ABCD Arq Bras Cir Dig

2025;38:e1875 Original Article

[Link]

APERITUMORAL
QUEDA DA PRESSÃO BUDDING PORTAL APÓS DESVASCULARIZAÇÃO
AS A PREDICTOR FOR LYMPH NODE
METASTASES IN COLORECTAL
ESOFAGOGÁSTRICA CARCINOMAS:
E ESPLENECTOMIA WHAT IS A
INFLUENCIA THE IMPORTANCE?
VARIAÇÃO
DO CALIBRE
BROTAMENTO DAS VARIZES
PERI-TUMORAL E ASPARA
COMO PREDITIVO TAXAS DE RESSANGRAMENTO
METÁSTASES NA
LINFONODAIS EM CARCINOMAS COLORRETAIS:
QUAL A IMPORTÂNCIA?
ESQUISTOSSOMOSE NO SEGUIMENTO EM LONGO PRAZO?
Emily Karoline Araujo Nonato dos SANTOS1 , Bruna Gama TRICHES1 , Guilherme Prestes da SILVA1 ,
Julia Costa
Does LINHARES
the drop
2
, Samya Hamad
in portal pressure MEHANNA1 , Marcela
after esophagogastric Santos CAVALCANTI
devascularization
3
and splenectomy
variation of variceal calibers and the rebleeding rates in schistosomiasis in late follow-up?
ABSTRACT – BACKGROUND: Microscopic analysis of tumor budding (TB) may be an essential
Walter de tool
predictive Biase SILVA-NETO
for regional
1
, Claudemiro
lymph node metastases QUIRESE
in colorectal
1
, Eduardo
cancer, especially Guimarães Horneaux de MOURA2 ,
among patients
Fabricio Ferreira COELHO , Paulo HERMAN
in intermediate stages, who exhibit3 considerable prognostic variability.
3 AIMS: The aim of this study
was to assess the predictive power of BT regarding the presence of lymph node metastases and its
association with other characteristics related to colorectal carcinoma progression. METHODS: This is
a cross-sectional, retrospective study with a quantitative approach, focusing on the review of medical
RESUMO
records-andRacional: O tratamento
histopathological depatients
reports of escolhawho para pacientes
underwent com hipertensão
oncologic portal
surgery for colorectal
esquistossomótica
cancer. RESULTS: A totalcomof 153
sangramento dewere
patient records varizes é a with
examined, desconexão ázigo-portal
a predominance mais
of the 61-70 age
group and a male
esplenectomia majority
(DAPE) (50.98%).àAdenocarcinoma
associada terapia endoscó[Link] otherwise
Porém,specified
estudoswas the most
mostram common
aumento
histological type (60.78%), with the majority exhibiting moderate differentiation (87.58%). From the
do calibre das varizes em alguns pacientes durante o seguimento em longo prazo. Objetivo:
total sample, 97 cases (63.39%) exhibited TB, with 51.55% classified as a high budding score. Invasion
Avaliar o impacto
of adipose da DAPEwas
tissue/subserosa e tratamento endoscópico
the most prevalent, pós-operatório
occurring in 46.41% of no comportamento
cases. Regional lymph
das
nodevarizes esofágicas
metastases e recidiva hemorrágica,
and angiolymphatic invasion were deobserved
pacientesin esquistossomóticos. Métodos:
66 and 101 patients, respectively.
Peritumoral budding as a predictor for lymph
Foram estudados
Cross-tabulation 36 pacientes
analysis showed acom seguimento
statistically superior
significant a cinco
association anos,TBdistribuídos
between em
and lymph node
node metastases in colorectal carcinomas: what
metastasis
dois grupos:(p<0.05).
queda da CONCLUSIONS:
pressão portal The relationship
abaixo de 30%between
e acimaTB deand
30%lymph node metastasis
comparados com o
highlights the significance of this histological factor in the risk stratification and prognosis of patients is its significance?
calibre das varizes esofágicas no pós-operatório precoce e tardio além do índice de recidiva
with colorectal cancer, complementing TNM staging. Therefore, the assessment of tumor budding is
hemorrágica. Resultados reports, potentially influencing additional therapeutic decisions.
crucial in histopathological
esofágicas Colorectal
KEYWORDS: que, durante o seguimento
Neoplasms. Lymphaticaumentaram de calibre e foram controladas com
Metastasis. Prognosis. Central Message
Evolução do calibre das varizes no período pré e pós-
Colorectal cancer (CRC) is the second-most
o comportamento do calibre das varizes no pós-operatório precoce nem tardio nem os operatório precoce e tardio
prevalent cancer in both sexes in Brazil, excluding
RESUMO – RACIONAL: A análise microscópica de brotamento peri-tumoral (BT) pode ser uma
índices de recidiva hemorrágica. Conclusão
importante ferramenta preditiva de metástases linfonodais regionais em casos de câncer colorretal, non-melanoma skin cancer, and is associated
principalmente entre pacientes em estágios intermediários, os quais apresentam marcante with significant morbidity and mortality. The
