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R: Right
Appendiceal Adenocarcinoma
https://t.me/medicina_free
Incidental
Finding
After
Appendectomy
Biopsy
(if Possible)
Found on
Imaging or
Colonoscopy
Appendiceal
Adenocarcinoma
H&P
CT C/A/P or MRI
A/P and CT
Chest,
CEA, CA19-9,
CA125, CRP,
Consider
Colonoscopy
Tumor Board
Consultation
Concerning
Radiologic
Features/
Laparoscopic
Evidence for
Peritoneal
Disease
Extraperitoneal
Disease
Consider
Clinical Trial or
Systemic
Therapy
Complete
Cytoreduction
Predicted
Incomplete
Cytoreduction
Predicted
Reassess for
Response
LARGE BOWEL
CRS + IPCT (Well-Differentiated Preferred)
Selective R Hemicolectomy*
CRS + IPCT
R Hemicolectomy
3 mo
Systemic Therapy
6 mo
Systemic
Therapy 3-6 mo
Node Positive
Systemic Therapy
6 mo
CRS + IPCT
R Hemicolectomy
CRS + IPCT
R Hemicolectomy
Progression
Response/
Complete CRS
Predicted
Systemic Therapy 3 mo
Second-Line Chemotherapy/
Clinical Trial/
Best Supportive Care
CRS + IPCT
R Hemicolectomy
Consider
Systemic
Chemotherapy
269
Systemic
Therapy 3 mo if
Received 3 mo
Prior to CRS
*If well-differentiated mucinous adenocarcinoma pathology
is confirmed by expert pathologist, then observation may be
considered (no R hemicolectomy). High-grade appendiceal
mucinous neoplasms and well-differentiated mucinous
adenocarcinoma may be treated similar to low-grade lesions.
CA19-9: Carbohydrate Antigen 19-9
CA125: Cancer Antigen 125CEA: Carcinoembryonic Antigen
CRP: C-reactive Protein
CRS: Cytoreductive Surgery
CT C/A/P: Computed Tomography of Chest/Abdomen/Pelvis
H&P: History and Physical
IPCT: Intraperitoneal Chemotherapy
MRI A/P: Magnetic Resonance Imaging of Abdomen/Pelvis
No Metastatic
Disease
peritoneal disease (cytology/gross),
consult “Peritoneal Disease” pathway
Right
Hemicolectomy*
If any intraoperative concern of
above
Node Negative Observe
FIG. 2 The 2018 Chicago Consensus Guidelines on the Management of Appendiceal Adenocarcinomas. (From Chicago Consensus Working Group.The Chicago
consensus on peritoneal surface malignancies: standards. Cancer.2020;126:2516–2524.)
the CRS group (24% vs. 13%, respectively). The results of these
studies on prospective clinical trials highlight the need for a multidisciplinary approach to selecting patients who will maximally
benefit from CRS versus HIPEC+ CRS. It also highlights the benefit
of cytoreduction in combination with NACT.
should include a thorough history and physical examination along
with axial imaging including CT of the chest, abdomen, and pelvis.
PET/CT may be useful in patients with non-mucinous tumors. Laboratory workup includes CEA, CA-19, and CA-125 levels and nutritional markers. A complete colonoscopy is also recommended if not
already completed. Diagnostic laparoscopy may be helpful for staging
Epidemiology
Peritoneal disease is present in about 8% of CRC patients at the time
of primary resection, and up to 25% of patients with recurrent CRS
will develop metastatic disease confined to the peritoneal surface.
Risk factors for peritoneal metastases include mucinous histology,
T4 cancers, vascular invasion, spontaneous or iatrogenic perforation,
and right-sided tumors, which overall confer a worse prognosis. The
presence of untreated visceral solid organ metastasis is a relative
contraindication to HIPEC and CRS.
and assessment of surgical eligibility given the poor sensitivity of axial
imaging for detecting peritoneal metastasis. In addition, small tumors
in specific locations such as the root of the mesentery and serosal surface of the small bowel are harder to detect on CT scan. PET/CT has a
sensitivity of 78% to 100% and is not uncommonly ordered before surgery. It is however associated with false-negative results for tumors that
are not PET/CT avid (mucinous tumors) or false-positive results for
inflammatory processes. There have been limited studies evaluating
the role of diffusion weight MRI in detecting subcentimeter deposits
in difficult anatomic locations, though it is not widely adopted given
the contraindications, costs, and availability.
Clinical Manifestations
Peritoneal metastases secondary to CRC may present with ascites
manifesting as increasing intraabdominal girth, pain, or small bowel
obstruction. However, just as often, synchronous peritoneal disease
may be asymptomatic and detected at the time of primary surgery
or on staging imaging. For patients with metachronous disease, it is
most common to identify peritoneal metastases during surveillance
given the intensity of imaging use in current practice.
Preoperative Workup
Patient selection is very important in determining the appropriateness of cytoreductive surgery and HIPEC. Preoperative evaluation
Patient Selection for Surgery
Patient selection is critical in determining who would most benefit
are patients with good performance status who have an ECOG/WHO
status of 1 or less, have adequate physiologic and organ function,
have a low/moderate PCI, and can receive systemic chemotherapy.
