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Gastrointestinal Pathology
Gastrointestinal Pathology
Edited by
Associate Editor:
Till S. Clauditz, MD
Associate Professor, Head of Gastrointestinal Pathology Service
Department of Pathology with Section Molecular Pathology and Cytology
University Medical Center Hamburg-Eppendorf,
Hamburg, Germany
This edition first published 2021
© 2021 John Wiley & Sons Ltd
All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means,
electronic, mechanical, photocopying, recording or otherwise, except as permitted by law. Advice on how to obtain permission to reuse material
from this title is available at http://www.wiley.com/go/permissions.
The right of Gregory Y. Lauwers and Michael B Wallace to be identified as the authors of the editorial material in this work has been asserted in
accordance with law.
Registered Offices
John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, USA
John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK
Editorial Office
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HB ISBN: 9780470658369
10 9 8 7 6 5 4 3 2 1
v
Contents
6 Gastric Neoplastic Conditions: Precursor Lesions and Early Gastric Cancer 125
Till S. Clauditz and Gregory Y. Lauwers
Index 369
vii
List of Contributors
Tissue sampling of the gastrointestinal tract at the time of ndoscopic Equipment for Tissue
E
endoscopy is the cornerstone of many gastrointestinal Sampling
diagnoses. The development of a flexible endoscope and
the subsequent ability to directly acquire tissue under Modern endoscopic equipment can be divided in two gen-
optical guidance has been one of the most important eral categories: the endoscope that allows access to the gas-
advancements in the field of gastroenterology throughout trointestinal tract and accessory devices that are typically
its history. Although tissue sampling can be performed passed through the working channel of the endoscope to
through nonendoscopic devices, the ability to directly cor- directly acquire tissue, including biopsy forceps, snares,
relate precise locations and target biopsies to specific areas fine-needle aspiration devices, and cytology brushes.
of disease is critical to our ability to diagnose and further Recent developments in tissue sampling include devices
understand gastrointestinal pathology. Many of the that are capable of wide-field, often definitive, endoscopic
advancements in our understanding of the basic pathol- resection of early neoplasia and invasive carcinoma.
ogy and molecular biology of gastrointestinal disease can A modern endoscope is a remarkably robust and versa-
be directly attributed to our ability to acquire tissue for tile instrument including a light source, optical lenses with
histological, molecular, and genetic analyses. An excellent a video capture device, image processing, and display
example is our deep understanding of the molecular equipment, and importantly for the purposes of tissue
pathology of colorectal cancer development from normal acquisition, an accessory channel ranging from 1 to 6 mm
colonic epithelium to adenoma to colorectal cancer, a dis- (typically 3–4 mm), which allows passage of devices for
covery made possible because of colonoscopic access to mechanical collection of tissue (Figures 1.1 and 1.2).
precursor lesions such as adenomatous polyps and early There is a general trade-off between the diameter of the
cancers. instrument and the ease and comfort with which it can be
In this chapter, we will review general principles of tissue passed through the natural orifices of the body such as the
acquisition at the time of endoscopy including the following mouth and anus. In general the larger the outer diameter,
topics: the larger the accessory channel is to accommodate larger
●● Endoscopic equipment for obtaining tissue including instruments for tissue acquisition. A fundamental limita-
endoscopic accessory channels, biopsy forceps, snare tion of most flexible endoscopes, as opposed to surgical
devices, needle aspiration and cytology brush. instruments, is that all accessories pass through a single
●● General principles of optimal sampling technique. access point of the endoscope. As compared to surgical
●● Methods of tissue preparation in the endoscopy labora- instruments with multiple access points, the endoscopic
tory to optimize diagnostic accuracy. devices do not typically allow triangulation to acquire a
●● The role of endoscopic ultrasound (EUS)-guided fine- large bulk tissue or resect entire organs. For this reason,
needle aspiration cytology. most tissue is sampled through pinch forceps, needle
Gastrointestinal Pathology: Correlative Endoscopic and Histologic Assessment, First Edition. Edited by Gregory Y. Lauwers and Michael B. Wallace.
© 2021 John Wiley & Sons Ltd. Published 2021 by John Wiley & Sons Ltd.
2 General Principles of Biopsy Diagnosis of GI Disorders
Jet B knife IT knife nano CO2 insufflator ST hood short type MucoUp
Zeon medical Olympus medical Olympus Medical Fujifilm medical Johnson and Johnson
Figure 1.3 (a) Tools for performing endoscopic resection including endoscopic submucosal dissection (ESD). Source: Zeon Medical.
(b) Standard and insulated tip electrocautery knives for incision and dissection. Source: © 2017 Korean Society of Gastrointestinal
Endoscopy. (c) CO2 insufflator for luminal distension, which is preferred to air given rapid reabsorption. Source: Olympus. (d) Distal
attachment hood to facilitate maintaining view within the submucosal space. Source: Fujifilm medical. (e) Injection fluid (hyaluronic
acid; Mucoup [Johnson and Johnson]) for submucosal lifting. Source: Gut and Liver.
Endoscopic Brush Cytolog 3
2 cm
issue Processing in the Endoscopy
T
Laboratory
(a) (b)
Figure 1.9 (a) and (b) Endoscopic ultrasound endoscope and guided fine-needle aspiration (EUS-FNA) device.
Specific Organ Sampling Method 5
N
on-oriented Samples
Increasingly, endoscopic resection is being used for defini- as Roswell Park Memorial Institute (RPMI) medium that
tive oncologic removal of precancerous and invasive lesions. allow subsequent flow cytometry. As a practical matter,
In these cases it is advantageous to orient the specimen so placement in such a preservative should be considered even
that precise staging as well as margin assessment can be per- when likelihood is low since cells preserved in such solution
formed. A typical situation is in endoscopic resection of can always be examined with routine cytological methods;
early neoplasia in the esophagus such as Barrett’s esopha- however, cells that are placed in formalin or alcohol cannot
gus. In this case a sample is frequently obtained through be evaluated for flow cytometry. The use of rapid on-site
endoscopic mucosal resection. Large pieces of tissue, typi- evaluation (ROSE) cytology has been shown in many stud-
cally 1–2 cm in diameter, can be obtained to a depth of the ies to increase diagnostic yield and reduce the need for
submucosa. In this case the sample should be removed from repeated procedures.
the patient in a way that does not damage or distort the tis-
sue. This is typically performed by suctioning the tissue into
a distal attachment cap/hood and then removing the endo- C
ulture Samples
scope. Alternative retrieval devices include a modified snare
with a protective net. These tissues should then be immedi- Samples obtained for culture should be placed in a sterile
ately oriented at the bedside typically by placing them on a specimen container. Sterile saline maybe needed to prevent
paraffin or similar firm block. The tissue should be flattened drying of the specimen. Attention should be paid to mini-
typically with the mucosal side up and the edges carefully mize contamination although it is recognized that the endo-
pinned so that the tissue remains flat (Figure 1.10). scope and the organs throughout which it is passed are not
sterile and is not possible to obtain a purely sterile access into
the gastrointestinal lumen. Contamination with oropharyn-
C
ytology Samples geal organisms or colonic organisms is not uncommon.
