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Pressurized intraperitoneal aerosol chemotherapy and its effect on gastric-cancer-derived peritoneal metastases: an overview

  • Miguel Alberto
  • Andreas Brandl
  • Pankaj Kumar Garg
  • Safak Gül-Klein
  • Mathias Dahlmann
  • Ulrike Stein
  • Beate RauEmail author
Review

Abstract

This manuscript aspires to portray a review of the current literature focusing on manifest peritoneal metastasis (PM) derived from gastric cancer and its treatment options. Despite the development of chemotherapy and multimodal treatment options during the last decades, mortality remains high worldwide. After refreshing important epidemiological considerations, the molecular mechanisms currently accepted through which PM occurs are revised. Palliative chemotherapy is the only recommended treatment option for patients with PM of gastric cancer according to the National Comprehensive Cancer Network guidelines, although cytoreductive surgery in combination with hyperthermic intraperitoneal chemotherapy demonstrated promising results in selected patients with regional PM and localized intraabdominal tumor spread. A novel treatment named pressurized intraperitoneal aerosol chemotherapy may have a promising future in improving overall survival with an acceptable postoperative complication rate and stabilizing quality of life during treatment. Additionally, the procedure has been proved to be safe for the patient and medical personnel and a feasible, repeatable method to deter metastatic proliferation. This overview comprehensively addresses this novel and promising treatment in the context of a scientifically and clinically challenging disease.

Keywords

Gastric cancer Peritoneal metastases Pressurized intraperitoneal aerosol chemotherapy Intraperitoneal chemotherapy Hyperthermic Intraperitoneal Chemotherapy Molecular mechanisms of peritoneal metastasis 

