Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 20, 2026.

Potential impact of invasive surgical procedures on primary tumor growth and metastasis

Maria Alieva, Jacco van Rheenen, Marike L. D. Broekman

Clinical & Experimental Metastasis · 2018 · Review

doi:10.1007/s10585-018-9896-8

Abstract

Surgical procedures such as tumor resection and biopsy are still the gold standard for diagnosis and (determination of) treatment of solid tumors, and are prognostically beneficial for patients. However, growing evidence suggests that even a minor surgical trauma can influence several (patho) physiological processes that might promote postoperative metastatic spread and tumor recurrence. Local effects include tumor seeding and a wound healing response that can promote tumor cell migration, proliferation, differentiation, extracellular matrix remodeling, angiogenesis and extravasation. In addition, local and systemic immunosuppression impairs antitumor immunity and contributes to tumor cell survival. Surgical manipulation of the tumor can result in cancer cell release into the circulation, thus increasing the chance of tumor cell dissemination. To prevent these undesired effects of surgical interventions, therapeutic strategies targeting immune response exacerbation or alteration have been proposed. This review summarizes the current literature regarding these local, systemic and secondary site effects of surgical interventions on tumor progression and dissemination, and discusses studies that aimed to identify potential therapeutic approaches to prevent these effects in order to further increase the clinical benefit from surgical procedures.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Tumor tissue resection and biopsy are still indispensable for diagnosis, cytoreduction and determination of subsequent treatment strategies of solid tumors and, importantly, to extend the patients’ lifespan or contribute to their cure. However, also a wide range of potential undesired effects have been associated with these procedures. Negative consequences of tumor invasive procedures not only include post-operative complications, such as hemorrhage, surgical site infections and venous-thromboembolic complications, but also changes affecting the remaining tumor cells, such as increased survival, proliferation and migration. An increasing body of evidence from clinical and experimental studies suggests that surgical trauma caused by biopsies or resections gives rise to a series of local and systemic events that can potentially promote tumor progression and metastatic disease. Surgical interventions disrupt the tumor and the surrounding tissue and result in tumor cell displacement to healthy tissue and release into the circulation. Moreover the inflicted surgical trauma initiates a wound healing response that activates a series of humoral and cellular cascades aimed at closing the wound. While necessary for normal tissue repair, the local and systemic alteration of the innate and adaptive immune responses can stimulate tumor cell malignant behavior, survival, angiogenesis and extravasation of circulating tumor cells.

These undesired effects have the potential to affect tumor progression and spread. However, this does not imply that surgical resection or biopsy should be abandoned since these effects may only hold true for a subset of patients and the prognostic benefit of these procedures still strongly outweigh their negative effects. Nevertheless, it will be important to fully understand their impact on tumor pathology in order to prevent these effects and develop adjuvant treatments that would make these procedures even safer and more beneficial for the patients.

In this review, we summarize existing data that illustrates the effects of surgery on tumor progression and discuss potential strategies to circumvent these undesired effects of surgical procedures.

Biopsies and tumor cell seeding

Fine needle aspirations (FNAs), in which a thin fine-gauge needle is inserted into the core of the tumor to aspirate tumor cells, are commonly performed to obtain tissue for diagnosis. This procedure has been associated not only with standard surgical complications as surgical site infections and hemorrhage, but also with a risk of tumor cell seeding along the needle track into the adjacent tissues. This risk is inherent to the procedure in which a needle transgresses and disrupts the tumor and is withdrawn. Histological evidence suggests that upon FNA tumor cells can be found in adjacent tissues. However, some studies question the viability of the remaining tumor cells. For example, in breast tumors undergoing biopsy the incidence of tumor cell seeding in the needle track seemed to decline as the time between the biopsy and the subsequent resection increased, suggesting that the displaced cells rarely survive.

The use of larger needles has also been associated with tumor seeding into the adjacent tissues. For example in brain malignancies, tumor cells could be found in the needle track after biopsy of gliomas (Fig. 1) or of brain metastases. However, the incidence of viable tumors and tumor recurrences along the track is low and hard to quantify. For hepatocellular carcinoma, a recent meta-analysis of the available literature showed that, overall the pooled estimate of a patient with seeding per 100 patients is 0.027 and that, per year the pooled estimate of a patient with seeding per 100 patients is 0.009. For other cancers, where FNA is a common practice, such as thyroid cancer, needle track seeding is extremely rare and only a few cases have been reported. Percutaneous FNA, performed on pancreatic tissue has also been associated with coelomic seeding. However distinct studies present conflicting results on the incidence of seeding and its risk for tumor progression. The use of endoscopic ultrasound-FNA allows a more accurate lesion sampling and thus may eliminate the risk of coelomic seeding. The risk of tumor seeding after needle biopsy in retroperitoneal sarcoma is estimated to be 0.37%, based on pooled data from four tertiary care centers. Even though the data is limited, few studies indicate that the use of vacuum assisted biopsy devices might reduce the risk of tumor seeding compared to the use of traditional devices.

Effect of tumor resections on tumor cell seeding

For many solid tumor types, resection is part of the treatment plan. Often, the aim of surgery is to completely resect a tumor (gross total resection), but partial resections are sometimes the only clinical option. Various tumors including chordoma and mixed epithelial stromal tumor of the kidney have also shown evidence of tumor seeding as a result of partial resections. Unfortunately, even gross total resection of tumors can result in local dissemination of cells. For example, it has been shown that piece meal resection of brain metastases increases the risk of leptomeningeal spread (LMS) resulting in worse outcomes for patients. In addition, recent evidence suggests that the risk of LMS is higher after surgery followed by stereotactic radiosurgery (SRS) than after SRS alone.

Other examples of tumor cell dissemination after resection include port-site recurrences after laparoscopic abdominal oncological surgeries, procedures with clear advantages associated with their minimally invasive character. Various factors seem to contribute to tumor seeding in this context. First, some factors might be tumor related. High-grade or high-stage tumors have been associated with a greater risk of seeding. Second, there might be wound related aspects that offer a tumor supportive environment. This process can contribute to tumor metastasis and will be discussed below. Third, there might be surgery-associated factors. For example, it has been suggested that the CO2 pneumoperitoneum plays a role in the development of these metastases as well as in the development of peritoneal carcinomatosis after laparoscopic surgery. Dry cold CO2 might induce peritoneal damage facilitating metastases, for example by creating a local immune suppressive micro-environment. Additionally, extensive manipulation of the tumor, has been associated with a higher risk of port site metastasis. Finally, not using a retrieval bag might facilitate port site metastasis. To prevent these metastases, studies that aim to improve safety of surgery, for instance by identifying alternatives for the cold CO2 insufflation, like those performed in mice by Carpentiri et al., are essential. In addition, it is important that surgeons are aware of the impact of the techniques they use and that they are properly trained to minimize the risk of tumor seeding, especially since training seems to decrease the risk of these unwanted negative effects of surgery.

Immune suppressive micro-environment

Next to effects on tumor cell seeding, surgical procedures induce changes in the local tumor microenvironment that can impact tumor cell gene expression and behavior. Tumors are largely infiltrated by immune cells that can exert both pro-tumoral and anti-tumoral effects. To escape immune surveillance exerted by anti-tumoral effectors, tumor cells often create an immunosuppressive microenvironment that favors tumor progression and metastatic spreading. Surgical procedures, as tumor resection and biopsy, can even further promote immunosuppressive infiltrates in the remaining tumor mass.

