Endoscopic Ultrasound in Solid Pancreatic Masses – Current State and Review of the Literature

Abstract

Some 25 years ago endoscopic ultrasound (EUS) was introduced in clinical practice for better visualization of pancreas. At the time of introduction EUS was superior to other methods in detection of pancreatic masses allowing tissue diagnosis by later introduced EUS-guided fine needle aspiration (FNA). During the time EUS was improved, electronic probes replaced mechanical probes adding ability of color Doppler, power Doppler, contrast enhanced endosonography as well as EUS elastography analysis. Meanwhile, CT technology has also experienced significant improvements raising the question whether EUS has lost ground in diagnostics of solid pancreatic masses. The aim of this review was to discuss the current evidence of clinical impact of EUS and EUS-FNA in evaluation of solid pancreatic masses with special emphasis on differentiation between benign and malignant pancreatic lesions. According to the literature, the detection of small pancreatic tumors, preoperative localization of pancreatic endocrine tumors and tissue sampling by fine-needle aspiration of pancreatic masses in cases with therapeutic consequences are considered firm indications for EUS. Cytological tissue analysis remains undisputed in differentiation benign from malignant lesions, but the question when FNA is needed is discussed. Color Doppler, power Doppler, contrast enhanced endosonography and especially elastography are also discussed as tools that are bringing additional information in evaluation of pancreatic masses, however insufficient for definitive judgment of the lesion’s nature. Pancreatic cancer staging as indication for EUS is discussed controversially, inconsistent results and conflicting evidence in literature making adequate conclusion impossible. However, this indicates that at least the role of EUS is no longer undisputed in this matter. Resuming the role of EUS we can state that despite some controversies EUS is very valuable method in evaluation of solid pancreatic masses and with EUS guided FNA is nowadays by far the best method for obtaining tissue diagnosis.

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Coll. Antropol. 34 (2010) 1: 337–340
Review
Endoscopic Ultrasound in Solid Pancreatic Masses
– Current State and Review of the Literature
Mario Tadi}1, Tajana [toos-Vei}2, Mirjana Vukeli}-Markovi}3, Josip ]uri}3, Marko Bani}3,5,
@eljko ^abrijan1, Ivica Grgurevi}1and Milan Kujund`i}1,4
1Department of Gastroenterology, University Hospital Dubrava, Zagreb, Croatia
2Department of Cytology, University Hospital Dubrava, Zagreb, Croatia
3Department of Radiology, University Hospital Dubrava, Zagreb, Croatia
4University of Zagreb, School of Medicine, Zagreb, Croatia
5University of Rijeka, School of Medicine, Rijeka, Croatia
A B S T R A C T
Some 25 years ago endoscopic ultrasound (EUS) was introduced in clinical practice for better visualization of pan-
creas. At the time of introduction EUS was superior to other methods in detection of pancreatic masses allowing tissue
diagnosis by later introduced EUS-guided fine needle aspiration (FNA). During the time EUS was improved, electronic
probes replaced mechanical probes adding ability of color Doppler, power Doppler, contrast enhanced endosonography as
well as EUS elastography analysis. Meanwhile, CT technology has also experienced significant improvements raising
the question whether EUS has lost ground in diagnostics of solid pancreatic masses. The aim of this review was to dis-
cuss the current evidence of clinical impact of EUS and EUS-FNA in evaluation of solid pancreatic masses with special
emphasis on differentiation between benign and malignant pancreatic lesions. According to the literature, the detection
of small pancreatic tumors, preoperative localization of pancreatic endocrine tumors and tissue sampling by fine-needle
aspiration of pancreatic masses in cases with therapeutic consequences are considered firm indications for EUS. Cyto-
logical tissue analysis remains undisputed in differentiation benign from malignant lesions, but the question when FNA
is needed is discussed. Color Doppler, power Doppler, contrast enhanced endosonography and especially elastography are
also discussed as tools that are bringing additional information in evaluation of pancreatic masses, however insufficient
for definitive judgment of the lesion’s nature. Pancreatic cancer staging as indication for EUS is discussed controver-
sially, inconsistent results and conflicting evidence in literature making adequate conclusion impossible. However, this
indicates that at least the role of EUS is no longer undisputed in this matter. Resuming the role of EUS we can state that
despite some controversies EUS is very valuable method in evaluation of solid pancreatic masses and with EUS guided
FNA is nowadays by far the best method for obtaining tissue diagnosis.