In fact, response to initial chemotherapy is often used as prognostic
marker to screen patients with rapidly evolving tumor biology. PCI
scores range from 0 to 39, with a score less than 12 considered most
favorable for resection. A PCI greater than 20 is typically considered
a contraindication to resection. Patients with a PCI between 12
and 20 may be determined on a case-by-case basis depending on
270 MANAGEMENT OF PERITONEAL SURFACE MALIGNANCIES
PET: Positron Emission Tomography
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Colorectal Cancer with Synchronous Peritoneal Metastasis
Newly Diagnosed
Colorectal
Adenocarcinoma with
Peritoneal Metastasis
Synchronous
H&P
CT C/A/P +/–MRI +/– PET
Complete Colonoscopy
with Biopsies
Pathology Review
Determine MSI, KRAS,
and BRAF Status
Pelvic MRI for Rectal
Cancer
CEA
Tumor Board
Consultation
CEA: Carcinoembryonic Antigen
CT C/A/P: Computed Tomography of Chest/Abdomen/Pelvis
CRS: Cytoreductive Surgery
H&P: History and Physical
IPCT: Intraperitoneal Chemotherapy
MRI A/P: Magnetic Resonance Imaging of Abdomen/Pelvis
MSI: Microsatellite Instability
PCI: Peritoneal Carcinomatosis Index
Peritoneal
Metastases
Only*
Widespread and/or
Unresectable Solid-
Organ Metastases
Patients with Resectable Liver and/or
Lung Metastases in the Context of
Associated
CRS +/– IPCT for
Selected Patients with
Low PCI
Chemotherapy for
3–6 mo
+/– Chemoradiotherapy
for Rectal Cancer
*Refer to Principles of Surgery for
Peritoneal Metastasis
Consider Palliative Surgery for
Symptomatic Patients
Restaging
Imaging
Systemic Chemotherapy
Best Supportive Care or
Clinical Trial
No
Progression
Progression
Consider
Diagnostic
Laparoscopy
Assess PCI,
Obtain
Biopsies as
Needed
Complete
Cytoreduction
Predicted
Incomplete
Cytoreduction
Predicted
Complete
Cytoreduction
Predicted
Incomplete
Cytoreduction
Predicted
CRS +/– IPCT
Finish First-Line or
Second-Line
Chemotherapy
Best Supportive Care
or Clinical Trial
Consider CRS +/– IPCT
Second-Line
Chemotherapy
(Preferred) or Best
Supportive Care or
Clinical Trial
Consider
Immunotherapy for
Patients with MSI-
High Tumors
Chemotherapy
(Total 6 mo),
Then Follow-Up
Reassess for
Potential CRS
Chemotherapy
(Total 6 mo),
Then Follow-Up
Reassess for
Potential CRS
FIG. 3 The 2018 Chicago Consensus Guidelines on the Management of Colorectal Cancers with Synchronous Peritoneal Metastasis. (From Chicago
Consensus Working Group.The Chicago consensus on peritoneal surface malignancies: standards. Cancer.2020;126:2516–2524.)
additional clinical parameters, such as extent of extraperitoneal
metastasis and tumor biology. A more conservative PCI cutoff of 17
has been proposed based on results of a prospective study by Goere
young age, and female gender. Prognosis of untreated gastric cancer
with peritoneal carcinomatous is quite poor, with a median 5-year
survival that approaches 0%.
et al., which showed no benefit of HIPEC + CRS in patients with
a PCI greater than 17. It is important to note that a preoperative
radiologic PCI score may not always correlate with an intraoperative PCI score, hence staging laparoscopy can be used as an adjunct
to assess borderline cases. The presence of malignant ascites, large
tumor burden, or multifocal bowel obstructions are relative contraindications to curative intent surgery in addition to the presence
of liver or lung metastasis that are untreated. Visceral metastases
should be considered for therapy on an individualized basis. Lastly,
the treatment options and timing for patients with synchronous or
metachronous lesions similar to appendiceal neoplasms should be
discussed among a multidisciplinary team. Figure 3 summarizes
the Chicago Consensus Guidelines on CRS and HIPEC in colorectal cancers.
Preoperative Workup
Preoperative workup includes history and physical examination,
upper endoscopic ultrasound, and endoscopic ultrasound with
biopsy for local regional staging. Imaging includes CT of the
chest, abdomen, and pelvis with contrast and PET/CT if there is
no evidence of M1 disease. HER2/NEU testing should be obtained
if metastatic disease is suspected. Molecular profiling to assess
for microsatellite stability and PDL1 positivity maybe helpful for
patients with unresectable disease. Genetic counseling is recom-
mended in young patients to evaluate for CDH1 mutations given
their high penetrance. Nutritional markers should be considered
in addition to smoking cessation and counseling. Patients typically
receive the most commonly used perioperative chemotherapy,
GASTRIC CANCER
Epidemiology and Clinical Manifestation
which includes FOLFOX, XELOX, FLOT, ECF, +/– radiation for 3
to 6 months followed by restaging and diagnostic laparoscopy with
peritoneal washings. Patients with advanced tumors, clinical T3
or greater, or node-positive disease should undergo laparoscopic
mortality rate of 8.9% after lung cancer (19.7%) and breast cancer
(12.9%), respectively. Overall 5-year survival approaches 90% in
staging with peritoneal washings to evaluate for extent of peritoneal
disease.
countries like Japan and varies between 10% and 30% in Western
countries. Peritoneal carcinomatosis occurs synchronously with
primary tumors in 14%% to 43% of patients with gastric cancer and
accounts for 35% of synchronous metastasis. Risk factors for peritoneal metastasis include extranodal involvement, diffuse infiltrated
type, signet cell histology, higher CEA levels, liver involvement,
Patient Selection for Surgery
All patients with biopsy-proven gastric cancer should be presented
to a multidisciplinary tumor board to discuss a tailored treatment
plan, which is largely dependent on the patient’s functional status and
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271
tumor biology. Generally, patients with low peritoneal disease burden
and lack of progression of disease after systemic therapy should be
restaged and considered for HIPEC + CRS. Various options include
early postoperative chemotherapy (EPIC) or bidirectional intraperitoneal and systemic induction chemotherapy before CRS + HIPEC.
Ideal candidates should be young (<70 years of age) and have a good
performance status, a PCI score <10, small nodules, a resectable primary tumor, no evidence of paraaortic lymphadenopathy, no liver or
extraperitoneal metastasis, and have responded well to NACT.
Hoptopp et al. found an overall increase in survival in patients
with gastric cancer and confirmed peritoneal metastasis who
underwent NACT with FLOT followed by CRS + HIPEC versus
chemotherapy alone (17 months vs. 6 months) in a single-center
study. A more recent advancement is the use of neoadjuvant intraperitoneal and systemic chemotherapy protocol/bidirectional intraperitoneal and systemic induction chemotherapy (NIPS/BISIC),
which aims to reduce the stage and increase the incidence of complete cytoreduction. By simultaneously administering intravenous
and intraperitoneal chemotherapy, the cancer cells are targeted
both from the peritoneal cavity and subperitoneal blood vessels.