Therapeutic Sampling
Increasingly, endoscopic resection methods are being
applied to early neoplasia the esophagus, particularly
Barrett’s esophagus and early squamous cell carcinoma.
These are largely confined to tumors suspected to be T1 or
nodular high-grade dysplasia. Endoscopic mucosal resec-
tion (EMR) methods generally involve an EMR device such
as a modified band ligator followed by snare resection of
the pseudopolyp (Figure 1.11–1.13).
Other methods include endoscopic submucosal dissection
(ESD) in which the lateral margins of the suspected area are
Figure 1.13 Area of resection at 6–12 o’clock includes the
incised with electrocautery knife followed by dissection along
entire region of suspected neoplasia at 9 o’clock. The remaining
the submucosal plane to obtain an en bloc specimen. EMR tissue at the 9 o’clock area represents intact deep submucosa
devices can typically obtain samples 1–2 cm in diameter into and muscularis propria.
Specific Organ Sampling Method 7
the depth of the mid-submucosa. Endoscopic submucosal Gastric Polyps Gastric polyps are very frequently
dissection can obtain samples of any lateral diameter and encountered, particularly in patients who are on chronic
generally to the base of the submucosa. proton pump inhibitor therapy. Current ASGE guidelines
One major advantage of these techniques is the ability to for management of gastric polyps suggest that polyp should
perform wide-field or en bloc resection and orient the sam- be sampled by biopsy. Fundic gland polyps larger than 1 cm
ple. Samples should be retrieved without causing trauma to should be removed by polypectomy. Hyperplastic polyps
the tissue, preferably by removal through the endoscopic larger than 5 mm should be removed by polypectomy, and
cap or through a snare-net as opposed to suctioning via the all adenomatous polyps should be removed by polypectomy.
accessory channel, which can traumatize or fragment the In patients who have numerous polyps, particularly where
tissue. Once retrieved the tissue should be handled as with endoscopic inspection is highly consistent with fundic
other endoscopic resection specimens by orienting the gland polyps, the largest of the polyps should be removed
specimen and pinning it on a fixed material such as a paraf- by polypectomy and representative sampling performed of
fin block. En bloc specimens can be oriented in terms of smaller polyps.
the oral and anal side of the lesion and assessed for lateral
and deep margins. For resections that are performed piece- Ulcer Disease Because of the potential for neoplasia in the
meal such as with multiband mucosectomy, the lateral setting of ulcers, numerous biopsies should be obtained
margins cannot be accurately assessed and so complete from the base as well as the margins of the ulcer to exclude
resection relies on the endoscopic inspection intralumi- malignancy. Cytology may also be helpful. Sampling for
nally. The specimens should still be oriented and assessed concurrent H. pylori infection should be performed as
for the deep margin. suggested above.
Therapeutic Sampling
Stomach
Endoscopic resection in early gastric cancer is now widely
Diagnostic Sampling performed throughout the world. The endoscopic resection
Major indications for diagnostic sampling of the stomach methods include endoscopic mucosal resection typically with
include assessment for Helicobacter pylori infection, diag- a cap-assisted device as in the esophagus, or injection of a sub-
nosis of gastritis, metaplastic atrophic change, gastric pol- mucosal agent such as saline followed by snare resection of
yps, and suspected neoplasia, particularly in the setting of the lifted tissue. Lesions larger than 1–2 cm should generally
gastric ulceration or early gastric cancer. be removed en bloc by endoscopic submucosal dissection
when early gastric cancer is suspected. Tissue should be han-
H. pylori Sampling Biopsy is one of several recommended dled in the same manner as discussed above in esophagus.
methods for H. pylori sampling that also includes urease
breath testing and stool testing for H. pylori antigen. When
Small Intestine
using endoscopic tissue sampling, there are two general
methods including non-histological testing of the tissue for Major indications for tissue sampling of the small intestine
the presence of urease using the traditional Campylobacter- include celiac disease as well as resection of early neoplasia.
like organism test (CLO-test). In this case, the tissue should
be placed in the standard agar well and visually inspected Diagnostic Sampling
for a pH change following the instructions for use in this Currently established protocols for sampling for celiac dis-
product. Histological sampling can also be performed with ease recommend four to six biopsies from the duodenum
one of two methods. One method is to take three biopsies including the duodenal bulb and distal duodenum.
including one from the angularis corpus antrum junction, All other suspicious areas should be sampled using rou-
one from the greater curvature of the corpus, and one from tine biopsy technique. Sampling of the papilla should be
the greater curvature of the antrum. Alternatively, the performed with caution as biopsy in this area can cause
updated Sydney protocol may be followed, which includes pancreatitis. When a suspected neoplastic lesion is seen in
five biopsies including one from the antrum lesser curve, the region of the papilla, it is preferred to take a biopsy that
antrum greater curve, gastric corpus lesser curve, and does not immediately injure the orifice of the bile duct or
greater curve, and one from the angularis of the stomach. the pancreas duct.
performed with injection followed by snare. There appears were obtained throughout the colon. Current guidelines rec-
to be higher risks of bleeding and perforation associated ommend biopsy of each colonic segment with four-quadrant
with endoscopic resection of duodenal lesions. This is par- biopsies every 10 cm from the cecum to the rectum for a
ticularly true were using cap-assisted devices where the minimum total of 33 biopsy samples. In cases where the
thin wall of the duodenum is suctioned into the cap lead- entire colon is not affected, four samples should be obtained
ing to inadvertent full-thickness resection. every 10 cm of the affected areas. More recently, it has been
Special attention is required for resection of lesions shown that using dye spray such as indigo carmine or meth-
involving the ampulla of Vater. In these cases, typically the ylene blue can identify areas of dysplasia with high accuracy
lesion is resected followed by placement of a stent in the and thus guide directed sampling without the need for ran-
pancreatic and bile duct orifice to prevent stricturing of dom biopsy. Biopsies should however also be assessed from
these and acute pancreatitis. each colonic segment to assess for inflammation.
