Influence of cytokines, circulating markers and growth factors on liver regeneration and post-hepatectomy liver failure: a systematic review and meta-analysis
Open accessAbstract
The pathophysiology of post-hepatectomy liver failure is not entirely understood but is rooted in the disruption of normal hepatocyte regeneration and homeostasis. Current investigations of post-hepatectomy liver failure and regeneration are focused on evaluation of circulating hepatic function parameters (transaminases, cholestasis, and coagulation parameters), volumetry and hepatic hemodynamics. However, identification of biochemical factors associated with regeneration and post hepatectomy liver failure is crucial for understanding the pathophysiology and identification of patients at risk. The objective of the present systematic review was to identify circulating factors associated with liver regeneration and post hepatectomy liver failure in patients undergoing hepatectomy. The quantitative analysis was intended if studies provided sufficient data. Electronic databases (MEDLINE via PubMed, Web of Knowledge, Cochrane Library and WHO International Clinical Trials Registry Platform) were searched for publications on cell signaling factors in liver regeneration and post-hepatectomy liver failure following liver resection in clinical setting. No date restriction was given. No language restriction was used. Studies were assessed using MINORS. This study was registered at PROSPERO (CRD42020165384) prior to data extraction. In total 1953 publications were evaluated for titles and abstracts after exclusion of duplicates. Full texts of 167 studies were further evaluated for inclusion. 26 articles were included in the review and 6 publications were included in the meta-analyses. High levels of serum hyaluronic acid even preoperatively are associated with PHLF but especially increased levels early after resection are predictive of PHLF with high sensitivity and specificity. Postoperative elevation of HA to levels between 100 and 500 ng/ml is increased the risk for PHLF ([OR] = 246.28, 95% [CI]: 11.82 to 5131.83; p = 0.0004) Inteleukin-6 levels show contradicting result in association with organ dysfunction. HGF positively correlates with liver regeneration. Overall, due to heterogeneity, scarcity, observational study design and largely retrospective analysis, the certainty of evidence, assessed with GRADE, is very low. High levels of serum hyaluronic acid show a strong association with PHLF and increased levels after resection are predictive of PHLF with high sensitivity and specificity, even on POD1. Interleukin-6 levels need to be studied further due to contradictive results in association with organ dysfunction. For HGF, no quantitative analysis could be made. Yet, most studies find positive correlation between high HGF levels and regeneration. Prospective studies investigating HGF and other growth factors, hyaluronic acid and interleukins 1 and 6 in correlation with liver regeneration measured sequentially through e.g. volumetry, and liver function parameters, preferably expanding the analysis to include dynamic liver function tests, are needed to sufficiently illustrate the connection between biomolecule levels and clinical outcomes.
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?
This heterogeneity precluded a meta-analysis, specifically in relation to a specific cut-off for early postoperative IL-6 levels to predict ISGLS-CR-PHLF in pre-defined cohorts (e.g., minor versus major resections).
“This precluded a meta-analysis, specifically in relation to a specific cut-off for early postoperative IL-6 levels to predict ISGLS-CR-PHLF in pre-defined cohorts (e.g., minor versus major resections) [31,40].”
