Role of endoscopic ultrasonography in the loco-regional staging of patients with rectal cancer

Table 1 The 2010 AJCC staging system for primary rectal cancer

Primary tumor (T)
TX	Primary tumor cannot be assessed
T0	No evidence of primary tumor
Tis	Carcinoma in situ: Intraepithelial or invasion of lamina propria
T1	Tumor invades submucosa
T2	Tumor invades muscularis propria
T3	Tumor invades through the muscularis propria into pericolorectal tissues
T4a	Tumor penetrates to the surface of the visceral peritoneum
T4b	Tumor directly invades or is adherent to other organs or structures
Regional lymph nodes (N)
NX	Regional lymph nodes cannot be assessed
N0	No regional nodal metastasis
N1	Metastasis in 1-3 regional lymph nodes
N1a	Metastasis in one regional lymph node
N1b	Metastasis in 2-3 regional lymph nodes
N1c	Tumor deposit(s) in the subserosa, mesentery, or non-peritonealized pericolic or perirectal tissues without regional nodal metastasis
N2	Metastasis in 4 or more regional lymph nodes
N2a	Metastasis in 4-6 regional lymph nodes
N2b	Metastasis in 7 or more regional lymph nodes
Distant metastasis (M)
M0	No distant metastasis
M1	Distant metastasis
M1a	Metastasis confined to one organ or site (i.e., liver, lung, ovary, non-regional node)
M1b	Metastases in more than one organ/site or the peritoneum

From ref.[3].

Table 2 Therapeutic strategy

cT1 cT2 cN0 cCRM-	Surgery alone
Any cT cN+ cT2 cT3 cN0 cCRM+	CRT
cT2 cT3 cN0 cCRM-	SCRT

C: Clinical stage; CRM: Circumferential resection margin; CRT: Standard chemotherapy + radiation therapy; SCRT: Short term chemotherapy + radiotherapy. From ref.[2].

Table 3 T staging (uT) of rectal cancer at endoscopic ultrasound, according to the infiltration depth

uT1 = tumor invasion limited to the mucosa and the submucosa; this is further divided into T1m, if the tumor infiltrates the mucosa, with normal muscolaris mucosa, and T1sm, when there is submucosal invasion (Figures 1 and 7)

uT2 = tumor infiltration of the muscolaris propria, with the tumor mass extended through the first 4 layers of the rectal wall. The outer layer corresponding to the muscolaris propria is smooth, meaning that the tumor is still limited to the rectal wall (Figure 2)

uT3 = tumor invasion of the perirectal fat, with an irregular 4th layer, which means that the tumor has spread outside the rectal wall (Figures 3 and 4)

uT4 = tumor infiltration of adjacent structures and organs, which are strictly connected to the rectal hypoechoic mass (Figure 5)

From ref.[9].

Table 4 Endoscopic ultrasound accuracy of T and N stage of rectal cancer

Ref.	Ptsno.	TStage	NStage	P/R	Tipe of EUS probe
Saitoh et al[13]	88	90%	75%	-	Flexible, radial, (7 MHz) Rigid, radial (5-7.5 MHz)
Feifel et al[14]	79	89%	-	P	Rigid, linear (3-7 MHz)
Yamashita et al[15]	122	78%	-	R	Rigid, linear (5.5-7 MHz)
Beynon et al[16]	100	93%	83%	-	Rigid
Rifkin et al[17]	102	72%	81%		Rigid, radial (7 MHz)
Hildebrandt et al[18]	113	-	78%	P	Rigid, radial (7 MHz)
Tio et al[19]	91	88%	-	-	Rigid
Katsura et al[20]	120	92%	-		Rigid, radial, (7 MHz)
Glaser et al[21]	154	86%	81%	P	Rigid, radial (7 MHz)
Herzog et al[22]	118	89%	80%	P	Rigid, radial (7 MHz)
Cho et al[23]	76	82%	70%	P	Flexible, radial (7 MHz)
Thaler et al[24]	36	88%	80%	P	Rotating wall transducer IR 1510 AKTM (Kretz) (5, 7.5, 10 MHz)
Nielson et al[25]	100	85%	-	-	Probe (7 MHz)
Sailer et al[26]	160	77%	83%	P	Rigid
Nishimori et al[27]	70	76%	69%		Flexible
Norton et al[28]	121	92%	65%	P	Flexible, radial (7.5-12 MHz)
Kim et al[29]	89	81%	63%		Rotating transducer (7.5 MHz)
Marone et al[30]	63	81%	70%	R	Flexible, radial (7.5-12 MHz)
Akasu et al[31]	154	96%	72%	R	Flexible, radial (7.5-12 MHz
Garcia-Aquilar et al[32]	545	69%	64%	P	Rigid, radial (7-10 MHz)
Harewood et al[12]	80	91%	82%	P	Flexible, radial (7.5-12 MHz)
Marusch et al[33]	422	63%	-	P	Rigid
Kauer et al[34]	458	69%	68%	R	Probe (7.5-10 MHz )
Vila et al[35]	120	83%	72%	P	Flexible, radial
Landman et al[36]	938	-	70%	P	Probe (10 MHz)
Halefoglu et al[37]	34	85%	76%	P	Probe (7-10 MHz)
Lin et al[38]	192	86%	78%	P	Flexible, radial (7.5-12 MHz)
Fernández-Esparrach et al[39]	90	95%	65%	P	Flexible, radial (5-20 MHz)
Ünsal et al[40]	31	80%	70%	R	Radial
Zhu et al[41]	110	91%	85%	-	Rigid, radial (5-10 MHz)
	4976
Mean		84	74
Range		63-96	63-85

uTN stage compared with pTN stage; no previous neoadjuvant therapy (NAT). P: Prospective; R: Retrospective; Pts: Patients; EUS: Endoscopic ultrasound.

Table 5 Accuracy of endoscopic ultrasound for each single T stage

Ref.	Year	No.	pT1	pT2	pT3	pT4
Akasu et al[31]	1997	164	86%	56%	93%	75%
Marone et al[30]	2000	63	80%	78%	84%	80%
Lin et al[38]	2011	192	86%	94%	86%	65%
Fernández-Esparrach et al[39]	2011	90	95%	76%	76%	95%
Zhu et al[41]	2013	110	93%	88%	88%	96%
Range		619	80%-95%	56%-94%	76%-93%	65%-96%
Mean			88%	78.4%	85.4%	80.2%

uTN stage compared with pTN stage; No previous neoadjuvant therapy (NAT).

Table 6 N staging at endoscopic ultrasound, according to the number of metastatic lymph nodes

uN1 = 1-3 positive nodes

uN2 = More than 4 metastatic lymph nodes

From ref.[9].

Table 7 Accuracy of endoscopic ultrasound in staging locally advanced rectal cancer after chemo-radiation

Ref.	Year	No.	T	Mistakes		N
				Over	Under
Vanagunas et al[90]	2004	82	48%	38%	14%	77%
Mao et al[92]	2006	25	72%	8%	12%	80%
Radovaanovic et al[94]	2008	44	75%	18%	7%	68%
Marone et al[91]	2011	85	61%	28%	7%	59%
Mean		236	64%	23%	10%	71%
Range			48%-75%	8%-38%	7%-14%	59%-80%

uTN stage compared with pTN stage; Previous neoadjuvant therapy (NAT). Over: Overstaging; Under: Understaging.