Several studies have examined the effectiveness of this therapy in
complete cytoreduction and improving survivorship. Yonemura et
al published a prospective study of 194 patients who had BIPSC
followed by CRS + HIPEC. Patients had (1) biopsy-proven peritoneal carcinomatosis, (2) no evidence of liver or lung metastasis, and
(3) good performance scores. In this study, 152 patients responded
to BIPSC and subsequently underwent CRS + HIPEC. Complete
cytoreduction was achieved in about 70% of these patients. Median
survival was 15.8 months in patients who had CRS + HIPEC after
BIPSC versus patients who did not (7 months). Completeness of
cytoreduction, pathologic response to NIPS, and PCI on multivariate analysis overall predicted survivorship. It is important to note
that the complication rate was 24%, which is similar to that found
in a study by Hultman et al., which also showed an improvement
in median survivorship (19 months vs. 14 months) but reported a
higher complication rate of 63%. This is most commonly caused
by anastomotic leak, sepsis, wound infections, and organ failure.
These studies show that appropriate patient selection and identification of patients with unresectable or disseminated disease who
are eligible for complete cytoreduction is paramount.
PERITONEAL MESOTHELIOMA
Epidemiology and Clinical Manifestation
Mesothelioma is a rare malignancy of serosal membranes. This
includes the pleura, peritoneum, pericardium, and the tunica vaginalis testes.The peritoneum is the second most common location
and is estimated to represent about 10% to 15% of all mesotheliomas. The highest incidence is reported in countries such as
New Zealand, the United Kingdom, and Australia, and the lowest
incidence is reported in countries such as Japan, Slovenia, and
Central Europe. The estimated incidence is 1.94 per 100,0000 and
0.41 per 100,000 for men and women, respectively, in the United
States. Mesothelioma is commonly associated with exposure to
asbestos, but 33% to 50% of patients diagnosed with malignant
pleural mesothelioma (MPM) have no prior asbestos exposures.
Other risk factors include exposure to radiation minerals such as
thorium, chronic peritonitis, and germline BRCA-1–associated
protein (BAP-1) gene mutation. Histologic classifications include
epithelioid, sarcomatous, and biphasic/mixed. About 75% of all
mesotheliomas are epithelioid in origin, which overall have the
most favorable prognosis.
Perioperative Workup
Making the diagnosis is often challenging as patients present with
mostly vague abdominal symptoms. On imaging, patients may
have ascites, evidence of omental caking, or mesenteric fatty infiltration. Definitive diagnosis is based on histology and pathologic
assessment, which could be obtained on percutaneous biopsy or
diagnostic laparoscopy. Diagnostic laparoscopy is indicated to
evaluate the extent of disease amenable to surgery. Pathologic
assessment is essential to differentiating subtypes of mesothelioma that may be more amenable to surgery versus chemotherapy alone. Epithelioid histology has overall the most favorable
response to HIPEC + CRS in contrast with sarcomatoid, biphasic
subtypes, which overall have a poorer prognosis and for which
surgery is less likely to offer a survival benefit. Furthermore, the
CA-125 and Ki-67 index are often obtained in addition to germline testing for a BAP-1 gene mutation.
Patient Selection for Surgery
The natural history of MPM is aggressive; without treatment,
median survival is approximately 6 months. Median survival with
systemic chemotherapy alone is approximately 16 months; however, it improves to approximately 40 months with HIPEC + CRS.
Patients with MPM are considered for surgical therapy with CRS/
HIPEC if their disease burden is amenable to resection of all or
nearly all (CC-0 or CC-1) visible disease and are suitably fit for
such extensive resection.
OVARIAN CANCER
Epidemiology and Clinical Manifestation
Ovarian cancer is associated with one of the highest mortalities
from gynecologic cancers in the world, with an estimated 5-year
survival rate of 39%. Despite efforts to screen for ovarian cancer,
35% to 43% of patients still present with advanced disease involving
the peritoneum at the time of diagnosis. Risk factors for peritoneal
disease include germline mutations, incomplete resection at initial
cytoreductive surgery, shorter treatment-free survival, higher FIGO
(International Federation of Gynecology and Obstetrics) stage, and
the present of malignant ascites. The most common type of ovarian
cancer is epithelial in origin; less common types include clear cell,
mucinous, carcinosarcoma, endometroid carcinoma, and malignant
germ cell tumors. Symptoms include early satiety, bloating, nonspecific abdominal pain, and urinary symptoms. Others may present
with massive ascites, which is typically associated with mucinous
neoplasms.
Preoperative Workup
The diagnosis is made based on clinical suspicion, imaging, and
tumor markers, with elevation of CA-125, inhibin, B-HCG, LDH,
and CEA levels being pathognomonic. Nutritional parameters, CBC,
and liver function tests and chemistries are routinely ordered. A
complete colonoscopy is recommended to evaluate for synchronous
gastrointestinal malignancies that can present similarly. Genetic
counseling is recommended for all patients given the incidence of
BRCA mutation, which may help guide adjuvant systemic therapy.
Surgery is the mainstay therapy and typically includes extensive
debulking and cytoreduction with a total abdominal hysterectomy
and bilateral salpingo-oophorectomy (TAH + BSO) but can include
appendectomy, colon or small bowel resection, cholecystectomy, and
omentectomy. Diagnostic laparoscopy is essential to quantify tumor
burden and identify patients whose disease is amenable to adequate
cytoreduction. The presence of omental caking, peritoneal and diaphragmatic extensive carcinomatosis, mesenteric retraction, bowel
and stomach infiltration, and spleen and/or liver superficial metastasis are typically assessed on laparoscopy. Importantly, these operations are typically conducted using a multidisciplinary approach
involving gynecology oncology and surgical oncology to improve the
chances of complete cytoreduction.