From The Role of Perioperative Interleukin-6 Serum Levels on Liver Dysfunction and Infectious Complications After Hepatectomy—A Systematic Review (2025) · cites this paper as [40]
The Discussion > IL-6 reports substantial heterogeneity and says optimal IL-6 thresholds need further study, which supports the difficulty of establishing a cut-off. But the Results > IL-6 report that the authors did perform a meta-analysis of IL-6 and organ dysfunction. Our copy does not establish that heterogeneity precluded the specific analysis of early IL-6 cut-offs for ISGLS-defined clinically relevant PHLF in minor-versus-major resection cohorts. (LLM, conf=0.88)
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
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Wang, G., Ma, R., Qiao, G., Wada, K., Aizawa, Y., & Satoh, T. (2015) · Integrative Medicine International · doi:10.1159/000368408 · Cited by 18,759 · see citing works
Slim, K., Nini, E., Forestier, D., Kwiatkowski, F., Panis, Y., & Chipponi, J. (2003) · ANZ Journal of Surgery · doi:10.1046/j.1445-2197.2003.02748.x · Cited by 7,603 · see citing works
Rahbari, N. N., Garden, O. J., Padbury, R., Brooke-Smith, M., Crawford, M., Adam, R., Koch, M., Makuuchi, M., Dematteo, R. P., Christophi, C., et al. (2011) · Surgery · doi:10.1016/j.surg.2010.10.001 · Cited by 2,319 · see citing works
Interleukin-1 in the pathogenesis and treatment of inflammatory diseases
Dinarello, C. A. (2011) · Blood · doi:10.1182/blood-2010-07-273417 · Cited by 2,248 · see citing works
Molecular cloning and expression of human hepatocyte growth factor
Nakamura, T., Nishizawa, T., Hagiya, M., Seki, T., Shimonishi, M., Sugimura, A., Tashiro, K., & Shimizu, S. (1989) · Nature · doi:10.1038/342440a0 · Cited by 2,158 · see citing works
Michalopoulos, G. K. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21172 · Cited by 1,384 · see citing works
The Brisbane 2000 Terminology of Liver Anatomy and Resections
Strasberg, S. M., Belghiti, J., Clavien, P., Gadžijev, E. M., Garden, J. O., Lau, W. Y., Makuuchi, M., & Strong, R. W. (2000) · HPB · doi:10.1016/s1365-182x(17)30755-4 · Cited by 1,308 · see citing works
Liver regeneration: biological and pathological mechanisms and implications
Michalopoulos, G. K., & Bhushan, B. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0342-4 · Cited by 998 · see citing works
IL-6 pathway in the liver: From physiopathology to therapy
Schmidt-Arras, D., & Rose-John, S. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.02.004 · Cited by 881 · see citing works
Huh, C.-G., Factor, V. M., Sánchez, A., Uchida, K., Conner, E. A., & Thorgeirsson, S. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306068101 · Cited by 750 · see citing works
Angiogenesis-Independent Endothelial Protection of Liver: Role of VEGFR-1
LeCouter, J. E., Moritz, D. R., Li, B., Phillips, G. D. L., Liang, X. H., Gerber, H., Hillan, K. J., & Ferrara, N. (2003) · Science · doi:10.1126/science.1079562 · Cited by 677 · see citing works
Searching for and selecting studies
Lefebvre, C., Glanville, J., Briscoe, S., Littlewood, A., Marshall, C., Metzendorf, M., Noel‐Storr, A., Rader, T., Shokraneh, F., Thomas, J., et al. (2019) · Cochrane Handbook for Systematic Reviews of Interventions · doi:10.1002/9781119536604.ch4 · Cited by 647 · see citing works
Nakamura, T., & Mizuno, S. (2010) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.86.588 · Cited by 548 · see citing works
Vollmar, B., & Menger, M. D. (2009) · Physiological Reviews · doi:10.1152/physrev.00027.2008 · Cited by 505 · see citing works
Met provides essential signals for liver regeneration
Borowiak, M., Garratt, A. N., Wüstefeld, T., Strehle, M., Trautwein, C., & Birchmeier, C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403412101 · Cited by 497 · see citing works
Expanding Criteria for Resectability of Colorectal Liver Metastases
