Invest Clin 63(2): 147 - 155, 2022 https://doi.org/10.54817/IC.v63n2a04

Corresponding Author. Changrui Sheng. Department of Ultrasound, Hwa Mei Hospital, University of Chinese Aca-

demy of Sciences, Xibei Road 41, Ningbo 315010, Zhejiang Province, China. E-mail: ostaobjjqrn@zohomail.com

Value of endorectal ultrasonography

in the assessment of invasion staging

of low rectal cancer with local progression

after neoadjuvant radiochemotherapy.

Shanshan Gao1, Changrui Sheng1, Liming Yan2, Hua Yin1, Jingjing Hu1, Zhiying Ye1

and Xiuzhi Wei1

1 Department of Ultrasound, Hwa Mei Hospital, University of Chinese Academy

of Sciences, Xibei Road 41, Ningbo 315010, Zhejiang Province, China.

2 Physical Examination Center, Hwa Mei Hospital, University of Chinese Academy

of Sciences, Xibei Road 41, Ningbo 315010, Zhejiang Province, China.

Key words: endorectal ultrasonography; low rectal cancer; local progression;

neoadjuvant radiochemotherapy; invasion; staging.

Abstract. Although stages T3 and T4 rectal cancer can be reduced

to T1 or T2 after neoadjuvant radiochemotherapy, the accuracy of the en-

dorectal ultrasonography (ERUS) for the post-radiochemotherapy evalua-

tion of low rectal cancer has seldom been reported. We aimed to investigate

the value of ERUS in the assessment of invasion staging in low rectal cancer

with local progression, and the factors affecting its accuracy, after neoad-

juvant radiochemotherapy. A total of 114 patients administered with neo-

adjuvant radiochemotherapy for stages II and III low rectal cancer (local

stage T3/T4) from February 2018 to December 2020 were enrolled in the

study. The changes in local lesions were evaluated using ERUS before and

after radiochemotherapy, and compared with the pathological T staging.

The accuracy of post-neoadjuvant radiochemotherapy re-staging examined

with ERUS was evaluated, and univariate analysis was used to identify the

factors affecting the accuracy. After neoadjuvant radiochemotherapy, the

blood flow distribution within the lesion significantly declined (P<0.05),

the max length and max thickness of the longitudinal axis of the lesion

were reduced (P<0.05), and the uT staging was decreased (P<0.05), when

compared with lesions before the treatment. Compared with postoperative

pathological T staging, the accuracies of ERUS in T1, T2, T3 and T4 stages

were 11.11%, 28.57%, 27.27% and 100%, respectively. Univariate analysis

148 Gao et al.

Investigación Clínica 63(2): 2022

Valor de la ultrasonografía endorectal en la evaluación

de la estadificación de la invasión del cáncer rectal bajo

con progresión local, después de administrar

radioquimioterapia neoadyuvante.

Invest Clin 2022; 63 (2): 147 – 155

Palabras clave: pancreatitis; cloruros; soluciones isotónicas; tiempo de internación.

Resumen. Aunque el cáncer de recto en estadios T3 y T4 se puede redu-

cir a T1 o T2 después de la radioquimioterapia neoadyuvante, rara vez se ha

informado la precisión de la ecografía endorrectal (ERUS) para la evaluación

posterior a la radioquimioterapia del cáncer de recto inferior. Nuestro obje-

tivo fue investigar el valor de ERUS en la evaluación de la estadificación de

la invasión en el cáncer de recto inferior con progresión local, después de la

radioquimioterapia neoadyuvante y los factores que afectan su precisión. Se

incluyeron en el estudio un total de 114 pacientes a los que se les administró

radioquimioterapia neoadyuvante para el cáncer de recto inferior en estadios

II y III (estadio local T3/T4), desde febrero de 2018 hasta diciembre de 2020.