Abbreviations

ANXA1

Anti-inflammatory protein Annexin 1

CAFs

Cancer associated fibroblasts

CAWS

Closed aerosol waste system

CCR

Transmembrane G protein-coupled chemokine receptors

CDH1

Calcium-dependent cell–cell adhesion molecule E-cadherin

CRS

Cytoreductive surgery

CTGF

Connective tissue growth factor

CXC/CC

Chemokines

ECM

Extracellular matrix

EMT

Epithelial-mesenchymal transition

HIF-1α

Hypoxia-inducible factor-1α

HIPEC

Hyperthermic intraperitoneal chemotherapy

miRNA

MicroRNAs

MMP

Matrix metalloproteinase

MS

Milky spots

MVD

Microvascular density

NCCN

National comprehensive cancer network

NIPS

Neoadjuvant intraperitoneal-systemic chemotherapy protocol

NRAGE

Neutrophin receptor-interacting melanoma antigen-encoding gene homolog

PCI

Peritoneal cancer index

PIPAC

Pressurized intraperitoneal aerosol chemotherapy

PM

Peritoneal metastasis

PTEN

Phosphatase and tensin homolog

S-1

Tegafur, 5-chloro-2-4-dihydroxypyridine and oxonic acid

TAMs

Tumor associated macrophages

VEGF

Vascular endothelial growth factor

α-SMA

Alpha-smooth muscle actin

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. 1.
    Thomassen I, Van Gestel YR, Van Ramshorst B et al (2013) Peritoneal carcinomatosis of gastric origin: a population-based study on incidence, survival and risk factors. Int J Cancer 134:622–628.  https://doi.org/10.1002/ijc.28373 CrossRefGoogle Scholar
  2. 2.
    Yang D, Hendifar A, Lenz C et al (2011) Survival of metastatic gastric cancer: significance of age, sex and race/ethnicity. J Gastrointest Oncol 2:77–84.  https://doi.org/10.3978/j.issn.2078-6891.2010.025 Google Scholar
  3. 3.
    van Baal JOAM, Van de Vijver KK, Nieuwland R et al (2017) The histophysiology and pathophysiology of the peritoneum. Tissue Cell 49:95–105.  https://doi.org/10.1016/j.tice.2016.11.004 CrossRefGoogle Scholar
  4. 4.
    American Cancer Society (2015) Global cancer facts & figs, 3rd edn. American Cancer Society, AtlantaGoogle Scholar
  5. 5.
    Balakrishnan M, George R, Sharma A, Graham DY (2017) Changing trends in stomach cancer throughout the world. Curr Gastroenterol Rep 19:36.  https://doi.org/10.1007/s11894-017-0575-8 CrossRefGoogle Scholar
  6. 6.
    Lu M, Yang Z, Feng Q et al (2016) The characteristics and prognostic value of signet ring cell histology in gastric cancer: a retrospective cohort study of 2199 consecutive patients. Medicine 95(27):e4052.  https://doi.org/10.1097/MD.0000000000004052 CrossRefGoogle Scholar
  7. 7.
    Sugarbaker PH (2018) Gastric cancer: prevention and treatment of peritoneal metastases. J Cancer Metastasis Treat 4:7.  https://doi.org/10.20517/2394-4722.2017.67 CrossRefGoogle Scholar
  8. 8.
    Sugarbaker PH, Yonemura Y (2000) Clinical pathway for the management of resectable gastric cancer with peritoneal seeding: best palliation with a ray of hope for cure. Oncology 58(2):96–107CrossRefGoogle Scholar
  9. 9.
    Gretschel S, Siegel R, Estévez-Schwarz L et al (2006) Surgical strategies for gastric cancer with synchronous peritoneal carcinomatosis. Br J Surg 93:1530–1535.  https://doi.org/10.1002/bjs.5513 CrossRefGoogle Scholar
  10. 10.
    Valastyan S, Weinberg RA (2011) Review tumor metastasis: molecular insights and evolving paradigms. Cell 147:275–292.  https://doi.org/10.1016/j.cell.2011.09.024 CrossRefGoogle Scholar
  11. 11.
    Pachmayr E, Treese C, Stein U (2017) Underlying mechanisms for distant metastasis-molecular biology. Visc Med 33(1):11–20.  https://doi.org/10.1159/000454696 CrossRefGoogle Scholar
  12. 12.
    Takeichi M (1993) Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 5:806–811.  https://doi.org/10.1016/0955-0674(93)90029-P CrossRefGoogle Scholar