Pawlik, T. M., Schulick, R. D., & Choti, M. A. (2008) · The Oncologist · doi:10.1634/theoncologist.2007-0142 · Cited by 450 · see citing works
Liver regeneration — mechanisms and models to clinical application
Forbes, S. J., & Newsome, P. N. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.97 · Cited by 413 · see citing works
Understanding GRADE: an introduction
Goldet, G., & Howick, J. (2013) · Journal of Evidence-Based Medicine · doi:10.1111/jebm.12018 · Cited by 390 · see citing works
Liver Resection and Surgical Strategies for Management of Primary Liver Cancer
Orcutt, S. T., & Anaya, D. A. (2018) · Cancer Control · doi:10.1177/1073274817744621 · Cited by 339 · see citing works
Tilg, H., Moschen, A. R., & Szabó, G. (2016) · Hepatology · doi:10.1002/hep.28456 · Cited by 319 · see citing works
Principles of Liver Regeneration and Growth Homeostasis
Michalopoulos, G. K. (2012) · Comprehensive physiology · doi:10.1002/cphy.c120014 · Cited by 267 · see citing works
Optimal literature search for systematic reviews in surgery
Gooßen, K., Tenckhoff, S., Probst, P., Grummich, K., Mihaljević, A. L., Büchler, M. W., & Diener, M. K. (2017) · Langenbeck s Archives of Surgery · doi:10.1007/s00423-017-1646-x · Cited by 247 · see citing works
Self-citationSchreckenbach, T., Liese, J., Bechstein, W. O., & Moench, C. (2012) · Digestive Surgery · doi:10.1159/000335741 · Cited by 232 · see citing works
Taniguchi, E., Sakisaka, S., Matsuo, K., Tanikawa, K., & Sata, M. (2001) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540104900112 · Cited by 215 · see citing works
Kingham, T. P., Correa‐Gallego, C., D'Angelica, M. I., Gönen, M., DeMatteo, R. P., Fong, Y., Allen, P. J., Blumgart, L. H., & Jarnagin, W. R. (2014) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2014.12.026 · Cited by 184 · see citing works
Apte, U. M., Gkretsi, V., Bowen, W. C., Mars, W. M., Luo, J., Donthamsetty, S., Orr, A., Monga, S. P., Wu, C., & Michalopoulos, G. K. (2009) · Hepatology · doi:10.1002/hep.23059 · Cited by 173 · see citing works
Collagens in the liver extracellular matrix bind hepatocyte growth factor
Schuppan, D., Schmid, M., Somasundaram, R., Ackermann, R., Ruehl, M., Nakamura, T., & Riecken, E. (1998) · Gastroenterology · doi:10.1016/s0016-5085(98)70642-0 · Cited by 167 · see citing works
Post-hepatectomy liver failure.
Kauffmann, R. M., & Fong, Y. (2014) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.2304-3881.2014.09.01 · Cited by 140 · see citing works
Guechot, J., Loria, A., Serfaty, L., Giral, P., GIBOUDEAU, J., & Poupon, R. Y. (1995) · Journal of Hepatology · doi:10.1016/0168-8278(95)80255-x · Cited by 117 · see citing works
Markers of liver regeneration—the role of growth factors and cytokines: a systematic review
Hoffmann, K., Nagel, A. J., Tanabe, K., Fuchs, J., Dehlke, K., Ghamarnejad, O., Lemekhova, A., & Mehrabi, A. (2020) · BMC Surgery · doi:10.1186/s12893-019-0664-8 · Cited by 94 · see citing works
Self-citationRahnemai‐Azar, A. A., Cloyd, J. M., Weber, S. M., Dillhoff, M., Schmidt, C. R., Winslow, E. R., & Pawlik, T. M. (2017) · Journal of Clinical and Translational Hepatology · doi:10.14218/jcth.2017.00060 · Cited by 94 · see citing works
Serum hepatocyte growth factor levels in hepatectomized and nonhepatectomized surgical patients
Tomiya, T., Tani, M., Yamada, S., Hayashi, S., Umeda, N., & Fujiwara, K. (1992) · Gastroenterology · doi:10.1016/0016-5085(92)91186-8 · Cited by 91 · see citing works
Hypoxia of the growing liver accelerates regeneration
Schadde, E., Tsatsaris, C., Swiderska‐Syn, M., Breitenstein, S., Urner, M., Schimmer, R. R., Booy, C., Z’graggen, B. R., Wenger, R. H., Spahn, D. R., et al. (2016) · Surgery · doi:10.1016/j.surg.2016.05.018 · Cited by 82 · see citing works