272 MANAGEMENT OF PERITONEAL SURFACE MALIGNANCIES
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Patient Selection for Surgery
HIPEC is typically considered in patients with stage III disease of
epithelial origin as the other cell types are less chemosensitive. Furthermore, NACT with interval CRS is considered in patients with
advanced-stage ovarian cancer who are not good candidates for
upfront primary debulking surgery (PDS) because of advanced age,
frailty, poor performance status, or for those in whom the disease
is unlikely to be optimally cytoreduced. This has the potential to
facilitate medical optimization and to downstage the disease. The
addition of HIPEC to CRS has been evaluated in several studies
in the recurrent setting. In a 2015 RCT, Spilotis found a 13-month
improvement in survival with HIPEC + CRS versus CRS alone. In
a retrospective cohort study of 584 patients with stage III epithelial
ovarian cancer, Lei et al. found an overall 15-month improvement
in survival in patients undergoing CRS + HIPEC versus CRS alone,
and patients with complete CRS had the most favorable survival
outcomes. In an RCT of 245 patients randomized to HIPEC + CRS
versus CRS alone, Van Driel et al. found an increase in overall
median survival in the HIPEC + CRS group at 45.7 months versus
33.9 months in the CRS group alone. The CHIPPI-1808 trial comparing HIPEC + NACT + CRS versus NACT + CRS should have
results by 2026 and perhaps may help improve patient selection and
justify the use of upfront HIPEC in the primary setting versus the
current standard of care, which is typically in the recurrent setting
with interval CRS.
Intraoperative Management and Technique
The Chicago Consensus Working group publishes a consensus
on peritoneal surface malignancies that includes guidelines for
standard operations and metrics. Generally speaking, a fellowship
experience with CRS + HIPEC, documentation of number of
cases, and availability of two surgeons are necessary in addition
to established criteria for institutional credentials. Process standards include confirmed tissue diagnosis, relevant tumor markers
depending on the cancer type, cross-sectional imaging, and ideally
registry of all patients in a data repository. Quality standards also
exist for reporting of pathology, intraoperative monitoring, perfusion equipment used, and rating of the completeness of intraoperative cytoreduction. A complete list of standards, quality, and
process measures is available online.
Preoperatively patients undergo mechanical bowel preparation
with oral antibiotics before surgery. Patients are positioned supine
for lithotomy if any concern of needing lower pelvic work; DVT
prophylaxis with SCDs and subcutaneous heparin in addition to
perioperative IV antibiotics are administered. It is important to
maintain good communication with anesthesia and the intraoperative room staff to ensure that the patient’s core body temperature is
maintained and that the patient is adequately being resuscitated to
maintain good urine output given insensible losses that can occur
during the operation. Adequate monitoring of cardiovascular and
fluid resuscitation is crucial in the intraoperative and postoperative
period. If not closely monitored and managed, patients are at risk
for abdominal hypertension, coagulopathy, decreased systemic
vascular resistance, and high-output cardiac failure in addition
to toxicities directly related to the chemotherapy agent being
used. Therefore, early determination of the need for recovery in
the intensive care unit (ICU) should be determined intraoperatively. Increasingly, intraoperative goal-directed fluid therapy and
enhanced recovery pathways have been implemented in various
institutions with the goal to improve postoperative outcomes. For
example, tools such as stroke volume variation are used to guide
fluid management and maintain urine output. This strategy overall
leads to less overall fluid administration and is associated with less
postoperative morbidity.
The procedure begins with an exploratory laparotomy with
complete evaluation of the extent of peritoneal metastasizes and
probability of complete cytoreduction through a midline incision.
Diagnostic laparoscopy may be undertaken before laparotomy if
there is concern that the extent of disease may preclude cytoreduction. Lysis of adhesions may be required if the patient already had
prior surgeries or malignant adhesions that may preclude safe entry.
A pre-cytoreduction PCI is assessed followed by complete cytoreductive surgery with the intent of removing all tumors greater than 0.25
cm. (CC-0 or CC-1). We generally inspect systematically the bilateral
diaphragm surfaces, lesser sac, small bowel and its mesentery, porta
hepatis, aortocaval groove (IVC bursa) near the caudate and pelvis,
and all solid organs. Once all sites have been inspected, we recommend running the small bowel in its entirety from the ligament of
Treitz to the ileocecal valve as well as inspecting the right and left
colon and its mesentery to the level of the sacral promontory. All
prior anastomoses should also be inspected in addition to incising
the nodal tissue at the ligament of Treitz, falciform ligament, and
triangular ligament for liver mobilization. Small lesions can be
removed sharply, but larger lesions that are infiltrative or cannot be
separated easily require formal resection. Generally, extensive small
bowel disease or nodal disease involving the root of the mesentery
are contraindications to complete cytoreduction. Complete cytoreduction typically requires an omentectomy, selective peritonectomy,
and visceral resection.
For HIPEC, most units prefer a closed technique, which overall
reduces exposure of the operative room team and decreases heat
dissipation. Other institutions utilize an open technique for delivery.
Mitomycin C, oxaliplatin, or doxorubicin is typically used. Selection
of the type of chemotherapy agent is typically based on tumor histology and institutional protocol. Several studies have shown no difference in progression-free survival comparing HIPEC with mitomycin
C versus oxaliplatin, the two most used chemotherapy agents. These
studies also suggest differences in side-effect profiles, suggesting that
more studies are needed.
The inflow and outflow cannulas as well as a temperature probe
are placed into the abdomen, and the incision is temporary closed.
Using a hyperthermia perfusion pump, 3 to 6 L of warm fluid is
instilled until abdominal distension based on intraoperative determination of peritoneal volume. The fluid is heated to about 40° to
43°C. Once the target temperature is achieved, the chemotherapy
agent is infused over 30 to 120 minutes. Once this is complete, the
abdomen is opened and reinspected. There is no known difference
in outcomes based on anastomosis pre- or post-HIPEC. The fascia
is closed, and a completeness cytoreduction score is assigned at the
end of the case. In early postoperative intraperitonealchemotherapy
(EPIC), the abdomen is filled with 1 L of lactated Ringer solution,
then mitomycin +/– cisplatin is given continuously or on postoperative day 1 and 2 at varying doses. In NIPs + HIPEC + CRS, patients
are given intravenous chemotherapy preoperatively and administered docetaxel and/or cisplatin intraperitoneally on day 1 and day
8. This is repeated three times, and laparotomy with cytoreduction is
performed 2 weeks after the last administration of intravenous chemotherapy. These alternatives have shown some promising results in
select populations.
Postoperative Management
Depending on institutional support (e.g., nursing levels, telemetry) patients are admitted to the floor, step-down unit, or ICU.