Both the innate and the adaptive immune systems contribute to this immune suppressive environment. In an experimental model of lung carcinoma, tumors that had undergone partial tumor resection were found infiltrated with immunosuppressive alternatively-activated macrophages and regulatory T cells (Tregs), which prevented CD8 T lymphocytes recruitment to the tumor and contributed to faster tumor recurrence. Infiltration of these immunosuppressive cells was stimulated by high levels of TGF-β and COX-2 found in the resection area. A study of oral squamous cell carcinomas showed that the number of alternatively activated macrophages in the tumor correlates with the size of the surgical trauma, with animals undergoing tumor resection having higher numbers of alternatively activated macrophages than animals that underwent a biopsy. Still, even small wounds to the tumor created by needle biopsy can rapidly promote pro-inflammatory factors such as S100A8, CXCL2, CCL3, and COX2 followed by a significant increase in the number of myeloid derived suppressor cells in the tumor. Eosinophils that controversially have been reported as indicators of both favorable and poor prognosis have also been found to infiltrate the tumor after biopsy in breast cancer patients.

Tumor cell transformation and changes in tumor cell behavior

In addition to creating an immunosuppressive environment, infiltrating immune cells in response to surgical trauma are a source of inflammatory cytokines, chemokines and growth factors. These factors are known for their ability to promote tumor cell proliferation, differentiation and migration. Numerous studies have found that tumor wounding by either resection or by biopsies stimulates tumor growth. Interestingly, the impact of wounding on tumor growth is distinct between tumor subtypes. For instance, luminal A breast tumor showed more Ki67 upon core needle biopsy compared to luminal B-HER2-tumors.

Different mechanisms explaining the local recurrence of the tumor have been proposed. Increase in levels of VEGF and endostatin in the wounded tissue potentiate neoangiogenesis, required for tumor growth. Mitogens, such as heparin-binding epidermal growth factor, platelet-derived growth factor, TGF-β, basic fibroblast growth factor present in the wound fluid support tumor growth rate. These growth factors can be secreted directly by the tumor cells, due to changes in their transcriptome; or by recruited and resident cells present in the wounded microenvironment. Surgical trauma caused by tumor resection of brain tumors promotes reactive astrogliosis, that can either directly induce tumor proliferation thought secretion of mitogens (e.g. SDF-1) or either through the recruitment of inflammatory cells such as macrophages.

Mathenge et al. reported that tumor biopsy promotes epithelial to mesenchymal transition (EMT) related changes in gene expression in the remaining tumor cells via an increase in TGF-β and SOX-4 production. This fundamental process in embryonic development plays a crucial role in tumor cell invasion. In glioma, surgical resection and biopsy have shown to promote tumor cell proliferation through transcriptome and secretome alterations of reactive astrocytes and recruitment of pro-inflammatory monocytes to the operative site.

Besides increased growth rate, surgical trauma can also enhance tumor cells’ migratory capacity, a key process in tumor cell local and systemic dissemination. The transition from epithelial to mesenchymal state that tumor cells can undergo upon biopsy, is reported to be necessary for tumor cells migratory behavior. Tumor cell migration and invasion in the surrounding tissue can be promoted by soluble factors as a consequence of changes in local tumor microenvironment and the inflammatory cell influx to the wounded site. The effects on local tumor cell invasive capacity are of particular importance for highly aggressive tumors such as high grade gliomas, in which local invasion prevents complete tumor resection and has a direct impact on patient’s outcome. For instance, reactive astrocytosis as a result of surgical resection can promote tumor cell invasion via the secretion of distinct paracrine factors (e.g. TGF-α, CXCL12, S1P, GDNF, MMP-2, MMP-9).

The development of intravital microscopy (IVM), a novel imaging technique that allows to visualize tumor cell behavior at single cell level in a living animal, has granted a deeper insight into the impact of small surgical interventions, such as biopsy, on tumor progression and determine the cellular mechanisms behind this process. Using IVM, we have previously shown that biopsy-like injury induces migration and proliferation of tumor cells via recruitment of monocytes and their differentiation to macrophages. Over the last decades it has been extensively reported that tumor associated macrophages are able to promote tumor cell migration thought secretion of matrix-remodeling proteins, cytokines and chemokines (e.g. MMP-2, MMP-9, TNF-α, VEGF, TGF-β, EGF). Some of these factors and others can also stimulate tumor proliferation and survival (e.g. EGF, PDGF, TGF-β1, HGF and FGF-2). Another study using IVM has shown that next to their ability to invade the surrounding tissue, human glioma cells have been shown to repopulate the surgical lesion area through directed migration to the wounded site. In some models, it has been shown that this recolonization is at least in part mediated by tumor microtubes that form a tumor cell network and contribute to tumor cell invasion, proliferation in unlesioned tumor and to radiotherapy resistance. Upon surgery, the neighboring tumor cells are able to extend new tumor microtubes and direct newly formed tumor cell nuclei towards the lesioned area to repopulate it.

Tumor cell release

With the advance of successful treatments that target primary tumor sites, metastatic disease management and prevention has become the main challenge for most solid tumor treatment strategies. However, surgical trauma results in systemic and secondary site changes that might favor the formation of new metastases and potentiate the growth of pre-existent micrometastases.

Because tumor cell dissemination to distant organs occurs via shedding of circulatory tumor cells (CTCs) into the lymphatic and blood vasculature, high CTC numbers are closely associated with metastatic disease progression and survival. Numerous studies from different types of cancer have reported cancer cell release into the circulation as a result of biopsy and surgical resection.

Even non-invasive medical interventions such as external tumor palpation have been shown to lead to increased numbers of CTCs during and immediately after the procedure in subcutaneous models of melanoma and breast cancer, suggesting that tumor cells release into the circulation is susceptible to external manipulation. However, CTCs release upon surgery and its impact on patients’ prognosis is still controversial, since some studies show no increase in CTC counts before and after surgery, while others find that CTC counts after surgery are not associated with recurrence free survival or overall survival.

Interestingly, a time-course experiment over several weeks performed by Juralti et al. found that CTC dynamics increased immediately after punch biopsy and stayed elevated for 6 weeks after the procedure, while complete tumor resection led to a decrease in CTC counts. This difference is likely to be due to the high efficiency of tumor cell resection that can be achieved in a subcutaneous pre-clinical model where the complete primary tumor can be eliminated, and thus the source of CTCs. However, in the clinic complete tumor resection can be very challenging, making partial or subtotal resections a reality. In these cases the remaining tumor cells can be a source of CTCs. In line with this notion Juralti et al. found that incomplete tumor resection led to an increased number of CTCs.

The mechanisms of CTC mobilization in the blood upon surgical trauma have yet to be clarified. The immediate shedding of CTCs in the bloodstream indicates passive intravasation due to mechanical pressure and vascular collapse. However in later stages the local inflammatory response, described above, could also impact tumor cell capacity for active intravasation via changes in tumor cell gene expression or changes in the microenvironment, that favor tumor cell migration and vascular permeability.

Systemic inflammation potentiates tumor cell survival in circulation and extravasation

Next to CTC release, invasive surgical interventions trigger changes in systemic inflammation that can impact the CTCs ability to survive and extravasate. Extensive evidence has shown that surgical interventions lead to an imbalance of the innate and adaptive immune regulatory mechanisms and impair immune functions. One of the effects of surgery is systemic immunosuppression of cells that participate in CTCs clearance and in the control of tumor cell dissemination: natural killers (NK) and phagocytic monocytes/macrophages. This process is triggered by the activation of the hypothalamic–pituitary–adrenal axis in response to surgical trauma stress. NK cell numbers and cytotoxic activity experience a rapid and prolonged (up to 10–30 days) decrease due to surgical interventions. Additionally, monocytes/macrophages phagocytic and chemotactic functions and antigen recognition mechanisms are compromised due to surgery and even as a result of anesthesia. Likewise, suppression of NKs and macrophages in a model of hepatic metastasis has shown to potentiate tumor cell uptake and outgrowth in the liver.

An increase in neutrophil counts in blood is triggered by surgical trauma. As a result, tumor cell survival, via NK cell suppression, is promoted and tumor cell extravasation is stimulated through IL-1 and matrix metalloproteases secretion. Moreover, in response to injury neutrophils expel granule and nuclear constituents (including DNA and histones) mixed with a variety of cytokines, known as neutrophil extracellular traps (NETs). These structures sequester CTCs from circulation and promote tumor cell invasion and metastatic outgrowth. Post-operative NET formations in a cohort of patients with liver resection for metastatic colorectal cancer were associated with the extent of surgical resection and resulted in an increased risk of recurrence. Indeed, NETs inhibition, described in a murine model of surgical stress, attenuates the development of metastasis triggered by the surgical intervention.