Los cambios en las lesiones locales se evaluaron mediante ERUS antes y des-

pués de la radioquimioterapia y se compararon con la estadificación patológica

T. Se evaluó la precisión de la re-estadificación examinada con ERUS, después

de la radioquimioterapia neoadyuvante y se utilizó un análisis univariado para

identificar los factores que afectan su precisión. Después de la radioquimiote-

rapia neoadyuvante, la distribución del flujo sanguíneo dentro de la lesión dis-

minuyó significativamente (P<0,05), la longitud máxima y el espesor máximo

del eje longitudinal de la lesión se redujeron (P<0,05) y la estadificación uT

disminuyó (P<0,05), en comparación con las lesiones antes del tratamiento.

En comparación con la estadificación T patológica posoperatoria, las precisio-

nes de ERUS en las etapas T1, T2, T3 y T4 fueron del 11,11%, 28,57%, 27,27% y

100%, respectivamente. El análisis univariable indicó que el tiempo de revisión

de ERUS, la estadificación T postoperatoria y la etapa de regresión rectal de

Wheeler fueron factores que afectaron la precisión de la re-estadificación con

ERUS. ERUS es más preciso para la re-estadificación de T4, el seguimiento seis

semanas después de la radioquimioterapia neoadyuvante y en tumores de baja

regresión, con un alto valor de aplicación para la evaluación de la eficacia de la

radioquimioterapia neoadyuvante para el cáncer rectal bajo.

Received: 08-09-2021 Accepted: 07-04-2022

indicated that review time of ERUS, post-operative T staging and Wheeler

rectal regression stage were factors affecting the accuracy of ERUS re-stag-

ing. ERUS is more accurate for T4 re-staging, follow-up reviewed six weeks

after neoadjuvant radiochemotherapy and low regression tumors, with a

high application value for the assessment of the efficacy of neoadjuvant

radiochemotherapy for low rectal cancer.

Ultrasonography for low rectal cancer 149

Vol. 63(2): 147 - 155, 2022

INTRODUCTION

Rectal cancer is a common malignancy

of the digestive system, and the incidence

rate exhibits an increasing trend annually1.

Different stages of rectal cancer should be ad-

ministered with different therapeutic strat-

egies. Local resection is feasible for early-

stage rectal cancer, and standard treatment

mode, neoadjuvant radiochemotherapy com-

bined with radical surgery, is recommended

for locally advanced rectal cancer2. Neoadju-

vant radiochemotherapy helps to reduce tu-

mor size, degrade the staging, increase the

sphincter preservation rate, reduce local re-

currence rate and prolong the survival time

of patients 3,4. The “watch-and-wait” strategy

can be adopted for rectal cancer patients

with clinical complete response after neo-

adjuvant radiochemotherapy. Hence, tumors

should be accurately re-staged after neoad-

juvant therapy.

The endorectal ultrasonography (ERUS)

offers an important means for preoperative

staging of the primary lesion of rectal cancer,

characterized by low cost, high efficiency,

and accurate rectal wall stratification, and

it is far superior to magnetic resonance im-

aging (MRI) in the differential diagnosis of

T1 and T2 stages 5,6. Although stages T3 and

T4 rectal cancer will be reduced to T1 or T2

after neoadjuvant radiochemotherapy, there

are currently only few reports on the accu-

racy of ERUS in the post-radiochemotherapy

evaluation of low rectal cancer 7. In this study,

ERUS was utilized to evaluate the primary le-

sion of stage T3 and T4 low rectal cancer be-

fore and after neoadjuvant radiochemothera-

py, aiming to evaluate the accuracy of ERUS

after radiochemotherapy and before surgery,

and to investigate the correlations between

clinical indices and accuracy.

MATERIALS AND METHODS

A total of 114 patients diagnosed as

low rectal cancer in our hospital from Febru-

ary 2018 to December 2020 were enrolled,

including 69 males and 45 females, aged

(57.3±6.2) years old. Digital anal examina-

tion showed that the distance between the

tumor lower edge and the anal verge was 4-7

cm. The inclusion criteria were as follows: a)

patients who were diagnosed with stage II or

III low rectal cancer (regional stage T3/T4)

