a Treatment Option in End-Stage Lung Disease
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Background: Lung transplantation is the final treatment option in the end stage of certain lung diseases, once all possible conservative treatments have been exhausted. Depending on the indication for which lung transplantation is performed, it can improve the patient’s quality of life (e.g., in emphysema) and/or prolong life expectancy (e.g., in cystic fibrosis, pulmonary fibrosis, and pulmonary arterial hypertension). The main selection criteria for transplant candidates, aside from the underlying pulmonary or cardiopulmonary disease, are age, degree of mobility, nutritional and muscular condition, and concurrent extrapulmonary disease. The pool of willing organ donors is shrinking, and every sixth candidate for lung transplantation now dies while on the waiting list.
Methods: We reviewed pertinent articles (up to October 2013) retrieved by a selective search in Medline and other German and international databases, including those of the International Society for Heart and Lung Transplantation (ISHLT), Eurotransplant, the German Institute for Applied Quality Promotion and Research in Health-Care (Institut für angewandte Qualitätsförderung und Forschung im Gesundheitswesen, AQUA-Institut), and the German Foundation for Organ Transplantation (Deutsche Stiftung Organtransplantation, DSO).
Results: The short- and long-term results have markedly improved in recent years: the 1-year survival rate has risen from 70.9% to 82.9%, and the 5-year survival rate from 46.9% to 59.6%. The 90-day mortality is 10.0%. The postoperative complications include acute (3.4%) and chronic (29.0%) transplant rejection, infections (38.0%), transplant failure (24.7%), airway complications (15.0%), malignant tumors (15.0%), cardiovascular events (10.9%), and other secondary extrapulmonary diseases (29.8%). Bilateral lung transplantation is superior to unilateral transplantation (5-year survival rate 57.3% versus 47.4%).
Conclusion: Seamless integration of the various components of treatment will be essential for further improvements in outcome. In particular, the follow-up care of transplant recipients should always be provided in close cooperation with the transplant center.
For patients with terminal lung conditions such chronic obstructive lung disease (COPD), lung transplantation (LuTx) offers treatment to improve quality of life and additionally, in those with certain other diseases—e.g., cystic fibrosis (CF), idiopathic pulmonary fibrosis (IPF), and pulmonary arterial hypertension (PAH)—to prolong life (1, 2, e1). It is used at the point when, despite treatment by all available conservative methods, the patient’s quality of life will be clearly impaired or life shortened if transplantation does not take place (3, 4, e2).
- Unilateral (single lung) transplantation (SLuTx)
- Bilateral (double lung) transplantation (DLuTx)
- Combined heart–lung transplantation (HLuTx)
- Transplantation of individual pulmonary lobes from living donors.
The last of these options is practiced in only a few centers in the world, and at present is burdened with the weight, not only of non-negligible risks for two healthy living donors, but also of an agglomeration of associated ethical difficulties, and for this reason it will not be discussed further in this article (e5).
Analysis of data from the relevant registries show that lung transplantations have been continually on the rise over the past 5 years, despite a reduction in numbers of willing donors. Worldwide, the increase is estimated at 30% (International Society for Heart and Lung Transplantation, ISHLT), while in Germany the figure is 19% (German Foundation for Organ Transplantation, DSO [Deutsche Stiftung Organtransplantation]). According to data from the ISHLT, 3519 lung transplantations were carried out worldwide in 2010, 298 of them in Germany (6, 7, e6). For 2012, the DSO recorded 357 organ transplantations (7). It is against the background of this positive development that the present article has been written to give an up-to-date overview of the topic of lung transplantation, and to answer questions on the key components of the therapy: recipient selection, contraindications, waiting lists, organ allocation procedures, surgical procedure, postoperative immune suppression, aftercare, early and late complications, rehabilitation, and recent long-term results (eFigure).
