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pmid:31824776

Overexpression of VEGF-C and MMP-9 predicts poor prognosis in Kazakh patients with esophageal squamous cell carcinoma.

Jiangfen Li · Yufang Xie · Xueli Wang · Chenhao Jiang · Xin Yuan · Anzhi Zhang · Chunxia Liu · Lijuan Pang · Feng Li · Jianming Hu

PeerJ · 2019 doi:10.7717/peerj.8182

Paper

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Experiment

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Data

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Analysis

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Record details sci_version · id · kind · revision · content_hash · schema · created_at · updated_at · generator
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pmid:31824776
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science-record
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sha256:1c4ec1fb0365ca48d93181758e7dab2ece8f3db5da74510ef216a6e4503333f0
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https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json
created_at
2026-11-01T15:40:53Z
updated_at
2026-11-01T22:44:24Z
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corpus-assay-engine
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paper object · 10 fields
state
complete
title
Overexpression of VEGF-C and MMP-9 predicts poor prognosis in Kazakh patients with esophageal squamous cell carcinoma.
doi
10.7717/peerj.8182
pmid
31824776
authors array · 10 items
[0]
Jiangfen Li
[1]
Yufang Xie
[2]
Xueli Wang
[3]
Chenhao Jiang
[4]
Xin Yuan
[5]
Anzhi Zhang
[6]
Chunxia Liu
[7]
Lijuan Pang
[8]
Feng Li
[9]
Jianming Hu
journal
PeerJ
year
2019
abstract
Vascular endothelial growth factor (VEGF) and Matrix metalloproteinases (MMPs) are believed to participate in infiltration of tumors. High mortality of esophageal squamous cell carcinoma (ESCC) related to its primary infiltration; however, it is not clear whether the expression of VEGF and MMPs is involved in this process. Screening of The Cancer Genome Atlas (TCGA) database showed that among the VEGF family and MMP9, VEGF-A, VEGF-C, and MMP-9 mRNA were overexpression in ESCC. This result was verified using the Oncomine database and in Kazakh patients with ESCC. Overexpression of VEGF-C and MMP-9 and positive association with advanced esophageal cancer and invading ESCC cells (Gene Expression Omnibus (GEO): GSE21293). Immunohistochemical staining revealed that VEGF-C and MMP-9 were overexpressed in Kazakh ESCCs. VEGF-C expression was related to invasive depth, tumor-node-metastasis (TNM) staging, lymphatic, and lymph node metastasis of ESCC. The linear association between them was further confirmed in TCGA database and the specimens from Kazakh patients with ESCC. Patients with both proteins expression had tumors with greater aggressiveness, suffered from poor prognosis compared with patients who did not express either protein or expressed protein alone. Both proteins expression predicted high invasiveness of ESCC, which is related to worse prognosis of Kazakh ESCCs.
claims array · 2 items
[0] object · 6 fields
id
claim-method
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Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. The Spearman method was applied to assess the relationship between each molecule. The relationship between proteins expression and clinical parameters were analyzed by ANOVA. Kaplan–Meier method and Cox proportional risk regression model was used to assessing patient outcomes, a P-Value < 0.05 was supposed to divergence significant.
kind
methodological
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null
evidence array · 1 item
[0] object · 3 fields
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source:pmid:31824776
locator
sections[7] "Statistical analysis" paragraph 2
quote
Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. The Spearman method was applied to assess the relationship between each molecule. The relationship between proteins expression and clinical parameters were analyzed by ANOVA. Kaplan–Meier method and Cox proportional risk regression model was used to assessing patient outcomes, a P-Value < 0.05 was supposed to divergence significant.
state
complete
[1] object · 6 fields
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claim-data-access
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The raw measurements are available in the Supplemental Files.
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methodological
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null
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sections[23] "Data Availability" paragraph 2
quote
The raw measurements are available in the Supplemental Files.