by ERUS and MRI for the first time, and ultra-

sound probe could scan the tumor complete-

ly through the intestinal cavity. b) those who

had no surgical contraindications, and were

administered with surgery at eight weeks after

neoadjuvant radiochemotherapy (2 Gy/time,

22 times, for a total radiotherapy dose of 44

Gy, while oral capecitabine 2500 mg/(m2·d),

bid for two weeks followed by one week rest

as one cycle, for two cycles. And c) those who

underwent neoadjuvant radiochemotherapy

and total mesorectal excision, with ERUS

examination at 4-8 weeks after neoadjuvant

therapy and before surgery, and postoperative

pathological staging and Wheeler rectal can-

cer regression grade (RCRG). The exclusion

criteria involved: a) patients whose dosage

of neoadjuvant radiochemotherapy did not

reach the standard, or b) those whose radi-

cal excision did not reach the requirement. In

the present study, the staging standard met

the National Comprehensive Cancer Network

(NCCN) guidelines of 2014.

METHODS

Philips iU 22 color Doppler ultrasound

system (Netherlands) with C8-4V intracavi-

tary ultrasonic probe was selected. The fre-

quency of ERUS was 5-10 MHz. The probe was

inserted into the rectal cavity to complete a

“360-degree view” of the tumor. The location,

length, diameter, shape, echo, and depth of

invasion, followed by the number, size, and

echo of the peri-intestinal lymph nodes were

observed, and the blood flow distribution in

the lesion, the max length of the longitudinal

axis of the lesion, the max thickness of the

tumor, and T staging (T1: hypoechoic shad-

ow is confined to the first three layers; T2:

hypoechoic shadow is present in the fourth

150 Gao et al.

Investigación Clínica 63(2): 2022

layer, but the fifth layer is smooth; T3: hy-

poechoic shadow is present in the fifth layer;

T4: hypoechoic shadow is present in the in-

testinal lining and partly surrounding tissues

or organs) were determined. Color Doppler

blood flow imaging grading was performed

according to the intensity of blood flow sig-

nals: grade 0: no blood flow signal, grade I:

blood flow signals of focal region, grade II:

multi-point and strip blood flow signals, and

grade III: large amounts of dot and strip blood

flow signals. ERUS was compared with path-

ological T staging to evaluate under-stage,

over-stage and accuracy, and the correlations

of patient’s age, gender, distance between the

lower edge of the tumor and the anus, review

time of ERUS, nerve invasion, vascular inva-

sion, lymph node metastasis, postoperative T

staging and Wheeler rectal cancer regression

grade with ERUS re-staging accuracy after

neoadjuvant radiochemotherapy were sub-

jected to univariate analysis to identify the

factors affecting the accuracy.

STATISTICAL ANALYSIS

SPSS 20.0 software was employed for

statistical analysis. Numerical data were ex-

pressed as percentage [n (%)] and analyzed

using chi-square test. Measurement data

were expressed as mean ± standard devia-

tion (χ ± s), and t-test was used for com-

parison between two groups. The factors

affecting the accuracy of post-neoadjuvant

radiochemotherapy re-staging examined

with ERUS was evaluated by logistic regres-

sion analysis. P<0.05 indicated that the dif-

ference was statistically significant.

RESULTS

Changes in indices after neoadjuvant

radiochemotherapy with ERUS

ERUS showed that the blood flow dis-

tribution within the lesion significantly

declined (χ2=159.723, p<0.001) after

neoadjuvant radiochemotherapy, when

compared with the pre-treatment lesion.

The max length of the longitudinal axis of

the lesion and the max thickness of the

tumor were reduced [(5.38±0.34) cm vs.

(2.15± 0.14) cm, (3.03±0.24) cm vs.

(0.96±0.12) cm] (t=93.792, p<0.001;

t=82.368, p<0.001). Compared with be-

fore pre-neoadjuvant radiochemotherapy,

uT staging had a significant difference

after neoadjuvant radiochemotherapy

(χ2=58.455, p<0.001) (Table 1).

Table 1

Changes in indices after neoadjuvant radiochemotherapy with ERUS (n=114).