Mehta, P. R., Ploutz-Snyder, R. J., Nandi, J., Rawlins, S., Sanderson, S. O., & Levine, R. A. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2007.01761.x · Cited by 82 · see citing works
Clavien, P., Camargo, C. A., Gorczynski, R. M., Washington, M. K., Levy, G. A., Langer, B., & Greig, P. D. (1996) · Hepatology · doi:10.1002/hep.510230623 · Cited by 81 · see citing works
Complications after liver surgery: a benchmark analysis
Bagante, F., Ruzzenente, A., Beal, E. W., Campagnaro, T., Merath, K., Conci, S., Akgül, Ö., Alexandrescu, S. T., Marques, H. P., Lam, V. W. T., et al. (2019) · HPB · doi:10.1016/j.hpb.2018.12.013 · Cited by 77 · see citing works
The profile of platelet α‐granule released molecules affects postoperative liver regeneration
Starlinger, P. P., Haegele, S., Offensperger, F., Oehlberger, L., Pereyra, D., Kral-Pointner, J. B., Schrottmaier, W. C., Badrnya, S., Reiberger, T., Ferlitsch, A., et al. (2015) · Hepatology · doi:10.1002/hep.28331 · Cited by 75 · see citing works
Das, B. C., Isaji, S., & Kawarada, Y. (2001) · World Journal of Surgery · doi:10.1007/s002680020059 · Cited by 72 · see citing works
Furchtgott, L., Chow, C. C., & Periwal, V. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.01.061 · Cited by 70 · see citing works
Liver Metastases From Breast Cancer: What Role for Surgery? Indications and Results
Golse, N., & Adam, R. A. (2017) · Clinical Breast Cancer · doi:10.1016/j.clbc.2016.12.012 · Cited by 65 · see citing works
Kimura, F., Itoh, H., Ambiru, S., Shimizu, H., Togawa, A., Yoshidome, H., Ohtsuka, M., Shimamura, F., Kato, A., Nukui, Y., et al. (2004) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2003.08.029 · Cited by 63 · see citing works
Kimura, F., Shimizu, H., Yoshidome, H., Ohtsuka, M., Kato, A., Yoshitomi, H., Nozawa, S., Furukawa, K., Mitsuhashi, N., Sawada, S., et al. (2006) · Journal of Surgical Research · doi:10.1016/j.jss.2005.10.025 · Cited by 62 · see citing works
CYTOKINE GENE EXPRESSION IN LIVER FOLLOWING MINOR OR MAJOR HEPATECTOMY IN RAT
Scotté, M., Masson, S., Lyoumi, S., Hiron, M., Ténière, P., Lebreton, J. P., & Daveau, M. (1997) · Cytokine · doi:10.1006/cyto.1997.0273 · Cited by 60 · see citing works
Starring role of toll-like receptor-4 activation in the gut-liver axis
Carotti, S. (2015) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v6.i4.99 · Cited by 57 · see citing works
Small for size liver remnant following resection: prevention and management.
Eshkenazy, R., Dreznik, Y., Lahat, E., Zakai, B. B., Zendel, A., & Ariche, A. (2014) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.2304-3881.2014.09.08 · Cited by 56 · see citing works
Hyaluronic acid as a biomarker of fibrosis in chronic liver diseases of different etiologies
Orasan, O. H., Ciulei, G., Cozma, A., Sava, M., & Dumitrascu, D. L. (2015) · Medicine and Pharmacy Reports · doi:10.15386/cjmed-554 · Cited by 50 · see citing works
Risk assessment for liver resection
Hoffmann, K., Hinz, U., Stravodimos, C., Knoblich, T., Schön, M. R., Büchler, M. W., & Mehrabi, A. (2018) · Surgery · doi:10.1016/j.surg.2018.06.024 · Cited by 48 · see citing works
Self-citationЕфимова, Е. А., Glanemann, M., Liu, L., Schumacher, G., Settmacher, U., Jonas, S., Langrehr, J. M., Neuhaus, P., & Nussler, A. K. (2004) · European Surgical Research · doi:10.1159/000079915 · Cited by 47 · see citing works
de Jong, K. P., von Geusau, B. A., Rottier, C. A., Bijzet, J., Limburg, P. C., de Vries, E. G. E., Fidler, V., & Slooff, M. J. H. (2001) · Journal of Hepatology · doi:10.1016/s0168-8278(00)00030-1 · Cited by 43 · see citing works
Is Hepatic Resection for Non-colorectal, Non-neuroendocrine Liver Metastases Justified?
Hoffmann, K., Bulut, S., Tekbaş, A., Hinz, U., Büchler, M. W., & Schemmer, P. (2015) · Annals of Surgical Oncology · doi:10.1245/s10434-015-4775-x · Cited by 43 · see citing works
Self-citationHow to expand the safe limits in hepatic resections?
