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Manzanedo, I.; Pereira, F.; Pérez-Viejo, E.; Serrano, �. Gastric Cancer with Peritoneal Metastases. Encyclopedia. Available online: https://encyclopedia.pub/entry/42986 (accessed on 23 April 2024).
Manzanedo I, Pereira F, Pérez-Viejo E, Serrano �. Gastric Cancer with Peritoneal Metastases. Encyclopedia. Available at: https://encyclopedia.pub/entry/42986. Accessed April 23, 2024.
Manzanedo, Israel, Fernando Pereira, Estíbalitz Pérez-Viejo, Ángel Serrano. "Gastric Cancer with Peritoneal Metastases" Encyclopedia, https://encyclopedia.pub/entry/42986 (accessed April 23, 2024).
Manzanedo, I., Pereira, F., Pérez-Viejo, E., & Serrano, �. (2023, April 12). Gastric Cancer with Peritoneal Metastases. In Encyclopedia. https://encyclopedia.pub/entry/42986
Manzanedo, Israel, et al. "Gastric Cancer with Peritoneal Metastases." Encyclopedia. Web. 12 April, 2023.
Gastric Cancer with Peritoneal Metastases
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This entry is adapted from the peer-reviewed paper 10.3390/cancers15061777

Gastric cancer (GC) has a poor prognostic and only one in four patients will have survived by 5 years after diagnosis. These poor results are due to the fact that most patients are diagnosed in advanced stages; peritoneal metastases (PM) are especially frequent and are difficult to treat. PM are considered a terminal stage of GC with a poor survival rate and are treated with palliative systemic chemotherapy. The treatment of PM from different origins has evolved; cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) have become the treatment of choice for many malignant diseases that affect the peritoneum. CRS and HIPEC have also been used for patients with GC and PM, achieving survival results that have never been achieved when using systemic chemotherapy alone. The use of HIPEC can even prevent the development of peritoneal recurrences in patients with locally advanced GC as adjuvant therapy, can reduce the volume of peritoneal disease as neoadjuvant therapy, and can control symptoms in a palliative setting.

gastric cancer peritoneal metastases HIPEC cytoreductive surgery

1. Introduction

Gastric cancer (GC) has a very poor prognosis and represents the third most common cause of cancer-related deaths in the world, despite being the fifth most commonly diagnosed type of cancer [1][2]. Only one in four patients will survive up to 5 years [3][4]. The majority of patients are diagnosed in advanced stages; peritoneal metastases (PM) are especially frequent and are present in 15–30% of patients at diagnosis [5][6][7]. Moreover, 40–60% of patients treated with a curative gastrectomy and systemic chemotherapy program will develop a peritoneal relapse as the only site of recurrence [6][7][8].
The treatment of GC depends on its stage, as determined by the American Joint Committee on Cancer (AJCC) tumor-node metastases (TNM) staging system, updated in 2018 [9]. Early and locally advanced GC can be treated with curative intent by surgery with or without systemic chemotherapy, depending on each case, and the 5-year survival rate for these cases can reach 55% [5][10].
However, the standard treatment for metastatic GC is still palliative systemic chemotherapy, with a poor prognosis and median overall survival (OS) of 6 months [3][11][12]. Advances in systemic treatments have improved the survival rates for patients with stage-4 disease, being able to achieve survival periods of up to 8–14 months in selected cases [11][13][14][15]; however, when PM are present, these results are worse, the patients survive less than 6 months, and there are no survivors after 5 years [3][11][16][17]. Even the patients with positive peritoneal cytology (microscopic PM) and without macroscopic nodes are classified at stage 4 and have a similar prognosis and the same treatment as the other metastatic GC patients [4].
Since the 1990s, the knowledge of PM development has made great progress; this has changed the classical belief that peritoneal implants constitute systemic disease, this now being considered a locally disseminated disease [18]. The treatment of PM by combining systemic chemotherapy, cytoreductive surgery (CRS), and hyperthermic intraperitoneal chemotherapy (HIPEC) has achieved encouraging results for different tumors that affect the peritoneum. CRS can remove the macroscopic disease (peritoneal nodules) through different peritonectomy procedures and visceral resections, while the microscopical disease is treated locally with intraperitoneal chemotherapy [19][20].
Currently, this multimodal treatment is the standard of care for pseudomyxoma peritonei and peritoneal mesothelioma [21][22]. In selected patients with PM due to colorectal cancer, CRS is an accepted treatment; the addition of HIPEC has been questioned after the negative results published from the PRODIGE-7 trial, but there are ongoing studies regarding its validation [23][24]. CRS, combined with systemic chemotherapy, is the standard treatment for advanced ovarian cancer, but evidence of the efficacy of HIPEC has increased in recent years regarding this disease [25]. This multimodal treatment has been also used to treat PM from GC, with encouraging results, according to different retrospective studies and several comparative studies [3][4][5][6][7][17][26][27][28][29].

