The DOI matches its Crossref record; 228 of the 228 references it cites were found in a registry or an index.
Exploiting the critical perioperative period to improve long-term cancer outcomes
Open accessAbstract
Evidence suggests that the perioperative period and the excision of the primary tumour can promote the development of metastases—the main cause of cancer-related mortality. This Review first presents the assertion that the perioperative timeframe is pivotal in determining long-term cancer outcomes, disproportionally to its short duration (days to weeks). We then analyse the various aspects of surgery, and their consequent paracrine and neuroendocrine responses, which could facilitate the metastatic process by directly affecting malignant tissues, and/or through indirect pathways, such as immunological perturbations. We address the influences of surgery-related anxiety and stress, nutritional status, anaesthetics and analgesics, hypothermia, blood transfusion, tissue damage, and levels of sex hormones, and point at some as probable deleterious factors. Through understanding these processes and reviewing empirical evidence, we provide suggestions for potential new perioperative approaches and interventions aimed at attenuating deleterious processes and ultimately improving treatment outcomes. Specifically, we highlight excess perioperative release of catecholamines and prostaglandins as key deleterious mediators of surgery, and we recommend blockade of these responses during the perioperative period, as well as other low-risk, low-cost interventions. The measures described in this Review could transform the perioperative timeframe from a prominent facilitator of metastatic progression, to a window of opportunity for arresting and/or eliminating residual disease, potentially improving long-term survival rates in patients with cancer.
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“The resulting physiological changes can create a protumorigenic or prometastatic environment, potentially facilitating cancer progression or recurrence [7].”
From Pancreatic resection with perioperative drug repurposing of propranolol and etodolac – the phase II randomized controlled PROSPER trial (2025) · cites this paper as [7]
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Items 201–228 of 228
Potentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences
Hodgson, D. M., & Knott, B. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00080-4 · Cited by 28
Psychosocial Influences in Oncology: An Expanded Model of Biobehavioral Mechanisms
LUTGENDORF, S. K., COSTANZO, E. S., & SIEGEL, S. D. (2007) · Psychoneuroimmunology · doi:10.1016/b978-012088576-3/50048-4 · Cited by 28
Ben‐Eliyahu, S., Shakhar, G., Shakhar, K., & Melamed, R. (2000) · British Journal of Cancer · doi:10.1054/bjoc.2000.1563 · Cited by 27
Self-citationPostow, M. A., Callahan, M. K., & Wolchok, J. D. (2011) · The Cancer Journal · doi:10.1097/ppo.0b013e31823261db · Cited by 26
Menstrual Cycle and Surgical Treatment of Breast Cancer: Findings From the NCCTG N9431 Study
Grant, C. S., Ingle, J. N., Suman, V. J., Dumesic, D. A., Wickerham, D. L., Gelber, R. D., Flynn, P. J., Weir, L. M., Intra, M., Jones, W. O., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.21.3603 · Cited by 25
Ross, L., Frederiksen, K., Boesen, S. H., Karlsen, R. V., Rasmussen, M. S., Sørensen, L. T., Jørgensen, T., Claësson, M. H., & Johansen, C. (2009) · Psycho-Oncology · doi:10.1002/pon.1524 · Cited by 24
Ateş, E., Yilmaz, S., Erkasap, S., İhtiyar, E., Kaya, Y., Pehlivan, T., Üstüner, Z., Yaşar, B., & Kiper, H. (2004) · PubMed · Cited by 24
Melamed, R., Rosenne, E., Benish, M., Goldfarb, Y., Levi, B. Z., & Ben‐Eliyahu, S. (2009) · Journal of Immunotherapy · doi:10.1097/cji.0b013e3181b0b146 · Cited by 22
Self-citationSchwartz, Y., Avraham, R., Benish, M., Rosenne, E., & Ben‐Eliyahu, S. (2007) · Breast Cancer Research and Treatment · doi:10.1007/s10549-007-9540-9 · Cited by 22