Asencio, J. M., Sabrido, J. L. G., & Olmedilla, L. (2014) · Journal of Hepato-Biliary-Pancreatic Sciences · doi:10.1002/jhbp.97 · Cited by 41 · see citing works
Measurement of Serum Hyaluronate as a Predictor of Human Liver Failure after Major Hepatectomy
Yachida, S., Wakabayashi, H., Kokudo, Y., Goda, F., Okada, S., Maeba, T., & Maeta, H. (2000) · World Journal of Surgery · doi:10.1007/s002689910057 · Cited by 38 · see citing works
Changes in Serum Levels of Growth Factors in Healthy Individuals After Living Related Liver Donation
Ефимова, Е. А., Glanemann, M., Nussler, A. K., Schumacher, G., Settmacher, U., Jonas, S., Nüssler, N. C., & Neuhaus, P. (2005) · Transplantation Proceedings · doi:10.1016/j.transproceed.2004.12.170 · Cited by 35 · see citing works
EGFR: A Master Piece in G1/S Phase Transition of Liver Regeneration
de l’Hortet, A. C., Gilgenkrantz, H., & Guidotti, J. (2012) · International Journal of Hepatology · doi:10.1155/2012/476910 · Cited by 35 · see citing works
Lee, S. C., Jeong, H. J., Choi, B. J., & Kim, S. (2015) · Journal of Surgical Research · doi:10.1016/j.jss.2015.02.025 · Cited by 34 · see citing works
Matsumoto, K., Miyake, Y., Umeda, Y., Matsushita, H., Matsuda, H., Takaki, A., Sadamori, H., Nouso, K., Yagi, T., Fujiwara, T., et al. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms141020877 · Cited by 33 · see citing works
Serum Hyaluronate Level for Predicting Subclinical Liver Dysfunction after Hepatectomy
Mizuguchi, T., Katsuramaki, T., Nobuoka, T., Kawamoto, M., Oshima, H., Kawasaki, H., Kikuchi, H., Shibata, C., & Hirata, K. (2004) · World Journal of Surgery · doi:10.1007/s00268-004-7389-1 · Cited by 32 · see citing works
Signal molecule-mediated hepatic cell communicationduring liver regeneration
Zheng, Z., Weng, S., & Yu, Y. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.5776 · Cited by 31 · see citing works
Inflammation and pro-resolution inflammation after hepatobiliary surgery
Cata, J. P., Velasquez, J. F., Ramirez, M. F., Vauthey, J.-N., Gottumukkala, V., Conrad, C., Kim, B. J., & Aloia, T. (2017) · World Journal of Surgical Oncology · doi:10.1186/s12957-017-1220-6 · Cited by 30 · see citing works
Darnis, B., Mohkam, K., Schmitt, Z., Ledochowski, S., Vial, J. P., Duperret, S., Vogt, C., Demian, H., Golse, N., Mezoughi, S., et al. (2015) · HPB · doi:10.1111/hpb.12434 · Cited by 27 · see citing works
Regulating factors of liver regeneration after hepatectomy
Tani, M., Tomiya, T., Yamada, S., Hayashi, S., Yahata, K., Tamura, Y., Akiyama, M., Kawai, S., Masaki, N., Fujiwara, K., et al. (1994) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00686664 · Cited by 26 · see citing works
Prediction of posthepatectomy hepatic functional reserve by serum hyaluronate
Yachida, S., Wakabayashi, H., Okano, K., & Suzuki, Y. (2009) · British journal of surgery · doi:10.1002/bjs.6560 · Cited by 26 · see citing works
Takeuchi, E., Nimura, Y., Nagino, M., Kurumiya, Y., Maeda, A., Kamiya, J., Kondo, S., Kanai, M., Miyachi, M., Uesaka, K., et al. (1997) · Hepatology · doi:10.1002/hep.510260502 · Cited by 24 · see citing works
Sparrelid, E., Johansson, H., Gilg, S., Nowak, G., Ellis, E. C. S., & Isaksson, B. (2018) · European Surgical Research · doi:10.1159/000488078 · Cited by 23 · see citing works