Lung transplantation is a highly complex treatment that carries considerable peri- and postoperative risks. It is a treatment option for patients whose pulmonary function, exercise capacity, and quality of life are drastically restricted and whose predicted 5-year survival is less than 50% (for indications and indication criteria, see Table 1 and Box 1) (8, 9, e7, e8, e9, e10, e11, e12, e13, e14). Which form of lung transplantation is carried out depends on the underlying disease. In terms of 5-year survival, DLuTx is superior to SLuTx (57.3% versus 47.4%), so the number of DLuTx procedures has been continually rising since the mid-1990s while the number of SLuTx has remained relatively constant (6). The number of HLuTx procedures carried out worldwide has remained relatively constant at a mean of 70 to 90 procedures per year (6).
Older patients have a poorer survival rate after lung transplantation than do younger ones (Figure 1a) (6, e6, e15, e16). For this reason, the surgical indications for SLuTx in patients over the age of 60, DLuTx in patients over the age of 55, and HLuTx in patients over the age of 50 should be tested with a critical eye (Figure 1b) (8). However, a patient’s actual age is not per se an exclusion criterion for transplantation (10, e17).
Evaluation of the patient’s biological age has proved useful for guidance (among other things for determining risk factors for cardiovascular and metabolic disease, and evaluation of data on lifestyle and psychosocial environment) (e18, e19).
The selection of suitable candidates to receive a transplant is done at the transplantation center, taking account of disease-specific factors, analysis of risk factors, and any contraindications present (Box 2) (11, 12, 13, 14, e7, e16, e20, e21). Poor physical status and severe organ dysfunction can be contraindications for transplantation in any age group. On the other hand, with intensive physiotherapeutic exercise and targeted rehabilitation, the condition even of patients with severe, advanced-stage chronic lung disease can be improved to the point at which they are ready to undergo transplantation (e22, e23, e24, e25).
Waiting list and organ allocation procedure
Early attendance at a transplantation center (there are 14 at present in Germany) is obligatory (Case illustration). The time at which a patient is placed on the waiting list is determined by the disease course and the expected waiting time until transplantation (Eurotransplant: <12 months for 74% of patients in 2012) (7, 15, e26, e27, e28, e29). A basic diagnostic program is followed by consultations between the patient and the transplantation team (Table 2a): based on symptoms, clinical findings, patient motivation, and the expected risk–benefit ratio between transplantation and the natural course of the disease, decisions are made about whether to carry out further investigations (“screening,” Table 2b) (16, e7, e18). Direct statistical comparison between predicted survival in the natural course of the underlying disease and actual survival after lung transplantation is not possible, however (9). Once the patient has been placed on the waiting list, the waiting time until transplantation takes place should be used to correct over- or underweight, update the patient’s immunization status, and carry out muscle strengthening exercise (17, 18, e25, e30, e31).
In December 2011, listing according to HU/U status (“highly urgent/urgent”) was replaced by a “lung allocation score” (LAS). Like listing by HU/U status, listing by LAS reflects the urgency of the transplantation, but is more transparent, because the LAS is calculated by an internet program (optn.transplant. hrsa.gov; www.eurotransplant.org/cms/index.php? page= las_calculator) that is accessible to both the doctor and the patient. This program sets the mortality rate of patients on the waiting list and the risk associated with lung transplantation against the benefit the patient would receive from transplantation (19, e32). The values calculated in this way are standardized on a scale of 0 to 100 and this gives the individual LAS. The value of the LAS correlates with the urgency of transplantation (e33, e34). All patients on the waiting list undergo outpatient check-ups at frequent intervals to test and document the indications for surgery in order to update and, if appropriate, increase the LAS.
In Germany, there are many more potential lung recipients than donated organs: lungs are harvested from only about one in five multiorgan donors, because the donors do not fulfill the minimum criteria for lung donation (Table 2c). Because of this relative lack of organs, about one in six German patients waiting for a lung transplant dies before receiving it (Eurotransplant 2012: 70 out of 459 patients, i.e., 15.3%). For this reason, at present a move is under way to extend the criteria for organ donation (e35, e36, e37, e38).