Key words: endoscopic ultrasonography, role of EUS, endoscopic ultrasound guided-fine needle aspiration, cytology,
pancreatic masses, small tumors, pancreatic malignancy
Introduction
Some 25 years ago endoscopic ultrasound (EUS) was
introduced in clinical practice for better visualization of
pancreas. At the time of introduction EUS was superior
to other available diagnostic methods for evaluation of
pancreatic diseases1–3. Transabdominal ultrasound was
unable to analyze whole organ due to intervening air in
bowels, and computed tomography (CT) scans of that
time was obviously inferior in detection of pancreatic
tumors1–3. EUS evaluates pancreas from very close prox-
imity, and the entire organ can be examined. However,
results from early studies4,5and studies on missed pan-
creatic tumors6indicate that EUS has lower accuracy for
the lesions located in the tail of pancreas. Technology of
EUS has improved, electrical probes replaced mechanical
probes giving opportunity for better image quality, ex-
panding diagnostic possibilities with color Doppler, po-
337
Received for publication July 31, 2009

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wer Doppler, contrast enhanced endosonography and
EUS elastography. In difficult issues such as making dif-
ferential diagnosis between benign and malignant le-
sions some papers report power Doppler7and contrast
enhanced EUS as a good tool8–10.Electronic linear probes
allowed real time tissue sampling by EUS guided fine
needle aspiration (FNA)11–15making EUS the method of
choice for obtaining tissue diagnosis in regions difficult
to reach such as pancreas. Furthermore, elastography,
the new and sophisticated ultrasound technology which
evaluates tissue hardness is proposed as the method that
can differentiate benign from malignant pancreatic le-
sions without tissue sampling16–18. However, during years
CT technology has been significantly improved raising
question if EUS has lost superiority in diagnostics of
pancreatic masses. The aim of this review was to discuss
the current evidence of clinical impact of EUS and EUS-
-FNA in evaluation of solid pancreatic masses with spe-
cial emphasis on differentiation between benign and ma-
lignant pancreatic lesions.
Detection of Pancreatic Masses
From its very beginning EUS was considered very ac-
curate in detection of pancreatic pathology, especially of
small pancreatic masses. The rate of detection of pancre-
atic cancer is considered high19,20. Detection rate is lower
in patients with chronic pancreatitis, short after acute
pancreatitis, in diffuse pancreatic tumors6and in low vol-
ume centers21,22. To obtain maximum yield from EUS it
should be preformed after contrast CT and before endo-
scopic retrograde cholangiopancreatography (ERCP)23,24.
However, EUS is inadequate for screening for pancreatic
masses with exception of special screening programs in
patients with familial risk of pancreatic cancer usually
after CT and followed with ERCP . Even when conducted
under study conditions the yield was relatively low, about
10%, even in patients with high risk for pancreatic can-
cer25,26. Therefore, EUS should not be used as a screen-
ing tool in population with small risk of pancreatic can-
cer. Quite consistent indication for EUS is localization of
pancreatic endocrine tumors after laboratorial confirma-
tion of the diagnosis27,28. The diagnosis in this case is
based on laboratory tests, while imaging the tumor by
EUS localizes tumor for easier surgical removal. The
other story are non-functional pancreatic endocrine tu-
mors, which are mostly incidental findings detected by
other imaging methods. Endosonographic appearance of
these lesions is similar to functional tumors, they are
typically well demarcated, hypoechoic lesions in the
pancreas. However, this morphological appearance is
far from sufficient to make diagnosis and FNA should
be preformed to obtain tissue diagnosis29–31. Conclusion:
EUS is still considered the method of choice for detec-
tion of small tumors, for localizing pancreatic endocrine
tumors and for evaluation of incidental lesions allowing
tissue sampling, but it is not suitable to be a screening
tool.
Differentiation of Benign from Malignant
Lesions: Is FNA Replaceable?