Another special situation is polypoid lesions in the distal
small intestine, which can now be accessed with deep ent- Therapeutic Sampling
eroscopy methods. Polyps are generally removed in the Endoscopic resection methods of flat and lateral spreading
same manner as polypoid lesions elsewhere in the gastro- colorectal polyps has expanded rapidly over last 10 years.
intestinal tract by snare polypectomy. Special circum- Most noninvasive neoplastic lesions of the colon can now
stances include numerous polyps such as those developed be removed through advanced endoscopic methods such as
in patients with Peutz–Jeghers syndrome. These can be EMR or ESD avoiding the need for surgery. Lesions less
particularly large and numerous. It may not be possible to than 2 cm can typically be removed en bloc with endo-
resect and retrieve all tissues. Because of the laborious pro- scopic mucosal resection involving injection of a fluid
cess of deep enteroscopy, it is often not feasible to extract cushion under the lesion followed by snare resection.
the endoscope with each large polypoid tissue. Thus diag- Where there is suspected early (mucosal or superficial sub-
nostic sampling can be performed by biopsy of the lesion or mucosal) invasive carcinoma, en bloc resection should be
fragmentation of the lesion with a snare followed by com- performed using either EMR or ESD depending on the size
plete therapeutic excision of the lesion. of the lesion. The tissue processing should be the same as
for other neoplastic lesions with orientation of the speci-
men and pinning of the specimen to assess the lateral and
Colon
deep margins (Figure 1.14).
Major indications for diagnostic sampling of the colon The final histological analysis allows for detailed staging,
include detection of both overt and microscopic colitis and as well as matching the corresponding histological and
surveillance for dysplasia in inflammatory bowel disease. endoscopic findings; note the lavender line overlays indi-
Perhaps the most commonly performed tissue sampling cating sites of advanced neoplasia. The close collaboration
in the field of gastroenterology involves removal of colorec- between pathologists and endoscopists further improves
tal polyps and tissue sampling of more advanced colorectal the accuracy of each procedure (Figure 1.15).
neoplasia.
Diagnostic Sampling S
ummary
In patients with chronic diarrhea and suspected microscopic
colitis, random biopsies should be taken throughout the The role of pathology in gastrointestinal endoscopy
colon including at least two biopsies from the right, trans- remains critical. Gastroenterologists should have a thor-
verse, descending, and sigmoid colon. For limited sampling ough knowledge of optimal methods of tissue removal and
the flexible sigmoidoscopy is also a reasonable approach. In initial processing to allow optimal diagnosis and therapeutic
this case at least two biopsies should be obtained from the results. Advances in endoscopic resection have allowed
sigmoid and descending colon as well as transverse colon if complete resection of many early cancers but require closer
this can be reached with the sigmoidoscope. cooperation between the endoscopist and pathologist to
In the setting of inflammatory bowel disease, biopsy sam- ensure the tissue is properly handled and staged. With
pling should be performed to establish the diagnosis and to EUS-FNA, the direct interaction of pathologist with rapid
assess the extent. For the initial diagnosis, the American on-site cytological evaluation has led to higher accuracy,
Society for gastrointestinal endoscopy recommends two biop- and reduced the need for repeat procedures. Finally,
sies from each of five sites including the ileum and rectum. advances in imaging will continue to improve the targeting
Surveillance of inflammatory bowel disease is a special cir- of tissue sampling and reduce the need for low-yield ran-
cumstance and is evolving. Traditionally, random biopsies dom sampling methods.
Summar 9
Figure 1.14 Endoscopic submucosal dissection (ESD) procedure. A flat neoplastic lesion is seen in panel 1–2 after staining with
cresyl violet. The margins are incised (panel 3) with the endoscope retroflexed (black tube). The submucosal plane is dissected with a
needle knife (panel 4). The final resection site (panel 5) and corresponding resection specimen prepared for pathology processing
(panel 6).
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Figure 1.15 Endoscopically resected en bloc well-differentiated adenocarcinoma 28 × 17 mm with superficial submucosal invasion
and no lymphovascular invasion and negative horizontal and vertical margins. This sample meets criteria for endoscopic curative
resection.
F
urther Reading
Al-Haddad, M. and Eloubeidi, M.A. (2008). Diagnostic and Kadri, S.R., Lao-Sirieix, P., O’Donovan, M. et al. (2010).
therapeutic applications of endoscopic ultrasound-guided Acceptability and accuracy of a non-endoscopic screening
punctures. Dig. Dis. 26 (4): 390–397. test for Barrett’s oesophagus in primary care: cohort study.
Basford, P., George, R., Nixon, E. et al. (2014). Endoscopic BMJ 341: c4372. https://doi.org/10.1136/bmj.c4372.
resection of sporadic duodenal adenomas: comparison of LeBlanc, J.K., Emerson, R.E., Dewitt, J. et al. (2010). A
endoscopic mucosal resection (EMR) with hybrid prospective study comparing rapid assessment of smears
endoscopic submucosal dissection (ESD) techniques and and ThinPrep for endoscopic ultrasound-guided fine-
the risks of late delayed bleeding. Surg. Endosc. 28 (5): needle aspirates. Endoscopy 42 (5): 389–394.
1594–1600. Levy, M.J., Reddy, R.P., Wiersema, M.J. et al. (2005). EUS-
da Cunha Santos, G., Boerner, S.L., and Geddie, W.R. (2011). guided trucut biopsy in establishing autoimmune
Maximizing the yield of lymph node cytology: lessons pancreatitis as the cause of obstructive jaundice.
learned from rapid onsite evaluation of image- and Gastrointest. Endosc. 61 (3): 467–472.
endoscopic-guided biopsies of hilar and mediastinal Mann, N.S., Mann, S.K., and Alam, I. (1999). The safety of
lymph nodes. Cancer Cytopathol. 119 (6): 361–366. hot biopsy forceps in the removal of small colonic polyps.
