Impact of CLAD Phenotype on Survival After Lung Retransplantation: A Multicenter Study
Open accessAbstract
Chronic lung allograft dysfunction (CLAD) remains a major problem after lung transplantation with no definitive treatment except redo lung transplantation (re-LTx) in selected candidates. However, CLAD is not a homogeneous entity and different phenotypes exist. Therefore, we aimed to evaluate the effect of CLAD phenotypes on survival after re-LTx for CLAD. Patients who underwent re-LTx for respiratory failure secondary to CLAD in four LTx centers between 2003 and 2013 were included in this retrospective analysis. Bronchiolitis obliterans syndrome (BOS) and restrictive CLAD (rCLAD) were distinguished using pulmonary function, radiology and explant lung histopathology. Patient variables pre- and post-re-LTx were collected and analyzed. A total of 143 patients underwent re-LTx for CLAD resulting in 94 BOS (66%) and 49 rCLAD (34%) patients. Unadjusted and adjusted survival after re-LTx for rCLAD was worse compared to BOS (HR = 2.60, 1.59-4.24; p < 0.0001 and HR = 2.61, 1.51-4.51; p = 0.0006, respectively). Patients waiting at home prior to re-LTx experienced better survival compared to hospitalized patients (HR 0.40; 0.23-0.72; p = 0.0022). Patients with rCLAD redeveloped CLAD earlier and were more likely to redevelop rCLAD. Survival after re-LTx for rCLAD is worse compared to BOS. Consequently, re-LTx for rCLAD should be critically discussed, particularly when additional peri-operative risk factors are present.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Younger age, lower acute graft dysfunction, and longer interval between primary and ReTx have all been previously linked to ReTx survival differences.
“These factors had all been previously linked to ReTx survival differences.3, 4, 5, 6, 7, 8, 10, 11, 12, 13”
From Lung retransplantation during the Lung Allocation Score era: Outcomes from a large single center (2026) · cites this paper as [13]
The Results section (Survival after re-LTx; page unavailable) reports that lower primary graft dysfunction (PGD) grades 48 hours after retransplantation were associated with better survival. It includes recipient age as an adjustment variable but does not report a survival benefit for younger recipients, and the passages found do not link a longer interval between primary transplantation and retransplantation to survival. (LLM, conf=0.86)
Experimental — accuracy not yet measuredOur observed CLAD-free survival at 3 and 5 years following ReTx was comparable to prior reports.
“Our observed CLAD-free survival at 3 and 5 years following ReTx was comparable to prior reports.8, 13”
From Lung retransplantation during the Lung Allocation Score era: Outcomes from a large single center (2026) · cites this paper as [13]
The Results (Second transplant characteristics; page unavailable) report CLAD-free survival after retransplantation and find it shorter for rCLAD than for BOS. The cited copy does not give 3- or 5-year CLAD-free survival estimates or compare those estimates with prior reports. Its Discussion compares overall survival, which is a different outcome. (LLM, conf=0.78)
Experimental — accuracy not yet measuredThere was no significant difference in the survival rate, but the survival rate was lower in patients who underwent lung re-transplantation.
“although there was no significant difference in the survival rate, the survival rate was lower in patients who underwent lung re-transplantation [33,34].”
From Indications for Lung Transplantation and Patient Selection (2022) · cites this paper as [33]
The Discussion (page unavailable) reports median survival of 5.3 years after retransplantation for BOS versus 6.1 years in registry data for primary transplantation, describing them as comparable; it reports much worse survival of 1.7 years for retransplantation with rCLAD. That supports a lower descriptive survival figure, but the paper does not report a significance test comparing retransplantation overall with primary transplantation, so it does not establish the claimed nonsignificant difference. (LLM, conf=0.84)
Experimental — accuracy not yet measuredA history of previous thoracic surgery, pleural disease, and pleural procedures may make the operation difficult and time-consuming and may cause massive bleeding, potentially increasing the incidence of mortality or graft dysfunction.
“A history of previous thoracic surgery, pleural disease, and pleural procedures may make the operation difficult and time-consuming and may cause massive bleeding, potentially increasing the incidence of mortality or graft dysfunction.”
From Indications for Lung Transplantation and Patient Selection (2022) · cites this paper as [33]
The Discussion (page unavailable) says pleural fibrosis in patients with restrictive CLAD may pose a surgical challenge during lung retransplantation. The Results (page unavailable) report longer operations, more blood transfusions, higher primary graft dysfunction scores, and worse survival in that group. The paper does not establish that a history of thoracic surgery or pleural procedures causes massive bleeding or the stated outcomes. (LLM, conf=0.86)
Experimental — accuracy not yet measuredA history of previous thoracic surgery, pleural disease, and pleural procedures is not a contraindication to lung transplantation.