Another systemic effect of surgery consists of an acute inflammatory response mediated by the release of inflammatory cytokines into circulation. TNF-α and IL-1 are some of the earliest and most potent systemic mediators of inflammation known to stimulate tumor cell adhesion, invasion and neoangiogenesis and potentiate metastasis formation. In addition to inflammatory cytokines, an increase in pro-angiogenic factors, such as VEGF and angiopoietin-2 in plasma has been reported after distinct surgical interventions.

In the peritoneal cavity tumor cell adhesion can be facilitated due to exposure of the extracellular matrix after mesothelial cell detachment in response to surgical trauma. This mechanism of regulation of peritoneal inflammation has been shown to lead to increased tumor cell adhesion in non-traumatized areas of the peritoneal cavity.

Metastatic burden can be potentiated by surgical interventions

Apart from supporting the establishment of new metastases from CTCs, systemic effects of surgical trauma can potentiate the progression of preexisting metastatic foci and contribute to the creation of so called pre-metastatic niches. Over the last decades, numerous clinical and preclinical reports strongly relate surgical interventions such as tumor resection and biopsy with an increased metastatic burden in different types of cancer. Different aspects of surgical interventions at the primary site ultimately contribute to tumor outgrowth at distant sites, some of which, such as tumor cell shedding in circulation, extravasation, immune cell modulation and pro-tumoral effects of inflammatory cytokines, have been discussed above. Surgical interventions to the primary tumor also exert direct effects on distant tumors. For instance, biopsy mediated acute inflammatory response promotes an increase in lung metastases, associated with neutrophils recruitment to the metastatic site that could be controlled with anti-inflammatory treatment or IL-6 inhibition. Recruited neutrophils induce metastatic progression thought activation of intracellular growth signaling pathways mediated by Toll-like receptor 9 and NETs. Additionally, Al-Sahaf et al. showed that upon primary tumor resection lung metastasis acquired an invasive and proangiogenic phenotype and increased proliferation, indicating that humoral responses to surgical trauma can also directly alter secondary tumor gene expression. Some effects of surgical interventions on tumor progression seem to be unrelated to the primary tumor, but rather a direct consequence of a normal wound healing response. In line with this, a wound to a tumor-free tissue has been shown to elicit systemic factors that promote tumor angiogenesis and proliferation.

The potentiation of metastatic progression can also be a consequence of an alteration in the inhibitory control exerted by the primary tumor. The primary tumor secretes factors that control the growth of secondary metastasis; and surgical resection of the primary tumor releases this inhibitory control. Regulation of angiogenesis plays a major role in this process. It is thought that both pro-angiogenic factors and inhibitors are secreted into the circulation by primary tumors, however inhibitors are more stable and can exert anti-angiogenic effects on distant micrometastases. As a result of primary tumor removal, angiogenesis inhibitors levels drop, an angiogenic switch takes place at distant tumor sites and gives rise to tumor expansion. Studies done by Folkman have elucidated the molecular mechanisms responsible for this effect with angiostatin and endostatin as main regulators.

Pre-metastatic niche formation as a consequence of surgery

Little is known about the effects of surgery on pre-metastatic niche formation. However, the systemic inflammation elicited in response to surgery could also contribute to the alteration of the microenvironment at distant sites and create pre-metastatic niches. In line with this idea hepatic ischemia–reperfusion injury has shown to increase circulating bone marrow-derived progenitor cells accompanied by a marked microvascular density in the liver that resulted in a higher incidence of liver metastases, upon tumor cell injection after injury. Hypoxic conditions at the primary tumor site created by decreased tissue perfusion upon a surgical intervention are also likely to stimulate pre-metastatic niche formation at distant sites. Conditioned medium derived from hypoxic mammary tumor cells has been reported to increase bone marrow-derived cell infiltration into the lung and rise the metastatic burden at this site. Future studies should focus on elucidating the mechanisms that contribute to the formation of pre-metastatic niches in response to surgical interventions at the primary tumor site.

Prevention of undesired tumor promoting effects of surgical interventions

Extensive evidence links therapeutic and diagnostic invasive interventions with a stimulation of tumor progression. This does not imply however that the current cancer management protocols should be abandoned, as in most cases they allow for cure or extend lifespan of patients, that otherwise would not be possible. Instead the increasing knowledge of the cellular and molecular mechanisms underlying this phenomenon offer a therapeutic possibility to prevent these adverse effects, making clinical interventions even more beneficial for the patient. Several prevention strategies have been proposed (Fig. 2).

Since immune alteration plays a main role in surgery induced tumor progression perioperative immune-modulators have been proposed to suppress undesired effects of surgery. For example, IL-2 treatment prior to surgery has shown to counteract surgery-induced immunosuppression and extend survival of colorectal cancer patients. Other modulators such as granulocyte macrophage-colony stimulating factor, IFN-α and TNF-α also improved postoperative immune functions. Although IL-2 and IFN-α treatments have shown severe side effects, some recent studies have reported that short-term administration schedules and drug delivery strategies induce only mild side-effects, suggesting that the use of these therapies should be further investigated to evaluate their potential to safely prevent surgery induced tumor progression. Another prospective strategy aimed to stimulate the adaptive immune response against the remaining tumor cells consists of the use of postoperative dendritic cell vaccines (DCV). In the last years the optimization of DCV for therapeutic purposes has renewed the interest towards this approach and the number of clinical trials testing DCV is currently rising.

An alternative approach is to utilize factors that would resolve the acute inflammation that is triggered by surgical procedures. Perioperative treatment with dexamethasone, a potent anti-inflammatory drug, has shown to prevent biopsy-induced tumor cell migration and proliferation by reducing monocytes recruitment to the injured site and reduced growth of biopsied tumors in multifocal glioblastoma patients. Other mediators of inflammation resolution such as Resolvin D1, Lipoxin A4 and 15-Epi-lipoxin A4 represent a therapeutic potential due to their capacity to attenuate systemic inflammation.

Stress induced by surgery triggers the activation of the hypothalamic–pituitary–adrenal axis that modulates the immune system response via neuroendocrine factors. Preclinical studies have shown that perioperative blockade of neuroendocrine factors by COX-2 inhibitors and β-blockers can prevent immune suppression and decrease surgery-induced local tumor growth and metastatic progression. This notion has been supported by recent clinical data that report, not only the safe use of these treatments in patients, but also their efficacy to inhibit inflammatory ligands (IL-6, C-reactive protein), preserve the levels of cytokines that enhance anti-tumor activity by NK and cytotoxic T cells (IL-12, IFN-γ), decrease tumor infiltration with pro-inflammatory monocytes and abrogate the activity of immune suppressive CD4 T cells. Importantly, in the excised tumor preoperative treatment showed to suppress molecular pathways related to metastatic progression. Although the impact of these treatments on long-term clinical outcome after surgery still needs to be assessed, the potential benefit of this approach is supported by studies that show association between the use of COX-2 inhibitors and β-blockers with progression-free survival in breast cancer patients.

Tumor growth inhibition with preoperative or directly postoperative chemotherapy or anti-angiogenic treatments has previously been studied and although in some cases these therapies have shown to improve long term-survival their use remains controversial. This is due not only to other studies where chemotherapy showed no benefit, but also because in some cases it seemed to elicit unwanted effects, similar to surgical trauma, that can contribute to tumor progression and spreading. Moreover the adverse side effects of chemotherapy such as a strong inflammatory response and impaired wound healing constitute an additional challenge for their wide use in the clinic.