2. Prevention of Development of PM in Locally Advanced GC

The peritoneal cavity is the most common site of tumor recurrence after radical gastrectomy with D2 lymphadenectomy in cases of locally advanced GC. Currently, the standard perioperative complementary therapy is systemic chemotherapy. In spite of correct treatment, peritoneal relapses will still occur in about 40% of patients [6][8][11]. Systemic chemotherapy has serious difficulties in penetrating the blood–peritoneal barrier and accessing the peritoneum; for this reason, other types of treatments have been sought that could act more effectively on the peritoneum [5]. If the drug is administered directly into the peritoneal cavity, the blood–peritoneal barrier will not allow it to penetrate into the bloodstream, at least partially; therefore, we can achieve high local concentrations of the drug without the side effects that are derived from its systemic administration.
The use of adjuvant HIPEC after a curative gastrectomy in patients with locally advanced GC, without PM, can prevent a peritoneal relapse. There are numerous studies showing the effectiveness of HIPEC as a prophylactic treatment (Table 1).
Table 1. Prophylactic hyperthermic intraperitoneal chemotherapy (HIPEC) for locally advanced gastric cancer without peritoneal metastases.

Author (Year)

Patient Number

Cytostatic

Morbidity

Survival Results

Fujimoto (1999) [30]

71 (surgery + HIPEC) vs. 70 (surgery alone)

MMC

2/71 vs. 2/70

4-year OS: 76% vs. 58%

Yonemura (2001) [31]

48 (surgery + HIPEC) vs. 44 (surgery + NIPEC) vs. 47 (surgery alone)

MMC + Cisplatin

19% vs. 14% vs. 19% (mortality: 4% vs. 0% vs. 4%)

5-year OS: 61% vs. 44% vs. 42%

Zhu (2006) [32]

41 (surgery + HIPEC) vs. 53 (surgery alone)

MMC+ Cisplatin

23% vs. 12%

4-year OS: 70% vs. 52%

Cui (2014) [33]

48 (surgery) vs. 48 (NAC + surgery) vs. 48 (surgery + HIPEC) vs. 48 (NAC + surgery + HIPEC)

Cisplatin

No differences

3-year OS: 35% vs. 62% vs. 58% vs. 75%

Desiderio (2017) [28]

731 (surgery + HIPEC) vs. 1079 (surgery alone)

MMC, cisplatin, etoposide

Higher risk in HIPEC group (RR = 2.17)

5-year OS better in HIPEC (RR = 0.82)

Xie (2020) [34]

51 (surgery + HIPEC) vs. 62 (surgery alone)

Cisplatin

No differences in severe morbidity (6% vs. 6%)

3-year OS 69% vs. 66% (p = 0.04)

Zhang (2022) [5]

561 (surgery + HIPEC) vs. 640 (surgery alone)