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PMC6896941
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The expression of VEGF-C in Kazakh esophageal squamous cell carcinoma (ESCC) and cancer adjacent normal (CAN) tissues.
structure object · 5 fields
pmcid
PMC6896941
section_index
11
section_title
VEGF-C and MMP-9 protein expression in Kazakh patients with ESCC is associated with progression of ESCC
row_count
3
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9
table object · 8 fields
label
Table 1
caption
The expression of VEGF-C in Kazakh esophageal squamous cell carcinoma (ESCC) and cancer adjacent normal (CAN) tissues.
rows array · 3 items
[0] array · 9 items
[0]
[1]
Cases (N)
[2]
0
[3]
+1
[4]
+2
[5]
+3
[6]
Mean rank
[7]
Z
[8]
P-value
[1] array · 9 items
[0]
ESCCs
[1]
100
[2]
4
[3]
24
[4]
45
[5]
27
[6]
123.54
[7]
−5.964
[8]
<0.001*
[2] array · 7 items
[0]
CANs
[1]
100
[2]
18
[3]
45
[4]
35
[5]
2
[6]
77.47
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section[11]/table-wrap[1]#table-1
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Correlation between expression of VEGF-C and clinicopathologic parameters in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
structure object · 5 fields
pmcid
PMC6896941
section_index
11
section_title
VEGF-C and MMP-9 protein expression in Kazakh patients with ESCC is associated with progression of ESCC
row_count
31
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5
table object · 8 fields
label
Table 2
caption
Correlation between expression of VEGF-C and clinicopathologic parameters in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
rows array · 31 items
[0] array · 4 items
[0]
Variable
[1]
Cases(N)
[2]
VEGF-C
[3]
P-value
[1] array · 5 items
[0]
[1]
[2]
Negative (0, 1)
[3]
Positive (2, 3)
[4]
[2] array · 1 item
[0]
Age (y)
[3] array · 5 items
[0]
≤Median (58 y)
[1]
52
[2]
14
[3]
38
[4]
0.540
[4] array · 4 items
[0]
>Median
[1]
48
[2]
14
[3]
34
[5] array · 1 item
[0]
Gender
[6] array · 5 items
[0]
Male
[1]
71
[2]
15
[3]
56
[4]
0.001*
[7] array · 4 items
[0]
Female
[1]
29
[2]
13
[3]
16
[8] array · 1 item
[0]
Tumor location
[9] array · 5 items
[0]
Upper
[1]
1
[2]
0
[3]
1
[4]
0.183
[10] array · 5 items
[0]
Middle
[1]
74
[2]
20
[3]
54
[4]
[11] array · 4 items
[0]
Lower
[1]
25
[2]
8
[3]
17
[12] array · 1 item
[0]
Histologic grade
[13] array · 5 items
[0]
Well
[1]
28
[2]
4
[3]
24
[4]
0.183
[14] array · 5 items
[0]
Moderate
[1]
49
[2]
16
[3]
33
[4]
[15] array · 4 items
[0]
Poor
[1]
23
[2]
8
[3]
15
[16] array · 1 item
[0]
Depth of invasion
[17] array · 5 items
[0]
T1–T2
[1]
37
[2]
16
[3]
21
[4]
<0.001*
[18] array · 4 items
[0]
T3–T4
[1]
63
[2]
12
[3]
51
[19] array · 1 item
[0]
Venous invasion
[20] array · 5 items
[0]
Negative
[1]
93
[2]
27
[3]
66
[4]
0.399
[21] array · 4 items
[0]
Positive
[1]
7
[2]
1
[3]
6
[22] array · 1 item
[0]
Lymphatic invasion
[23] array · 5 items
[0]
Negative
[1]
29
[2]
16
[3]
13
[4]
<0.001*
[24] array · 4 items
[0]
Positive
[1]
71
[2]
12
[3]
59
[25] array · 1 item
[0]
Nodal status
[26] array · 5 items
[0]
pN−
[1]
47
[2]
22
[3]
25
[4]
<0.001*
[27] array · 4 items
[0]
pN+
[1]
53
[2]
6
[3]
47
[28] array · 1 item
[0]
TNM stage
[29] array · 5 items
[0]
I–II
[1]
61
[2]
26
[3]
35
[4]
<0.001*
[30] array · 4 items
[0]
III–IV
[1]
39
[2]