Concluding remarks

Clinical and preclinical evidence indicate that both biopsies and tumor resections can have multiple effects that stimulate tumor progression, metastatic spreading and outgrowth. However, given the variety of surgical procedures, tumor types and stages that are encountered in the clinical practice, the conclusions drawn from these studies cannot be generalized. For instance, in early stage tumors, surgical procedures might have no impact on tumor progression because tumor cells still lack the genetic makeup necessary to acquire malignant features when a pro-inflammatory microenvironment is induced.

Moreover, the benefit of these surgical procedures for appropriate diagnosis and extended survival is undeniable and outweighs the potential negative effects, advocating against their discontinuation. Instead, the described findings show the importance of future studies addressed to further elucidate the cellular and molecular mechanisms behind these processes. This will allow to develop novel approaches to mitigate the local and systemic undesired effects of surgical interventions and even further improve the clinical benefit of these procedures.

References 167

  1. 1.

    McCutcheon BA, et al. Predictors of surgical site infection following craniotomy for intracranial neoplasms: an analysis of prospectively collected data in the American College of Surgeons National Surgical Quality Improvement Program Database. World Neurosurg. 2016;88:350-358.

    Not in our library10.1016/j.wneu.2015.12.068

  2. 2.

    Cote DJ, Dubois HM, Karhade AV, Smith TR. Venous thromboembolism in patients undergoing craniotomy for brain tumors: a U.S. nationwide analysis. Semin Thromb Hemost. 2016;42:870-876.

    Not in our library10.1055/s-0036-1592306

  3. 3.

    Senders JT, et al. Venous thromboembolism and intracranial hemorrhage after craniotomy for primary malignant brain tumors: a National Surgical Quality Improvement Program analysis. J Neurooncol. 2018;136:135-145.

    Not in our library10.1007/s11060-017-2631-5

  4. 4.
    Preventing inflammation inhibits biopsy-mediated changes in tumor cell behavior · 2017
    Not checked
  5. 5.

    Tagliabue E, et al. Role of HER2 in wound-induced breast carcinoma proliferation. Lancet. 2003;362:527-533.

    Not in our library10.1016/s0140-6736(03)14112-8

  6. 6.

    Al-Sahaf O, Wang JH, Browne TJ, Cotter TG, Redmond HP. Surgical injury enhances the expression of genes that mediate breast cancer metastasis to the lung. Ann Surg. 2010;252:1037-1043.

    Not in our library10.1097/sla.0b013e3181efc635

  7. 7.

    Bogden AE, Moreau JP, Eden PA. Proliferative response of human and animal tumours to surgical wounding of normal tissues: onset, duration and inhibition. Br J Cancer. 1997;75:1021-1027.

    Not in our library10.1038/bjc.1997.175

  8. 8.

    Estourgie SH, Nieweg OE, Kroon BB. High incidence of in-transit metastases after sentinel node biopsy in patients with melanoma. Br J Surg. 2004;91:1370-1371.

    Not in our library10.1002/bjs.4692

  9. 9.

    Hansen NM, Ye X, Grube BJ, Giuliano AE. Manipulation of the primary breast tumor and the incidence of sentinel node metastases from invasive breast cancer. Arch Surg. 2004;139:634-639.

    Not in our library10.1001/archsurg.139.6.634

  10. 10.

    Hobson J, et al. Acute inflammation induced by the biopsy of mouse mammary tumors promotes the development of metastasis. Breast Cancer Res Treat. 2013;139:391-401.

    Not in our library10.1007/s10549-013-2575-1

  11. 11.

    Lange PH, Hekmat K, Bosl G, Kennedy BJ, Fraley EE. Acclerated growth of testicular cancer after cytoreductive surgery. Cancer. 1980;45:1498-1506.

    Not in our library10.1002/1097-0142(19800315)45:6<1498::aid-cncr2820450633>3.0.co;2-7

  12. 12.

    Peeters CF, de Waal RM, Wobbes T, Westphal JR, Ruers TJ. Outgrowth of human liver metastases after resection of the primary colorectal tumor: a shift in the balance between apoptosis and proliferation. Int J Cancer. 2006;119:1249-1253.

    Not in our library10.1002/ijc.21928

  13. 13.

    Stroncek JD, Reichert WM, Reichert WM. Overview of wound healing in different tissue types. Indwelling neural implants: strategies for contending with the in vivo environment. 2008.

    Not in our library

  14. 14.

    Sakurai M, Okamura J, Seki K, Kuroda C. Needle tract implantation of hepatocellular carcinoma after percutaneous liver biopsy. Am J Surg Pathol. 1983;7:191-195.

    Not in our library10.1097/00000478-198303000-00010

  15. 15.

    Lundstedt C, Stridbeck H, Andersson R, Tranberg KG, Andren-Sandberg A. Tumor seeding occurring after fine-needle biopsy of abdominal malignancies. Acta Radiol. 1991;32:518-520.

    Not in our library

  16. 16.

    Shyamala K, Girish HC, Murgod S. Risk of tumor cell seeding through biopsy and aspiration cytology. J Int Soc Prev Community Dent. 2014;4:5-11.

    Not in our library10.4103/2231-0762.129446

  17. 17.

    Diaz LK, Wiley EL, Venta LA. Are malignant cells displaced by large-gauge needle core biopsy of the breast? AJR Am J Roentgenol. 1999;173:1303-1313.

    Not in our library10.2214/ajr.173.5.10541110

  18. 18.

    Pierallini A, et al. Metastasis along the stereotactic biopsy trajectory in glioblastoma multiforme. Acta Neurochir (Wien). 1999;141:1011-1012.

    Not in our library10.1007/s007010050410

  19. 19.

    Steinmetz MP, Barnett GH, Kim BS, Chidel MA, Suh JH. Metastatic seeding of the stereotactic biopsy tract in glioblastoma multiforme: case report and review of the literature. J Neurooncol. 2001;55:167-171.

    Not in our library10.1023/a:1013873431159

  20. 20.

    Karlsson B, Ericson K, Kihlstrom L, Grane P. Tumor seeding following stereotactic biopsy of brain metastases. Report of two cases. J Neurosurg. 1997;87:327-330.

    Not in our library10.3171/jns.1997.87.2.0327

  21. 21.

    Pinggera D, et al. Serious tumor seeding after brainstem biopsy and its treatment-a case report and review of the literature. Acta Neurochir (Wien). 2017;159:751-754.

    Not in our library10.1007/s00701-017-3102-7

  22. 22.

    Silva MA, et al. Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut. 2008;57:1592-1596.

    Not in our library10.1136/gut.2008.149062

  23. 23.

    Karwowski JK, Nowels KW, McDougall IR, Weigel RJ. Needle track seeding of papillary thyroid carcinoma from fine needle aspiration biopsy. A case report. Acta Cytol. 2002;46:591-595.

    Not in our library10.1159/000326884

  24. 24.

    Warshaw AL. Implications of peritoneal cytology for staging of early pancreatic cancer. Am J Surg. 1991;161:26-29.

    Not in our library10.1016/0002-9610(91)90356-i

  25. 25.

    Leach SD, et al. Significance of peritoneal cytology in patients with potentially resectable adenocarcinoma of the pancreatic head. Surgery. 1995;118:472-478.

    Not in our library10.1016/s0039-6060(05)80361-7

  26. 26.

    Chang KJ. Endoscopic ultrasound-guided fine needle aspiration in the diagnosis and staging of pancreatic tumors. Gastrointest Endosc Clin N Am. 1995;5:723-734.

    Not in our library

  27. 27.

    Wilkinson MJ, et al. Percutaneous core needle biopsy in retroperitoneal sarcomas does not influence local recurrence or overall survival. Ann Surg Oncol. 2015;22:853-858.

    Not in our library10.1245/s10434-014-4059-x

  28. 28.

    Hwang SY, et al. Safety and accuracy of core biopsy in retroperitoneal sarcomas. Asia Pac J Clin Oncol. 2016;12:e174-178.

    Not in our library10.1111/ajco.12125

  29. 29.

    Berger-Richardson D, Swallow CJ. Needle tract seeding after percutaneous biopsy of sarcoma: risk/benefit considerations. Cancer. 2017;123:560-567.