Eloubeidi, M.A., Tamhane, A., Jhala, N. et al. (2006). Digestion 60 (1): 74–76.
Agreement between rapid onsite and final cytologic Monkemuller, K.E., Fry, L.C., Jones, B.H. et al. (2004).
interpretations of EUS-guided FNA specimens: Histological quality of polyps resected using the cold
implications for the endosonographer and patient versus hot biopsy technique. Endoscopy 36 (5): 432–436.
management. Am. J. Gastroenterol. 101 (12): 2841–2847. Phoa, K.N., van Vilsteren, F.G., Weusten, B.L. et al. (2014).
Falk, G.W., Rice, T.W., Goldblum, J.R., and Richter, J.E. Radiofrequency ablation vs endoscopic surveillance for
(1999). Jumbo biopsy forceps protocol still misses patients with Barrett esophagus and low-grade dysplasia: a
unsuspected cancer in Barrett’s esophagus with high-grade randomized clinical trial. JAMA 311 (12): 1209–1217.
dysplasia. Gastrointest. Endosc. 49 (2): 170–176. Qumseya, B.J., Wang, H., Badie, N. et al. (2013). Advanced
Gupta, N., Mathur, S.C., Dumot, J.A. et al. (2012). Adequacy imaging technologies increase detection of dysplasia and
of esophageal squamous mucosa specimens obtained neoplasia in patients with Barrett’s esophagus: a meta-
during endoscopy: are standard biopsies sufficient for analysis and systematic review. Clin. Gastroenterol.
postablation surveillance in Barrett’s esophagus? Hepatol. 11 (12): 1562–1570. e1561–e1562.
Gastrointest. Endosc. 75 (1): 11–18. Sakamoto, T., Matsuda, T., Nakajima, T., and Saito, Y. (2012).
Hikichi, T., Irisawa, A., Bhutani, M.S. et al. (2009). Efficacy of endoscopic mucosal resection with
Endoscopic ultrasound-guided fine-needle aspiration of circumferential incision for patients with large colorectal
solid pancreatic masses with rapid on-site cytological tumors. Clin. Gastroenterol. Hepatol. 10 (1): 22–26.
evaluation by endosonographers without attendance of Sharaf, R.N., Shergill, A.K., Odze, R.D. et al. (2013).
cytopathologists. J. Gastroenterol. 44 (4): 322–328. Endoscopic mucosal tissue sampling. Gastrointest. Endosc.
Humphris, J.T.J., Kwok, A., and Katelaris, P.H. (2007). Cold 78 (2): 216–224.
snare polypectomy for diminutive polyps: an assessment of Trier, J.S. (1971). Diagnostic value of peroral biopsy of the
the risk of incomplete removal of small adenomas. proximal small intestine. N. Engl. J. Med. 285 (26): 1470–1473.
Gastrointest. Endosc. 69: AB207. Vogelstein, B., Fearon, E.R., Hamilton, S.R. et al. (1988).
Ichise, Y., Horiuchi, A., Nakayama, Y., and Tanaka, N. (2011). Genetic alterations during colorectal-tumor development.
Prospective randomized comparison of cold snare N. Engl. J. Med. 319 (9): 525–532.
polypectomy and conventional polypectomy for small Wang, K.K. and Sampliner, R.E. (2008). Updated guidelines
colorectal polyps. Digestion 84 (1): 78–81. 2008 for the diagnosis, surveillance and therapy of Barrett’s
Ikematsu, H., Yoda, Y., Matsuda, T. et al. (2013). Long-term esophagus. Am. J. Gastroenterol. 103 (3): 788–797.
outcomes after resection for submucosal invasive Watanabe, T., Itabashi, M., Shimada, Y. et al. (2012). Japanese
colorectal cancers. Gastroenterology 144 (3): 551–559. Society for Cancer of the Colon and Rectum (JSCCR)
quiz e514. guidelines 2010 for the treatment of colorectal cancer. Int.
Johanson, J.F., Frakes, J., and Eisen, D. (2011). Computer- J. Clin. Oncol. 17 (1): 1–29.
assisted analysis of abrasive transepithelial brush biopsies Wu, L., Li, P., Wu, J. et al. (2012). The diagnostic accuracy of
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Collaborative Group. Dig. Dis. Sci. 56 (3): 767–772. Dis. 14 (4): 416–420.
11
N
ormal Histology, Variations I nfectious Esophagitis
The esophagus has a pearly white and smooth surface Definition, General Features, Predisposing Factors
under which a network of small vessels is seen (Figure 2.1)
Infection is a common cause of esophagitis, particularly in
except for the distal esophageal sphincter where prominent
immunocompromised patients but can also occur in appar-
longitudinal and palisading vessels (exceeding 100 mm in
ently immunocompetent hosts with certain predisposing
diameter) are observed and used to define the esophago-
conditions. Fungi (Candida species) and viruses are
gastric junction.
responsible for most cases of infectious esophagitis, and
dual infections may be encountered. Bacterial, mycobacte-
Microscopic Features rial, and parasitic esophagitis (e.g. Chagas disease due to
Trypanosoma cruzi) are rarely encountered in esophageal
The esophageal mucosa is composed of a non-keratinizing
biopsy material.
flat stratified squamous epithelium, lamina propria, and
muscularis mucosae (Figure 2.2; Table 2.1). The squamous Fungal Esophagitis
epithelium is 10–20 cell layers thick measuring 300–500 μm Fungal infection due to Candida albicans is the most
in thickness. The prickle cells contain a large quantity of common cause of infectious esophagitis.
cytoplasmic glycogen, which stains positively with periodic Predisposing conditions are broad and include HIV
acid–Schiff (PAS). The basal proliferative zone, the cuboidal infection/AIDS, other immunosuppressed conditions such
or polyhedral basal and parabasal cells account for 15% or as organ transplant, prolonged corticosteroid therapy as
less of the epithelial thickness. A small number of special- well as other conditions such as diabetes, malignancy, anti-
ized cell types, including T lymphocytes, Langerhans cells, biotic therapy, acid-suppressive therapy, and pregnancy.