2
[3]
37
locator
section[11]/table-wrap[2]#table-2
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Correlation between VEGF-C/MMP-9 expression and clinicopathologic parameters in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
structure object · 5 fields
pmcid
PMC6896941
section_index
12
section_title
VEGF-C and MMP-9 are positively and linearly correlated in Kazakh patients with ESCC, and their overexpression predicts increased tumor aggressiveness
row_count
30
column_count
6
table object · 8 fields
label
Table 3
caption
Correlation between VEGF-C/MMP-9 expression and clinicopathologic parameters in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
rows array · 30 items
[0] array · 6 items
[0]
Variable
[1]
Cases(N)
[2]
VEGF-C (−)MMP-9 (−)
[3]
VEGF-C (+)or MMP-9 (+)
[4]
VEGF-C (+)MMP-9 (+)
[5]
P-value
[1] array · 1 item
[0]
Age (y)
[2] array · 6 items
[0]
≤Median (58 y)
[1]
52
[2]
13
[3]
13
[4]
26
[5]
0.660
[3] array · 5 items
[0]
>Median
[1]
48
[2]
7
[3]
17
[4]
24
[4] array · 1 item
[0]
Gender
[5] array · 6 items
[0]
Male
[1]
71
[2]
13
[3]
19
[4]
39
[5]
0.254
[6] array · 5 items
[0]
Female
[1]
29
[2]
7
[3]
11
[4]
11
[7] array · 1 item
[0]
Tumor location
[8] array · 6 items
[0]
Upper
[1]
1
[2]
0
[3]
1
[4]
0
[5]
0.379
[9] array · 6 items
[0]
Middle
[1]
74
[2]
14
[3]
21
[4]
39
[5]
[10] array · 5 items
[0]
Lower
[1]
25
[2]
6
[3]
8
[4]
22
[11] array · 1 item
[0]
Histologic grade
[12] array · 6 items
[0]
Well
[1]
28
[2]
4
[3]
5
[4]
19
[5]
0.006*
[13] array · 6 items
[0]
Moderate
[1]
49
[2]
11
[3]
19
[4]
19
[5]
[14] array · 5 items
[0]
Poor
[1]
23
[2]
5
[3]
6
[4]
12
[15] array · 1 item
[0]
Depth of invasion
[16] array · 6 items
[0]
T1–T2
[1]
37
[2]
12
[3]
10
[4]
15
[5]
0.001*
[17] array · 5 items
[0]
T3–T4
[1]
63
[2]
8
[3]
20
[4]
35
[18] array · 1 item
[0]
Venous invasion
[19] array · 6 items
[0]
Negative
[1]
93
[2]
19
[3]
30
[4]
44
[5]
0.006*
[20] array · 6 items
[0]
Positive
[1]
7
[2]
1
[3]
0
[4]
6
[5]
[21] array · 1 item
[0]
Lymphatic invasion
[22] array · 6 items
[0]
Negative
[1]
29
[2]
15
[3]
7
[4]
7
[5]
<0.001*
[23] array · 6 items
[0]
Positive
[1]
71
[2]
5
[3]
23
[4]
43
[5]
[24] array · 1 item
[0]
Nodal status
[25] array · 6 items
[0]
pN−
[1]
47
[2]
17
[3]
16
[4]
14
[5]
<0.001*
[26] array · 5 items
[0]
pN+
[1]
53
[2]
3
[3]
14
[4]
36
[27] array · 1 item
[0]
TNM stage
[28] array · 6 items
[0]
I–II
[1]
61
[2]
19
[3]
22
[4]
20
[5]
<0.001*
[29] array · 5 items
[0]
III–IV
[1]
39
[2]
1
[3]
8
[4]
30
locator
section[12]/table-wrap[1]#table-3
[4] object · 16 fields
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section[12]/table-wrap[2]#table-4
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Stratified analysis of correlation between clinicopathologic features and VEGF-C and MMP-9 expression in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
structure object · 5 fields
pmcid
PMC6896941
section_index
12
section_title
VEGF-C and MMP-9 are positively and linearly correlated in Kazakh patients with ESCC, and their overexpression predicts increased tumor aggressiveness
row_count
20
column_count
7
table object · 8 fields
label
Table 4
caption
Stratified analysis of correlation between clinicopathologic features and VEGF-C and MMP-9 expression in Kazakh esophageal squamous cell carcinoma (ESCC) tissues.