Patients with larger cytoreductions or significant comorbidities
benefit from ICU management. Patients are generally at risk of
postoperative ileus. Commonly, a nasogastric tube is placed at the
time of surgery. Early ambulation and incentive spirometry are
strongly encouraged. If extensive diaphragm stripping or resection
is performed, some patients with respiratory comorbidities may
benefit from chest tubes. Patients are typically managed with fluid
restriction after the initial resuscitative phase, which typically is in
the first 72 hours. Early discontinuation of intravenous fluids when
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273
tolerating a regular diet and/or adequately resuscitated is encouraged. Though ERAS protocols for HIPEC + CRS have not been
widely adopted, they do show some promising results in reducing
length of stay for patients undergoing HIPEC + CRS, though no
RCT has been conducted to date. In general, patients remain in
the hospital until they have adequate return of bowel function and
pain control. Initially some patients may have electrolyte and metabolic derangement caused by fluid shifts and should be monitored
closely. Risk factors associated with increased risk of complications
include number of anastomosis performed, diaphragm resection,
number of blood transfusions required, and thermal bowel injuries.
Overall postcomplication rates are described between 10% and
40%, depending on the series. Average length of stay is approximately 7 to 10 days. Advanced age, malnutrition, and multiple
visceral resections are associated with an increased length of stay,
hence early intervention to identify patients at most risk is crucial
to obtaining quality long-term outcomes for HIPEC and CRS.
S u g g e S t e d R e a d i n g S
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Management ofLower
Gastrointestinal
Bleeding
Anna Liveris, MD, and Peter Muscarella II, MD
INTRODUCTION
Lower gastrointestinal bleeding (LGIB) is a frequently encountered
and complex clinical problem for surgeons. Classically defined as
gastrointestinal (GI) bleeding emanating from any point distal to
the ligament of Treitz, LGIB can originate anywhere from the small
bowel to the anus and accounts for an estimated 30% of all GI bleeding. Nearly all LGIB can be isolated to the colon and rectum, with
diverticular bleeding being the most common cause. Less than 10%
of LGIB originates from the small bowel or anus. Aggressive resuscitation, accurate localization, and control of bleeding are the primary
goals of treatment for patients who present with hemorrhagic shock.
A systematic approach to diagnosis and management is pivotal in
reducing morbidity and mortality.
Etiology
LGIB can be further categorized as massive, moderate, or occult.
Massive bleeds are the most life-threatening, with mortality rates
approaching 20%. Despite this, more than 80% of all LGIB will
resolve spontaneously, and the overall mortality rate is about 4%.
Patients presenting with massive LGIB are usually >65 years and
present with hematochezia or bright red blood per rectum in the
setting of hemodynamic instability. The most common causes are
diverticulosis and angiodysplasia. Interestingly, one-third of patients
with presumed massive LGIB will have an upper GI source, so assessing for risk factors of peptic ulcer disease is important.
Moderate and occult bleeding can occur at any age. Moderate
LGIB presents as hematochezia or melena in a hemodynamically stable patient. The differential diagnosis is broad (Table 1). Occult LGIB
is otherwise asymptomatic, except for microcytic anemia resulting
from chronic blood loss. The differential diagnosis of these patients
includes malignancy, inflammatory conditions, ischemia, and congenital causes such as bleeding Meckel’s diverticula.
Epidemiology
Approximately 30% of all patients presenting with major GI bleeding
are found to have bleeding distal to the ligament of Treitz. Among
patients with presumed LGIB, 80% originate distal to the ileocecal
valve, with only 10% originating from the small bowel. The remaining cases usually arise in the upper GI tract. The overall incidence of
LGIB is notably higher in older adult patients, particularly those who
are on multiple medications.
Diverticulosis accounts for over 40% cases of LGIB and often
presents as painless hematochezia. Diverticular bleeding frequently
recurs, and the prevalence increases in patients older than 80 years of
age or in those with chronic constipation. Ischemic colitis accounts
for 20% of LGIB and is also more prevalent in the elderly. This may
occur in response to reduced mesenteric flow to the colon caused
by decreased cardiac output, vasospasm, or atherosclerotic disease.
Treatment is generally supportive and conservative unless there is
evidence of full-thickness necrosis and/or peritonitis. The watershed
area of the splenic flexure is a common location for ischemic colitis,
and involvement of this area on imaging should alert the clinician to
the possibility of this diagnosis. The most common cause of LGIB
in patients younger than 50 years of age is benign anorectal disease,
TABLE 1 Differential Diagnosis of Lower
Gastrointestinal Bleeding
Anatomic Source of Bleeding Etiologies
Small intestine Angiodysplasia
Crohn’s disease
Mesenteric ischemia
Recent surgery/trauma
Meckel’s diverticulum
Dieulafoy’s lesion
Aortoenteric fistula
Intussusception
Colon Diverticulosis
Neoplasm
Angiodysplasia
Inflammatory bowel disease
Recent colorectal surgery/trauma
Recent colonoscopy/
polypectomy
Ischemic colitis
Infectious colitis
Enterohemorrhagic
Escherichia coli (EHEC)
Salmonella
Campylobacter
Shigella
Cytomegalovirus
Entamoeba histolytica
Fecal impaction
Aortoenteric fistula
Rectum Radiation proctitis
Neoplasm
Angiodysplasia
Rectal varices
Fecal impaction
Inflammatory bowel disease
Solitary rectal ulcer
Rectal prolapse
Recent colorectal surgery/trauma
Anus Hemorrhoids
Anal fissure
Inflammatory bowel disease
Local trauma
Perianal variceal disease
usually hemorrhoids or anal fissures. The possibility of inflammatory
bowel disease (IBD) or NSAID-induced mucosal ulceration should
also be considered in these patients. Post-polypectomy bleeding can
result in brisk bleeding following colonoscopy and polypectomy.
Risk factors include age greater than 65 years and polyp size larger
than 1 cm. Though the bleeding is usually self-limited, presentation
can be delayed for up to 1 week after the procedure; therefore ascertaining the history of colonoscopy with polypectomy is crucial.