endocrine cells, and melanocytes are also present in the Infection due to Candida tropicalis and Candida
deep/parabasal epithelium. The lamina propria consists of (Torulopsis) glabrata has also been described, as well as
loose connective tissue with scattered inflammatory cells, infection due to other fungi such as Histoplasma capsula-
vessels, nerves, and small mucous glands. The lamina propria tum and Aspergillus species.
papillae normally extend into the epithelium for 1/3–1/2 of its
thickness. The muscularis mucosae is a thick layer of Viral Esophagitis
smooth muscle bundles oriented longitudinally. In the dis- Herpes simplex (HSV) is the most common etiology of viral
tal 1–2 cm of the esophagus, the basal zone, papillae, and esophagitis, and also occurs primarily in the setting of
intraepithelial cells may be more prominent, and include immunosuppression, such as solid organ and bone marrow
rare eosinophils. Esophageal mucosal biopsies typically transplantation, underlying malignancy, chemotherapy,
include the squamous epithelium and scant lamina propria. and HIV infection (AIDS). These patients may also have
The muscularis mucosae is seldom present, and better iden- disseminated infection at the time of diagnosis. It can also
tified in esophageal mucosal resection specimens. develop in healthy adults including pregnant women and
Gastrointestinal Pathology: Correlative Endoscopic and Histologic Assessment, First Edition. Edited by Gregory Y. Lauwers and Michael B. Wallace.
© 2021 John Wiley & Sons Ltd. Published 2021 by John Wiley & Sons Ltd.
12 Esophagus Inflammatory Conditions
Bacterial Esophagitis
Clinically significant bacterial esophagitis occurs almost
exclusively in immunocompromised patients. Secondary
bacterial colonization of areas of prior esophageal injury
Figure 2.1 Endoscopic appearance of distal esophagus with
normal squamous mucosa. and ulceration is more common. Bacterial invasion of squa-
mous mucosa or the deeper layers is required to establish a
diagnosis of primary bacterial esophagitis. Gram-positive
bacteria are the most common causative organisms (includ-
ing Staphylococcus aureus, Staphylococcus epidermidis,
Streptococcus viridans, and beta-hemolytic streptococci).
Mycobacterial Esophagitis
The rare mycobacterial esophagitis typically occurs in the set-
ting of advanced immunosuppression. Both Mycobacterium
tuberculosis complex and Mycobacterium avium complex can
be encountered.
Parasitic Esophagitis
Chagas disease involving the esophagus is an important
cause of esophageal dysfunction (dysphagia) in endemic
regions, such as Latin America. However, the organism
and its pathologic effects are typically not identified on
biopsy specimens.
Figure 2.2 Normal esophagus squamous mucosa with normal
stratified non-keratinizing epithelium.
Clinical Features and Endoscopic
Characteristics
Table 2.1 Normal esophageal mucosa. Clinical and endoscopic features are specific to each con-
dition. For candidal esophagitis, symptoms vary from
Epithelium: none (especially in patients with mild disease from
Non-keratinizing squamous epithelium chronic inhaled steroids) to severe dysphagia and
Glycogen rich odynophagia in immunosuppressed patients. Candida
10–20 cells thick (300–500 μm) appears as a white, cottage cheese-like exudate, which is
Basal proliferative zone up to 15% partially adherent to the epithelium (Figure 2.3). HSV and
Few scattered parabasal T lymphocytes and other specialized CMV both cause ulcerations. HSV ulcers are typically
cells small, 1–3 mm, whereas CMV ulcers may be both deep
Lamina propria: and wide. Biopsy yield for the virus is highest from the
Papillary length 1/3 to 1/2 of epithelial thickness
edge of HSV ulcers and from the center of CMV ulcers. In
practice, both are usually obtained. Other infections’ eti-
Muscularis mucosae
ologies may have nonspecific findings. The inflammatory
Infectious Esophagiti 13
Figure 2.3 Endoscopic appearance of white exudate typical of Figure 2.4 Debris of slough off superficial squamous
Candida albicans in a patient on chronic inhaled corticosteroid. epithelium with fungal hyphae and acute inflammation.
Microscopic Features
Candida
The biopsies typically show an active esophagitis with a
mixed inflammatory infiltrate of neutrophils, lymphocytes,
and eosinophils. Neutrophils are often present in small, Figure 2.5 PAS stain of Figure 2.4 illustrating the fungal
superficial clusters associated with parakeratosis or squa- elements of Candida albicans.
mous debris, which may be a diagnostic clue. Prominent
intraepithelial neutrophils may be associated with detached squamous cells. However, in immuno-
abscesses, erosions, or ulcerations. The inflammatory compromised hosts, deeper tissue invasion within
response may be minimal in severely immunocompro- ulcers and erosions may be seen. Candida are often
mised patients. conspicuous in routinely stained sections, although
their appearance is enhanced with periodic acid–
Yeast forms of C. albicans and pseudohyphae (with Schiff (PAS, Figure 2.5) or Grocott methenamine
refractile cell walls) are usually present in superfi- silver (GMS) stains. In Candida (Torulopsis) glabrata
cial desquamated keratin debris (Figure 2.4). The infections, only small budding yeast forms are seen,
yeast are 3–5 μm in diameter basophilic oval forms which may mimic histoplasmosis.
while the, nonseptate sausage-like pseudohyphae Candida can colonize preexisting ulcers or dam-
are 3–5 μm in diameter and are arranged perpendic- aged mucosa of any etiology, and in such cases the
ular to the epithelial surface. Occasional septate possibility of dual infection or pathology should be
hyphae can be present. The presence of psuedohy- considered. Also, when Candida yeast forms are pre-
phal and hyphal forms correlates with active infec- sent only in desquamated keratin debris unassoci-
tion. Most infections are superficial with isolated, ated with inflammation or endoscopic findings, carry
intraepithelial fungal forms, and organisms in over from an oral infection should be suspected.
14 Esophagus Inflammatory Conditions
Figure 2.6 Multinucleated basal keratinocytes typical of HSV Figure 2.7 Erosive esophagitis with prominent granulation and
esophagitis. atypical cellular elements.
