research Institute, Beijing, P. R. China

    Jing Zhao & Xiaoman Cao

  2. Department of Thoracic Surgery, Beijing Chest Hospital, Capital Medical University, Beijing Tuberculosis and Thoracic Tumor Research Institute, Beijing, P. R. China

    Yunsong Li & Dongjie Yan

  3. Department of Science and Technology, Beijing Chest Hospital, Capital Medical University, Beijing Tuberculosis and Thoracic Tumor Research Institute, No 9, Bei guan Street, Tong Zhou District, Beijing, 101149, P. R. China

    Fangchao Liu

  4. Department of Cellular and Molecular Biology, Beijing Chest Hospital, Capital Medical University, Beijing Tuberculosis and Thoracic Tumor Research Institute, No 9, Bei guan Street, Tong Zhou District, Beijing, 101149, P. R. China

    Shuye Lin & HongYun Ruan

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Contributions

J.Z. and H.R. wrote the main manuscript text and X.C. prepared Figs. 1, 2, 3 and 4. All authors reviewed the manuscript.

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Correspondence to Fangchao Liu, Shuye Lin or HongYun Ruan.

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Approved by the Ethics Committee of Beijing Chest Hospital, Capital Medical University (Ethics No: Clinical Research 2018 (43)).Clinical data were extracted from the hospital’s electronic medical records system. publication of such data does not compromise anonymity or confidentiality. Any participants will fully anonymous. The Ethics Committee of Beijing Chest Hospital of Capital Medical University waived the written informed consent of the patients in this study.

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Zhao, J., Cao, X., Li, Y. et al. Prognostic analysis of destroyed-lung patients with preoperative massive hemoptysis: a 20-year retrospective study. BMC Pulm Med 24, 402 (2024). https://doi.org/10.1186/s12890-024-03205-4

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BMC Pulmonary Medicine

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