History and Physical Examination
The differential diagnosis for LGIB is broad, so a thorough history and physical examination is necessary. The history may suggest a cause of LGIB and can inform decision-making regarding
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diagnostic evaluation and management. Key details in the history
should include the quantity, quality, and frequency of the bleeding,
specifically whether the bleeding is recurrent or sporadic. Inquiry
into other associated symptoms such as presence of abdominal pain,
nausea, vomiting, or a recent change in bowel habits is also warranted. The clinician should specifically inquire about prior episodes
of LGIB, history of abdominopelvic radiation, trauma, symptomatic
arrhythmias, liver disease or cirrhosis, HIV status, and recent endoscopic or surgical procedures. A detailed review of the patient’s medications including antiplatelet agents, anticoagulants, and NSAIDs
as well as a family history of colon cancer or inflammatory bowel
disease should also be noted.
Abdominal examination and digital rectal examination should be
completed in all patients presenting with LGIB. Abdominal examination may reveal tenderness, distension, or a mass. Digital rectal
examination is important to inspect for anorectal pathology such as
hemorrhoids or fissures. Additionally, the quality of the stool in the
rectal vault, whether it is impacted, dark melena, maroon-colored, or
frank blood, should be documented. Importantly, the clinician should
pay close attention to the patient’s vital signs at all points during the
history and physical examination as any hemodynamic instability warrants a rapid resuscitation and aggressive diagnostic effort.
MANAGEMENT
All patients presenting with LGIBshould be triaged and evaluated
immediately as decompensation can be rapid. Administration of
supplemental oxygen, the establishment of intravenous lines access
with two large-bore peripheral venous catheters, and placement on
a cardiopulmonary monitor should be performed initially. Infusion
of crystalloid solutions should be started immediately to resuscitate
the patient. Laboratory examination should include a complete blood
count, metabolic panel, liver function tests, lactate, coagulation studies, and a type and screen.
important to minimize mortality. Aggressive efforts to correct coagulopathy and metabolic derangements before surgical intervention
should be undertaken, although salvage procedures may be required
in rare cases. This will be discussed further in later sections.
Special Hematologic Considerations
Early identification of hematologic disorders or medications is mandatory during the resuscitative process. Laboratory studies, including
traditional coagulation studies and possibly TEG, should be obtained
during the initial workup. Anticoagulants and antiplatelet agents
should be discontinued, and reversal should be considered in patients
with hemodynamic instability or ongoing bleeding. For patients who
are therapeutic or supratherapeutic on warfarin, a prothrombin concentrate complex should be considered. Vitamin K and fresh-frozen
plasma can also be utilized for this purpose, but prothrombin complex
concentrate has the advantage of rapid reversal with lower fluid volumes. In recent years, idarucizumab has become more readily available
to reverse dabigatran. Although not widely available yet, andexanet
alfa has also been approved by the US Food and Drug Administration
(FDA) for the reversal of apixaban and rivaroxaban. Currently, there
is no specific reversal agent for antiplatelet agents such as aspirin and
clopidogrel. Most clinicians favor early platelet transfusion and/or
desmopressin administration in the setting of active hemorrhage. Cardiology consultation should be considered for patients who have had
drug-eluting cardiac stents placed within the past year because they are
at risk for stent thrombosis if dual antiplatelet agents are discontinued,
and this can contribute to mortality. It may be reasonable to continue
aspirin therapy in some of these patients. Desmopressin administration can be particularly useful to reverse coagulopathy in the uremic
patient. For patients with inherited or acquired coagulation disorders,
specific reversal agents and therapies should be guided in consultation
with the hematology service. More specialized laboratory studies may
be indicated in some patients.
Resuscitation and Transfusion
Appropriate resuscitation of a patient with LGIB is crucial to minimize
morbidity. The process should begin as described earlier as soon as it
is recognized that the patient is actively bleeding. For patients with
evidence of multiple comorbidities or massive LGIB, a critical care
consultation and monitoring in a critical care setting is warranted.
Most patients with moderate or occult LGIB present without
signs of instability. These patients may warrant less aggressive resuscitation with crystalloid during their initial workup and evaluation.
Transfusion should be initiated to correct any overt coagulopathy
and to maintain a hemoglobin >7 g/dL for most patients. Some
patients, particularly those with other comorbidities, may require a
higher goal hemoglobin and should be treated on an individual basis.
International normalized ratio (INR) should be corrected to <1.5,
and platelets should be transfused to >50,000/L.
The massive LGIB patient who presents in hemorrhagic shock
is similar to a trauma patient. Therefore, activation of a massive
transfusion protocol and the use of empiric blood product ratios of
1:1:1 of packed red blood cells to fresh-frozen plasma to platelets in
order to correct coagulopathy is effective. Early use of fresh-frozen
plasma and platelets should be considered. The end goals of resuscitation are correction of coagulopathy and hemodynamic support.
A policy of permissive hypotension with systolic blood pressure >90
mm Hg is sufficient for most patients. Although crystalloid solutions
may be indicated in other cases of LGIB, care should be taken to
avoid the overuse of crystalloids in this subset of patients because
this may contribute to bowel edema and other complications such
as abdominal compartment syndrome or respiratory failure. The use
of thromboelastography (TEG) may also be a useful adjunct for the
care of the hemodynamically unstable LGIB patient in centers where
this technology is available. Prompt progression to the next phases
of management, bleeding localization and hemorrhagic control, is
Localization
The first step in management and hemorrhage control is localization of the bleeding site. As previously discussed, LGIB has a broad
differential, and identifying the source of bleeding is tantamount to
further management.
Nasogastric Lavage
An upper GI source should always be considered in patients with
suspected LGIB, particularly in patients with hemodynamic instability, brisk bleeding, or unrevealing evaluation of the lower GI tract.