Cytologic brushings are also very useful in the diag- esophagitis, CMV rarely infects the squamous epithelium,
nosis of Candida esophagitis, as the organisms are and preferentially involves endothelial cells, stromal cells,
readily identified on Papanicolaou stained smears. and glandular epithelium. Therefore, biopsies of the ulcer
bed should preferentially be performed when CMV esophagi-
Herpes Simplex (HSV) tis is suspected (Figure 2.7). CMV cytopathic effect is charac-
If HSV infection is suspected, in addition to biopsies for terized by nuclear enlargement with classic “owl eye” large
histology, fresh tissue can be sent for viral culture to con- intranuclear inclusions, and granular, eosinophilic cytoplas-
firm the diagnosis and identify strains that may be resistant mic inclusions (Figure 2.8a). Smaller, atypical intranuclear
to acyclovir. HSV infection is associated with ulceration inclusions may be present and are more subtle, simulating
and a mixed inflammatory infiltrate of intraepithelial neu- activated fibroblasts. These infected cells are best identified
trophils, eosinophils, and lymphocytes, as well as aggre- by immunohistochemical staining (Figure 2.8b). CMV may
gates of macrophages that can be a diagnostic clue. HSV coexist with HSV and Candida infection in some cases.
infects squamous cells of intact or denuded epithelium and
is best identified at the edge of an ulcer and in cells within Bacterial Esophagitis
the ulcer slough. Therefore, optimal histologic diagnosis Sheets of bacteria are typically present with associated
requires sampling of the ulcer edge rather than the ulcer necrosis and mucosal erosion, highlighted by a tissue Gram
bed. The typical viral cytopathic effects include multinu- stain. Inflammation may be scant or absent in neutropenic
cleation, ground glass nuclei, and dense intranuclear patients.
eosinophilic inclusions with a thickened nuclear mem-
brane and a clear halo (Cowdry type A inclusion bodies) Mycobacterial Esophagitis
(Figure 2.6). Viral inclusions and multinucleated cells are Histologic features include subepithelial and mural
not always identifiable in biopsies, and ancillary immuno- necrotic and non-necrotic granulomas with fibrosis and
histochemistry (IHC) staining for HSV may be required. chronic inflammation. Acid fast bacilli can be recognized
Concomitant infection of Candida, cytomegalovirus, or on Ziehl–Neelsen stain in approximately 2/3 of cases.
bacteria can exist, particularly in immunocompromised
patients. Varicella Zoster Virus has been associated with
Immunohistochemical Studies and Molecular
esophagobronchial fistula formation.
Features
Cytomegalovirus (CMV) IHC staining for HSV (HSV 1 and 2 cocktail stain) may be
Culture is not used routinely, and does not distinguish the useful for suspected infections if diagnostic inclusions are not
simple presence of CMV from active infection; however, readily identified on H&E sections. Similarly, IHC for CMV is
culture may be useful for identifying drug resistance. useful to highlight infected cells without typical CMV mor-
Ulceration and granulation tissue formation with associ- phology, and may be more sensitive than light microscopy.
ated acute inflammation is common. In contrast to HSV PCR for M. tuberculosis may be useful in selected cases.
Gastroesophageal Reflux Diseas 15
(a) (b)
Figure 2.8 High-magnification evaluation of Figure 2.7 demonstrated (a) endothelial CMV infection (b) confirmed by
immunohistochemistry.
eosinophil predominant mucosal inflammation. EOE rep- Clinical Features and Endoscopic
resents a type 2 (Th2) helper T cell and cytokine-mediated Characteristics
disorder involving genetic predisposition, environmental
Eosinophilic esophagitis (EOE) is increasing in prevalence
exposures, and allergic background. Food-based antigens
and often seasonal with spikes during typically airborne
appear to be the dominant mediators of EOE, although aer-
allergy season. It presents with dysphagia to solids, classi-
oallergens may also act as triggers in susceptible patients.
cally with pills sticking. Other atopic symptoms are com-
Since it was first established as a distinct clinicopatho-
mon. At endoscopy, the esophagus has white punctate
logic entity in 1993, EOE has become an increasingly rec-
spots (eosinophilic microabscess), rings, longitudinal fur-
ognized cause of dysphagia and esophageal dysfunction,
rows (Figure 2.12), and desquamates easily with insuffla-
particularly among patients refractory to medical treat-
tion or dilation. In late stages, the esophagus may be very
ment of gastroesophageal reflux disease.
narrowed and poorly distensible.
EOE is reported worldwide, with highest prevalence in
the United States and Western Europe. It occurs more fre-
quently in children and young adults, although it is increas- Microscopic Features
ingly recognized in older adults, and is more common in Esophageal biopsies are required to diagnose EOE.
males (male-to-female ratio of 3–4 : 1). A history of other Eosinophils are generally absent from the esophageal squa-
allergic conditions may be present, such as asthma and mous epithelium in normal individuals. The histologic
atopic dermatitis, as well as peripheral eosinophilia, which hallmark is the presence of an increased number of eosino-
are more common in children. phils within the squamous epithelium (Figure 2.13).
Current diagnostic criteria for EOE include a combina- Although there is no exact threshold number that estab-
tion of clinical and pathologic features (Table 2.3). lishes a diagnosis, 15 eos/HPF (peak count) in at least one
biopsy is considered a “minimum” threshold.
Table 2.3 Definition of eosinophilic esophagitis and diagnostic Eosinophilia may be patchy, and it is recommended
criteria.
that two to four biopsies from at least two locations in
Symptoms related to esophageal dysfunction the esophagus should be taken to maximize diagnostic
Eosinophil-predominant inflammation on esophageal biopsy, yield. The distribution of eosinophilia is important, as
characteristically consisting of a peak value of 15 eosinophils they may be identified in both proximal and distal biop-
per high-power field (EOS/HPF) sies or be more prominent in proximal biopsies.
Mucosal eosinophilia is isolated to the esophagus and persists Practically, only intact eosinophils with visible nuclei
after a PPI trial should be counted and eosinophilic granules should not
Secondary causes of esophageal eosinophilia excluded be included, although degranulated eosinophils may be
(Table 2.5) a useful clue.
A response to treatment (dietary elimination; topical Other histologic findings may be present although none
corticosteroids) supports the diagnosis of EOE, but is not of these should be considered pathognomonic. These fea-
required.
tures include moderate-marked reactive basal hyperplasia,
(a) (b)
Figure 2.12 Endoscopic appearance of eosinophilic esophagitis (a) with so-called feline esophagus appearance and (b) with
extensive white microabcesses. Subtle circular rings and longitudinal furrows also present.