Group Pre-neoadjuvant

radiochemotherapy

Post-neoadjuvant

radiochemotherapy χ2/t p

Blood flow (n) χ2=159.723 <0.001

0 0 42

Ⅰ0 51

Ⅰ51 15

Ⅰ63 6

Max length (cm) 5.38±0.34 2.15±0.14 t=93.792 <0.001

Max thickness (cm) 3.03±0.24 0.96±0.12 t=82.368 <0.001

uT stage(n) χ2=58.455 <0.001

T1 0 12

T2 0 36

T3 63 52

T4 51 24

Ultrasonography for low rectal cancer 151

Vol. 63(2): 147 - 155, 2022

ERUS and pathological T staging after

neoadjuvant radiochemotherapy

Compared with postoperative patho-

logical T staging, ERUS showed 88.89% of

over-stage in T1 stage, 21.43% of under-stage

and 50% of over-stage in T2 stage, 45.45% of

under-stage and 27.27% of over-stage in T3

stage, 0 of under-stage and over-stage in T4

stage, and 21.05% of under-stage and 47.37%

of over-stage in T stage (overall), and the ac-

curacies of ERUS in T1, T2, T3, T4 and T stag-

es (overall) were 11.11%, 28.57%, 27.27%,

100% and 31.58%, respectively (Table 2).

Clinicopathological factors affecting

ERUS re-staging accuracy after

neoadjuvant radiochemotherapy

Univariate and multivariate logistic

analyses indicated that review time of ERUS,

post-operative T staging and Wheeler rectal

regression stage were factors affecting ERUS

re-staging accuracy. ERUS was more accu-

rate in patients with review time of ERUS ≥6

weeks after neoadjuvant radiochemotherapy,

ypT4 and RCRG3 (Tables 3 and 4).

DISCUSSION

The incidence rate of low rectal can-

cer is higher among colorectal tumors.

The anatomical structure of the low rec-

tum is different from that of the high rec-

tum, and the effect of radical surgery is

poor for low locally advanced rectal cancer

in the past, with a poor prognosis. With

the extensive development, the role of

neoadjuvant radiochemotherapy with the

advantages of increasing the radical cure

rate of low locally advanced rectal cancer,

reducing the recurrence rate, increas-

ing the sphincter preservation rate and

prolong the survival time, has been con-

firmed 7,8. In the NCCN guidelines, it has

been definitely proposed to perform neo-

adjuvant radiochemotherapy for stages II

and III low rectal cancer (regional stage

T3 and T4). For low rectal cancer within

5 cm from the anus, ERUS has unique ad-

vantages 9. In a previous study, it showed

that the accuracy of ultrasound is 63-96%

in the preoperative staging of low rectal

cancer, which is 87-98% in MRI 10. Howev-

er, there are still few reports on the evalu-

ation value of ERUS after neoadjuvant ra-

diochemotherapy and before surgery.

The accuracy of ultrasound in different

locations of rectal cancer differs greatly dur-

ing the determination of the degree of inva-

sion of the primary rectal cancer. Especially,

ultrasound endoscopic scanning is required for

middle and upper rectal cancer, which greatly

affects the accuracy, but for low rectal cancer,

intracavitary ultrasound probes can easily and

completely scan the primary lesion to evaluate

the length, thickness, depth of invasion, blood

flow, and circumferential margins 11,12. Under

ERUS, the normal rectal wall is a 5-layer struc-

ture with a thickness of 2-3 mm with alternat-

ing high and low echoes, containing mucosa,

mucosal muscle, submucosa, propria muscle,

serous membrane and subserosal layer, sur-

rounding with adipose tissues, mesangial fascia

Table 2

EURS and pathological T staging after neoadjuvant radiochemotherapy.

