The Value of Serum Immunoglobulin G Glycome in the Preoperative Discrimination of Peritoneal Metastasis from Advanced Gastric Cancer

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Abstract

Background: Peritoneal metastasis, associated with poor prognosis in gastric cancer, is difficult to discriminate from advanced gastric cancer preoperatively. However, operative diagnosis could bring both mental and physical trauma and economic burden for patients. Consequently, a non-invasive biomarker is necessary to reduce the burden of operative diagnosis and improve survival quality of patients. This study aims to elucidate the correlation between Immunoglobulin G (IgG) N-glycome and peritoneal metastasis and find potential biomarkers in preoperative discrimination of peritoneal metastasis from advanced gastric cancer based on the comprehensive sample set.

Methods: A total of 373 gastric cancer patients were enrolled and randomly sorted into training cohort (n=249) and validation cohort (n=124). The IgG N-glycome composition was analyzed by ultra-performance liquid chromatography.

Results: Twenty-four glycan peaks were directly detected and 15 traits based on the same structures were evaluated between peritoneal metastasis group and advanced gastric cancer group. Several differences in IgG glycosylation were found: sialylation and fucosylation were increased in peritoneal metastasis, while neutral glycosylation, monogalacosylation and bisecting GlcNAc were decreased. Based on the significant glycomics profile, a glyco-model composed of five glycan peaks (GP6, GP9, GP11, GP21 and GP23) was established with area under the receiver operating characteristic curve (AUC) value of 0.80 (training cohort) and 0.77 (validation cohort), which showed good potential in discriminating peritoneal metastasis from advanced gastric cancer. The diagnostic performance of this model was further validated in a combined cohort (AUC=0.79). Two patients with gastric cancer were selected to perform and demonstrate the usage of the diagnostic workflow.

Conclusions: Here we firstly present IgG glycome profiles in a large number of preoperative peritoneal metastasis serums. The IgG glycan was highly associated with peritoneal metastasis. These findings enhance the understanding of peritoneal metastasis. Besides, our results suggested that the newly established glyco-model could be a reliable predictor of the presence of peritoneal metastasis in patients with advanced gastric cancer.

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Most cited references 25

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High Throughput Isolation and Glycosylation Analysis of IgG–Variability and Heritability of the IgG Glycome in Three Isolated Human Populations*

Maja Pučić Baković, Ana Knežević, Jana Vidič … (2011)

All immunoglobulin G molecules carry N-glycans, which modulate their biological activity. Changes in N-glycosylation of IgG associate with various diseases and affect the activity of therapeutic antibodies and intravenous immunoglobulins. We have developed a novel 96-well protein G monolithic plate and used it to rapidly isolate IgG from plasma of 2298 individuals from three isolated human populations. N-glycans were released by PNGase F, labeled with 2-aminobenzamide and analyzed by hydrophilic interaction chromatography with fluorescence detection. The majority of the structural features of the IgG glycome were consistent with previous studies, but sialylation was somewhat higher than reported previously. Sialylation was particularly prominent in core fucosylated glycans containing two galactose residues and bisecting GlcNAc where median sialylation level was nearly 80%. Very high variability between individuals was observed, approximately three times higher than in the total plasma glycome. For example, neutral IgG glycans without core fucose varied between 1.3 and 19%, a difference that significantly affects the effector functions of natural antibodies, predisposing or protecting individuals from particular diseases. Heritability of IgG glycans was generally between 30 and 50%. The individual's age was associated with a significant decrease in galactose and increase of bisecting GlcNAc, whereas other functional elements of IgG glycosylation did not change much with age. Gender was not an important predictor for any IgG glycan. An important observation is that competition between glycosyltransferases, which occurs in vitro, did not appear to be relevant in vivo, indicating that the final glycan structures are not a simple result of competing enzymatic activities, but a carefully regulated outcome designed to meet the prevailing physiological needs.

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Postoperative outcome and sites of recurrence in patients following curative resection of gastric cancer.