“However, these are not contraindications to lung transplantation”
From Indications for Lung Transplantation and Patient Selection (2022) · cites this paper as [33]
The Methods (Patient selection; page unavailable) include patients who underwent lung retransplantation, showing that a prior transplant operation did not categorically preclude another one. The cited passages do not address pleural disease or pleural procedures as contraindications, so those parts of the claim are unsupported. (LLM, conf=0.78)
Experimental — accuracy not yet measured
About 45% of transplant patients had undergone treatment for chest conditions.
“about 45% of transplant patients had undergone treatment for chest conditions”
From Indications for Lung Transplantation and Patient Selection (2022) · cites this paper as [33]
The Results (Second transplant characteristics; page unavailable) say that 62 patients—about 44% of those with admission data—were admitted to a ward or ICU while awaiting retransplantation. Admission is not the same as having undergone treatment for chest conditions. The Patient selection section identifies patients undergoing retransplantation for chronic lung allograft dysfunction, but our copy does not report the claimed treatment history for about 45% of patients. (LLM, conf=0.75)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The impact of recipient body mass index on survival after lung transplantation
Allen, J. G., Arnaoutakis, G. J., Weiss, E. S., Merlo, C. A., Conte, J. V., & Shah, A. S. (2010) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2010.05.005 · Cited by 128 · see citing works
Outcomes after Lung Retransplantation in the Modern Era
Kawut, S. M., Lederer, D. J., Keshavjee, S., Wilt, J. S., Daly, T., D'Ovidio, F., Sonett, J. R., Arcasoy, S. M., & Barr, M. L. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200707-1132oc · Cited by 119 · see citing works
Self-citationLong-term outcome after pulmonary retransplantation
Strueber, M., Fischer, S., Gottlieb, J., Simon, A. R., Goerler, H., Gohrbandt, B., Welte, T., & Haverich, A. (2006) · The Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2005.12.059 · Cited by 97 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 14
- [1]Yusen RD Christie JD Edwards LB Kucheryavaya AY Benden C Dipchand AI The Registry of the International Society for Heart and Lung Transplantation: thirtieth adult lung and heart-lung transplant report--2013; focus theme: age J Heart Lung Transplant 2013 10 32 10 965 978 24054805
- [2]Kawut SM Lung retransplantation Clin Chest Med 2011 6 32 2 367 377 21511096 PMC3081645
- [3]Brugiere O Thabut G Castier Y Mal H Dauriat G Marceau A Lung retransplantation for bronchiolitis obliterans syndrome: long-term follow-up in a series of 15 recipients Chest 2003 6 123 6 1832 1837 12796157
- [5]Verleden GM Raghu G Meyer KC Glanville AR Corris P A new classification system for chronic lung allograft dysfunction J Heart Lung Transplant 2014 2 33 2 127 133 24374027
- [6]Sato M Waddell TK Wagnetz U Roberts HC Hwang DM Haroon A Restrictive allograft syndrome (RAS): a novel form of chronic lung allograft dysfunction J Heart Lung Transplant 2011 7 30 7 735 742 21419659
- [7]Todd JL Jain R Pavlisko EN Finlen Copeland CA Reynolds JM Snyder LD Impact of forced vital capacity loss on survival after the onset of chronic lung allograft dysfunction Am J Respir Crit Care Med 2014 1 15 189 2 159 166 24325429 PMC3983891
- [8]Verleden GM Vos R Verleden SE De WW De Vleeschauwer SI Willems-Widyastuti A Survival determinants in lung transplant patients with chronic allograft dysfunction Transplantation 2011 9 27 92 6 703 708 21836537
- [9]Christie JD Carby M Bag R Corris P Hertz M Weill D Report of the ISHLT Working Group on Primary Lung Graft Dysfunction part II: definition. A consensus statement of the International Society for Heart and Lung Transplantation J Heart Lung Transplant 2005 10 24 10 1454 1459 16210116
- [10]Greer M Dierich M De Wall C Suhling H Rademacher J Welte T Phenotyping established chronic lung allograft dysfunction predicts extracorporeal photopheresis response in lung transplant patients Am J Transplant 2013 4 13 4 911 918 23406373
- [11]Estenne M Maurer JR Boehler A Egan JJ Frost A Hertz M Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria J Heart Lung Transplant 2002 3 21 3 297 310 11897517
- [12]Schafers HJ Hausen B Wahlers T Fieguth HG Jurmann M Borst HG Retransplantation of the lung. A single center experience Eur J Cardiothorac Surg 1995 9 6 291 295 7546799
- [14]Saito T Liu M Binnie M Sato M Hwang D Azad S Distinct Expression Patterns of Alveolar "Alarmins" in Subtypes of Chronic Lung Allograft Dysfunction Am J Transplant 2014 5 1 24787265
- [15]Verleden SE Ruttens D Vandermeulen E Van Raemdonck DE Vanaudenaerde BM Verleden GM Elevated bronchoalveolar lavage eosinophilia correlates with poor outcome after lung transplantation Transplantation 2014 1 15 97 1 83 89 24157472
- [17]Ofek E Sato M Saito T Wagnetz U Roberts HC Chaparro C Restrictive allograft syndrome post lung transplantation is characterized by pleuroparenchymal fibroelastosis Mod Pathol 2013 3 26 3 350 356 23018877
Cited by
Sorted by citations
Leard, L. E., Holm, A. M., Valapour, M., Glanville, A. R., Attawar, S., Aversa, M., Campos, S. V., Christon, L. M., Cypel, M., Dellgren, G., et al. (2021) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2021.07.005 · Cited by 821 · see citing works
“1,139,140 Pneumothorax / Pleurodesis : When possible, management of a pneumothorax in a patient who may be a potential lung transplant candidate should be discussed with a transplant center.”