rows array · 20 items
[0] array · 7 items
[0]
Variable
[1]
VEGF-C(−)MMP-9(−)
[2]
VEGF-C(+)MMP-9(+)
[3]
P-value
[4]
VEGF-C(+)orMMP-9(+)
[5]
VEGF-C(+)MMP-9(+)
[6]
P-value
[1] array · 1 item
[0]
Histologic grade
[2] array · 7 items
[0]
Well
[1]
4
[2]
19
[3]
0.382
[4]
5
[5]
19
[6]
0.001*
[3] array · 7 items
[0]
Moderate
[1]
11
[2]
19
[3]
[4]
19
[5]
19
[6]
[4] array · 5 items
[0]
Poor
[1]
5
[2]
12
[3]
6
[4]
12
[5] array · 1 item
[0]
Depth of invasion
[6] array · 7 items
[0]
T1–T2
[1]
12
[2]
15
[3]
<0.001*
[4]
10
[5]
15
[6]
0.970
[7] array · 5 items
[0]
T3–T4
[1]
8
[2]
35
[3]
20
[4]
35
[8] array · 1 item
[0]
Venous invasion
[9] array · 7 items
[0]
Negative
[1]
19
[2]
44
[3]
0.693
[4]
30
[5]
44
[6]
0.005*
[10] array · 5 items
[0]
Positive
[1]
1
[2]
6
[3]
0
[4]
6
[11] array · 1 item
[0]
Lymphatic invasion
[12] array · 7 items
[0]
Negative
[1]
15
[2]
7
[3]
<0.001*
[4]
7
[5]
7
[6]
0.067
[13] array · 5 items
[0]
Positive
[1]
5
[2]
43
[3]
23
[4]
43
[14] array · 1 item
[0]
Nodal status
[15] array · 7 items
[0]
pN−
[1]
17
[2]
14
[3]
<0.001*
[4]
16
[5]
14
[6]
0.007*
[16] array · 5 items
[0]
pN+
[1]
3
[2]
36
[3]
14
[4]
36
[17] array · 1 item
[0]
TNM stage
[18] array · 7 items
[0]
I–II
[1]
19
[2]
20
[3]
<0.001*
[4]
22
[5]
20
[6]
<0.001*
[19] array · 5 items
[0]
III–IV
[1]
1
[2]
30
[3]
8
[4]
30
locator
section[12]/table-wrap[2]#table-4
[5] object · 16 fields
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asset:table:pmid:31824776:5
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section[13]/table-wrap[1]#table-5
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null
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Univariate and multivariate analysis of overall survival (OS) of esophageal squamous cell carcinoma (ESCC).
structure object · 5 fields
pmcid
PMC6896941
section_index
13
section_title
VEGF-C and MMP-9 protein overexpression predicts poor prognosis in Kazakh ESCCs
row_count
14
column_count
8
table object · 8 fields
label
Table 5
caption
Univariate and multivariate analysis of overall survival (OS) of esophageal squamous cell carcinoma (ESCC).