Y Kakeji, K Sugimachi, E Tokunaga … (2000)

Recurrence occurs in a variety of forms and in different organs after 'curative resection' of gastric cancer. This study investigated the postoperative prognosis for each type of recurrence. From 1969 to 1988, 939 patients with gastric cancer underwent curative resection; data on 130 of 207 patients who died with recurrence were analysed. Attention was focused on the site of recurrence and the postoperative outcome. Haematogenous recurrence was evident in 54 per cent (70 of 130 patients), peritoneal recurrence in 43 per cent (56 of 130), lymph node recurrence in 12 per cent (16 of 130) and local recurrence in 22 per cent (29 of 130). Thirty-three patients (25 per cent) had recurrences at multiple sites. Peritoneal and local recurrences were related to infiltrative growth, in contrast to haematogenous and lymphatic recurrences. There were no statistical differences in survival time among each type of recurrence and survival was not related to the number of sites of recurrence. Survival did not depend on factors of sex, age, tumour location, tumour size, depth of invasion, tissue differentiation, histological growth pattern, lymphatic and vascular involvement, lymph node metastasis and extent of lymph node dissection. The clinicopathological characteristics of gastric cancer determine the type of recurrence, although the clinical outcome is the same for each type of tumour and is not related to the number of sites of recurrence.

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Imaging in assessing hepatic and peritoneal metastases of gastric cancer: a systematic review

Zhen Wang, Jun-qiang Chen (2011)

Background Hepatic and peritoneal metastases of gastric cancer are operation contraindications. Systematic review to provide an overview of imaging in predicting the status of liver and peritoneum pre-therapeuticly is essential. Methods A systematic review of relevant literatures was performed in Pubmed/Medline, Embase, The Cochrane Library and the China Biological Medicine Databases. QUADAS was used for assessing the methodological quality of included studies and the bivariate model was used for this meta-analysis. Results Totally 33 studies were included (8 US studies, 5 EUS studies, 22 CT studies, 2 MRI studies and 5 18F-FDG PET studies) and the methodological quality of included studies was moderate. The result of meta-analysis showed that CT is the most sensitive imaging method [0.74 (95% CI: 0.59-0.85)] with a high rate of specificity [0.99 (95% CI: 0.97-1.00)] in detecting hepatic metastasis, and EUS is the most sensitive imaging modality [0.34 (95% CI: 0.10-0.69) ] with a specificity of 0.96 (95% CI: 0.87-0.99) in detecting peritoneal metastasis. Only two eligible MRI studies were identified and the data were not combined. The two studies found that MRI had both high sensitivity and specificity in detecting liver metastasis. Conclusion US, EUS, CT and 18F-FDG PET did not obtain consistently high sensitivity and specificity in assessing liver and peritoneal metastases of gastric cancer. The value of laparoscopy, PET/CT, DW-MRI, and new PET tracers such as 18F-FLT needs to be studied in future.

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Author and article information

Journal

Journal ID (nlm-ta): J Cancer

Journal ID (iso-abbrev): J Cancer

Journal ID (publisher-id): jca

Title: Journal of Cancer

Publisher: Ivyspring International Publisher (Sydney )

ISSN (Electronic): 1837-9664

Publication date Collection: 2019

Publication date (Electronic): 2 June 2019

Volume: 10

Issue: 12

Pages: 2811-2821

Affiliations

[1 ]NHC Key Laboratory of Glycoconjugates Research, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan University, Shanghai, China

[2 ]Department of General Surgery, Zhongshan Hospital, Fudan University, Shanghai, China

[3 ]Obstetrics and Gynecology Hospital, Fudan University, Shanghai, China

Author notes

✉ Corresponding authors: Xuefei Wang, Phone and Fax number: 86-21-64041990; Email: wang.xuefei@ 123456zs-hospital.sh.cn . Shifang Ren, Phone and Fax number: +86-21-54237701; Email: renshifang@ 123456fudan.edu.cn

Competing Interests: The authors have declared that no competing interest exists.

Article

Publisher ID: jcav10p2811

DOI: 10.7150/jca.31380

PMC ID: 6584920

PubMed ID: 31258789

SO-VID: d7143839-138e-43f7-b902-056c424bc978

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This is an open access article distributed under the terms of the Creative Commons Attribution (CC BY-NC) license ( https://creativecommons.org/licenses/by-nc/4.0/). See http://ivyspring.com/terms for full terms and conditions.

The Value of Serum Immunoglobulin G Glycome in the Preoperative Discrimination of Peritoneal Metastasis from Advanced Gastric Cancer

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Most cited references 25

High Throughput Isolation and Glycosylation Analysis of IgG–Variability and Heritability of the IgG Glycome in Three Isolated Human Populations*

Postoperative outcome and sites of recurrence in patients following curative resection of gastric cancer.

Imaging in assessing hepatic and peritoneal metastases of gastric cancer: a systematic review

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