Bleeding peptic ulcers, angiodysplasia, or esophageal varices can often
manifest as visible blood in the stool. Clearly, management diverges
drastically if the source of bleeding is in the upper GI tract. Nasogastric
lavage has classically been recommended as the first step in determining an upper versus lower GI source, particularly in the unstable
patient. A nasogastric tube is inserted bedside, and then the contents
of the stomach are suctioned. Alternatively, 200 to 300 mL saline is
instilled into the tube and then suctioned back to look for blood or coffee grounds in the stomach. Fluid with bile present but without blood
is considered to be a negative lavage. The lack of bilious fluid suggests
inadequate evaluation of the post-pyloric region. A clear effluent is
considered nondiagnostic and is not uncommon. Disadvantages of
nasogastric lavage include patient discomfort and lack of therapeutic
benefit. Nasogastric lavage has fallen out of favor in recent years and
should be reserved for cases of suspected upper GI hemorrhage to
improve visualization at the time of endoscopy. The authors liberally
employ the use of upper endoscopy for the evaluation and management of GI bleeding because of its numerous advantages.
Anoscopy/Rigid Sigmoidoscopy
In patients with a strong suspicion for GI bleeding from the anorectum or distal sigmoid, anoscopy or rigid sigmoidoscopy should
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be considered. Anoscopy can be quickly performed with little to no
sedation at the bedside by inserting a tubular instrument into the
patient’s anus to visualize hemorrhoids, anal fissures, fecal impaction, or local trauma to the anus. Anoscopy can also be therapeutic
as it can be used to assist with banding or other treatment of bleeding hemorrhoids. Rigid sigmoidoscopy is also a technically simple
bedside procedure but generally requires additional sedation. The
instrument is longer and allows for insufflation, which can facilitate
visualization of the rectal and distal sigmoid mucosa. Both procedures can be uncomfortable for the patient and provide limited
visualization of the most distal GI tract. When possible, flexible
sigmoidoscopy or colonoscopy is preferred.
Colonoscopy
When there is a high degree of suspicion for a colorectal source of
LGIB, colonoscopy is the modality of choice to localize the source
if possible. It has been shown to correctly identify the location of
LGIBin more than 75% of patients. Colonoscopy is performed using
a flexible scope guided from the anus through the entirety of the rectum and colon until the ileocecal valve is reached. Colonoscopy can
detect discrete sources of bleeding, such diverticula, angiodysplasia,
and tumors, as well as more diffuse sources of bleeding, such as
inflammatory bowel disease, ischemic colitis, and radiation proctitis.
An important benefit of the procedure is the ability to perform
therapeutic intervention. Bleeding should only be ascribed to lesions
with stigmata of recent hemorrhage, including visualized bleeding,
exposed blood vessels, or adherent clots. Colonoscopic hemostasis can
be achieved with dilute epinephrine injections (1:10,000) in 1 to 2 mL
aliquots up to 30 mL total. This result is usually temporary, and a second hemostatic method is recommended. Epinephrine injections are
best suited to facilitate site identification in cases of active or copious
bleeding. Endoclip placement results in hemostasis for nearly all diverticular bleeds with stigmata of recent hemorrhage and in nearly 70%
with other forms of LGIB (Fig. 1). Other endoscopic techniques for
hemostasis include bipolar electrocoagulation, heater probe cautery,
argon plasma coagulation, and rubber band ligation. Angiodysplasia
is particularly amenable to argon plasma coagulation (Fig. 2). Rubber
band ligation has the highest rates of rebleeding and can add significant procedure time depending on the site. Tattooing is recommended
to expedite site identification in the event of recurrent bleeding, particularly if surgical intervention is determined to be necessary.
The timing of colonoscopy in the evaluation of LGIB remains
controversial. Ideally, a bowel prep should be attempted to maximize visualization during the procedure. Notably, early colonoscopy
performed while the patient is actively bleeding has been shown to
improve diagnostic yield. Colonoscopic evaluation following bowel
FIG. 1 (A) Colonic diverticulum with stigmata of recent hemorrhage. (B) Successful endoscopic clipping of bleeding diverticulum. (Courtesy Daniel S. Behin,
MD, Montefiore Medical Center/Albert Einstein College of Medicine, New York.)
FIG. 2 Cecal angiodysplasia before (A) and after (B) endoscopic argon beam plasma coagulation. (Courtesy Daniel S. Behin, MD, Montefiore Medical Center/
Albert Einstein College of Medicine, New York.)
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preparation is generally recommended within the first 24 hours of
admission for patients with LGIB.
If the patient is not stable enough for endoscopic evaluation,
radiologic evaluation or surgical intervention should be considered
as an alternative. Colonoscopy should also be deferred if there is suspicion for active diverticulitis as this reportedly increases the risk of
perforation. Other procedural risks include mucosal injury and the
general risks of anesthesia/sedation.
Computed Tomographic Angiography
Computed tomographic angiography (CTA) is an important diagnostic tool for the evaluation of active LGIB. The study is performed
using intravenous contrast timed such that active arterial extravasation from a vessel into the lumen of the small bowel can be visualized
on a multidetector helical CT scanner. Extravasation of intravenous
contrast into the lumen of the bowel, or an active “blush,” constitutes
a positive finding (Fig. 3). This study has a sensitivity close to 90%
and can detect bleeding rates as low as 0.3 mL/min to 0.5 mL/min.
Localization accuracy is as high as 97% in patients with high transfusion requirements and/or hemodynamic instability. Unfortunately,
CTA has a relatively low specificity of 85%.
CTA is widely available, fast, minimally invasive, and does not
require any bowel preparation or oral contrast administration. As
a result, it is very useful in hemodynamically unstable patients who
do not have time to undergo bowel preparation before intervention
and are transiently responding to resuscitation. CTA is also useful in
identifying other causes of LGIB such as ischemic colitis and can be
used to evaluate the small bowel. Disadvantages include the requisite for active hemorrhage at the time of the study, possible allergic
reaction to intravenous contrast, radiation exposure, difficulty with
precise localization of a small-intestinal source, and lack of direct
therapeutic application.
Nuclear Scintigraphy with Technetium-99m
Like CTA, nuclear scintigraphy allows for radiographic location of
LGIB and is purely a diagnostic test. The patient’s red blood cells are
tagged with the radiotracer Technetium-99m (
into the patient followed by sequential imaging. Nuclear scintigraphy
is a far more sensitive test than CTA as it can detect bleeding rates as
FIG. 3 Active extravasation of contrast in the hepatic flexure of a patient
with lower gastrointestinal bleeding identified by CTA. (Courtesy Michael F
Petroziello, MD, Roswell Park Cancer Institute Hospital, Buffalo, NY.)