operatórios
variabilidadeprecoces ou tardios.
prognóstica. OBJETIVOS: A comparação entrepreditivo
Avaliar o poder a quedado deBTpressão do portal
em relação e as
à presença Mensagem
prognosis ofcentral
CRC is based on the disease stage
de metástases linfonodais, bem como sua associação com outras características relacionadas à Aaccording to theázigo-portal
desconexão TNM classification. However,
e esplenectomia
progressãoEsquistossomose
DESCRITORES: do carcinoma mansoni.
colorretal. MÉTODOS:
Hipertensão Trata-se
portal. de Pressão
Cirurgia. estudo na
transversal,
veia [Link] com
Varizes esofágicas there is considerable
apresenta variabilitynain diminuição
importante impacto outcomes
abordagem quantitativa, com revisão de prontuários médicos e laudos anatomopatológicos de
e gástricas. and prognosis
precoce do calibre among patientsesofágicas
das varizes at identical
na
pacientes submetidos a cirurgia oncológica por câncer colorretal. RESULTADOS: Foram analisados stages, especially in
esquistossomose; intermediate
entretanto, stagesque
parece (II and
a
153 prontuários de pacientes, predominando a faixa etária de 61-70 anos, com uma maioria III). Thus, additional
associação strategies
com a terapia for stratifying
endoscópica the
é a maior
masculina (50,98%). O adenocarcinoma sem especificação foi o tipo histológico mais comum risk of recurrence
responsável and da
pelo controle metastasis, designed to
recidiva hemorrágica.
(60,78%), -com
ABSTRACT a maioria mostrando
Background: moderada
The treatment diferenciação
of choice (87,58%).
for patients Da amostra
with total, 97 with
schistosomiasis casos enhance the treatment of CRC patients, present
(63,39%) apresentaram BT, com 51,55% classificados como alto escore de brotamento. A invasão a favorable alternative by utilizing the tumor
previous episode of varices is bleeding esophagogastric devascularization and
em tecido adiposo/subserosa foi a mais prevalente, ocorrendo em 46,41% dos casos. Metástases splenectomy
budding (TB) marker.
(EGDS) in association
em linfonodos with
regionais e postoperative endoscopicforam
embolização angiolinfática therapy. However,
observadas emstudies havepacientes,
66 e 101 shown Perspectiva
varices recurrence
respectivamente. especially
A análise after
cruzada long-term
indicou follow-up.
uma associação Aim: To assess
estatisticamente the impact
significativa one
entre BT Este estudo avaliou o impacto tardio no índice
metástaseoflinfonodal
behavior esophageal(p<0,05). CONCLUSÕES:
varices and bleeding A relação entre after
recurrence BT e metástase linfonodal
post-operative destaca a
endoscopic de ressangramento de pacientes submetidos ao
importância
treatment ofdeste fator submitted
patients histológico na
to estratificação
EGDS. Methods: de risco e prognóstico
Thirty-six emsubmitted
patients pacientes com câncer
to EGDS Perspectives
tratamento cirúrgico e endoscópico. A queda na
colorretal, complementando o estadiamento TNM. Portanto, a avaliação do brotamento tumoral é
This study highlights the significant relationship
crucial em laudos anatomopatológicos, podendo influenciar decisões terapêuticas adicionais.
portal pressure drop, more or less Metástase
than 30%,Linfática.
and compared with the behavior of esophageal betweendothe
variação presence
calibre of TBquando
das varizes and lymph node
comparado
DESCRITORES: Neoplasias Colorretais. Prognóstico.
varices and the rate of bleeding recurrence. Results ometastasis,
seu diâmetroemphasizing the importance
no pré e pós-operatório precoce ofe
tumor A budding
tardio. comparação as entre
a detectable
a queda dehistological
pressão
late post-operative varices caliber when compared the pre-operative data was observed prognostic
portal e as factor
taxas de in ressangramento,
patients with colorectal
também
despite an increase in diameter during follow-up that was controlled by endoscopic therapy. cancer. TNM staging remains the primary
Conclusion stratification
evidenciar se method;
apenas a however, assessing other
terapia endoscópica, ou
variceal calibers when comparing pre-operative and early or late post-operative diameters. prognosticmenos
operações predictors in CRC
complexas patients
poderão is crucial
controlar o
The comparison between the portal pressure drop and the rebleeding rates was also not for oncological
sangramento das treatment
varizes. decisions.