    Not in our library10.1002/cncr.30370

  30. 30.

    Michalopoulos NV, et al. Needle tract seeding after vacuum-assisted breast biopsy. Acta Radiol. 2008;49:267-270.

    Not in our library10.1080/02841850701775030

  31. 31.

    Fernandes Cabral DT, Zenonos GA, Fernandez-Miranda JC, Wang EW, Gardner PA. Iatrogenic seeding of skull base chordoma following endoscopic endonasal surgery. J Neurosurg. 2017.

    Not in our library10.3171/2017.6.jns17111

  32. 32.

    Farias JA, Laryea J, Gokden N, Kamel MH. Peritoneal seeding following incomplete resection of mixed epithelial stromal tumor of the kidney: first case report. Urol Ann. 2016;8:114-117.

    Not in our library10.4103/0974-7796.171493

  33. 33.

    Ahn JH, et al. Risk for leptomeningeal seeding after resection for brain metastases: implication of tumor location with mode of resection. J Neurosurg. 2012;116:984-993.

    Not in our library10.3171/2012.1.jns111560

  34. 34.

    Ma R, et al. Risk of leptomeningeal carcinomatosis in patients with brain metastases treated with stereotactic radiosurgery. J Neurooncol. 2018;136:395-401.

    Not in our library10.1007/s11060-017-2666-7

  35. 35.

    Lee SD, et al. Laparoscopic versus open surgery for stage I rectal cancer: long-term oncologic outcomes. World J Surg. 2013;37:646-651.

    Not in our library10.1007/s00268-012-1846-z

  36. 36.

    Tsivian A, Sidi AA. Port site metastases in urological laparoscopic surgery. J Urol. 2003;169:1213-1218.

    Not in our library10.1097/01.ju.0000035910.75480.4b

  37. 37.

    Vergote I, Marquette S, Amant F, Berteloot P, Neven P. Port-site metastases after open laparoscopy: a study in 173 patients with advanced ovarian carcinoma. Int J Gynecol Cancer. 2005;15:776-779.

    Not in our library10.1111/j.1525-1438.2005.00135.x

  38. 38.
    Inhibition of peritoneal dissemination of colon cancer by hyperthermic CO2 insufflation: A novel approach to prevent intraperitoneal tumor spread. · 2017
    Not checked
  39. 39.

    Peng Y, et al. Heated and humidified CO2 prevents hypothermia, peritoneal injury, and intra-abdominal adhesions during prolonged laparoscopic insufflations. J Surg Res. 2009;151:40-47.

    Not in our library10.1016/j.jss.2008.03.039

  40. 40.

    Rosario MT, et al. Does CO2 pneumoperitoneum alter the ultra-structuture of the mesothelium? J Surg Res. 2006;133:84-88.

    Not in our library10.1016/j.jss.2005.09.032

  41. 41.

    van den Tol PM, et al. Reduction of peritoneal trauma by using nonsurgical gauze leads to less implantation metastasis of spilled tumor cells. Ann Surg. 1998;227:242-248.

    Not in our library10.1097/00000658-199802000-00014

  42. 42.

    Mathew G, et al. Wound metastases following laparoscopic and open surgery for abdominal cancer in a rat model. Br J Surg. 1996;83:1087-1090.

    Not in our library10.1002/bjs.1800830815

  43. 43.

    Mutter D, et al. Increased tumor growth and spread after laparoscopy vs laparotomy: influence of tumor manipulation in a rat model. Surg Endosc. 1999;13:365-370.

    Not in our library10.1007/s004649900991

  44. 44.

    Iwamura M, et al. Port site recurrence of renal cell carcinoma following retroperitoneoscopic radical nephrectomy with manual extraction without using entrapment sac or wound protector. J Urol. 2004;171:1234-1235.

    Not in our library10.1097/01.ju.0000110611.55559.f3

  45. 45.

    Carpinteri S, et al. Peritoneal tumorigenesis and inflammation are ameliorated by humidified-warm carbon dioxide insufflation in the mouse. Ann Surg Oncol. 2015;22(Suppl 3):1540-1547.

    Not in our library10.1245/s10434-015-4508-1

  46. 46.

    Lee SW, Gleason NR, Bessler M, Whelan RL. Port site tumor recurrence rates in a murine model of laparoscopic splenectomy decreased with increased experience. Surg Endosc. 2000;14:805-811.

    Not in our library10.1007/s004640000231

  47. 47.

    Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19:1423-1437.

    Not in our library10.1038/nm.3394

  48. 48.

    Kitamura T, Qian BZ, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15:73-86.

    Not in our library10.1038/nri3789

  49. 49.

    Mathenge EG, et al. Core needle biopsy of breast cancer tumors increases distant metastases in a mouse model. Neoplasia. 2014;16:950-960.

    Not in our library10.1016/j.neo.2014.09.004

  50. 50.

    Predina J, et al. Changes in the local tumor microenvironment in recurrent cancers may explain the failure of vaccines after surgery. Proc Natl Acad Sci USA. 2013;110:E415-E424.

    Not in our library10.1073/pnas.1211850110

  51. 51.

    Weber M, et al. Macrophage polarisation changes within the time between diagnostic biopsy and tumour resection in oral squamous cell carcinomas—an immunohistochemical study. Br J Cancer. 2015;113:510-519.

    Not in our library10.1038/bjc.2015.212

  52. 52.

    Luna-More S, Florez P, Ayala A, Diaz F, Santos A. Neutral and acid mucins and eosinophil and argyrophil crystalloids in carcinoma and atypical adenomatous hyperplasia of the prostate. Pathol Res Pract. 1997;193:291-298.

    Not in our library10.1016/s0344-0338(97)80006-4

  53. 53.

    Ishibashi S, et al. Tumor-associated tissue eosinophilia in human esophageal squamous cell carcinoma. Anticancer Res. 2006;26:1419-1424.

    Not in our library

  54. 54.

    da Silva JM, et al. Eosinophil depletion protects mice from tongue squamous cell carcinoma induced by 4-nitroquinoline-1-oxide. Histol Histopathol. 2014;29:387-396.

    Not in our library10.14670/hh-29.387

  55. 55.

    von Wasielewski R, et al. Tissue eosinophilia correlates strongly with poor prognosis in nodular sclerosing Hodgkin’s disease, allowing for known prognostic factors. Blood. 2000;95:1207-1213.

    Not in our library

  56. 56.

    Szalayova G, et al. Human breast cancer biopsies induce eosinophil recruitment and enhance adjacent cancer cell proliferation. Breast Cancer Res Treat. 2016;157:461-474.

    Not in our library10.1007/s10549-016-3839-3

  57. 57.

    Eming SA, Krieg T, Davidson JM. Inflammation in wound repair: molecular and cellular mechanisms. J Investig Dermatol. 2007;127:514-525.

    Not in our library10.1038/sj.jid.5700701

  58. 58.
    Stimulation of tumour growth by wound-derived growth factors · 1999
    No notice
  59. 59.

    Hofer SO, Shrayer D, Reichner JS, Hoekstra HJ, Wanebo HJ. Wound-induced tumor progression: a probable role in recurrence after tumor resection. Arch Surg. 1998;133:383-389.

    Not in our library10.1001/archsurg.133.4.383

  60. 60.

    Okolie O, et al. Reactive astrocytes potentiate tumor aggressiveness in a murine glioma resection and recurrence model. Neuro Oncol. 2016;18:1622-1633.

    Not in our library10.1093/neuonc/now117

  61. 61.

    Chen X, et al. Surgery time interval and molecular subtype may influence Ki67 change after core needle biopsy in breast cancer patients. BMC Cancer. 2015;15:822.

    Not in our library10.1186/s12885-015-1853-1

  62. 62.

    Wu FP, Hoekman K, Meijer S, Cuesta MA. VEGF and endostatin levels in wound fluid and plasma after breast surgery. Angiogenesis. 2003;6:255-257.