Cisplatin, MMC, etoposide

No differences (RR = 1.15)

3-year OS better in HIPEC (RR = 0.63)
HIPEC: Hyperthermic intraperitoneal chemotherapy; MMC: mitomycin C; OS: overall survival; NIPEC: normothermic intraperitoneal chemotherapy; NAC: neoadjuvant chemotherapy.
Despite these results, HIPEC has not been established as an adjuvant therapy to prevent peritoneal recurrence in the Western world. Most of the studies in this context have been published in Asia; this fact generates the eternal scientific dilemma of whether the results obtained in Asian patients can be extrapolated to Western patients. The GASTRICHIP trial is a European study (French, with the collaboration of a few Spanish centers) that evaluates the effect of HIPEC as adjuvant therapy in locally advanced GC [35]. The recruitment has concluded, and the results will be published soon. Indeed, the safety results of the first 200 patients enrolled in the trial were presented at the second Congress of the International Society for the Study of Pleura and Peritoneum, 2021, and there were no differences in morbidity seen between the groups [36].

3. Treatment of PM of GC Origin

The treatment of PM of GC origin is complex and aggressive, with limited results; therefore, the correct identification of patients is essential to choose the appropriate treatment for each one. When a patient is diagnosed with GC with PM, it is essential to assess the extent of the disease. The volume of peritoneal disease must be carefully evaluated to identify those patients that are potentially curable; diagnostic laparoscopy is required to establish this peritoneal disease extension using the peritoneal cancer index (PCI) [37]. The abdominal cavity is divided into 13 anatomical regions, and each area is given a value from 0 to 3, based on the volume of peritoneal disease in that region; therefore, a numerical value is set, ranging from 0 to 39.
The value of PCI is essential when selecting patients for CRS treatment with HIPEC because the volume of peritoneal disease is an independent prognostic factor. In addition, complete cytoreduction is necessary to obtain good survival results. PCI and the grade of completeness of cytoreduction are related factors, assessed via the completeness cytoreduction score (CCS) according to the residual tumor, this being CCS-0 for no macroscopic residue, CCS-1 for the macroscopic residue of < 2.5 mm, CCS-2 for 2.5 mm to 2.5 cm tumoral residue and CCS-3 with a residual tumor of > 2.5 cm [38]); the possibility of achieving cytoreduction at CCS-0 is inversely proportional to PCI. Several studies in the last few years have recommended a PCI limit to propose curative treatment [7][17][39].
Nowadays, CRS and HIPEC represent a treatment for selected patients with GC and PM that has had the best survival results published (Table 2).
Table 2. Treatment with cytoreductive surgery (CRS) and the hyperthermic intraperitoneal chemotherapy (HIPEC) of peritoneal metastases of gastric cancer origin.

Author (Year)

Patients Number

Cytostatic

Morbidity

Survival Results

Glehen (2010) [17]

159 (CRS + HIPEC)

MMC, Cisplatin, Oxaliplatin

Grade 3–4: 27.8%. Mortality: 6.5%

Median OS: 9.2 months; 5-year OS: 13%

Yang (2011) [26]

34 (CRS + HIPEC) vs. 34 (CRS)

MMC + Cisplatin

14.7% vs. 11.7%. Mortality: 0%

Median OS: 11 vs. 6.5 months

Desiderio (2017) [28]

289 (CRS + HIPEC) vs. 331 (CRS)

MMC, Cisplatin, Etoposide

Higher risk in HIPEC group (RR = 2.15, p < 0.01)

Median OS: 11 vs. 7 months

Manzanedo (2019) [7]

88 (CRS + HIPEC)

Cisplatin, Doxorubicin, MMC, Oxaliplatin

Grade III-IV D-C: 31%. Mortality: 3.4%

Median OS: 21.2 months; 3-year OS: 30.9%

Bonnot (2019) [27]

180 (CRS + HIPEC) vs. 97 (CRS)