HEADINGS: Schistosomiasis mansoni. Portal hypertension. Surgery. Portal pressure.

Esophageal and gastric varices.

[Link]/revistaabcd/ [Link]/revista_abcd [Link]/Revista-ABCD-109005301640367 [Link]/company/revista-abcd

[Link]/abcdrevista [Link]/abcdrevista [Link]/abcdrevista

From 1Faculdade
Trabalho realizado no Evangélica
1
Serviço deMackenzie do eParaná,
Cirurgia Geral Medical
Aparelho Course
Digestivo, – Curitibade(PR),
Departamento Brazil;
Clínica Faculdade
Cirúrgica,
2
Pequeno
Faculdade Príncipe,
de Medicina, Medical Course
Universidade Federal –deCuritiba (PR), Brazil
Goiás, Goiânia, GO,
Faculdade
Brasil;
3 2
ServiçoEvangélica Mackenzie
de Endoscopia, Hospital dodas
Paraná, Department
Clínicas of Pathology
e Departamento – Curitiba (PR),
de Gastroenterologia, Brazil. de Medicina, Universidade de São Paulo, São Paulo, SP, Brasil; 3Serviço de
Faculdade
Cirurgia do Fígado, Hospital das Clínicas e Departamento de Gastroenterologia, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brasil
How to cite this article: Santos EKAN, Triches BG, Silva GP, Linhares JC, Mehanna SH, Cavalcanti MS. Peritumoral budding as a predictor for lymph node metastases
in colorectal
Como citar essecarcinomas: what
artigo: de Biase is the importance?
Silva-Neto WB, Quirese C,ABCD Arq Bras
De Moura EGH,Cir Dig. FF,
Coelho 2025;38e1875. [Link]
Herman P. A queda da pressão portal após desvascularização esofagogástrica e esplenectomia

/10.1590/0102-672020210001e1581
Correspondence: Financial source: None
Samya Hamad Mehanna. Conflict of interests: None
Correspondência:
E-mail: samyahm88@[Link] Received: 03/07/2024
Walter De Biase da Silva Neto
Accepted: 12/14/2024
E-mail: wbiase123@[Link]; Recebido para publicação: 17/09/2020
Editorial Support: National Council for Scientific
biase@[Link] andpublicação:
Aceito para Technological Development (CNPq).
14/12/2020

ABCD Arq Bras Cir Dig 2021;34(2):e1581 1/4

1/5
ORIGINAL ARTICLE

INTRODUCTION predominantly in the age group of 61–70 years. Figure 1 shows

C
the distribution of CRC patients by age group (n=153).
olorectal cancer (CRC) is the second-most prevalent Adenocarcinoma not otherwise specified (NOS) was the
cancer in both sexes in Brazil, excluding non-melanoma most prevalent histological type, present in 93 patients (60.78%)
skin cancer, and is associated with significant of the cases. Table 1 shows the degree of tumor differentiation,
morbidity and mortality11. The prognosis of CRC is largely based with the majority classified as moderately differentiated, totaling
on the disease stage according to the TNM classification12. 134 cases (87.58%).
However, there is significant variability in outcomes and prognosis Table 2 shows that in 66 patients (43.13%), at least one
among patients at identical stages, especially in intermediate metastasis in regional lymph nodes was detected in the surgical
stages (II and III)16. Therefore, additional strategies to stratify specimen.
the risk of recurrence and metastasis, aiming to enhance the The analysis of tumor invasion depth (pathological
treatment of CRC patients, may provide beneficial alternatives staging T) of the samples showed a significant number of cases
through the utilization of the tumor budding (TB) marker14. classified as pT3 (46.41%), characterized by tumor cell invasion
TB is a phenomenon where single isolated cells or small into the pericolic adipose tissue, followed by pT4a (30.07%),
clusters of up to four cells are present at the invasive front which includes infiltration to the serosal surface. Additionally,
of the tumor, indicating the tumor’s capacity to infiltrate the the presence of pT2 (16.69%), characterized by the infiltration
extracellular matrix and lymphatic vessels to reach regional of the muscularis propria, was also particularly noteworthy.
lymph nodes19. This process has been associated with worse The relationship between tumor depth and lymph node metastasis
prognosis, including higher local recurrence, distant metastases, presence was analyzed and presented in Table 3. There was a
and reduced survival in CRC patients16. In 2016, the International statistically significant association between tumor invasiveness
Tumor Budding Consensus Conference (ITBCC) standardized and the probability of lymph node involvement (p<0.05).
TB assessment in CRC patients into three distinct groups based Angiolymphatic embolization was examined and found
on the number of buds identified under microscopy: in 101 patients (66.01%). However, in 53 cases (34.64%), it was
1. Low TB group: a maximum of four buds in the assessment not identified.
field (hotspot area); TB identification was described in 97 cases (63.39%),
2. Intermediate TB group: between five and nine buds; classified into low, intermediate, and high scores, as shown in
3. High TB group: 10 or more buds8. Table 4. Over half of these cases had the highest score.
The association between TB and lymph node metastasis
The aim of this study was to assess the predictive power was considered significant (p<0.05) since 51 of the 66 patients
of TB regarding the presence of lymph node metastases, and with lymph node metastasis had TB. Conversely, most patients
other characteristics of tumor progression in CRC, in a Brazilian without lymph node involvement had positive TB (Figure 2).
university hospital. Furthermore, the sensitivity and specificity of peritumoral