Eosinophilic Esophagiti 19
Differential Diagnosis
Clinical
Dysphagia and rings in the esophagus can occur from any
inflammatory condition. Even eosinophils may be present
in GERD alone. EOE typically requires a confirmatory
biopsy from the upper and lower esophagus showing
Figure 2.13 Characteristic histology of eosinophilic esophagitis
with basal cell hyperplasia, marked eosinophilic infiltrate with
eosinophilic infiltrates. Desquamative conditions that
eosinophilic microabscesses. should be excluded include bullous pemphigoid and
lichen planus. These typically require deep biopsies and
special immunofluorescence staining; thus, communica-
tion between endoscopist and pathologist is critical.
eosinophilic microabscesses (superficial aggregates of
4 eosinophils), superficial layering of eosinophils, and Microscopic
subepithelial fibrosis. The presence of subepithelial fibro- The histologic appearance of EOE is not specific, and
sis is also associated with eosinophils in the lamina propria mucosal infiltration by eosinophils is a component of
and correlates with fibro-stenotic complications of EOE, a variety of other esophageal inflammatory conditions
but may not be identifiable depending on biopsy depth. (Table 2.4).
Other inflammatory cells, such as lymphocytes and mast GERD and PPI-responsive esophageal eosinophilia
cells, can also be increased. When reporting the cases, a exhibit considerable histologic overlap with EOE. In an
note is useful to summarize additional relevant histologic untreated patient, fewer numbers of eosinophils with dis-
features and to provide an overall assessment of the case tal predominance may be suggestive of GERD. Correlation
based on all available biopsies (including prior biopsies, if with response to PPI therapy is paramount.
applicable). For example, active esophagitis with intraepi- In eosinophilic gastroenteritis, obtaining biopsy speci-
thelial eosinophils (peak count of # per HPF) followed by a mens from the stomach and duodenum and other clinical
note. When large numbers of eosinophils are present (e.g. symptoms such as nausea, vomiting, and diarrhea may be
>40 per HPF), an exact count may be difficult and it is helpful in establishing a diagnosis.
appropriate to report the peak count as such (e.g. “peak The presence of granulomas is helpful in diagnosing
count of >40 per HPF”). esophageal involvement by Crohn’s disease, but they are
uncommon. Eosinophils may also be admixed with neutro-
phils and lymphocytes, and involvement of other parts of
Immunohistochemical Studies and Molecular
the GI tract is typically present.
Features
Infections are recognized by the identification of viral
Currently, the examination of esophageal mucosal biopsies inclusions (such as HSV), and fungal or parasitic organ-
by hematoxylin and eosin (H&E) stained sections, with isms. Mixed inflammation with neutrophils may also be
clinical correlation, remains the most reliable diagnostic present. Rare cases of HSV esophagitis occurring in a back-
test for EOE. The diagnostic value of ancillary studies in ground of EOE have been described.
20 Esophagus Inflammatory Conditions
Table 2.4 Endoscopic and histologic features of the major causes of infectious esophagitis.
Table 2.5 Conditions associated with esophageal eosinophilia Elimination Diet; SFED) or suppression with topical corti-
in the differential diagnosis of EOE. costeroids, which can be from a swallowed metered dose
inhaler, or from peroral viscous budesonide. For late-stage,
GERD
fibrotic disease, repeated, carefully monitored esophageal
PPI-responsive esophageal eosinophilia
dilation is effective.
Eosinophilic gastrointestinal diseases
Crohn’s disease
Infection (Candida, HSV, parasites)
Hypereosinophilic syndrome L
ymphocytic Esophagitis
Achalasia
Definition, General Features, Predisposing
Drug hypersensitivity injury
Factors
Vasculitis
Pemphigus This uncommon and poorly characterized condition is his-
Connective tissue diseases tologically defined as the presence of dense lymphocytic
infiltrates involving the esophageal mucosa without con-
Graft versus host disease (GVHD)
comitant evidence of significant active inflammation. It is
described in approximately 1/1000 esophageal biopsies,
In drug-induced esophageal eosinophilia, there is a tem- predominantly affecting older females (median age
poral relationship and resolution when the offending agent 63 years). This controversial entity lacks clearly defined
is withdrawn. clinical associations in adults, and likely represents a non-
specific reaction pattern to a wide variety of mucosal
Ancillary Studies (if Applicable) insults (Table 2.6), including GERD, medications, infec-
IHC for virus (HSV) and/or special stains for fungi (GMS, tion, motility disorders, and other immune-mediated dis-
PAS-diastase) are indicated if infection is suspected. orders. In the pediatric population, lymphocytic esophagitis
has been described in association with Crohn’s disease and
celiac disease.
Prognosis, Evolution, and Clinical
Management
Clinical and Endoscopic Characteristics
EOE is initially treated with proton pump inhibitors. There
is emerging evidence that PPIs affect specific inhibition of About 75% of patients present with esophageal symptoms,
the chemokine, eotaxin, which blunts eosinophil infiltra- most commonly dysphagia or odynophagia, which may
tion. It may be difficult to distinguish GERD-associated raise the suspicion of eosinophilic esophagitis. Similarly,
eosinophilia from EOE in this subgroup. For those that do the endoscopic impression may suggest eosinophilic
not respond to PPI, options include identification and esophagitis, with the presence of rings, furrows, plaques,
avoidance of food antigens (typically through a Six Food and strictures.
Drug-Induced Esophagiti 21
Prognosis
Follow-up clinical and biopsy data are limited, although in
some patients sequential biopsies have demonstrated per-
sistent lymphocytosis, suggesting a chronic process.