Self-citationGoldfarb, Y., Shapiro, H., Singer, P., Kalderon, Y., Levi, B. Z., Glasner, A., Benish, M., & Ben‐Eliyahu, S. (2011) · Clinical Nutrition · doi:10.1016/j.clnu.2011.10.015 · Cited by 21
Self-citationSammour, T., Kahokehr, A. A., Zargar‐Shoshtari, K., & Hill, A. G. (2010) · Journal of Surgical Research · doi:10.1016/j.jss.2010.10.009 · Cited by 21
Novaković, S., Stegel, V., Kopitar, A. N., Ihan, A., & Novaković, B. J. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.09.067 · Cited by 20
Tziakas, D. N., Chalikias, G. K., Stakos, D., Παπάνας, Ν., Chatzikyriakou, S. V., Mitrousi, K., Maltezos, E. S., & Boudoulas, H. (2008) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2007.07.063 · Cited by 20
The impact of surgical extent and sex on the hepatic metastasis of colon cancer
Sorski, L., Levi, B. Z., Shaashua, L., Neeman, E., Benish, M., Matzner, P., Hoffman, A., & Ben‐Eliyahu, S. (2013) · Surgery Today · doi:10.1007/s00595-013-0768-1 · Cited by 19
Self-citationCancer in transplant recipients
Detry, O., Honoré, P., Meurisse, M., & Jacquet, N. J. (2000) · Transplantation Proceedings · doi:10.1016/s0041-1345(99)00908-2 · Cited by 17
Böhm, M., Ittenson, A., Klatte, T., Schierbaum, K. F., Röhl, F. W., ANSORGE, S., & Allhoff, E. P. (2003) · Folia Biologica · doi:10.14712/fb2003049020063 · Cited by 16
Kerros, C., Brood, I., Sola, B., Jauzac, P., & Allouche, S. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.01.010 · Cited by 15
Psychological factors in immunomodulation induced by cancer surgery: A review
Garssen, B., Boomsma, M. F., & Beelen, R. H. J. (2010) · Biological Psychology · doi:10.1016/j.biopsycho.2010.05.006 · Cited by 15
Hazut, O., Shaashua, L., Benish, M., Levi, B., Sorski, L., Benjamin, B., Hoffman, A., Zmora, O., & Ben‐Eliyahu, S. (2011) · International Journal of Clinical Pharmacology and Therapeutics · doi:10.5414/cp201550 · Cited by 13
Self-citationKlatte, T., Ittenson, A., Roehl, F.-W., Ecke, M., Allhoff, E. P., & HM, M. B. (2008) · Onkologie · doi:10.1159/000112214 · Cited by 12
Timing of breast cancer surgery during the luteal menstrual phase may improve prognosis.
Lemon, H. M., & Rodriguez‐Sierra, J. F. (1996) · PubMed · Cited by 12
Timing of breast surgery in premenopausal breast cancer patients
Samuel, M., Khin, L. W., Brennan, V. K., & Yong, W. S. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003720.pub2 · Cited by 10
Goldfarb, Y., Levi, B. Z., Sorski, L., Frenkel, D., & Ben‐Eliyahu, S. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.07.242 · Cited by 10
Self-citationLenhard, V., Maassen, G., & Opelz, G. (1985) · PubMed · Cited by 7
Smith, D. A. B., Conkling, P., Richards, D., Flores, M. R. C., Nemunaitis, J. J., Boyd, T. E., Mita, A. C., Bourdonnaye, G. D. L., Wages, D. S., & Bexon, A. S. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2012.30.15_suppl.e18047 · Cited by 4
Improved outcomes with beta blocker use in epithelial ovarian cancer patients
Watkins, J., Thaker, P. H., Nick, A. M., Ramondetta, L. M., Kumar, S., Matsuo, K., Lutgendorf, S., Ramirez, P. T., & Sood, A. K. (2013) · Gynecologic Oncology · doi:10.1016/j.ygyno.2013.04.134 · Cited by 2
Matzner, P., Shaashua, L., Sorski, L., Levi, B., Melamed, R., Rosenne, E., Benbenishty, A., Horowitz, M., & Ben‐Eliyahu, S. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.07.099 · Cited by 1
Self-citationSorski, L., Levi, B., Shaashua, L., Matzner, P., Rosenne, E., & Ben‐Eliyahu, S. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.07.077 · Cited by 1
Self-citation
Research works printed but not linked: 3
- Page, G. G., Ben-Eliyahu, S., Yirmiya, R. & Liebeskind, J. C. Morphine attenuates surgery-induced enhancement of metastatic colonization in rats. Pain 54, 21–28 (1993). · DOI
- Kurz, A., Sessler, D. I. & Lenhardt, R. Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N. Engl. J. Med. 334, 1209–1215 (1996). · DOI
- Rader, D. J. & Hobbs, H. H. in Harrisons Principles of Internal Medicine 16th edn Ch. 335 (ed. Kasper D. L.) 2286–2319 (McGraw-Hill, 2005).