Aryal, B., Shimizu, T., Kadono, J., Furoi, A., Komokata, T., Inoue, M., Ikeda, S., Fukukura, Y., Nakamura, M., Yamakuchi, M., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150446 · Cited by 22 · see citing works
Sasturkar, S. V., David, P., Sharma, S., Sarin, S. K., Trehanpati, N., & Pamecha, V. (2015) · Liver Transplantation · doi:10.1002/lt.24373 · Cited by 22 · see citing works
Importance of platelet-derived growth factors in liver regeneration
Starlinger, P. P., & Assinger, A. (2016) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2016.1158100 · Cited by 21 · see citing works
Increased growth factor expression after hepatic and pancreatic resection
Justinger (1994) · Oncology Reports · doi:10.3892/or_00000175 · Cited by 21 · see citing works
Meyer, J., Balaphas, A., Combescure, C., Morel, P., Gonelle‐Gispert, C., & Bühler, L. H. (2019) · HPB · doi:10.1016/j.hpb.2019.01.016 · Cited by 20 · see citing works
Kimura, F., Miyazaki, M., Suwa, T., Kakizaki, S., Itoh, H., Kaiho, T., & Nakajima, N. (2008) · European Surgical Research · doi:10.1159/000129445 · Cited by 20 · see citing works
Mathematical Model of Liver Regeneration in Human Live Donors
Periwal, V., Gaillard, J. R., Needleman, L., & Doria, C. (2014) · Journal of Cellular Physiology · doi:10.1002/jcp.24482 · Cited by 19 · see citing works
Dłuzniewska, J., Zolich, D., Polański, J. A., Zając, L., Sitkiewicz, D., & Łukomska, B. (2002) · PubMed · Cited by 15 · see citing works
Interleukin-6 release in the hepatic blood outflow during normothermic liver ischaemia in humans
Guidi, L., Tricerri, A., Costanzo, M., Adducci, E., Ciarniello, M., Errani, A. R., COSMO, G. D., Barattini, P., Frasca, D., Bartoloni, C., et al. (2003) · Digestive and Liver Disease · doi:10.1016/s1590-8658(03)00156-7 · Cited by 14 · see citing works
Maeda, A., Nagino, M., Takeuchi, E., Sano, T., Kurumiya, Y., & Nimura, Y. (1999) · British journal of surgery · doi:10.1046/j.1365-2168.1999.01065.x · Cited by 11 · see citing works
Krieg, A. H., Esch, J. S. A., Schmelzle, M., Tustas, R. Y., El-Karmi, A., Hosch, S. B., & Knoefel, W. T. (2006) · Transplantation Proceedings · doi:10.1016/j.transproceed.2006.10.111 · Cited by 11 · see citing works
Serum levels of HGF, IL-6, and TGF-α after benign liver tumor resection
Kornasiewicz, O., Grąt, M., Dudek, K., Lewandowski, Z., Gorski, Z., Zieniewicz, K., & Krawczyk, M. (2015) · Advances in Medical Sciences · doi:10.1016/j.advms.2015.01.008 · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [26]Anastasia Lemekhova OGNKH. Cytokines, growth factors and liver response (regeneration and post hepatectomy liver failure) to liver resections: A systematic review and meta-analysis.
Cited by
Sorted by citations
Value of Liver Function Tests in Cirrhosis
Sharma, P. (2021) · Journal of Clinical and Experimental Hepatology · doi:10.1016/j.jceh.2021.11.004 · Cited by 90 · see citing works
Malignant JAK-signaling: at the interface of inflammation and malignant transformation
Perner, F., Pahl, H. L., Zeiser, R., & Heidel, F. H. (2025) · Leukemia · doi:10.1038/s41375-025-02569-8 · Cited by 68 · see citing works
The role of gut microbiota in liver regeneration
Xu, Z., Jiang, N., Xiao, Y., Yuan, K., & Wang, Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1003376 · Cited by 39 · see citing works
Pleiotrophin and metabolic disorders: insights into its role in metabolism