  13. 13.
    Peng Z, Wang C, Fang E et al (2014) Role of epithelial-mesenchymal transition in gastric cancer initiation and progression. World J Gastroenterol 20:5403–5410.  https://doi.org/10.3748/wjg.v20.i18.5403 CrossRefGoogle Scholar
  14. 14.
    Chang M-C, Jeng J-H (2011) Tumor Cell-Induced Platelet Aggregation. In: Schwab M (ed) Encyclopedia of cancer. Springer, Berlin, p 3793–3795CrossRefGoogle Scholar
  15. 15.
    Yutaka Y, Yoshio E, Tohru O, Takuma S (2006) Recent advances in the treatment of peritoneal dissemination of gastrointestinal cancers by nucleoside antimetabolites. Cancer Sci 98:11–18.  https://doi.org/10.1111/j.1349-7006.2006.00350.x Google Scholar
  16. 16.
    Kanda M, Kodera Y (2016) Molecular mechanisms of peritoneal dissemination in gastric cancer. 22:6829–6840.  https://doi.org/10.3748/wjg.v22.i30.6829
  17. 17.
    Cheng T, Wu M, Lin J, Lin M (2012) Annexin A1 is associated with gastric cancer survival and promotes gastric cancer cell invasiveness through the formyl peptide receptor/extracellular signal-regulated kinase/integrin beta-1-binding protein 1 pathway. Cancer 118(23):5757–5767.  https://doi.org/10.1002/cncr.27565 CrossRefGoogle Scholar
  18. 18.
    Singh J, Sharma A, Ahuja N (2017) Genomics of peritoneal surface malignancies. J Perit.  https://doi.org/10.4081/joper.2017.62 Google Scholar
  19. 19.
    Liu J, Geng X, Li Y (2016) Milky spots: omental functional units and hotbeds for peritoneal cancer metastasis. Tumor Biol 5715–5726.  https://doi.org/10.1007/s13277-016-4887-3
  20. 20.
    Liebermann-Meffert D, White H, Vaubel E (1983) The greater OMENTUM. Springer, BerlinCrossRefGoogle Scholar
  21. 21.
    Miao ZF, Wang ZN, Zhao TT et al (2014) Peritoneal milky spots serve as a hypoxic niche and favor gastric cancer stem/progenitor cell peritoneal dissemination through hypoxia-inducible factor 1α. Stem Cells 32:3062–3074.  https://doi.org/10.1002/stem.1816 CrossRefGoogle Scholar
  22. 22.
    Quail DF, Joyce JA (2013) Microenvironmental regulation of tumor progression and metastasis. Nat Med 19:1423–1437.  https://doi.org/10.1038/nm.3394 CrossRefGoogle Scholar
  23. 23.
    Yan Y, Wang L-F, Wang R-F (2015) Role of cancer-associated fibroblasts in invasion and metastasis of gastric cancer. World J Gastroenterol 21:9717.  https://doi.org/10.3748/wjg.v21.i33.9717 CrossRefGoogle Scholar
  24. 24.
    Mura G, Verdelli B (2016) The features of peritoneal metastases from gastric cancer. J Cancer Metastasis Treat 2:365.  https://doi.org/10.20517/2394-4722.2016.19 CrossRefGoogle Scholar
  25. 25.
    Cao L, Hu X, Zhang J et al (2014) The role of the CCL22-CCR4 axis in the metastasis of gastric cancer cells into omental milky spots. J Transl Med 12:267.  https://doi.org/10.1186/s12967-014-0267-1 CrossRefGoogle Scholar
  26. 26.
    Chen G, Chen SM, Wang X et al (2012) Inhibition of chemokine (CXC motif) ligand 12/chemokine (CXC motif) receptor 4 axis (CXCL12/CXCR4)-mediated cell migration by targeting mammalian target of rapamycin (mTOR) pathway in human gastric carcinoma cells. J Biol Chem 287:12132–12141.  https://doi.org/10.1074/jbc.M111.302299 CrossRefGoogle Scholar
  27. 27.
    Zhang LL, Liu J, Lei S et al (2014) PTEN inhibits the invasion and metastasis of gastric cancer via downregulation of FAK expression. Cell Signal 26:1011–1020.  https://doi.org/10.1016/j.cellsig.2014.01.025 CrossRefGoogle Scholar
  28. 28.
    Takatsuki H, Komatsu S, Sano R et al (2004) Adhesion of gastric carcinoma cells to peritoneum mediated by α3β1 integrin (VLA-3). Cancer Res 64:6065–6070.  https://doi.org/10.1158/0008-5472.CAN-04-0321 CrossRefGoogle Scholar