EURS stage(n) Total EURS stage

uT1 uT2 uT3 uT4 Over staging Underestimate staging Accuracy

ypT1 3 9 15 0 27 0 88.89% (24/27) 11.11% (3/27)

ypT2 9 12 18 3 42 21.43% (9/42) 50.00% (21/42) 28.57% (12/42)

ypT3 0 15 9 9 33 45.45% (15/33) 27.27% (9/33) 27.27% (9/33)

ypT4 0 0 0 12 12 0 0 100.00%(12/12)

Total 12 36 52 24 114 21.05% (24/114) 47.37%(54/114) 31.58% (36/114)

152 Gao et al.

Investigación Clínica 63(2): 2022

outside the adipose tissues, and the primary

lesion is characterized by irregularly shaped

masses, with uneven low echoes, some mul-

tiple micro-calcifications, different depths of

invasion into intestinal wall, disappearance of

normal intestinal wall structure, abundant ar-

teriovenous blood flow in the tumor, and high

resistance of arterial blood flow 13,14.

Table 3

Univariate analysis results of factors affecting ERUS re-staging accuracy after

neoadjuvant radiochemotherapy

Item n ERUS stage

Accurate (n=36) Inaccurate (n=78) χ2p

Age (years) 1.661 0.197

≤60 48 12 36

>60 66 24 42

Gender 3.013 0.083

Male 69 26 43

Female 45 10 35

Distance from low margin of

tumor to anus (cm) 2.537 0.111

<3 60 15 45

≥3 54 21 33

Follow up check of ERUS (weeks) 9.204 0.002

<6 42 6 36

≥6 72 30 42

Nerve invasion 0.506 0.477

Negative 93 28 65

Positive 21 8 13

Vessel invasion 0.050 0.822

Negative 27 9 18

Positive 87 27 60

Lymph node metastasis 0.201 0.654

Negative 51 15 36

Positive 63 21 42

Post-operation stage 37.948 <0.001

ypT1 27 3 24

ypT2 42 12 30

ypT3 33 9 24

ypT4 12 12 0

PCRG 21.732 <0.001

PCRG1 33 3 30

PCRG2 39 9 30

PCRG3 42 24 18

Ultrasonography for low rectal cancer 153

Vol. 63(2): 147 - 155, 2022

After neoadjuvant radiochemotherapy,

the primary tumor is prone to pathological

features such as necrosis, fibrosis, reduced

density, and decreased blood supply, and the

original 5-layer structure of the intestinal

wall is destroyed, so that MRI or ERUS re-

staging accuracy is poor 15. Compared with

before pre-neoadjuvant radiochemotherapy,

ERUS showed that the blood flow distribu-

tion within the lesion significantly declined,

the max length of the longitudinal axis of

the lesion and the max thickness of tumor

were significantly reduced, most stage T3 or

T4 rectal cancer was reduced to T1 or T2,

and the uT staging was decreased after neo-

adjuvant radiochemotherapy.

These results demonstrated that ERUS

is of clinical guiding significance in the

evaluation of tumor length, thickness and

blood flow after radiochemotherapy, and

can effectively evaluate the efficacy of adju-

vant therapy. Compared with postoperative

pathological T re-staging, the results dis-

played that ERUS showed 88.89% of over-

stage in T1 stage, 21.43% of under-stage

and 50% of over-stage in T2 stage, 45.45%

of under-stage and 27.27% of over-stage in

T3 stage, 0 of under-stage and over-stage

in T4 stage, and 21.05% of under-stage and

47.37% of over-stage in T stage (overall),

and the accuracy of ERUS in T1, T2, T3, T4

and T stage (overall) was 11.11%, 28.57%,

27.27%, 100% and 31.58%, respectively.

The above results suggested that ERUS has

extensive under-stage in T1 and T2 stages,

and the accuracy is extremely poor. The

reason may be that neoadjuvant therapy is

absolutely effective for the primary lesion

of T1 and T2 re-staging, and the 5-layer

structure of the intestinal wall is difficult

to distinguish. Because of tumor regres-

sion, fibrous interstitial tissue prolifera-

tion, reduced distribution of tumor cells in

the interstitium, and decreased blood flow

of the tumor, the accuracy of the stratifica-

tion of the mucosal layer, mucosal muscle,

submucosal layer and muscularis propria is

poor, and the fibrous interstitial tissue with

incomplete shrinkage may be mistaken

for residual tumors, resulting in excessive

staging 16. A previous study indicated that

the total accuracy of ERUS T staging after

neoadjuvant radiochemotherapy is 48%,

with 38% of over-staging and 14% of under-

staging, tumor regresses notably in the pri-

mary tumor that is sensitive to radiochemo-

therapy, and the accuracy of re-staging is

poor 17, similar to the results of this study.