Ballesteros-Pla, C., Sánchez‐Alonso, M. G., Pizarro‐Delgado, J., Zuccaro, A., Sevillano, J., & Ramos, P. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1225150 · Cited by 22 · see citing works
Nishio, T., Taura, K., Koyama, Y., Ishii, T., & Hatano, E. (2023) · Annals of Gastroenterological Surgery · doi:10.1002/ags3.12692 · Cited by 19 · see citing works
Murtha-Lemekhova, A., Fuchs, J., Feiler, S., Schulz, E. R., Teroerde, M., Kalkum, E., Klotz, R., Billeter, A. T., Probst, P., & Hoffmann, K. (2022) · BMC Medicine · doi:10.1186/s12916-022-02239-x · Cited by 18 · see citing works
Self-citationLao, W.-L., Sang, S., Huang, L.-C., Yi, S., Guo, M., Dong, H., Zhou, G., & Chen, Z. (2024) · BMC Anesthesiology · doi:10.1186/s12871-023-02392-7 · Cited by 14 · see citing works
Portal Hemodynamics in Liver Resection and Transplantation
Rela, M., Rammohan, A., Rajalingam, R., & Clavien, P. (2024) · Annals of Surgery · doi:10.1097/sla.0000000000006304 · Cited by 11 · see citing works
Vassanasiri, W., Rungsakulkij, N., Suragul, W., Tangtawee, P., Muangkaew, P., Mingphruedhi, S., & Aeesoa, S. (2022) · Perioperative Medicine · doi:10.1186/s13741-022-00283-y · Cited by 10 · see citing works
Basal MET phosphorylation is an indicator of hepatocyte dysregulation in liver disease
de Lara, S. B., Kemmer, S., Biermayer, I., Feiler, S., Vlasov, A., D’Alessandro, L. A., Helm, B., Mölders, C., Dieter, Y., Ghallab, A., et al. (2024) · Molecular Systems Biology · doi:10.1038/s44320-023-00007-4 · Cited by 10 · see citing works
Self-citationRole of mitogens in normal and pathological liver regeneration
Vosough, M., Shokouhian, B., Sharbaf, M. A., Solhi, R., Heidari, Z., Seydi, H., Hassan, M., Ezhilarasan, D., & Najimi, M. (2025) · Hepatology Communications · doi:10.1097/hc9.0000000000000692 · Cited by 8 · see citing works
Glucagon-like peptide-1 and glucagon-like peptide-2 regulation during human liver regeneration
Ammann, M., Santol, J., Pereyra, D., Kalchbrenner, T., Wuerger, T., Laengle, J., Smoot, R. L., Hulla, W., Laengle, F., & Starlinger, P. (2023) · Scientific Reports · doi:10.1038/s41598-023-43283-8 · Cited by 8 · see citing works
Molecular Pathways Governing the Termination of Liver Regeneration
de Haan, L. R., van Golen, R. F., & Heger, M. (2024) · Pharmacological Reviews · doi:10.1124/pharmrev.123.000955 · Cited by 9 · see citing works
Exploring the roles of non-coding RNAs in liver regeneration
Li, P., Ma, X., Huang, D., & Gu, X. (2024) · Non-coding RNA Research · doi:10.1016/j.ncrna.2024.04.003 · Cited by 8 · see citing works
The Effect of Growth Factors on Vaginal Wound Healing: A Systematic Review and Meta-analysis
van Velthoven, M. J. J., Gudde, A. N., Struijs, F., Oosterwijk, E., Roovers, J., Güler, Z., Hooijmans, C. R., & Kouwer, P. H. J. (2023) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2022.0225 · Cited by 7 · see citing works
Blood flow‐induced angiocrine signals promote organ growth and regeneration
Follert, P., Große‐Segerath, L., & Lammert, E. (2024) · BioEssays · doi:10.1002/bies.202400207 · Cited by 8 · see citing works
Kofler, A., Trattner, M., Mairinger, V., Urban, I., Søreide, K., Stättner, S., & Primavesi, F. (2025) · Cancers · doi:10.3390/cancers17193120 · Cited by 4 · see citing works
“This precluded a meta-analysis, specifically in relation to a specific cut-off for early postoperative IL-6 levels to predict ISGLS-CR-PHLF in pre-defined cohorts (e.g., minor versus major resections) [31,40].”