    Not in our library10.1023/b:agen.0000029410.32264.b0

  63. 63.

    Hormbrey E, Han C, Roberts A, McGrouther DA, Harris AL. The relationship of human wound vascular endothelial growth factor (VEGF) after breast cancer surgery to circulating VEGF and angiogenesis. Clin Cancer Res. 2003;9:4332-4339.

    Not in our library

  64. 64.

    Barbero S, et al. Stromal cell-derived factor 1alpha stimulates human glioblastoma cell growth through the activation of both extracellular signal-regulated kinases 1/2 and Akt. Cancer Res. 2003;63:1969-1974.

    Not in our library

  65. 65.

    O’Brien ER, Howarth C, Sibson NR. The role of astrocytes in CNS tumors: pre-clinical models and novel imaging approaches. Front Cell Neurosci. 2013;7:40.

    Not in our library10.3389/fncel.2013.00040

  66. 66.

    Weil S, et al. Tumor microtubes convey resistance to surgical lesions and chemotherapy in gliomas. Neuro Oncol. 2017;19:1316-1326.

    Not in our library10.1093/neuonc/nox070

  67. 67.

    Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer. 2003;3:362-374.

    Not in our library10.1038/nrc1075

  68. 68.

    Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124:263-266.

    Not in our library10.1016/j.cell.2006.01.007

  69. 69.

    Beerling E, et al. Plasticity between epithelial and mesenchymal states unlinks emt from metastasis-enhancing stem cell capacity. Cell Rep. 2016;14:2281-2288.

    Not in our library10.1016/j.celrep.2016.02.034

  70. 70.

    Parsa AT, et al. Prognostic significance of intracranial dissemination of glioblastoma multiforme in adults. J Neurosurg. 2005;102:622-628.

    Not in our library10.3171/jns.2005.102.4.0622

  71. 71.

    Wijnenga MMJ, et al. Does early resection of presumed low-grade glioma improve survival? A clinical perspective. J Neurooncol. 2017;133:137-146.

    Not in our library10.1007/s11060-017-2418-8

  72. 72.

    Hoelzinger DB, Demuth T, Berens ME. Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J Natl Cancer Inst. 2007;99:1583-1593.

    Not in our library10.1093/jnci/djm187

  73. 73.

    Liu L, et al. Astrocyte elevated gene-1 upregulates matrix metalloproteinase-9 and induces human glioma invasion. Cancer Res. 2010;70:3750-3759.

    Not in our library10.1158/0008-5472.can-09-3838

  74. 74.

    Le DM, et al. Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator-plasmin cascade. J Neurosci. 2003;23:4034-4043.

    Not in our library10.1523/jneurosci.23-10-04034.2003

  75. 75.

    Alieva M, Ritsma L, Giedt RJ, Weissleder R, van Rheenen J. Imaging windows for long-term intravital imaging: general overview and technical insights. Intravital. 2014;3:e29917.

    Not in our library10.4161/intv.29917

  76. 76.

    Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141:52-67.

    Not in our library10.1016/j.cell.2010.03.015

  77. 77.

    Hagemann T, et al. Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases. Carcinogenesis. 2004;25:1543-1549.

    Not in our library10.1093/carcin/bgh146

  78. 78.

    Du R, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13:206-220.

    Not in our library10.1016/j.ccr.2008.01.034

  79. 79.

    Massague J. TGFbeta in cancer. Cell. 2008;134:215-230.

    Not in our library10.1016/j.cell.2008.07.001

  80. 80.

    Wyckoff J, et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004;64:7022-7029.

    Not in our library10.1158/0008-5472.can-04-1449

  81. 81.

    O’Sullivan C, Lewis CE, Harris AL, McGee JO. Secretion of epidermal growth factor by macrophages associated with breast carcinoma. Lancet. 1993;342:148-149.

    Not in our library10.1016/0140-6736(93)91348-p

  82. 82.

    Lewis C, Murdoch C. Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. Am J Pathol. 2005;167:627-635.

    Not in our library10.1016/s0002-9440(10)62038-x

  83. 83.

    Osswald M, et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015;528:93-98.

    Not in our library10.1038/nature16071

  84. 84.

    Steeg PS. Targeting metastasis. Nat Rev Cancer. 2016;16:201-218.

    Not in our library10.1038/nrc.2016.25

  85. 85.

    Cristofanilli M, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004;351:781-791.

    Not in our library10.1056/nejmoa040766

  86. 86.

    Pantel K, Brakenhoff RH, Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer. 2008;8:329-340.

    Not in our library10.1038/nrc2375

  87. 87.

    Kusukawa J, et al. Dissemination of cancer cells into circulation occurs by incisional biopsy of oral squamous cell carcinoma. J Oral Pathol Med. 2000;29:303-307.

    Not in our library10.1034/j.1600-0714.2000.290703.x

  88. 88.

    Hu XC, Chow LW. Fine needle aspiration may shed breast cells into peripheral blood as determined by RT-PCR. Oncology. 2000;59:217-222.

    Not in our library10.1159/000012164

  89. 89.

    Louha M, et al. Liver resection and needle liver biopsy cause hematogenous dissemination of liver cells. Hepatology. 1999;29:879-882.

    Not in our library10.1002/hep.510290348

  90. 90.

    Yamaguchi K, Takagi Y, Aoki S, Futamura M, Saji S. Significant detection of circulating cancer cells in the blood by reverse transcriptase-polymerase chain reaction during colorectal cancer resection. Ann Surg. 2000;232:58-65.

    Not in our library10.1097/00000658-200007000-00009

  91. 91.

    Papavasiliou P, Fisher T, Kuhn J, Nemunaitis J, Lamont J. Circulating tumor cells in patients undergoing surgery for hepatic metastases from colorectal cancer. Proc (Bayl Univ Med Cent). 2010;23:11-14.

    Not in our library10.1080/08998280.2010.11928572

  92. 92.

    Pesta M, Fichtl J, Kulda V, Topolcan O, Treska V. Monitoring of circulating tumor cells in patients undergoing surgery for hepatic metastases from colorectal cancer. Anticancer Res. 2013;33:2239-2243.

    Not in our library

  93. 93.

    Juratli MA, et al. In vivo long-term monitoring of circulating tumor cells fluctuation during medical interventions. PLoS ONE. 2015;10:e0137613.

    Not in our library10.1371/journal.pone.0137613

  94. 94.

    Juratli MA, et al. Real-time monitoring of circulating tumor cell release during tumor manipulation using in vivo photoacoustic and fluorescent flow cytometry. Head Neck. 2014;36:1207-1215.

    Not in our library10.1002/hed.23439

  95. 95.

    Sandri MT, et al. Changes in circulating tumor cell detection in patients with localized breast cancer before and after surgery. Ann Surg Oncol. 2010;17:1539-1545.

    Not in our library10.1245/s10434-010-0918-2

  96. 96.

    van Dalum G, et al. Circulating tumor cells before and during follow-up after breast cancer surgery. Int J Oncol. 2015;46:407-413.

    Not in our library10.3892/ijo.2014.2694

  97. 97.

    Markar SR, et al. Significance of microscopically incomplete resection margin after esophagectomy for esophageal cancer. Ann Surg. 2016;263:712-718.

    Not in our library10.1097/sla.0000000000001325

  98. 98.

    Rickles AS, et al. High rate of positive circumferential resection margins following rectal cancer surgery: a call to action. Ann Surg. 2015;262:891-898.

    Not in our library10.1097/sla.0000000000001391

  99. 99.

    Marchegiani G, et al. Patterns of recurrence after resection of IPMN: who, when, and how? Ann Surg. 2015;262:1108-1114.

    Not in our library10.1097/sla.0000000000001008

  100. 100.

    Bockhorn M, Jain RK, Munn LL. Active versus passive mechanisms in metastasis: do cancer cells crawl into vessels, or are they pushed? Lancet Oncol. 2007;8:444-448.

    Not in our library10.1016/s1470-2045(07)70140-7

  101. 101.