The results of this study showed that ERUS

was more accurate for T4 re-staging, be-

cause T4 re-staging indicates ineffective or

extremely poor effect of neoadjuvant radio-

chemotherapy. Studies have displayed that

the accuracy of ERUS and MRI is close to

100% in T4 stage with larger tumor, so the

depth of invasion is more accurate, and the

evaluation accuracy is higher. Further uni-

variate analysis showed that review time of

ERUS, postoperative T staging and Wheeler

rectal cancer regression grade are factors

Table 4

Multivariate logistic analysis results of factors affecting ERUS re-staging accuracy

after neoadjuvant radiochemotherapy.

Item Regression

coefficient

Standard

error Wald χ2OR 95% CI p

Review time of ERUS

≥6 weeks 2.203 0.297 5.389 1.727 1.063~2.804 0.004

ypT4 2.687 0.172 6.835 2.010 1.928~4.400 0.000

PCRG3 2.236 0.238 4.623 2.581 1.689~3.479 0.022

Constant term 1.784 0.348 76.436 6.053 0.006

154 Gao et al.

Investigación Clínica 63(2): 2022

affecting ERUS re-staging accuracy in low

rectal cancer. The accuracy is higher in pa-

tients with review time of ERUS ≥6 weeks.

The reason may be that the edema begins to

subside 4 weeks after radiotherapy, and the

boundary of tumor regression is more obvi-

ous, achieving the maximum effect at 6-8

weeks. Hence, ERUS can more accurately

distinguish the intestinal wall level after six

weeks. Patients with ypT4 and PCRG3 have

poor response of tumor to radiochemother-

apy, consistent with RCR3 of regression,

and higher accuracy of T4 staging men-

tioned above. ERUS is poorly accurate for

regional re-staging of obvious regression af-

ter radiochemotherapy, and more accurate

for T4 re-staging of unobvious regression

after radiochemotherapy. Besides, different

operators with experience, different types

of probes and fuselages are also factors that

affect the results of ERUS.

In conclusion, ERUS can effectively

allow the evaluation of the efficacy of low

rectal cancer after neoadjuvant radioche-

motherapy, including length, volume and

blood flow. However, it is poorly accurate

for those with prominent effect of neoad-

juvant radiochemotherapy and T staging

with effective regression, and more accu-

rate for those primary lesions with non-

prominent effect of neoadjuvant radioche-

motherapy and poor tumor regression.

Besides, ERUS has a higher accuracy for

the review time at 6 weeks after neoadju-

vant radiochemotherapy. Regardless, this

study still has limitations. First, the sam-

ple size is small, and further verification

is needed with a large population. Second,

the scan range of ERUS is limited, which

cannot display tumors in the upper rectal

segment. Third, ERUS does not work well

for rectal cancer in the immediate vicin-

ity of the anus or mesorectal lymph nodes.

Particularly, patients after receiving neo-

adjuvant radiotherapy probably cannot

tolerate the pain during examination be-

cause the mucosa is damaged.

Financial support

This study was financially supported

by Supported by Medical Scientific Re-

search Foundation of Zhejiang Province (No.

2021KY1021).

Author’s ORCID numbers

• Shanshan Gao: 0000-0002-5921-1131

• Changrui Sheng:

0000-0002-9011-7178

• Liming Yan: 0000-0002-4602-5137

• Hua Yin: 0000-0003-1896-066X

• Jingjing Hu: 0000-0002-0214-5372

• Zhiying Ye: 0000-0003-2829-1068

• Xiuzhi Wei: 0000-0003-1310-141X

Authors contribution

SG and CS designed this study and pre-

pared this manuscript; LY, HY, JH, ZY and XW

performed this study and analyzed the clini-

cal data. All authors have approved the sub-

mission and publication of this manuscript.

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