METHODS
This is an observational, retrospective study with a quantitative
approach, conducted in Curitiba (PR), Brazil. Medical records
from the Mackenzie Evangelical University Hospital (HUEM)
were examined, along with histopathological results of resected
surgical specimens from patients who underwent oncological
surgery for CRC between November 2019 and June 2022.
Patients with missing data in medical records and/or incomplete
histopathological analyses were excluded. Multiple variables,
such as sex, age, type/grade of histological neoplasia, depth of
invasion, angiolymphatic embolization, lymph node metastases,
and TB assessment, were considered. Figure 1 - Distribution of patients with colorectal cancer by
For analysis, the data were exported to a Microsoft Office age groups (n=153).
Excel spreadsheet, where descriptive statistics were used,
including absolute numbers and percentages. The chi-squared Table 1 - Distribution of colorectal cancer differentiation
test was performed when applicable with a significance level degree (n=153).
of <0.05. The study was approved by the HUEM Research Differentiation degree n %
Ethics Committee (nº 70071623.7.0000.0103), in accordance
with Resolution no. 466/12 of the National Research Council, Moderately differentiated 134 87.58
which regulates scientific research in human subjects. The data Poorly differentiated 16 10.45
obtained were compared with the literature on the subject. Well-differentiated 3 1.96
Total 153 100

RESULTS Table 2 - Distribution of colorectal cancer patients according

to lymph node involvement (n=153).
From November 2019 to June 2022, 153 CRC cases were
recorded at the hospital’s high-complexity center that met the Lymph node involvement n %
inclusion criteria for this study. The distribution between sexes Not involved 87 57.14
was similar, with a slight predominance of males, accounting Involved 66 42.86
for 50.98% of the cases. Age ranged from 35 to 94 years, as
Total 153 100
shown in Figure 1, with a mean of 62.76±12.02 and with 30.07%

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 PERITUMORAL BUDDING AS A PREDICTOR FOR LYMPH NODE METASTASES IN COLORECTAL CARCINOMAS: WHAT IS THE IMPORTANCE?

budding for regional lymph node involvement were 77.27% and Although the mechanism of TB formation in colorectal
47.13%, respectively, with a positive predictive value of 52.58%. cancer is not yet fully understood, the predominant theory
Additionally, the ROC (receiver operating characteristic) suggests that at least some types of budding represent an
curve analysis for TB on lymph node involvement in CRC
patients revealed an area under the curve (AUC) of 0.622, as
shown in Figure 3. This value indicates moderate accuracy of TB Table 4 - Distribution of budding score according to classification
in distinguishing between cases with and without lymph node into high, intermediate, or low (n=97).
involvement. Moreover, likelihood ratios were calculated, with Budding score n %
a positive likelihood ratio of approximately 1.46 suggesting
High 50 51.55
that a positive TB test result increases the probability of lymph
node involvement by approximately 46%. In contrast, a negative Intermediate 26 26.80
likelihood ratio of approximately 0.46 indicates that a negative Low 21 21.65
result reduces the probability of lymph node involvement by
Total 97 100
approximately 46%.
Finally, TB was associated with lymph node metastasis,
histological grade, invasion depth, and angiolymphatic embolization.
However, the latter exhibited no statistical significance, as
shown in Table 5.