rows array · 14 items
[0] array · 4 items
[0]
Variable
[1]
Cases (N)
[2]
Univariate analysis
[3]
Multivariate analysis
[1] array · 8 items
[0]
[1]
[2]
HR
[3]
95% CI
[4]
P-value
[5]
HR
[6]
95% CI
[7]
P-value
[2] array · 8 items
[0]
Age (>58 y vs ≤58 y)
[1]
100
[2]
0.859
[3]
0.603–1.225
[4]
0.402
[5]
[6]
[7]
[3] array · 8 items
[0]
Sex (female vs male)
[1]
100
[2]
1.029
[3]
0.679–1.557
[4]
0.894
[5]
[6]
[7]
[4] array · 8 items
[0]
Histologic grade (moderate + poor vs well)
[1]
100
[2]
1.148
[3]
0.760–1.734
[4]
0.511
[5]
[6]
[7]
[5] array · 8 items
[0]
Tumor location (middle vs upper + lower)
[1]
100
[2]
1.193
[3]
0.756–1.885
[4]
0.448
[5]
[6]
[7]
[6] array · 8 items
[0]
Venous invasion (positive vs negative)
[1]
100
[2]
3.569
[3]
1.624–4.064
[4]
<0.001*
[5]
1.242
[6]
0.653–2.363
[7]
0.508
[7] array · 8 items
[0]
Lymphatic invasion (positive vs negative)
[1]
100
[2]
2.404
[3]
1.344–4.297
[4]
0.003*
[5]
1.418
[6]
0.768–2.619
[7]
0.264
[8] array · 8 items
[0]
Depth of invasion (T3 + T4 vs T1 + T2)
[1]
100
[2]
1.583
[3]
1.061–2.364
[4]
0.025*
[5]
0.999
[6]
0.637–1.567
[7]
0.997
[9] array · 8 items
[0]
Nodal metastasis (+ vs −)
[1]
100
[2]
2.821
[3]
1.897–4.195
[4]
<0.001*
[5]
1.078
[6]
0.507–2.292
[7]
0.845
[10] array · 8 items
[0]
TNM stage (III + IV vs I + II)
[1]
100
[2]
3.449
[3]
2.036–5.034
[4]
<0.001*
[5]
2.646
[6]
1.379–5.078
[7]
0.03*
[11] array · 8 items
[0]
VEGF-C (+ vs −)
[1]
100
[2]
2.074
[3]
1.318–3.700
[4]
0.017*
[5]
1.834
[6]
0.718–4.689
[7]
0.205
[12] array · 8 items
[0]
MMP-9 (+ vs −)
[1]
100
[2]
1.854
[3]
1.219–2.820
[4]
0.004*
[5]
2.226
[6]
0.670–7.389
[7]
0.191
[13] array · 8 items
[0]
VEGF-C/MMP-9 (both + vs VEGF-C or MMP-9 −)
[1]
100
[2]
1.760
[3]
1.185–2.612
[4]
0.005*
[5]
0.432
[6]
0.121–1.548
[7]
0.198
locator
section[13]/table-wrap[1]#table-5
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analysis object · 4 fields
state
complete
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id
method-1
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group_comparison
specific
anova
label
Group comparison
dsl_operations array · 4 items
[0]
group_summary
[1]
welch_t
[2]
bootstrap_mean_difference
[3]
group_comparison_anova
missing_operations array · 0 items
parameters object · 0 fields
data_shapes array · 1 item
[0]
two_or_more_groups_continuous
evidence object · 3 fields
score
1
band
verbatim
quote
Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. The Spearman method was applied to assess the relationship between each molecule. The relationship between proteins expression and clinical parameters were analyzed by ANOVA. Kaplan–Meier method and Cox proportional risk regression model was used to assessing patient outcomes, a P-Value < 0.05 was supposed to divergence significant.