Despite advances in diagnostic imaging techniques,
the differentiation between pancreatic cancer and benign
lesions is difficult32–36. Morphological analysis of endo-
sonographic image in B mode, as well as Doppler analy-
sis, power Doppler analysis and contrast enhanced analy-
sis of pancreatic masses did not fulfilled initial good
expectations. Elastographic evaluation of tissue hard-
ness gives additional information about evaluated mass
and can differentiate benign masses from malignant in
some cases, but in number of cases differentiation is im-
possible. EUS elastography is superior in differentiation
to EUS B mode analysis and can be used as a second line
for better characterization of pancreatic masses after
negative FNA as well as for targeting which node to eval-
uate by FNA37–41.
EUS-FNA is an effective and accurate method for
providing tissue diagnosis in patients with suspected
pancreatic masses36,42,43. Moreover, EUS-FNA has re-
placed endoscopic retrograde cholangiopancreatography
and brush cytology for obtaining tissue since it has a
higher success rate and is associated with fewer com-
plications42. EUS-FNA differentiates precisely benign
and malignant lesions, having high positive predictive
value while negative predictive value is lower44–46. Not
finding malignant cells in aspirated material does not
rule out malignancy, so false negative findings empha-
sized in many studies are problem of this method35,44–51.
Another problem are indeterminate, suspecious or atypical
cytological findings, which occur from 7.8 to 10.9%46–49.
Some groups of authors, as well as our group, advocate
repeated EUS-FNA procedure for enhancing the yield of
FNA in negative or suspicious cytological findings43,46,50.
In experienced hands the technique is quite simple. After
the lesion is identified endosonographically the FNA nee-
dle is inserted through the working channel of the echo-
endoscope. Color Doppler sonography is performed in or-
der to avoid vessels in the needle track. The needle is
advanced into the targeted lesion under ultrasonogra-
phic guidance. The stylet is removed when the tip of the
needle is inside the lesion. Constant negative pressure
using a syringe attached to the proximal end of FNA nee-
dle is applied while doing back-and-forth movements.
In order to get best out of EUS-FNA, attending cytol-
ogist should be informed about the patient’s clinical sta-
tus, laboratory findings and imaging studies46,49,53,54. The
value of direct communication between endosonogra-
phist and attending cytologist is priceless for obtaining
good samples. For quick assessment of specimen on site
evaluation can be done. Direct smears of aspirated mate-
rial are prepared and based on its macroscopic appear-
ance the selected slide is stained with Hemacolor (Merck
KGaA, Germany) for rapid on-site evaluation (ROSE).
ROSE enables rapid assessment of sample adequacy55,
and can give preliminary diagnosis56. In cases when the
needle was clearly seen in lesion, experienced cytologist
can asses specimen adequacy by macroscopic specimen
M. Tadi} et al.: Endoscopic Ultrasound in Pancreatic Masses, Coll. Antropol. 34 (2010) 1: 337–340
338

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analysis46,57. Additional samples for ancillary studies (flow
cytometry, immunocytochemistry or molecular studies)
can be taken when necessary. For definitive evaluation,
slides are air-dried and stained with May-Grünwald-
-Giemsa. Passes are repeated until a definitive diagnosis
is reached, or when the team believes that further sam-
pling would not increase the possibility of obtaining a de-
finitive diagnosis. The most commonly used needles are
22 gauge needles. Newly developed 19 gauge true cut
needles that can provide cylinder for a histological as-
sessment did not justify expectations and have not im-
proved sensitivity58–63.
While performing FNA in iresectable tumors has no
adversaries, FNA in resectable tumors is debatable. So-
me authors advocate avoiding FNA in resectable pancre-
atic adenocarcinoma since it will not alter management
of the patient64, and other demand cytological diagnoses
in this cases36,42–44. The fact that management will not be
influenced by presumed FNA finding, problem with false
negative cytological findings and risk of complications
may support a no FNA stand. However, complications
are rare and mild, with tumor seeding as most fearful
complication65. Still, there is only one documented tumor
seeding after EUS-FNA of solid pancreatic masses from
the beginnings of EUS-FNA world wide66. Since there is
no way to accurately differentiate benign from malignant
lesions by any other method then with tissue diagnosis
obtained by EUS-FNA it is hard to say that every de-
tected small solid lesion deserve to be surgically re-
moved. Holding this taught, this group of authors pro-
spectively conducted a study with repeated EUS-FNA
procedures in small solid pancreatic masses46where in 22
of 46 cases lesions were found to be benign even after re-
peated EUS-FNA procedures. Follow up period was at
least 22 months and there was only one false negative
finding. So, EUS-FNA reduced number of unnecessary
surgery in patients with small solid pancreatic masses. In
conclusion, EUS-FNA is the method of choice for differen-
tiation benign and malignant lesions. However, there is
no consensus should EUS-FNA be performed in small
solid pancreatic lesions.