DISCUSSION
Most of the 153 patients with CRC surgically treated in
a high-complexity center were male (50.98%). These findings
align with current data from the World Health Organization
(WHO) for Brazil, where CRC exhibits an almost equal distribution
between sexes, with males accounting for 49.6% of the total
CRC cases6,18. The American Cancer Society (ACS) estimates that
in 2022, there were 80,690 new cases among males, compared ROC: receiver operating characteristic; AUC: area under the curve.
to 70,340 new cases among females1.
Figure 2 - Relationship between lymph node involvement and
The predominant age group in this study was between
tumor budding.
61 and 70 years, with a mean age of 62 years. Age assessment
is crucial as it is a risk factor for CRC development, with cases
being more common in patients over 50 years and significantly
increasing with each decade. The average age at diagnosis is
72 years for women and 68 years for men10. A Brazilian study
of 521 cases found an average age of 63 years, with an affected
range between the fifth and the eighth decades of life3.
The most widely used and gold-standard pathological staging
system for CRC evaluation is the TNM system, recommended by
the American Joint Committee on Cancer (AJCC), which considers
tumor invasion depth (T); the number of compromised lymph
nodes (N); and the presence or absence of distant metastases
(M)12,20. Our study showed a prevalence of 71 (46.41%) cases
with infiltration into the pericolic adipose tissue, corresponding
to pT3, which is also described as predominant in the global
literature3,4,17. Additionally, at least one lymph node metastasis
was identified in 66 patients (42.86%). A similar value has been
described in the literature13.
TB was identified in 97 (63.39%) cases, with the majority
classified as high scores, corresponding to 51.55% of the results. Figure 3 - The blue curve shows the test performance; the
Furthermore, a statistically significant association was found dashed gray line shows a test with no discriminative
between peritumoral budding and the presence of lymph node ability. The area under the curve of 0.622 indicates
metastasis (p<0.05), with 77.27% sensitivity. moderate test accuracy.

Table 3 - Tissue invasion depth (T) in colorectal cancer (n=153).

Tissue infiltration pT n % Lymph node metastasis (n) p-value
Mucosa pTis 1 0.65 0
Submucosa pT1 4 2.6 0
Muscularis propria pT2 24 16.69 3
Adipose tissue pT3 71 46.41 33
Serosa pT4a 46 30.07 27
Adjacent organs pT4b 7 4.58 3
Total - 153 100 66 0.0032

ABCD Arq Bras Cir Dig 2025;38:e1875 3/5

ORIGINAL ARTICLE

Table 5 - Age, sex, lymph node involvement, angiolymphatic

macroscopic sampling, or the fact that these were initial cases
invasion, histological grade, and invasion depth in CRC
and TB had not yet resulted in subsequent embolization.
patients with and without tumor budding (n=153).
The ITBCC recommends the assessment of TB using
Tumor budding hematoxylin and eosin-stained histological slides, and a hotspot
Present (n) Absent (n) p-value at the invasive tumor front (standard field size of 0.785 mm2).
To assist this analysis, the consensus provides a table for
97 56
standardizing this count across various microscopes8. According
Age (mean) 62.65 62.86 0.877* to ITBCC, TB should be included in CRC protocols and described
Sex (n) in patients’ pathology reports due to its prognostic, clinical,
and therapeutic value. Thus, this histopathological evaluation
Male 52 27
should always be described. In the present study, information
Female 45 30 was sourced from radical surgical specimens; nonetheless, TB
Lymph node metastasis (n) identification is particularly important in endoscopic resections
Present 51 15
of early cases, such as polypectomies and mucosectomies8.
0.0034† In recent years, there has been a growing increase in CRC
Absent 46 41 diagnosis, with local resection surgery considered curative in
Angiolymphatic invasion (n) the absence of metastases5. TNM classification remains the
Present 68 33 primary staging stratification method. However, evaluating
0.2192† other new prognostic predictors in CRC patients is uniquely
Absent 29 23
important in therapeutic decision-making in oncology.
Histological grade (n)
Well-differentiated 0 3
Moderately differenti-
ated
90 44 0.0131† CONCLUSIONS
Poorly differentiated 7 9 This study established a significant relationship between
Invasion depth the presence of TB and lymph node metastasis, emphasizing
Mucosa 0 1 the relevance of tumor budding as a detectable histological
prognostic factor in patients with colorectal cancer.
Submucosa 0 4
Muscularis propria 15 9
0.068†
Adipose tissue 45 26
Serosa 32 14
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