BackgroundHoetzenecker, K., Donahoe, L., Yeung, J. C., Azad, S., Fan, E., Ferguson, N. D., Del Sorbo, L., de Perrot, M., Pierre, A., Yasufuku, K., et al. (2018) · The Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2017.09.161 · Cited by 164 · see citing works
Self-citationOutcomes following lung re-transplantation in patients with cystic fibrosis
Chan, E. G., Hyzny, E. J., Ryan, J. P., Morrell, M. R., Pilewski, J., & Sanchez, P. G. (2022) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2021.12.002 · Cited by 23 · see citing works
Lung retransplantation in the modern era
Rucker, A. J., Nellis, J. R., Klapper, J. A., & Hartwig, M. G. (2021) · Journal of Thoracic Disease · doi:10.21037/jtd-2021-25 · Cited by 23 · see citing works
Salman, J., Ius, F., Sommer, W., Siemeni, T., Fleissner, F., Alhadidi, H., Kugler, C., Avsar, M., Haverich, A., Warnecke, G., et al. (2019) · Progress in Transplantation · doi:10.1177/1526924819835815 · Cited by 15 · see citing works
Self-citationIndications for Lung Transplantation and Patient Selection
Son, J., & Shin, C. (2022) · Journal of Chest Surgery · doi:10.5090/jcs.22.057 · Cited by 9 · see citing works
“According to a recent report, about 45% of transplant patients had undergone treatment for chest conditions, and although there was no significant difference in the survival rate, the survival rate was lower in patients who underwent lung re-transplantation [33,34].”
BackgroundMichel, E., Galen Hartwig, M., & Sommer, W. (2022) · Thoracic Surgery Clinics · doi:10.1016/j.thorsurg.2021.12.001 · Cited by 6 · see citing works
Lung retransplantation during the Lung Allocation Score era: Outcomes from a large single center
Laothamatas, K., Salvatori, C., Grewal, H. S., Sonnick, M., Vasilescu, E.-R., Shah, L., Robbins, H., DiMango, A., Magda, G., Stanifer, B. P., et al. (2026) · JHLT open · doi:10.1016/j.jhlto.2026.100501 · Cited by 4 · see citing works
Worth a Double Take? An In-Depth Review of Lung Retransplantation
Dawodu, G., Gulati, S., Bugacov, H., Laskey, D., Housman, B., Seethamraju, H., & Scheinin, S. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12237418 · Cited by 4 · see citing works
- Authors
- Verleden, S. E., Todd, J. L., Sato, M., Palmer, S. M., Martinu, T., Pavlisko, E. N., Vos, R., Neyrinck, A., Van Raemdonck, D., Saito, T., Oishi, H., Keshavjee, S., Greer, M., Warnecke, G., Gottlieb, J., & Haverich, A.
- Affiliations
- KU Leuven (BE)
- Duke Medical Center (US)
- University Health Network (CA)
- Medizinische Hochschule Hannover (DE)
- Corresponding author
- Verleden, S.E.
- ORCID
- Venue
- American Journal of Transplantation
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 15
- Issue
- 8
- Pages
- 2223-2230
- ISSN
- 1600-6135 (ISSN-L)
- PMC
- PMC4943073
- OpenAlex
- W1540147815
- Cited by
- 123
- References
- 3
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 7 · 2023: 12 · 2022: 7 · 2021: 18 · 2020: 12 · 2019: 16 · 2018: 21 · 2017: 10 · 2016: 9
- FWCI
- 13.44
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- American Journal of Transplantation (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Lirias (submittedVersion, other-oa)
- Funders
- Fonds Wetenschappelijk Onderzoek (12G8715N)
- Clinical trials in organ transplantation (UO1-AI113315)
- Topics
- Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
- Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Keywords
- chronic lung allograft dysfunction, lung retransplantation, bronchiolitis obliterans syndrome, post-transplant survival, respiratory failure
- MeSH terms
- Adult, Female, Humans, Male, Middle Aged, Phenotype, Survival Rate, Lung Transplantation, Primary Graft Dysfunction, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review