  29. 29.
    Nishimori H, Yasoshima T, Denno R et al (2000) A novel experimental mouse model of peritoneal dissemination of human gastric cancer cells: different mechanisms in peritoneal dissemination and hematogenous metastasis. Jpn J Cancer Res 91:715–722.  https://doi.org/10.1111/j.1349-7006.2000.tb01004.x CrossRefGoogle Scholar
  30. 30.
    Yonemura Y, Endou Y, Fujita H et al (2000) Role of MMP-7 in the formation of peritoneal dissemination in gastric cancer. Gastric Cancer 3:63–70CrossRefGoogle Scholar
  31. 31.
    Chen C-N, Chang C-C, Lai H-S et al (2015) Connective tissue growth factor inhibits gastric cancer peritoneal metastasis by blocking integrin α3β1-dependent adhesion. Gastric Cancer 18:504–515.  https://doi.org/10.1007/s10120-014-0400-0 CrossRefGoogle Scholar
  32. 32.
    Saito Y, Sekine W, Sano R et al (2010) Potentiation of cell invasion and matrix metalloproteinase production by alpha3beta1 integrin-mediated adhesion of gastric carcinoma cells to laminin-5. Clin Exp Metastasis 27:197–205.  https://doi.org/10.1007/s10585-010-9314-3 CrossRefGoogle Scholar
  33. 33.
    Li S-G, Ye Z-Y, Zhao Z-S et al (2008) Correlation of integrin β3 mRNA and vascular endothelial growth factor protein expression profiles with the clinicopathological features and prognosis of gastric carcinoma. World J Gastroenterol 14:421.  https://doi.org/10.3748/wjg.14.421 CrossRefGoogle Scholar
  34. 34.
    Carmignani CP, Sugarbaker TA, Bromley CM, Sugarbaker PH (2003) Intraperitoneal cancer dissemination: Mechanisms of the patterns of spread. Cancer Metastasis Rev 22:465–472.  https://doi.org/10.1023/A:1023791229361 CrossRefGoogle Scholar
  35. 35.
    Takebayashi K, Murata S, Yamamoto H et al (2014) Surgery-induced peritoneal cancer cells in patients who have undergone curative gastrectomy for gastric cancer. Ann Surg Oncol 21:1991–1997.  https://doi.org/10.1245/s10434-014-3525-9 CrossRefGoogle Scholar
  36. 36.
    Yang S, Feng R, Pan ZC et al (2015) A comparison of intravenous plus intraperitoneal chemotherapy with intravenous chemotherapy alone for the treatment of gastric cancer: a meta-analysis. Sci Rep 5:1–12.  https://doi.org/10.1038/srep12538 Google Scholar
  37. 37.
    Ishigami H, Fujiwara Y, Fukushima R et al (2018) Phase III trial comparing intraperitoneal and intravenous paclitaxel plus S-1 versus cisplatin plus S-1 in patients with gastric cancer with peritoneal metastasis: PHOENIX-GC trial. J Clin Oncol 36:1922–1929.  https://doi.org/10.1200/JCO.2018.77.8613 CrossRefGoogle Scholar
  38. 38.
    Canbay E, Mizumoto A, Ichinose M et al (2014) Outcome data of patients with peritoneal carcinomatosis from gastric origin treated by a strategy of bidirectional chemotherapy prior to cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in a single specialized center in Japan. Ann Surg Oncol 21:1147–1152.  https://doi.org/10.1245/s10434-013-3443-2 CrossRefGoogle Scholar
  39. 39.
    Yang X-J, Huang C-Q, Suo T et al (2011) Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy improves survival of patients with peritoneal carcinomatosis from gastric cancer: final results of a phase III randomized clinical trial. Ann Surg Oncol 18:1575–1581.  https://doi.org/10.1245/s10434-011-1631-5 CrossRefGoogle Scholar
  40. 40.
    Rudloff UDO, Langan RC, Mullinax JE et al (2014) Impact of maximal cytoreductive surgery plus regional heated intraperitoneal chemotherapy (HIPEC) on outcome of patients with peritoneal carcinomatosis of gastric origin: results of the GYMSSA trial. J Surg Oncol, 110(3):275–284.  https://doi.org/10.1002/jso.23633 CrossRefGoogle Scholar
  41. 41.