Staging of Pancreatic Cancer
Tumor staging is the most debatable indication for
EUS in pancreatic cancer patients. At the time of intro-
ducing this method, EUS was superior to other methods
in detection of pancreatic masses, but even the early
studies were not consistent for superiority in staging.
Some studies considered EUS inferior67,68and other su-
perior to other imaging methods69–71.
It is difficult to make conclusion in this matter since
criteria for resectability used in these studies were differ-
ent. It is fair to say that the choice of method should be
up to personal opinion of clinician and availability of
quality equipment and experienced personal.
Resuming the role of EUS we can state that despite
some controversies EUS is very valuable method in eval-
uation of solid pancreatic masses and with guided FNA is
nowadays by far the best method for obtaining tissue di-
agnosis.
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M. Tadi}
Department of Gastroenterology, University Hospital Dubrava, Av. Gojka [u{ka 6, 10040 Zagreb, Croatia
e-mail: mtadic@kbd.hr
ENDOSKOPSKI ULTRAZVUK U DIJAGNOSTICI SOLIDNIH TVORBI GU[TERA^E – TRENUTNO
STANJE I PREGLED LITERATURE
S A @ E T A K
Prije otprilike 25 godina endoskopski ultrazvuk (EUS) uveden je u klini~ki praksu kako bi omogu}io bolji pregled
promjena u gu{tera~i. U to vrijeme, EUS je bio nadmo}an ostalim metodama u otkrivanju tvorbi u gu{tera~i, a uz
kasnije uvedenu citolo{ku punkciju vo|enu EUS-om omogu}eno je i postavljanje tkivne dijagnoze. Tijekom vremena
EUS je tehnolo{ki napredovao. Mehani~ka sonda zamijenjena je elektroni~kom koja je omogu}ila dodatne analize obo-
jenim Dopplerom i power Dopplerom, te analizu kontrastom poja~anim EUS-om i EUS elastografiju. Istovremeno je
znatno napredovala i tehnologija kompjuterizirane tomografije (CT) te neki autori postavljaju pitanje je li EUS izgubio
prednost u dijagnostici solidnih tvorbi gu{tera~e. Cilj ovog pregleda je iznijeti najnovije literaturne dokaze o utjecaju
EUS-a i EUS-FNA na dijagnostiku promjena u gu{tera~i s posebnim osvrtom na razlikovanje dobro}udnih od zlo}udnih
promjena. Prema podatcima iz literature, neupitne indikacije za EUS su otkrivanje malih tumora gu{tera~e, preopera-
tivna lokalizacija endokrinih tumora te dobivanje uzoraka za tkivnu dijagnozu u slu~ajevima kad to ima utjecaj na
daljnji postupak s bolesnikom. Citolo{ka tkivna dijagnoza je i dalje neupitna za razlikovanje malignog od benignog,
me|utim postavlja se pitanje kad je tkivna dijagnoza i citolo{ka punkcija neophodna. Prema literaturnim podatcima
obojeni Doppler, power Doppler, EUS poja~an kontrastom i EUS elastografija su se pokazali kao metode koje nude
dodatne informacije u evaluaciji solidnih promjena gu{tera~e, ali nedovoljno da bi otkrile definitivnu prirodu lezije.
Uloga EUS-a u procjeni pro{irenosti tumora gu{tera~e je prema literaturnim podatcima kontroverzna, a kako neki
upu}uju na superiornost EUS-a a drugi na superiornost CT-a nije mogu}e dati kvalitetan zaklju~ak. Me|utim, to uka-
zuje da EUS nije neprikosnoven u procjeni pro{irenosti tumora.
M. Tadi} et al.: Endoscopic Ultrasound in Pancreatic Masses, Coll. Antropol. 34 (2010) 1: 337–340
340