    Harney AS, et al. Real-time imaging reveals local, transient vascular permeability, and tumor cell intravasation stimulated by TIE2hi macrophage-derived VEGFA. Cancer Discov. 2015;5:932-943.

    Not in our library10.1158/2159-8290.cd-15-0012

  102. 102.

    Angele MK, Chaudry IH. Surgical trauma and immunosuppression: pathophysiology and potential immunomodulatory approaches. Langenbecks Arch Surg. 2005;390:333-341.

    Not in our library10.1007/s00423-005-0557-4

  103. 103.

    Ni Choileain N, Redmond HP. Cell response to surgery. Arch Surg. 2006;141:1132-1140.

    Not in our library10.1001/archsurg.141.11.1132

  104. 104.

    Lin E, Calvano SE, Lowry SF. Inflammatory cytokines and cell response in surgery. Surgery. 2000;127:117-126.

    Not in our library10.1067/msy.2000.101584

  105. 105.

    Hogan BV, Peter MB, Shenoy HG, Horgan K, Hughes TA. Surgery induced immunosuppression. Surgeon. 2011;9:38-43.

    Not in our library10.1016/j.surge.2010.07.011

  106. 106.

    Riccardi C, Santoni A, Barlozzari T, Puccetti P, Herberman RB. In vivo natural reactivity of mice against tumor cells. Int J Cancer. 1980;25:475-486.

    Not in our library10.1002/ijc.2910250409

  107. 107.

    Rushfeldt C, Sveinbjornsson B, Seljelid R, Smedsrod B. Early events of hepatic metastasis formation in mice: role of Kupffer and NK-cells in natural and interferon-gamma-stimulated defense. J Surg Res. 1999;82:209-215.

    Not in our library10.1006/jsre.1998.5532

  108. 108.

    Heuff G, et al. Enhanced tumour growth in the rat liver after selective elimination of Kupffer cells. Cancer Immunol Immunother. 1993;37:125-130.

    Not in our library10.1007/bf01517045

  109. 109.

    Bayon LG, et al. Role of Kupffer cells in arresting circulating tumor cells and controlling metastatic growth in the liver. Hepatology. 1996;23:1224-1231.

    Not in our library10.1002/hep.510230542

  110. 110.

    Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med. 1995;332:1351-1362.

    Not in our library10.1056/nejm199505183322008

  111. 111.

    Kimura F, Shimizu H, Yoshidome H, Ohtsuka M, Miyazaki M. Immunosuppression following surgical and traumatic injury. Surg Today. 2010;40:793-808.

    Not in our library10.1007/s00595-010-4323-z

  112. 112.

    Cristaldi M, et al. Lymphocytic subpopulation changes after open and laparoscopic cholecystectomy: a prospective and comparative study on 38 patients. Surg Laparosc Endosc. 1997;7:255-261.

    Not in our library

  113. 113.

    Lennard TW, et al. The influence of surgical operations on components of the human immune system. Br J Surg. 1985;72:771-776.

    Not in our library10.1002/bjs.1800721002

  114. 114.

    Brune IB, et al. Normal T lymphocyte and monocyte function after minimally invasive surgery. Surg Endosc. 1998;12:1020-1024.

    Not in our library10.1007/s004649900772

  115. 115.

    Sietses C, et al. A prospective randomized study of the systemic immune response after laparoscopic and conventional Nissen fundoplication. Surgery. 1999;126:5-9.

    Not in our library10.1067/msy.1999.98702

  116. 116.

    Wu GJ, et al. Propofol specifically inhibits mitochondrial membrane potential but not complex I NADH dehydrogenase activity, thus reducing cellular ATP biosynthesis and migration of macrophages. Ann N Y Acad Sci. 2005;1042:168-176.

    Not in our library10.1196/annals.1338.019

  117. 117.

    Chen RM, et al. Propofol suppresses macrophage functions and modulates mitochondrial membrane potential and cellular adenosine triphosphate synthesis. Anesthesiology. 2003;98:1178-1185.

    Not in our library10.1097/00000542-200305000-00021

  118. 118.

    Cook EJ, et al. Post-operative neutrophil-lymphocyte ratio predicts complications following colorectal surgery. Int J Surg. 2007;5:27-30.

    Not in our library10.1016/j.ijsu.2006.05.013

  119. 119.

    Tabuchi Y, Shinka S, Ishida H. The effects of anesthesia and surgery on count and function of neutrophils. J Anesth. 1989;3:123-131.

    Not in our library10.1007/s0054090030123

  120. 120.

    Spiegel A, et al. Neutrophils suppress intraluminal NK cell-mediated tumor cell clearance and enhance extravasation of disseminated carcinoma cells. Cancer Discov. 2016;6:630-649.

    Not in our library10.1158/2159-8290.cd-15-1157

  121. 121.

    Brinkmann V, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532-1535.

    Not in our library10.1126/science.1092385

  122. 122.

    Cools-Lartigue J, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Investig. 2013.

    Not in our library10.1172/jci67484

  123. 123.

    Park J, et al. Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci Transl Med. 2016;8:361ra138.

    Not in our library10.1126/scitranslmed.aag1711

  124. 124.

    Tohme S, et al. Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Cancer Res. 2016;76:1367-1380.

    Not in our library10.1158/0008-5472.can-15-1591

  125. 125.

    Sawai H, et al. Interleukin-1alpha enhances integrin alpha(6)beta(1) expression and metastatic capability of human pancreatic cancer. Oncology. 2003;65:167-173.

    Not in our library10.1159/000072343

  126. 126.

    Mackay F, Loetscher H, Stueber D, Gehr G, Lesslauer W. Tumor necrosis factor alpha (TNF-alpha)-induced cell adhesion to human endothelial cells is under dominant control of one TNF receptor type, TNF-R55. J Exp Med. 1993;177:1277-1286.

    Not in our library10.1084/jem.177.5.1277

  127. 127.

    Bates RC, Mercurio AM. Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol Biol Cell. 2003;14:1790-1800.

    Not in our library10.1091/mbc.e02-09-0583

  128. 128.

    Voronov E, et al. IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci USA. 2003;100:2645-2650.

    Not in our library10.1073/pnas.0437939100

  129. 129.

    Jing Y, et al. Tumor necrosis factor-alpha promotes tumor growth by inducing vascular endothelial growth factor. Cancer Investig. 2011;29:485-493.

    Not in our library10.3109/07357907.2011.597812

  130. 130.

    Sturm JW, et al. Influence of TNFA on the formation of liver metastases in a syngenic mouse model. Int J Cancer. 2003;107:11-21.

    Not in our library10.1002/ijc.11320

  131. 131.

    Yano S, et al. Multifunctional interleukin-1beta promotes metastasis of human lung cancer cells in SCID mice via enhanced expression of adhesion-, invasion- and angiogenesis-related molecules. Cancer Sci. 2003;94:244-252.

    Not in our library10.1111/j.1349-7006.2003.tb01428.x

  132. 132.

    Belizon A, et al. Major abdominal surgery increases plasma levels of vascular endothelial growth factor: open more so than minimally invasive methods. Ann Surg. 2006;244:792-798.

    Not in our library10.1097/01.sla.0000225272.52313.e2

  133. 133.

    Shantha Kumara HM, et al. Colorectal resection, both open and laparoscopic-assisted, in patients with benign indications is associated with proangiogenic changes in plasma angiopoietin 1 and 2 levels. Surg Endosc. 2009;23:409-415.

    Not in our library10.1007/s00464-008-0132-5

  134. 134.

    Oosterling SJ, et al. Anti-beta1 integrin antibody reduces surgery-induced adhesion of colon carcinoma cells to traumatized peritoneal surfaces. Ann Surg. 2008;247:85-94.

    Not in our library10.1097/sla.0b013e3181588583

  135. 135.

    Yung S, Chan TM. Intrinsic cells: mesothelial cells—central players in regulating inflammation and resolution. Perit Dial Int. 2009;29(Suppl 2):S21-S27.