targets array · 0 items
gaps array · 0 items
capability object · 3 fields
state
complete
requirements array · 1 item
[0] object · 6 fields
capability_id
capability:computational_analysis
label
Computational analysis platform
assay_families array · 9 items
[0]
meta_analysis
[1]
machine_learning
[2]
survival_analysis
[3]
statistical_regression
[4]
pca
[5]
molecular_docking
[6]
network_analysis
[7]
differential_expression
[8]
gwas
candidate
Automated Assays Laravel application and simulated adapters
gaps array · 0 items
readiness object · 8 fields
state
blocked
tier
R4
blocked_on
data:accession_absent
axes object · 3 fields
method object · 5 fields
tier
R1
expressible
true
required_operations array · 4 items
[0]
group_summary
[1]
welch_t
[2]
bootstrap_mean_difference
[3]
group_comparison_anova
missing_operations array · 0 items
basis
The paper names the method it used and the corpus's method extractor maps it onto the DSL catalogue: anova.
capability object · 4 fields
tier
R1
capability_id
capability:computational_analysis
availability_state
owned
basis
The computational analysis is owned. The physical bench the paper used is not, so a physical validation cannot be run here.
data object · 6 fields
tier
R4
reachable
false
accessions array · 0 items
resolved_accessions array · 0 items
statements array · 1 item
[0]
The raw measurements are available in the Supplemental Files.
basis
The paper names no accession to its source data, so the data has to come from the authors.
can_run object · 3 fields
dsl_operations array · 4 items
[0]
group_summary
[1]
welch_t
[2]
bootstrap_mean_difference
[3]
group_comparison_anova
assets array · 6 items
[0]
source:pmid:31824776
[1]
asset:table:pmid:31824776:1
[2]
asset:table:pmid:31824776:2
[3]
asset:table:pmid:31824776:3
[4]
asset:table:pmid:31824776:4
[5]
asset:table:pmid:31824776:5
steps array · 1 item
[0]
run_analysis
must_build object · 5 fields
dsl_operations array · 0 items
converters array · 0 items
readers array · 0 items
capabilities array · 0 items
data_gaps array · 1 item
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data:geo:None
gaps array · 1 item
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data:accession_absent
review object · 5 fields
state
partial
machine_critique object · 5 fields
kind
extraction_review
reader object · 5 fields
model
MiniMax-M3.1-Flash
provider
minimax
provider_family
minimax
read_at
2026-10-31T18:53:42Z
independence
single_reader
evidence_check object · 2 fields
method
verbatim
availability
verbatim
calls
3
usage object · 3 fields
prompt_tokens
39020
completion_tokens
2661
cached_tokens
784
stages array · 1 item
[0] object · 4 fields
id
extraction
state
complete
reader
MiniMax-M3.1-Flash
provider
minimax
gaps array · 3 items
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review.independent_reader
[1]
review.machine_critique
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review.human_critique
execution object · 5 fields
state
absent
status
not_run
mode
null
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gaps array · 1 item
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provenance object · 7 fields
entities array · 3 items
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id
pmid:31824776
type
paper
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pmid:31824776
[1] object · 3 fields
id
source:pmid:31824776
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manuscript
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PMID 31824776 full text
[2] object · 3 fields
id
data:geo:None
type
dataset
label
GEO None
activities array · 3 items
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id
activity-reading-sci-2026-11-01
type
classification
used array · 3 items
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id
pmid:31824776
type
paper
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pmid:31824776
[1] object · 3 fields
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source:pmid:31824776
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manuscript
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PMID 31824776 full text
[2] object · 3 fields
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data:geo:None
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dataset