    Glehen O, Gilly FN, Arvieux C et al (2010) Peritoneal carcinomatosis from gastric cancer: a multi-institutional study of 159 patients treated by cytoreductive surgery combined with perioperative intraperitoneal chemotherapy. Ann Surg Oncol 17:2370–2377.  https://doi.org/10.1245/s10434-010-1039-7 CrossRefGoogle Scholar
  42. 42.
    Magge D, Zenati M, Mavanur A et al (2014) Aggressive locoregional surgical therapy for gastric peritoneal carcinomatosis. Ann Surg Oncol 21:1448–1455.  https://doi.org/10.1245/s10434-013-3327-5 CrossRefGoogle Scholar
  43. 43.
    Harmon RL, Sugarbaker PH (2005) Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol 2:3.  https://doi.org/10.1186/1477-7800-2-3 CrossRefGoogle Scholar
  44. 44.
    Lagast N, Carlier C, Ceelen WP (2018) Pharmacokinetics and tissue transport of intraperitoneal chemotherapy. Surg Oncol Clin N Am 27:477–494.  https://doi.org/10.1016/j.soc.2018.02.003 CrossRefGoogle Scholar
  45. 45.
    Carlier C, Mathys A, De Jaeghere E et al (2017) Tumour tissue transport after intraperitoneal anticancer drug delivery. Int J Hyperth 33:534–542.  https://doi.org/10.1080/02656736.2017.1312563 CrossRefGoogle Scholar
  46. 46.
    Jacquet P, Stuart OA, Chang D, Sugarbaker PH (1996) Effects of intra-abdominal pressure on pharmacokinetics and tissue distribution of doxorubicin after intraperitoneal administration. Anticancer Drugs 7:596–603CrossRefGoogle Scholar
  47. 47.
    Esquis P, Consolo D, Magnin G et al (2006) High intra-abdominal pressure enhances the penetration and antitumor effect of intraperitoneal cisplatin on experimental peritoneal carcinomatosis. Ann Surg 244:106–112.  https://doi.org/10.1097/01.sla.0000218089.61635.5f CrossRefGoogle Scholar
  48. 48.
    Facy O, Al Samman S, Magnin G et al (2012) High pressure enhances the effect of hyperthermia in intraperitoneal chemotherapy with oxaliplatin: an experimental study. Ann Surg 256:1084–1088.  https://doi.org/10.1097/SLA.0b013e3182582b38 CrossRefGoogle Scholar
  49. 49.
    Kusamura S, Luca F, Baratti D et al (2018) Phase II randomized study on tissue distribution of cisplatin according to different levels of intra abdominal pressure during HIPEC: preliminary results. NCT02949791. Eur J Surg Oncol 44:e7.  https://doi.org/10.1016/j.ejso.2018.07.029 CrossRefGoogle Scholar
  50. 50.
    Tempfer CB, Hilal Z, Dogan A et al (2018) Concentrations of cisplatin and doxorubicin in ascites and peritoneal tumor nodules before and after pressurized intraperitoneal aerosol chemotherapy (PIPAC) in patients with peritoneal metastasis. Eur J Surg Oncol 44:1112–1117.  https://doi.org/10.1016/j.ejso.2018.04.020 CrossRefGoogle Scholar
  51. 51.
    Cho H-K, Lush RM, Bartlett DL et al (1999) Pharmacokinetics of cisplatin administered by continuous hyperthermic peritoneal perfusion (CHPP) to patients with peritoneal carcinomatosis. J Clin Pharmacol 39:394–401.  https://doi.org/10.1177/00912709922007967 CrossRefGoogle Scholar
  52. 52.
    Khosrawipour V, Khosrawipour T, Kern AJP et al (2016) Distribution pattern and penetration depth of doxorubicin after pressurized intraperitoneal aerosol chemotherapy (PIPAC) in a postmortem swine model. J Cancer Res Clin Oncol 142:2275–2280.  https://doi.org/10.1007/s00432-016-2234-0 CrossRefGoogle Scholar
  53. 53.
    Coccolini F, Acocella F, Morosi L et al (2017) High penetration of paclitaxel in abdominal wall of rabbits after hyperthermic intraperitoneal administration of Nab-Paclitaxel compared to standard paclitaxel formulation. Pharm Res 34:1180–1186.  https://doi.org/10.1007/s11095-017-2132-4 CrossRefGoogle Scholar
  54. 54.