D
rug-Induced Esophagitis
(a) (b)
Figure 2.16 (a) Iron tablet erosive esophagitis with fibrinopurulent debris. (b) The Prussian Blue iron stain is diagnostic.
recognized by characteristic viral cytopathic effect. In rare appearance to the mucosa. Sloughing esophagitis has also
cases, exuberant granulation tissue and excessive exudates been included under the terms esophagitis dissecans super-
mimic the gross appearance of a neoplasm. If eosinophils ficialis and acute necrotizing esophagitis, which includes
are prominent, reflux or eosinophilic esophagitis may broader inclusion criteria and more diverse causes of
enter into the differential diagnosis. GVHD should be esophageal injury. It occurs in middle-aged to older adults
excluded if prominent apoptosis is present, such as with (median age 56 years), frequently with debilitating comor-
mycophenolate injury. Finally, lichen planus involvement bidities and who are commonly on multiple medications,
of the proximal esophagus with stricture formation can especially central nervous system depressants and drugs
also mimic drug injury. In all of these considerations, the known to cause esophageal mucosal injury. It most likely
clinical context is critical to the evaluation of the histo- represents a form of direct contact injury, rather than an
pathologic findings. ischemic injury, and may represent a unique pattern of
drug-induced esophagitis. Acute necrotizing esophagitis
Prognosis, Evolution and Clinical Management (“black esophagus”) is a rare condition that arises in debili-
tated patients with severe comorbidities such as hypoper-
Most cases are self-limited and resolve without complica- fusion, sepsis, diabetic ketoacidosis, and malignancy, and
tions. Discontinuing the suspected caustic agent and sup- results from the combining effect of ischemia and corrosive
portive management, such as PPI therapy, hydration, injury of gastric contents. A rare case occurring in a child
sucralfate, or topical anesthetics, typically results in an who was associated with a history of vomiting has also
uneventful recovery. Local epinephrine may be needed for been reported.
active bleeding. Dilatation may be required if strictures
develop, and surgical management is rarely needed for
severe complications such as perforation. Most patients Clinical and Endoscopic Characteristics
can resume their medications with recommendations for Dysphagia, odynophagia, chest pain, heartburn, vomiting
proper administration, which will assist in avoiding recur- or cough are reported in 45% of patients, include. The mid-
rent injury. distal esophagus is most commonly involved. Endoscopy
reveals white plaques or membranes, and there may be
sloughing of the epithelium as well as other nonspecific
S
loughing Esophagitis
findings such as erythema, erosions, rings, or webs. In
black esophagus, the sloughing necrotic membrane may
Definition, General Features, Predisposing
appear blackened (Figure 2.17). The clinical presentation is
Factors
distinctive with bleeding and a characteristic diffuse cir-
Sloughing esophagitis is characterized by extensive super- cumferential black mucosal discoloration of the distal
ficial squamous mucosal necrosis or desquamation, associ- esophagus with an abrupt transition at the gastroesopha-
ated with endoscopic plaques imparting a sloughing geal junction.
Another Random Document on
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of houses, or a sharp bend in the road, a barricade may be made in
one part and a passage round one end left for traffic.
Inundations. They may be formed by damming streams at
convenient points, specially in the valleys, or by damming up the
arches of bridges. In the latter case, care must be taken not to
endanger the stability of the bridge. The ditches of field works form
a good obstacle when flooded. Destroyed trenches in front of a
breastworks may be filled with water, and with barbed wire thrown
into it, will prove an effective obstacle.
Fougasses. These are used in connection with obstacles and are
really land mines loaded with stones, bricks, etc. An excavation is
made in conical shape with an axis inclined to about 40 degrees
toward the enemy horizon. A box of powder is then placed in a
recess at the bottom and on the box is placed a wooden platform or
shield 3 to 4 inches thick, over which stones are piled.
A fuse is placed in a groove cut at the back of the excavation. A
line of least resistance must be so arranged that by placing the
excavated earth on the back edge of the fougasse, the powder will
act in the direction of the axis and not vertically. A fougasse charged
with 80 pounds of powder may be constructed in this manner to
throw five tons of brick and stone over a surface about 160 yards
long by 120 yards wide.
All of the foregoing are labors of working parties, as well as
construction of dugouts, carrying of supplies, ammunition, etc.,
drainage and building of the trenches and the many other jobs
behind the lines. Always, no matter how small the job, careful
forethought must be given to the planning and arrangement
necessary to carry it out.
ORGANIZATION OF BOMBING
SQUADS
Every infantry soldier must and does receive instruction in
grenade throwing. Some men do not possess the temperament and
qualifications necessary to make efficient bombers, and for this
reason in every platoon there should be a bombing squad of one
N. C. O. and 8 men, with a higher degree of training and efficiency
as bomb throwers than the remainder, although all hope must not be
given up for the remainder.
These men are available either to work with the platoon or to
provide a reserve of bombers for any special job, such as raids,
cutting-out parties, and clearing trenches just occupied. Only the
very best men in each platoon should be chosen, taking into
consideration physique, courage and steadiness, although it is not
always the big man physically that makes the best bomber. The
responsibility for the training of these men rests with the battalion
and company commanders.
TRAINING
The first step is to overcome a man’s natural fear of the grenade
itself. This is only done by explaining how it is to be used, the
method of lighting and the length of time taken for the fuse to burn.
A good idea is to have some of the fuses of the length used lighted
and the men told to count while the fuse burns out. Dummy
grenades with fuses attached can then be introduced and the men
taught to light them, observing carefully how long it takes for the
fuse to burn down to the grenade.
The second step is to develop accuracy in throwing. Normally,
the bomb should be bowled overhand, although it is certainly not
wrong to throw, but it has been found in tests that a man throwing
bombs has tired a great deal quicker than a man bowling them
overhand.
Stick grenades may be thrown over short distances like a dart,
although this is unhandy and can only be done by a carefully trained
man. Great care must be taken while in the trenches in throwing
percussion bombs, as very often a man swinging his arm back to
throw such a bomb has exploded it in the trench, with disaster to
himself and those near him.
Men should be taught to throw standing, kneeling and prone. It
should be impressed upon them from the beginning that if a
grenade with a time fuse is dropped in the act of throwing there is
ample time to pick it up and throw it out of the trench before it
explodes, but this must be done immediately.
A B
* * * * *
Second bombing party—
Formation as above. The head of the party must be in
touch with the rear of the first party. Officer
commanding in rear of second party.
* * * * *
Third and fourth bombing party—
Formation as above. Second in command in touch with
rear of fourth party.
Machine gun detachment, if available or considered
necessary.
1
The Nobel lighter consists of two cardboard
tubes, one fitting over the other. Inside the top
end of the outer tube there is a layer of friction
composition; fixed to the top end of the inner
tube is a forked brass friction head, which is held
in position by a safety pin fastened through both
tubes. Inside the other end of the inner tube is a
small copper band, into which the fuse is fitted.
At the joint of the two tubes there is a narrow
tape band with a loose end. To light the fuse,
pull off tape and safety pin, then press down
outer tube and turn slightly. This lighter has a
five-second fuse attached.