99m
Tc) and re-injected
low as 0.1 mL/min. An important advantage of this study is its ability to detect bleeding occurring up to 24 hours after tracer injection
as the radio-labeled red blood cells remain detectable. The half-life
99m
of
Tc allows for sequential imaging several times in a 24-hour
period.
Despite the high sensitivity rates, nuclear scintigraphy results in
false localization rates approaching 25% have been reported, making
it less accurate than CTA. This study is best suited as a screening
tool for hemodynamically stable patients with scant, intermittent
bleeding and not for definitive localization. Arteriography is generally warranted in the event of a positive study for localization and
possible therapeutic intervention. Surgical intervention, particularly
segmental resection, should not be guided by the results of nuclear
scintigraphy.
Angiography
Angiography offers the advantages of accurate localization and the
opportunity for therapeutic intervention, and it is a particularly
useful option in patients with unstable vital signs requiring ongoing blood transfusions. Appropriate indications include copious
bleeding precluding colonoscopic evaluation and positive extravasation on CTA or nuclear scintigraphy. For the latter, angiography
further localizes the source of bleeding and potentially allows for
hemorrhage control. These patients require little to no sedation, and
access is usually obtained through the femoral artery. Fluoroscopic
visualization is used to identify extravasation following selective
mesenteric arterial cannulation and injection of contrast material.
Angiography can detect bleeding at rates as low as 0.5 mL/min and
has a high sensitivity for LGIB. Overall, it is a better test for patients
with profuse, active bleeding than for those with scant, intermittent
bleeding.
Embolization can be attempted for patients with positive localization during angiography. Super subselection with microcatheters and
microcoil embolization are preferred when possible. Embolization,
including highly selective embolization, is clinically successful in
the majority of cases, with demonstrated bleeding resolution rates
of 75% to 90%, depending on the location (Fig. 4). Other therapeutic options include intraarterial infusion with vasopressin, a
potent vasoconstrictor, which is effective in substantially decreasing
bleeding. These maneuvers may eliminate the need for emergent
operation and facilitate continued resuscitation followed by surgical intervention under more controlled circumstances. For cases
of venous bleeding, embolization of the venous system is possible,
though not frequently undertaken.
Many have advocated for the preferential use of angiography in
frail patients with severe comorbidities for whom an emergent operation would carry a prohibitively high mortality. Angiography is usually reserved for hemodynamically unstable patients or patients with
a continued transfusion requirement. Unfortunately, the rebleeding
rate is not insignificant and approaches 20% in some studies. Potential risks of angiography include bowel ischemia, contrast allergy or
nephropathy, the risks of sedation, pseudoaneurysm, hematoma,
and other vascular complications at the access site. Table 2 outlines
and compares salient characteristic features of the various radiologic
diagnostic and treatment options.
For patients with intermittent, obscure LGIB that has not been
identified via other methods, provocative angiography is a technique
that can be utilized. During this procedure, a therapeutic dose of
anticoagulant is administered with the goal of provoking the bleeding lesion into an active hemorrhage so it can be captured on angiography. The lesion is then embolized in the same fashion as described
previously. Systemic anticoagulation is usually achieved with heparin
and followed by incremental and selective transcatheter injection of
urokinase and a vasodilator, such as nicardipine. Multiple studies
have shown that this procedure has an acceptable risk profile, including minimal risk of bleeding complications from the anticoagulant.
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Ai
BCiD
ii ii
Ei ii iiFi
FIG. 4 Bleeding at the hepatic flexure of the colon secondary to diverticulosis in two patients. Multiplanar reconstruction (MPR) and volume-rendered 3D
reconstruction of arterial-phase CT images reveal arterial bleeding from the peripheral branch of the right colic artery (A and B) and the middle colic artery
(C and D). Pre- and postembolization images demonstrate extravasation of contrast from the involved vessels and resolution of bleeding, respectively (E and
F). (From Tsurukiri J, Ueno M, Kaneko N. Bleeding at the hepatic flexure of the colon secondary to diverticulosis. Clin Gastroenterol Hepatol. 2012;10:e11–e12.)
TABLE 2 Radiologic Imaging Tests for Evaluation of Lower Gastrointestinal Bleeding with Their Associated
Characteristics
Bleeding Detection Rate
Study Invasive Procedure
(mL/min)
Localization Intervention
CTA – 0.3–0.5 + –
NS – 0.1 – –
Angiography + 0.5 + +
CTA, Computed tomographic angiography; NS, nuclear scintigraphy.
Nearly one-third of patients with a previously unidentified source
of LGIB have a source identified with provocative angiography.
Bleeding lesions can be treated by embolization or surgical resection.
Resection is the preferred treatment for hypervascular neoplasms
and can be useful for selected patients with angiodysplasia. If surgical
resection is being considered and no mass lesion is identified at the
time of selective arteriography, a microcatheter should be left in the
feeding artery. The patient should be brought to the operating room
in an expeditious fashion for surgical exploration. Injection of the
catheter with blue dye will allow for visualization of the involved
segment and can be used to guide the extent of resection.
Capsule Endoscopy
Although the majority of LGIB is colonic in origin, some cases of
obscure bleeding originate from the small bowel. Capsule endoscopy
is a useful modality for the subset of patients who have persistent
bleeding and negative endoscopic evaluations of the colon and foregut. The patient swallows a pill-sized capsule that contains a small
camera. The camera takes intermittent photographs as it travels
through the patient’s GI tract, and the photos are retrieved after the
capsule is returned. The images are reviewed carefully to determine
the source of bleeding. Capsule endoscopy is therefore best suited
for hemodynamically normal patients who have chronic GI bleeding with a suspected small intestinal source. Diagnostic accuracy
is good with sensitivities and specificities of approximately 90%
and 95%, respectively. Diagnostic yield is improved in patients with
acute bleeding and in those taking anticoagulants. The procedure
is noninvasive and has an overall low complication rate; however,
complications may include battery failure, capsule retention, and
bowel perforation. Other disadvantages include the lack of potential for localization or therapeutic intervention. Patients may be
administered a test capsule made of absorbable material before the
Capacity for
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