The conflicts over the practice of allocating abdominal organs, currently much discussed, raise the question of the status quo of organ allocation. Especially in regard to lung transplantation, it may be noted that, with the “multiple eye principle,” together with the complex data collection included in LAS generation and the obligatory transplantation conferences held at the large centers, the required transparency has already been in place for a long time.
Operative time for a SLuTx is 2 to 3 hours; for a DLuTx it is about 4 to 6 hours. A cardiopulmonary bypass is used in about 20% of LuTx, if right heart failure and an excessive rise in pulmonary blood pressure occur during tentative clamping of the pulmonary artery, or if limited gas exchange occurs during one-lung ventilation (20, 21, e39). In addition to being technically simpler, not employing extracorporeal circulation has the advantage of resulting in less reperfusion injury to the allograft in the postoperative period (21). In isolated LuTx, the airway anastomosis on the main bronchi is carried out either end-to-end or using the so-called telescope technique; in HLuTx it is performed en bloc in the region of the distal trachea (e40, e41). The bronchial arterial supply is transected proximally and nonselectively anastomosed in LuTx, with the result that bronchial mucosal ischemia often occurs in the anastomotic region (e42, e43, e44, e45). Retrograde revascularization occurs over the course of several weeks (e46, e47). Minimally invasive procedures (anterolateral thoracotomy without sternotomy) have cosmetic advantages compared to classical thoracosternotomy, and reduce postoperative pain and wound healing disorders. They also leave important structural elements of the thorax intact (e17). Once transferred to the intensive care unit, many patients can be extubated after as little as 24 hours.
Postoperative immune suppression and aftercare
Since the lung has its own immunological competence, transports the entire cardiac output, and thus possesses a large immune-active interaction area, particularly intensive immune suppression is needed after lung transplantation (e48). Normally, immune suppression is achieved with the triple combination of a calcineurin inhibitor (CNI) (ciclosporin A, tacrolimus), a cell cycle inhibitor (azathioprine, mycophenolate mofetil), and prednisolone (22, 23, e49, e50, e51). In recent years, the introduction of the mammalian target of rapamycin (mTOR) inhibitors (sirolimus and everolimus) and of the anti-CD25 antibody (daclizumab, basiliximab—induction therapy only) has widened the range of combinations (24, 25, e52, e53, e54). As to the incidence of chronic transplant rejection, randomized controlled studies have failed to indicate clear superiority of any of the above-named drug groups (26). Triple immune suppression is continued for the rest of life, unless severe adverse effects occur (23).
Infection prophylaxis is with valganciclovir in the case of cytomegalovirus (CMV) (or, where donor and recipient are CMV-negative, with aciclovir) (27, e55, e56, e57, e58, e59, e60), and with lifelong administration of cotrimoxazole in the case of Pneumocystis jrovecii pneumonia (28).
Follow-up care after lung transplantation includes monitoring of transplant function, assessment for known complications of transplantation by lung function tests, as well as clinical, radiological, chemical, and microbiological investigations (18, 29, e61, e62, e63, e64, e65). For early identification of problems on the tightrope walk between chronic organ rejection (bronchiolitis obliterans syndrome [BOS], incidence 38.9% within 5 years) and infection, organ recipients carry out an outpatient lung function measurement at home every day of their lives (30, e66). Usually, lung function increases at first and reaches a relatively stable plateau after 3 to 6 months. If function deteriorates (drop in functional 1-second capacity, [FEV1] by ≥10% of the baseline value), or newly developed cough, mucus, fever, or breathlessness occur, the transplantation center should be contacted immediately for further diagnostic investigation, which may be invasive (e8, e67). In addition to infection and rejection, recurrences of the underlying disease (e.g., sarcoidosis, pulmonary histiocytosis X, or lymphangioleiomyomatosis) may occur in the allograft after LuTx (30, e61, e68, e69), and these must be included in the differential diagnosis.