    Jung DH, Son SY, Oo AM et al (2016) Feasibility of hyperthermic pressurized intraperitoneal aerosol chemotherapy in a porcine model. Surg Endosc 30:4258–4264.  https://doi.org/10.1007/s00464-015-4738-0 CrossRefGoogle Scholar
  55. 55.
    Galluzzi L, Vitale I, Michels J et al (2014) Systems biology of cisplatin resistance: past, present and future. Cell Death Dis 5:e1257–e1218.  https://doi.org/10.1038/cddis.2013.428 CrossRefGoogle Scholar
  56. 56.
    Barenholz Y (2012) Doxil®—the first FDA-approved nano-drug: lessons learned. J Control Release 160:117–134.  https://doi.org/10.1016/j.jconrel.2012.03.020 CrossRefGoogle Scholar
  57. 57.
    Franco Y, Vaidya T, Ait-Oudhia S (2018) Anticancer and cardio-protective effects of liposomal doxorubicin in the treatment of breast cancer. Breast Cancer Targets Ther 10:131–141.  https://doi.org/10.2147/BCTT.S170239 CrossRefGoogle Scholar
  58. 58.
    Bharadwaj R, Yu H (2004) The spindle checkpoint, aneuploidy, and cancer. Oncogene 23:2016Google Scholar
  59. 59.
    Brito DA, Yang Z, Rieder CL (2008) Microtubules do not promote mitotic slippage when the spindle assembly checkpoint cannot be satisfied. J Cell Biol 182:623 LP–L629CrossRefGoogle Scholar
  60. 60.
    Solaß W, Hetzel A, Nadiradze G et al (2012) Description of a novel approach for intraperitoneal drug delivery and the related device. Surg Endosc 26:1849–1855.  https://doi.org/10.1007/s00464-012-2148-0 CrossRefGoogle Scholar
  61. 61.
    Solass W, Kerb R, Mürdter T et al (2014) Intraperitoneal chemotherapy of peritoneal carcinomatosis using pressurized aerosol as an alternative to liquid solution: first evidence for efficacy. Ann Surg Oncol 21:553–559.  https://doi.org/10.1245/s10434-013-3213-1 CrossRefGoogle Scholar
  62. 62.
    Jacquet P, Sugarbaker PH (1996) Clinical research methodologies in diagnosis and staging of patients with peritoneal carcinomatosis. Cancer Treat Res 82:359–374CrossRefGoogle Scholar
  63. 63.
    Ametsbichler P, Böhlandt A, Nowak D, Schierl R (2018) Occupational exposure to cisplatin/oxaliplatin during pressurized intraperitoneal aerosol chemotherapy (PIPAC)?. Eur J Surg Oncol.  https://doi.org/10.1016/j.ejso.2018.05.020 Google Scholar
  64. 64.
    Solaß W, Giger-Pabst U, Zieren J, Reymond MA (2013) Pressurized intraperitoneal aerosol chemotherapy (PIPAC): occupational health and safety aspects. Ann Surg Oncol 20:3504–3511.  https://doi.org/10.1245/s10434-013-3039-x CrossRefGoogle Scholar
  65. 65.
    Weinreich J, Struller F, Sautkin I et al (2018) Chemosensitivity of various peritoneal cancer cell lines to HIPEC and PIPAC: comparison of an experimental duplex drug to standard drug regimens in vitro. Investig New Drugs.  https://doi.org/10.1007/s10637-018-0641-6 Google Scholar
  66. 66.
    Tempfer CB, Giger-Pabst U, Seebacher V et al (2018) A phase I, single-arm, open-label, dose escalation study of intraperitoneal cisplatin and doxorubicin in patients with recurrent ovarian cancer and peritoneal carcinomatosis. Gynecol Oncol 150:23–30.  https://doi.org/10.1016/j.ygyno.2018.05.001 CrossRefGoogle Scholar
  67. 67.
    Sleeman JP (2017) PIPAC puts pressure on peritoneal metastases from pancreatic cancer. Clin Exp Metastasis 34:291–293.  https://doi.org/10.1007/s10585-017-9851-0 CrossRefGoogle Scholar
  68. 68.
    Struller F, Horvath P, Solass W et al (2017) Pressurized intraperitoneal aerosol chemotherapy with low-dose cisplatin and doxorubicin (PIPAC C/D) in patients with gastric cancer and peritoneal metastasis (PIPAC-GA1). J Clin Oncol 35:99.  https://doi.org/10.1200/JCO.2017.35.4_suppl.99 CrossRefGoogle Scholar
  69. 69.
    Nadiradze G, Giger-Pabst U, Zieren J et al (2016) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) with low-dose cisplatin and doxorubicin in gastric peritoneal metastasis. J Gastrointest Surg 20:367–373.  https://doi.org/10.1007/s11605-015-2995-9 CrossRefGoogle Scholar