Predicting liver regeneration following major resection
Dehlke, K., Krause, L., Tyufekchieva, S., Murtha-Lemekhova, A., Mayer, P., Vlasov, A., Klingmüller, U., Mueller, N. S., & Hoffmann, K. (2022) · Scientific Reports · doi:10.1038/s41598-022-16968-9 · Cited by 4 · see citing works
Self-citationLee, J. Z., Ng, S. J. K. K., & Shelat, V. G. (2025) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v16.i4.109860 · Cited by 2 · see citing works
Al-Qabandi, W., & Dhaunsi, G. S. (2024) · Growth Factors · doi:10.1080/08977194.2024.2407566 · Cited by 2 · see citing works
Trimming the fat myth: adipose tissue’s role in liver regeneration
Peloso, A., & Golse, N. (2024) · HepatoBiliary Surgery and Nutrition · doi:10.21037/hbsn-24-181 · Cited by 2 · see citing works
Zhang, S., Ma, Y., Chen, X., Wu, S., & Chen, G. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2024.1429564 · Cited by 1 · see citing works
Pu, J., Zhao, Y., Zhang, S., Wu, T., Liu, R., Yuan, T., He, S., Hao, Q., & Zhu, H. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1529297 · Cited by 1 · see citing works
Peptide hormones and bile acids shaping immune tolerance of the liver: implications and applications
van Niekerk, G., Kumpanenko, Y., Degryse, J., Fevery, J., & Dallmeier, K. (2025) · Protein & Cell · doi:10.1093/procel/pwaf096 · Cited by 1 · see citing works
Relationship of immunonutritional factor with changes in liver volume after portal vein embolization
Nanashima, A., Tanoue, Y., Yano, K., Hiyoshi, M., İmamura, N., Hamada, T., Kai, K., Kitamura, E., Suzuki, Y., Tahira, K., et al. (2022) · Surgery Open Science · doi:10.1016/j.sopen.2022.05.012
Analysis of Influencing Factors on Liver Regeneration after Hepatectomy for Hepatocellular Carcinoma
刘, 洪. (2023) · Advances in Clinical Medicine · doi:10.12677/acm.2023.134959
Kidney transplantation: the recipient
(2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23571-9.00018-9
Быков, И. М., Shevchenko, A. S., Tsymbalyuk, I., Popov, K. A., Tutarisheva, S. M., Сергеевна, У. Е., Storozhuk, A. P., & Esaulenko, E. E. (2024) · Innovative medicine of Kuban · doi:10.35401/2541-9897-2024-9-1-144-151
Oh, Y. J., Choi, G., Kim, J. M., & Rhu, J. (2026) · Scientific Reports · doi:10.1038/s41598-026-57137-6
Lipid Metabolism and Hepatic Growth Factors: A Mendelian Randomization Study
钟, 文. (2025) · Advances in Clinical Medicine · doi:10.12677/acm.2025.1541057
Murtha-Lemekhova, A., Fuchs, J., Feiler, S., Schulz, E., Teroerde, M., Kalkum, E., Klotz, R., Billeter, A., Probst, P., & Hoffmann, K. (2022) · Figshare · doi:10.6084/m9.figshare.19101828
Self-citationFunctional Study of the Liver: Nonimaging Tests
Kokudo, T., & Kokudo, N. (2026) · Springer eBooks · doi:10.1007/978-3-032-10997-2_8
Okabayashi, T., Tabuchi, M., Tokumaru, T., Uemura, S., & Tamura, S. (2026) · Nutrition and Cancer · doi:10.1080/01635581.2026.2713786
Agrawal, H., Gupta, N., & Tanwar, H. (2026) · Artificial Intelligence in Gastroenterology · doi:10.35712/aig.v7.i2.116057
Ko, I., Choi, H. I., Park, S. B., Shin, H. P., Jeon, J. W., & Lee, S. H. (2026) · Medicina · doi:10.3390/medicina62091819
Wang, T., Bacot, S. M., Patterson, K., Friedman, D., Taylor, C., Hong, H., Liu, J., Avigan, M., Hayashi, P. H., Rule, J. A., et al. (2026) · Liver International · doi:10.1111/liv.70895
- Authors
- Murtha-Lemekhova, A., Fuchs, J., Ghamarnejad, O., Nikdad, M., Probst, P., & Hoffmann, K.
- Affiliations
- Heidelberg University (DE)
- Corresponding author
- Hoffmann, Katrin
- Venue
- Scientific Reports
- Published
- 2021-07-02
- Volume
- 11
- Issue
- 1
- Pages
- 13739-13739
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC8253792
- OpenAlex
- W3175338931
- Cited by
- 36
- References
- 79
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 10 · 2023: 5 · 2022: 6 · 2021: 1
- FWCI
- 0.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Medizinische Fakultät Heidelberg der Universität Heidelberg
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
- Keywords
- post-hepatectomy liver failure, liver regeneration, hepatectomy, hyaluronic acid, interleukin-6, hepatocyte growth factor, cytokines, circulating biomarkers, risk prediction, hepatocyte proliferation, liver fibrosis, liver function tests, coagulation parameters, cholestasis, transaminases, hepatic hemodynamics
- MeSH terms
- Clinical Trials as Topic, Female, Hepatectomy, Humans, Liver, Liver Function Tests, Liver Regeneration, Male, Risk Factors, Cytokines, Liver Failure, Intercellular Signaling Peptides and Proteins
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