Early and late complications
The most serious complications during the first month after LuTx are primary graft dysfunction (PGD), donor-mediated pneumonia or pneumonia of other primary infectious origin, antibody-mediated hyperacute rejection (fairly rare), problems with the vascular and bronchial anastomoses, and periods of acute cellular rejection (31, e18, e70, e71, e72, e73, e74) (Table 3a). Average 90-day mortality is 10% (6).
PGD is the most frequent cause of death in the first 30 days after LuTx (10% to 25%) (6, 31). The clinical features are similar to those of acute respiratory distress syndrome (ARDS), and mortality is between 50% and 73% (6, 31). Most cases of PGD are caused by ischemia–reperfusion injury. More rarely, infections and rejection reactions may act as triggers (31).
Rejection: clinical features and diagnosis
One-off or recurrent periods of rejection increase the probability of BOS, reduce graft function permanently, and hence endanger the patient’s long-term survival (26, e75, e76). Since most acute rejections of lung allografts occur within the first 2 years after transplantation (33.9%), accurate diagnosis and staging of rejection are essential during this period in particular (e77, e78, e79, e80, e81). Clinical signs of acute cellular rejection are nonspecific symptoms such as fatigue, raised body temperature, dyspnea, cough, increased mucus, hypoxemia, drop in FEV1, interstitial infiltrates, and pleural effusions (32). Higher-grade rejection can be accompanied by acute breathlessness with dramatic symptoms (e82). Spirometry can indicate infections and rejection reactions (drop in FEV1), but cannot distinguish between them (e83). Similarly, thoracic imaging can indicate nonspecific changes and hence the possibility of a rejection reaction, but only indirectly (e.g., by showing septal thickening, infiltrates, pleural effusions) (e61). For clinical follow-up after LuTx, bronchoscopy with bronchoalveolar lavage (eosinophilia, lymphocyte proliferation) and transbronchial biopsy (lymphocytic infiltration) have become established as standard techniques for rejection diagnosis, due to their high sensitivity and specificity (33, e84, e85, e86, e87).
Treatment of acute rejection is in accordance with the following parameters. The standard therapy is intravenous administration of 500 to 1000 mg methylprednisolone (15 mg/kg body weight per day) on each of 3 successive days (e88). In the case of steroid-refractory or early recurrent rejection, the immunosuppressive treatment is altered (e.g., change of CNI or exchange of CNI for mTOR inhibitors) (e89). Alternatively—although they are associated with considerable early and late toxicity—monoclonal or polyclonal antibodies may be given.
Infections are the main cause of death in the first year after transplantation (ISHLT Registry: 38.0%; AQUA Institute: 35%) (e6). In addition to the medical immune suppression, the fact that the lung, unlike other transplantable solid organs, is permanently directly exposed to the environment means that there is an increased risk of infection (34, e90, e91, e92). Furthermore, the lack of cough reflex in the transplant, together with simultaneous reduction of mucociliary clearance due to denervation and interruption of the lymphatics, also play a role (34, e93). Three out of four graft infections occur in the airways, either due to pathogen transfer from the donor or to pathogens descending from the upper airways in recipients who already have chronic bacterial colonization (e.g., those with bronchiectasia or cystic fibrosis) (34, e94, e95, e96). Other predisposing factors are airway stenosis and postoperative ischemia, especially in the area of the anastomosis due to epithelial damage (e41, e42, e43, e47, e97). The incidence of postoperative pneumonia is markedly higher after LuTx than, for example, after heart transplantation (6, e98). During hospitalization, gram-negative pathogens predominate, whereas during the outpatient phase, infections by pneumococci, Hemophilus species, and atypical pathogens prevail (34).