  70. 70.
    Alyami M, Gagniere J, Sgarbura O et al (2017) Multicentric initial experience with the use of the pressurized intraperitoneal aerosol chemotherapy (PIPAC) in the management of unresectable peritoneal carcinomatosis. Eur J Surg Oncol 43:2178–2183.  https://doi.org/10.1016/j.ejso.2017.09.010 CrossRefGoogle Scholar
  71. 71.
    Odendahl K, Solass W, Demtröder C et al (2015) Quality of life of patients with end-stage peritoneal metastasis treated with pressurized intraperitoneal aerosol chemotherapy (PIPAC). Eur J Surg Oncol 41:1379–1385.  https://doi.org/10.1016/j.ejso.2015.06.001 CrossRefGoogle Scholar
  72. 72.
    Girshally R, Demtröder C, Albayrak N et al (2016) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) as a neoadjuvant therapy before cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. World J Surg Oncol 14:253.  https://doi.org/10.1186/s12957-016-1008-0 CrossRefGoogle Scholar
  73. 73.
    Nowacki M, Grzanka D, Zegarski W (2018) Pressurized intraperitoneal aerosol chemotheprapy after misdiagnosed gastric cancer: case report and review of the literature. World J Gastroenterol 24:2130–2136.  https://doi.org/10.3748/wjg.v24.i19.2130 CrossRefGoogle Scholar
  74. 74.
    Chan DL, Sjoquist KM, Goldstein D et al (2017) The effect of anti-angiogenic agents on overall survival in metastatic oesophago-gastric cancer: a systematic review and meta-analysis. PLoS ONE 12:e0172307.  https://doi.org/10.1371/journal.pone.0172307 CrossRefGoogle Scholar
  75. 75.
    Thuss-Patience PC, Kretzschmar A, Dogan Y et al (2011) Docetaxel and capecitabine for advanced gastric cancer: investigating dose-dependent efficacy in two patient cohorts. Br J Cancer 105:505–512.  https://doi.org/10.1038/bjc.2011.278 CrossRefGoogle Scholar
  76. 76.
    Khomiakov V, Ryabov A, Bolotina LV et al (2017) Bidirectional chemotherapy in gastric cancer (GC) with peritoneal carcinomatosis (PC) combining intravenous chemotherapy with intraperitoneal chemotherapy with low-dose cisplatin and doxorubicin administered as a pressurized aerosol: an open-label, phase. J Clin Oncol 35:e15532–e15532.  https://doi.org/10.1200/JCO.2017.35.15_suppl.e15532 CrossRefGoogle Scholar
  77. 77.
    Alyami M, Bonnot PE, Villeneuve L et al (2018) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) for nonresectable peritoneal carcinomatosis from gastric cancer. J Clin Oncol 36:149.  https://doi.org/10.1200/JCO.2018.36.4_suppl.149 CrossRefGoogle Scholar
  78. 78.
    Tempfer CB, Rezniczek GA, Ende P (2015) Pressurized intraperitoneal aerosol chemotherapy with cisplatin and doxorubicin in women with peritoneal carcinomatosis: a cohort study. Anticancer Res 35:6723–6730Google Scholar
  79. 79.
    Khomyakov V, Ryabov A, Ivanov A et al (2016) Bidirectional chemotherapy in gastric cancer with peritoneal metastasis combining intravenous XELOX with intraperitoneal chemotherapy with low-dose cisplatis and Doxorubicin administered as a pressurized aerosol: an open-label, phase-2 study (PIPAC-GA2). 1:159–166.  https://doi.org/10.1515/pap-2016-0017
  80. 80.
    Blanco A, Giger-Pabst U, Solass W et al (2013) Renal and hepatic toxicities after pressurized intraperitoneal aerosol chemotherapy (PIPAC). Ann Surg Oncol 20:2311–2316.  https://doi.org/10.1245/s10434-012-2840-2 CrossRefGoogle Scholar
  81. 81.
    Ndaw S, Hanser O, Kenepekian V et al (2018) Occupational exposure to platinum drugs during intraperitoneal chemotherapy. Biomonitoring and surface contamination. Toxicol Lett.  https://doi.org/10.1016/j.toxlet.2018.05.031 Google Scholar