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GEO None
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agent:corpus-assay-engine
[1] object · 4 fields
id
activity-read-31824776
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extraction
used array · 1 item
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source:pmid:31824776
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agent:minimax-reader
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activity-resolve-None
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accession_resolution
used array · 1 item
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agent
agent:corpus-assay-engine
agents array · 2 items
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id
agent:corpus-assay-engine
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software
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Corpus assay engine
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id
agent:minimax-reader
type
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MiniMax literature reader
source_run_id
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dsl_catalogue_fingerprint
343fb30756ba6ec3
capability_table_fingerprint
2cb3e42f047d2ecf
snapshot_id
ba34b49490d9bfaf
lineage object · 4 fields
parent_id
pmid:31824776
parent_hash
sha256:bcfcd97cba6d814f6281b86500be42f249d773e48e89c414896729f8e935dedb
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null
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execution.not_run
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review.human_critique
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review.independent_reader
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step:obtain_source_data blocked on data:accession_absent
assays array · 2 items
[0] object · 11 fields
role
data_generation
definition_version
99e1195c7d6f
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support_state
partial
source_hashes object · 1 field
assay_lexicon
99e1195c7d6f
confidence
0.99
evidence array · 3 items
[0]
s (Gene Expression Omnibus (GEO): GSE21293). Immunohistochemical staining revealed that VEGF-C and MMP-9 were
[1]
SCC To confirm the above predictive results, IHC was carried out (Fig. 3). We classified the
[2]
antly related to it (Fig. 4C). Consistently, IHC analysis demonstrated a positively and linea
order_basis
paper_text_order:802
id
assay:1
[1] object · 11 fields
role
analysis
definition_id
group_comparison
definition_version
f2132e96ae6c7a4e
required_operations array · 4 items
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dsl_catalogue
f2132e96ae6c7a4e
evidence array · 1 item
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Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. The Spearman method was applied to assess the relationship between each molecule. The relationship between proteins expression and clinical parameters were analyzed by ANOVA. Kaplan–Meier method and Cox proportional risk regression model was used to assessing patient outcomes, a P-Value < 0.05 was supposed to divergence significant.
order_basis
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Complete file
{"sci_version": "1.2", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:31824776", "kind": "science-record", "revision": 8, "content_hash": "sha256:1c4ec1fb0365ca48d93181758e7dab2ece8f3db5da74510ef216a6e4503333f0", "created_at": "2026-11-01T15:40:53Z", "updated_at": "2026-11-01T22:44:24Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Overexpression of VEGF-C and MMP-9 predicts poor prognosis in Kazakh patients with esophageal squamous cell carcinoma.", "doi": "10.7717/peerj.8182", "pmid": "31824776", "authors": ["Jiangfen Li", "Yufang Xie", "Xueli Wang", "Chenhao Jiang", "Xin Yuan", "Anzhi Zhang", "Chunxia Liu", "Lijuan Pang", "Feng Li", "Jianming Hu"], "journal": "PeerJ", "year": 2019, "abstract": "Vascular endothelial growth factor (VEGF) and Matrix metalloproteinases (MMPs) are believed to participate in infiltration of tumors. High mortality of esophageal squamous cell carcinoma (ESCC) related to its primary infiltration; however, it is not clear whether the expression of VEGF and MMPs is involved in this process. Screening of The Cancer Genome Atlas (TCGA) database showed that among the VEGF family and MMP9, VEGF-A, VEGF-C, and MMP-9 mRNA were overexpression in ESCC. This result was verified using the Oncomine database and in Kazakh patients with ESCC. Overexpression of VEGF-C and MMP-9 and positive association with advanced esophageal cancer and invading ESCC cells (Gene Expression Omnibus (GEO): GSE21293). Immunohistochemical staining revealed that VEGF-C and MMP-9 were overexpressed in Kazakh ESCCs. VEGF-C expression was related to invasive depth, tumor-node-metastasis (TNM) staging, lymphatic, and lymph node metastasis of ESCC. The linear association between them was further confirmed in TCGA database and the specimens from Kazakh patients with ESCC. Patients with both proteins expression had tumors with greater aggressiveness, suffered from poor prognosis compared with patients who did not express either protein or expressed protein alone. Both proteins expression predicted high invasiveness of ESCC, which is related to worse prognosis of Kazakh ESCCs.", "claims": [{"id": "claim-method", "statement": "Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. The Spearman method was applied to assess the relationship between each molecule. The relationship between proteins expression and clinical parameters were analyzed by ANOVA. 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"section[12]/table-wrap[2]#table-4"}}, {"id": "asset:table:pmid:31824776:5", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:5cbc80b7a141621cc5ae787feaa011b45cdb912d16837c796fd43dd11fefb9ac", "bytes": 1582, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[13]/table-wrap[1]#table-5", "version": null, "note": "Univariate and multivariate analysis of overall survival (OS) of esophageal squamous cell carcinoma (ESCC).", "structure": {"pmcid": "PMC6896941", "section_index": 13, "section_title": "VEGF-C and MMP-9 protein overexpression predicts poor prognosis in Kazakh ESCCs", "row_count": 14, "column_count": 8}, "table": {"label": "Table 5", "caption": "Univariate and multivariate analysis of overall survival (OS) of esophageal squamous cell carcinoma (ESCC).", "rows": [["Variable", "Cases (N)", "Univariate analysis", "Multivariate analysis"], ["", "", "HR", "95% CI", "P-value", "HR", "95% CI", "P-value"], ["Age (>58 y vs ≤58 y)", "100", "0.859", "0.603–1.225", "0.402", "", "", ""], ["Sex (female vs male)", "100", "1.029", "0.679–1.557", "0.894", "", "", ""], ["Histologic grade (moderate + poor vs well)", "100", "1.148", "0.760–1.734", "0.511", "", "", ""], ["Tumor location (middle vs upper + lower)", "100", "1.193", "0.756–1.885", "0.448", "", "", ""], ["Venous invasion (positive vs negative)", "100", "3.569", "1.624–4.064", "<0.001*", "1.242", "0.653–2.363", "0.508"], ["Lymphatic invasion (positive vs negative)", "100", "2.404", "1.344–4.297", "0.003*", "1.418", "0.768–2.619", "0.264"], ["Depth of invasion (T3 + T4 vs T1 + T2)", "100", "1.583", "1.061–2.364", "0.025*", "0.999", "0.637–1.567", "0.997"], ["Nodal metastasis (+ vs −)", "100", "2.821", "1.897–4.195", "<0.001*", "1.078", "0.507–2.292", "0.845"], ["TNM stage (III + IV vs I + II)", "100", "3.449", "2.036–5.034", "<0.001*", "2.646", "1.379–5.078", "0.03*"], ["VEGF-C (+ vs −)", "100", "2.074", "1.318–3.700", "0.017*", "1.834", "0.718–4.689", "0.205"], ["MMP-9 (+ vs −)", "100", "1.854", "1.219–2.820", "0.004*", "2.226", "0.670–7.389", "0.191"], ["VEGF-C/MMP-9 (both + vs VEGF-C or MMP-9 −)", "100", "1.760", "1.185–2.612", "0.005*", "0.432", "0.121–1.548", "0.198"]], "row_count": 14, "column_count": 8, "numeric_cells": 77, "header_rows": 2, "locator": "section[13]/table-wrap[1]#table-5"}}], "gaps": []}, "analysis": {"state": "complete", "methods": [{"id": "method-1", "family": "group_comparison", "specific": "anova", "label": "Group comparison", "dsl_operations": ["group_summary", "welch_t", "bootstrap_mean_difference", "group_comparison_anova"], "missing_operations": [], "expressible": true, "parameters": {}, "data_shapes": ["two_or_more_groups_continuous"], "evidence": {"score": 1.0, "band": "verbatim", "quote": "Student’s t-test and Nonparametric Test were applied to find the difference in mRNA and proteins expression between the ESCC and CAN sets. 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