Cited by
Sorted by citations
ESPEN guideline: Clinical nutrition in surgery
Weimann, A., Braga, M., Carli, F., Higashiguchi, T., Hübner, M., Kłęk, S., Laviano, A., Ljungqvist, O. H., Lobo, D. N., Martindale, R. G., et al. (2017) · Clinical Nutrition · doi:10.1016/j.clnu.2017.02.013 · Cited by 1,978
Cytotoxic CD8+ T cells in cancer and cancer immunotherapy
Raskov, H., Orhan, A., Christensen, J. P., & Gögenur, I. (2021) · British Journal of Cancer · doi:10.1038/s41416-020-01048-4 · Cited by 1,687
ESPEN expert group recommendations for action against cancer-related malnutrition
Arends, J., Baracos, V., Bertz, H., Bozzetti, F., Calder, P. C., Deutz, N. E. P., Erickson, N., Laviano, A., Lisanti, M. P., Lobo, D. N., et al. (2017) · Clinical Nutrition · doi:10.1016/j.clnu.2017.06.017 · Cited by 1,305
Surgery for Cancer: A Trigger for Metastases
Tohme, S. T., Simmons, R. L., & Tsung, A. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-1536 · Cited by 822
Improving cancer immunotherapy through nanotechnology
Goldberg, M. S. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0186-9 · Cited by 628
Metadata
- Authors
- Horowitz, M., Neeman, E., Sharon, E., & Ben-Eliyahu, S.
- Affiliations
- Tel Aviv University (IL)
- Rabin Medical Center (IL)
- Venue
- Nature Reviews Clinical Oncology
- Published
- 2015-01-20
- Volume
- 12
- Issue
- 4
- Pages
- 213-226
- ISSN
- 1759-4774 (ISSN-L)
- 1759-4782
- PMC
- PMC5497123
- OpenAlex
- W2078505577
- Semantic Scholar
- e262754c5c3cffc0898230df898629f73cd9a8d0
- Cited by
- 487
- References
- 228
- Citations by year
- 2026: 36 · 2025: 33 · 2024: 39 · 2023: 48 · 2022: 60 · 2021: 60 · 2020: 55 · 2019: 40 · 2018: 42 · 2017: 38 · 2016: 22 · 2015: 14
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Clinical Oncology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA172138)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Health Sciences › Medicine › Surgery › Enhanced Recovery After Surgery
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- perioperative period, metastasis, surgical stress response, catecholamines, prostaglandins, anesthesia, analgesia, hypothermia, blood transfusion, tissue damage, sex hormones, nutritional status, paracrine signaling, neuroendocrine response, residual disease, cancer survival
- MeSH terms
- Humans, Immune Tolerance, Neoplasm Metastasis, Neoplasms, Nutritional Status, Prognosis, Recurrence, Stress, Physiological, Stress, Psychological, Treatment Outcome, Perioperative Care, Perioperative Period
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