    Not in our library

  136. 136.

    Abramovitch R, Marikovsky M, Meir G, Neeman M. Stimulation of tumour angiogenesis by proximal wounds: spatial and temporal analysis by MRI. Br J Cancer. 1998;77:440-447.

    Not in our library10.1038/bjc.1998.70

  137. 137.

    O’Reilly MS, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88:277-285.

    Not in our library10.1016/s0092-8674(00)81848-6

  138. 138.

    O’Reilly MS, et al. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell. 1994;79:315-328.

    Not in our library10.1016/0092-8674(94)90200-3

  139. 139.

    Holmgren L, O’Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med. 1995;1:149-153.

    Not in our library10.1038/nm0295-149

  140. 140.

    Lim C, et al. Hepatic ischemia-reperfusion increases circulating bone marrow-derived progenitor cells and tumor growth in a mouse model of colorectal liver metastases. J Surg Res. 2013;184:888-897.

    Not in our library10.1016/j.jss.2013.04.069

  141. 141.

    Govaert KM, et al. Hypoxia after liver surgery imposes an aggressive cancer stem cell phenotype on residual tumor cells. Ann Surg. 2014;259:750-759.

    Not in our library10.1097/sla.0b013e318295c160

  142. 142.

    Sceneay J, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res. 2012;72:3906-3911.

    Not in our library10.1158/0008-5472.can-11-3873

  143. 143.

    Brivio F, et al. Preoperative interleukin-2 subcutaneous immunotherapy may prolong the survival time in advanced colorectal cancer patients. Oncology. 1996;53:263-268.

    Not in our library10.1159/000227571

  144. 144.

    Brivio F, et al. Effects of IL-2 preoperative immunotherapy on surgery-induced changes in angiogenic regulation and its prevention of VEGF increase and IL-12 decline. Hepatogastroenterology. 2002;49:385-387.

    Not in our library

  145. 145.

    Oosterling SJ, et al. Preoperative granulocyte/macrophage colony-stimulating factor (GM-CSF) increases hepatic dendritic cell numbers and clustering with lymphocytes in colorectal cancer patients. Immunobiology. 2006;211:641-649.

    Not in our library10.1016/j.imbio.2006.06.010

  146. 146.

    Kutza J, Gratz I, Afshar M, Murasko DM. The effects of general anesthesia and surgery on basal and interferon stimulated natural killer cell activity of humans. Anesth Analg. 1997;85:918-923.

    Not in our library10.1097/00000539-199710000-00037

  147. 147.

    Liu G, et al. Effective modulation of CD4(+)CD25 (+ high) regulatory T and NK cells in malignant patients by combination of interferon-alpha and interleukin-2. Cancer Immunol Immunother. 2012;61:2357-2366.

    Not in our library10.1007/s00262-012-1297-2

  148. 148.

    Ladenstein R, et al. Dose finding study for the use of subcutaneous recombinant interleukin-2 to augment natural killer cell numbers in an outpatient setting for stage 4 neuroblastoma after megatherapy and autologous stem-cell reinfusion. J Clin Oncol. 2011;29:441-448.

    Not in our library10.1200/jco.2009.23.5465

  149. 149.

    Shimizu K, et al. Clinical utilization of postoperative dendritic cell vaccine plus activated T-cell transfer in patients with intrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Sci. 2012;19:171-178.

    Not in our library10.1007/s00534-011-0437-y

  150. 150.

    Shimizu K, et al. Postoperative dendritic cell vaccine plus activated T-cell transfer improves the survival of patients with invasive hepatocellular carcinoma. Hum Vaccin Immunother. 2014;10:970-976.

    Not in our library10.4161/hv.27678

  151. 151.

    Aranda F, et al. Trial watch: adoptive cell transfer for anticancer immunotherapy. Oncoimmunology. 2014;3:e28344.

    Not in our library10.4161/onci.28344

  152. 152.

    Cata JP, et al. Inflammation and pro-resolution inflammation after hepatobiliary surgery. World J Surg Oncol. 2017;15:152.

    Not in our library10.1186/s12957-017-1220-6

  153. 153.

    Martin CR, et al. Resolvin D1 and lipoxin A4 improve alveolarization and normalize septal wall thickness in a neonatal murine model of hyperoxia-induced lung injury. PLoS ONE. 2014;9:e98773.

    Not in our library10.1371/journal.pone.0098773

  154. 154.

    Ueda T, et al. Combination therapy of 15-epi-lipoxin A4 with antibiotics protects mice from Escherichia coli-induced sepsis. Crit Care Med. 2014;42:e288-e295.

    Not in our library10.1097/ccm.0000000000000162

  155. 155.

    Benish M, et al. Perioperative use of beta-blockers and COX-2 inhibitors may improve immune competence and reduce the risk of tumor metastasis. Ann Surg Oncol. 2008;15:2042-2052.

    Not in our library10.1245/s10434-008-9890-5

  156. 156.

    Qadri SS, et al. Surgically induced accelerated local and distant tumor growth is significantly attenuated by selective COX-2 inhibition. Ann Thorac Surg. 2005;79:990-995.

    Not in our library10.1016/j.athoracsur.2004.07.042

  157. 157.

    Shaashua L, et al. Perioperative COX-2 and beta-adrenergic blockade improves metastatic biomarkers in breast cancer patients in a phase-II randomized trial. Clin Cancer Res. 2017;23:4651-4661.

    Not in our library10.1158/1078-0432.ccr-17-0152

  158. 158.

    Zhou L, et al. Propranolol attenuates surgical stress-induced elevation of the regulatory T cell response in patients undergoing radical mastectomy. J Immunol. 2016;196:3460-3469.

    Not in our library10.4049/jimmunol.1501677

  159. 159.

    Melhem-Bertrandt A, et al. Beta-blocker use is associated with improved relapse-free survival in patients with triple-negative breast cancer. J Clin Oncol. 2011;29:2645-2652.

    Not in our library10.1200/jco.2010.33.4441

  160. 160.

    Forget P, et al. Do intraoperative analgesics influence breast cancer recurrence after mastectomy? A retrospective analysis. Anesth Analg. 2010;110:1630-1635.

    Not in our library10.1213/ane.0b013e3181d2ad07

  161. 161.

    van der Hage JA, et al. Improved survival after one course of perioperative chemotherapy in early breast cancer patients. long-term results from the European Organization for Research and Treatment of Cancer (EORTC) Trial 10854. Eur J Cancer. 2001;37:2184-2193.

    Not in our library10.1016/s0959-8049(01)00294-5

  162. 162.

    Sertoli MR, et al. Randomized cooperative study of perioperative chemotherapy in breast cancer. J Clin Oncol. 1995;13:2712-2721.

    Not in our library10.1200/jco.1995.13.11.2712

  163. 163.

    Nissen-Meyer R, Kjellgren K, Malmio K, Mansson B, Norin T. Surgical adjuvant chemotherapy: results with one short course with cyclophosphamide after mastectomy for breast cancer. Cancer. 1978;41:2088-2098.

    Not in our library10.1002/1097-0142(197806)41:6<2088::aid-cncr2820410604>3.0.co;2-j

  164. 164.

    Shantha Kumara HM, et al. Perioperative GMCSF limits the proangiogenic plasma protein changes associated with colorectal cancer resection. Eur J Surg Oncol. 2009;35:295-301.

    Not in our library10.1016/j.ejso.2008.07.012

  165. 165.
    Preoperative chemotherapy for non-small-cell lung cancer: a systematic review and meta-analysis of individual participant data · 2014
    No notice
  166. 166.

    Nordlinger B, et al. Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial. Lancet Oncol. 2013;14:1208-1215.

    Not in our library10.1016/s1470-2045(13)70447-9

  167. 167.

    Emmenegger U, Kerbel RS. Cancer: chemotherapy counteracted. Nature. 2010;468:637-638.

    Not in our library10.1038/468637a

Cited by papers we hold 4

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.