The prevalence of clinically significant airway complications is 10% to 15% (35, e99). Within the first 6 postoperative months, the interruption of the bronchial arterial supply to the donor lung can lead to ischemic necrosis at the bronchial anastomoses (e97). This may be expressed by obstructive granulation tissue (stricture, atelectasis), dehiscence, infections, or bronchomalacia (e100, e101). In addition to the extent of the ischemia in the area of the anastomosis, other risk factors are size disproportion between donor and recipient, and Aspergillus spp. colonization (e102, e103, e104). Treatment options include bronchial stent implantation, bronchoscopic balloon dilation, intrabronchial disobliteration techniques (argon plasma coagulation, laser and cryotherapy) and surgical revision, among others (e104, e105).
Five years after LuTx, 37% of patients show chronic renal failure (glomerular filtration rate [GFR] <50% of the norm) (e106) (Table 3b). Five percent of transplanted patients require dialysis because of preexisting concomitant disease or CNI therapy.
Five years after transplantation, 82% of patients are suffering from arterial hypertension, 58% from hyperlipoproteinemia, and 41% from diabetes mellitus (6). However, cardiovascular diseases are the cause in only 5% of deaths (32). The reason for this is the younger average age of transplanted patients and their lower life expectancy compared to the normal population. For antihypertensive therapy, angiotensin converting enzyme (ACE) inhibitors and calcium antagonists are preferred; verapamil and diltiazem raise the concentration of immune suppressants. In the early postoperative period, atrial tachycardia often occurs, caused by electrolyte disturbances, hypoxemia, ischemia, or atrial reentry mechanisms. Pharmacologically, particular attention must be paid to drugs that prolong the Q–T interval (e107).
Within the first 5 years after transplantation, 15% of patients with lung transplants develop malignant tumors (Table 3c) (6, 36, 37, 38, e108, e109). For skin tumors, exposure to the sun plays an important role, so these tumors are variably distributed in different regions of the world. The incidence of lymphoma is related both to Epstein–Barr virus infection and to the amount of lymph tissue transferred (e110).
The patient’s preoperative physical constitution, together with muscle status, transplant function, complications, immune suppression, and potential risks over the long term, necessitate a structured rehabilitation program (39). In addition to stamina, interval, and strength training, respiratory therapy and physiotherapy, psychological counseling, and nutritional advice are given, to educate the patient about the effects of immune suppression and possible concomitant diseases (diabetes mellitus, renal failure, over- or underweight), and to treat them (e111, e112).
After about 6 to 12 months, patients can gradually start to go back to work or retrain for an occupation involving light physical work, provided anti-infection measures are taken (e113).
Recent long-term results
Compared to the natural course (40, e114), increased survival rates among transplanted patients are reported particularly for the first postinterventional year. In the long term, mainly organ-specific problems occur (eTable a and b) (e6). Irrespective of survival time, what is most important to patients is the marked improvement in quality of life (2, e1, e115, e116). To further optimize long-term results, intensive pulmonological support and follow-up care in the transplantation centers and obligatory close collaboration with patients’ resident practitioner and local hospitals are essential.
The authors thank Katrin Pitzer-Hartert, MA, for editorial input in the preparation of this manuscript.
Conflict of interest statement
Dr. Senbaklavaci has received a research grant (third-party funding) in chest surgery from the German Society for Thoracic and Cardiovascular Surgery (DGTHG, Deutsche Gesellschaft für Thorax-, Herz- und Gefäßchirurgie)
The other authors declare that no conflict of interest exists.
Manuscript received on 25 March 2013, revised version accepted on
12 November 2013.
Translated from the original German by Kersti Wagstaff, MA.
Klinik und Poliklinik für Herz-, Thorax- und Gefäßchirurgie
Universitätsmedizin der Johannes Gutenberg-Universität Mainz
@For e-references please refer to:
eBox and eTable:
Department of Hematology, Pneumology and Oncology at the University Medical Center of the Johannes Gutenberg University Mainz: Dr. med. Fischer, Prof. Dr. med. Buhl
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