  82. 82.
    Jansen-Winkeln B, Thieme R, Haase L et al (2018) Perioperative sicherheit der intraperitonealen aerosolchemotherapie. Der Chir.  https://doi.org/10.1007/s00104-018-0667-5 Google Scholar
  83. 83.
    Graversen M, Detlefsen S, Pfeiffer P et al (2018) Severe peritoneal sclerosis after repeated pressurized intraperitoneal aerosol chemotherapy with oxaliplatin (PIPAC OX): report of two cases and literature survey. Clin Exp Metastasis 35:103–108.  https://doi.org/10.1007/s10585-018-9895-9 CrossRefGoogle Scholar
  84. 84.
    Nowacki M, Alyami M, Villeneuve L et al (2018) Multicenter comprehensive methodological and technical analysis of 832 pressurized intraperitoneal aerosol chemotherapy (PIPAC) interventions performed in 349 patients for peritoneal carcinomatosis treatment: an international survey study. Eur J Surg Oncol.  https://doi.org/10.1016/j.ejso.2018.02.014 Google Scholar
  85. 85.
    Dumont F, Senellart H, Pein F et al (2018) Phase I/II study of oxaliplatin dose escalation via a laparoscopic approach using pressurized aerosol intraperitoneal chemotherapy (PIPOX trial) for nonresectable peritoneal metastases of digestive cancers (stomach, small bowel and colorectal): rationale and design. Pleura Perit.  https://doi.org/10.1515/pp-2018-0120 Google Scholar
  86. 86.
    Goetze TO, Al-Batran SE, Pabst U et al (2018) Pressurized intraperitoneal aerosol chemotherapy (PIPAC) in combination with standard of care chemotherapy in primarily untreated chemo naive upper gi-adenocarcinomas with peritoneal seeding—A phase II/III trial of the AIO/CAOGI/ACO. Pleura Perit.  https://doi.org/10.1515/pp-2018-0113 Google Scholar
  87. 87.
    Eveno C, Jouvin I, Pocard M (2018) PIPAC EstoK 01: pressurized intraperitoneal aerosol chemotherapy with cisplatin and doxorubicin (PIPAC C/D) in gastric peritoneal metastasis : a randomized and multicenter phase II study. Pleura Perit 1–7.  https://doi.org/10.1515/pap-2018-0116
  88. 88.
    Minnaert A-K, Dakwar GR, Benito JM et al (2017) High-pressure nebulization as application route for the peritoneal administration of sirna complexes. Macromol Biosci 17:1700024.  https://doi.org/10.1002/mabi.201700024 CrossRefGoogle Scholar
  89. 89.
    Ceelen WP, Van de Sande L (2018) PIPAC Nab-pac for stomach, pancreas, breast and ovarian cancer (PIPAC-nabpac). https://clinicaltrials.gov/ct2/show/NCT03304210
  90. 90.
    Mortensen MB (2017) Treatment of Peritoneal carcinomatosis with pressurized intraperitoneal aerosol chemotherapy—(PIPAC-OPC2). https://clinicaltrials.gov/ct2/show/NCT03287375
  91. 91.
    So J, Guowei K (2017) Pressurized Intraperitoneal aerosol chemotherapy (PIPAC) with oxaliplatin in patients with peritoneal carcinomatosis (PIPAC). https://clinicaltrials.gov/ct2/show/NCT03172416

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Miguel Alberto
    • 1
  • Andreas Brandl
    • 1
  • Pankaj Kumar Garg
    • 2
  • Safak Gül-Klein
    • 1
  • Mathias Dahlmann
    • 3
    • 4
    • 5
  • Ulrike Stein
    • 3
    • 4
    • 5
  • Beate Rau
    • 1
    Email author
  1. 1.Department of SurgeryCampus Virchow Klinikum – Campus Mitte, Charité – University Hospital BerlinBerlinGermany
  2. 2.Department of Surgery, Guru Teg Bahadur HospitalUniversity College of Medical Sciences, University of DelhiDelhiIndia
  3. 3.Translational Oncology of Solid Tumors, Experimental and Clinical Research CenterCharité University Hospital BerlinBerlinGermany
  4. 4.Max-Delbrück-Center for Molecular Medicine in the Helmholtz AssociationBerlinGermany
  5. 5.German Cancer Consortium (DKTK)HeidelbergGermany

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