MMC, Cisplatin, Oxaliplatin

53.7% vs. 55.3%. Mortality: 7.4% vs. 10.1%

Median OS: 18.8 vs. 12.1 months; 5-year OS: 19.9% vs. 6.4%

Rau (2020) [29]

235 (CRS + HIPEC)

MMC, Cisplatin, Doxorubicin, Oxaliplatin

Grade III-IV D-C: 17%. Mortality: 5.1%

Median OS: 13 months; 5-year OS: 6%

Zhang (2022) [5]

384 (CRS + HIPEC) vs. 307 (CRS)

MMC, Cisplatin, Doxorubicin, Etoposide

No morbidity differences

Higher mean OS in HIPEC group (4.67 months)

Martins (2022) [6]

299 (CRS + HIPEC) vs. 176 (CRS)

MMC, Cisplatin, Etoposide

No morbidity differences

A 5-year OS, 3 times higher in HIPEC (RR = 3.25, p = 0.010)
CRS: Cytoreductive surgery; HIPEC: hyperthermic intraperitoneal chemotherapy; MMC: Mitomycin C; NA: not available; OS: overall survival; D-C: Dindo–Clavien classification.

4. Palliative Treatment

A high percentage of patients with GC will have unresectable disease and their treatment should be aimed at symptom control. Most symptoms are secondary to the development of ascites, which can cause pain, dyspnea, early satiety, or fatigue [11].
Laparoscopic HIPEC has been used to reduce ascites and improve the symptoms. Different studies have shown an improvement in the symptoms of 95% of patients. Facchiano et al. published a systematic review of 76 patients treated with palliative laparoscopic HIPEC; 95% of these patients showed ascites control without severe morbidity [40].
Pressurized intraperitoneal aerosol chemotherapy (PIPAC) is a new administration technique involving chemotherapy via laparoscopy. This therapy has been described for palliative patients with unresectable PM [41]. In 2019, Alyami et al. published a systematic review that included 838 patients with PM (185 from GC); the clinical response rate was 50% to 91% [42]. The same authors published a retrospective analysis in 2021 that included only patients with unresectable PM of GC origin. They reported 163 PIPACs in 42 patients; major complications were observed in 3% of patients, the OS was 19 months, and 6 patients (14%) were converted to CRS and HIPEC [43]. There are many ongoing studies on PIPAC when used as palliative treatment as well as neoadjuvant therapy to reduce the tumor burden and enable rescue CRS. PIPAC is approved in Europe but is not yet approved for use in the United States. The results of PIPAC are promising, but it is an expensive treatment that requires an invasive and repeated procedure [44]. Until now, PIPAC has not been compared with any other treatments (laparoscopic HIPEC, systemic chemotherapy plus biologic therapy, normothermic intraperitoneal chemotherapy in cycles), so it is still premature to draw too optimistic a conclusion about its results.
In summary, laparoscopic HIPEC and PIPAC are two good alternatives as palliative treatments in patients with unresectable PM. Both treatments are even being tested as conversion therapy to rescue patients in order to achieve complete cytoreduction. In the future, we will have more answers when the ongoing studies are completed (for example, the CHIMERA trial, NCT04597294 in the context of laparoscopic HIPEC, or trial PIPAC_VEROne, NCT05303714, for PIPAC).
New treatments based on molecular alterations, such as trastuzumab for HER2-positive patients or immunotherapy (nivolumab or pembrolizumab) in patients with microsatellite instability or PDL-1 overexpression, are being used in a palliative context with very good results. There are even studies underway using these drugs as neoadjuvant therapy, presenting surprising results. This immunotherapy may change the prognosis in highly specific cases and, in the future, we may need to rethink the treatment of patients in cases that today are considered palliative.

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Israel Manzanedo
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Fernando Pereira
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Estíbalitz Pérez-Viejo
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Ángel Serrano
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Update Date: 13 Apr 2023
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