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20. Stier EA, Baranoski AS. Human papillomavirus-related diseases in HIV-infected individuals.
Curr Opin Oncol. 2008;20(5):541–6.
21. Weis SE, Vecino I, Pogoda JM, Susa JS. Treatment of high-grade anal intraepithelial neoplasia
with infrared coagulation in a primary care population of HIV-infected men and women. Dis
Colon Rectum. 2012;55(12):1236–43.
22. Marks DK, Goldstone SE. Electrocautery ablation of high-grade anal squamous intraepithelial
lesions in HIV-negative and HIV-positive men who have sex with men. J Acquir Immune Defic
Syndr. 2012;59(3):259–65.
23. Pineda CE, Berry JM, Welton ML. High resolution anoscopy and targeted treatment of high-
grade squamous intraepithelial lesions. Dis Colon Rectum. 2006;49(1):126.
24. Graham BD, Jetmore AB, Foote JE, Arnold LK. Topical 5-fluorouracil in the management of
extensive anal Bowen’s disease: a preferred approach. Dis Colon Rectum. 2005;48(3):444–50.
25. Fox PA, Nathan M, Francis N, et al. A double-blind, randomized controlled trial of the use of
imiquimod cream for the treatment of anal canal high-grade anal intraepithelial neoplasia in
HIV-positive MSM on HAART, with long-term follow-up data including the use of open-label
imiquimod. AIDS. 2010;24(15):2331–5.
26. Richel O, de Vries HJ, van Noesel CJ, Dijkgraaf MG, Prins JM. Comparison of imiquimod,
topical fluorouracil, and electrocautery for the treatment of anal intraepithelial neoplasia in
HIV-positive men who have sex with men: an open-label, randomised controlled trial. Lancet
Oncol. 2013;14(4):346–53.
27. Kreuter A, Hochdorfer B, Stucker M, et al. Treatment of anal intraepithelial neoplasia in patients
with acquired HIV with imiquimod 5 % cream. J Am Acad Dermatol. 2004;50(6):980–1.
28. Richel O, Wieland U, de Vries HJ, et al. Topical 5-fluorouracil treatment of anal intraepithelial
neoplasia in human immunodeficiency virus-positive men. Br J Dermatol.
2010;163(6):1301–7.
29. Snyder SM, Siekas L, Aboulafia DM. Initial experience with topical fluorouracil for treatment
of HIV-associated anal intraepithelial neoplasia. J Int Assoc Physicians AIDS Care.
2011;10(2):83–8.
30. Wieland U, Brockmeyer NH, Weissenborn SJ, et al. Imiquimod treatment of anal intraepithe-
lial neoplasia in HIV-positive men. Arch Dermatol. 2006;142(11):1438–44.
31. Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer
Cytopathol. 2011;119(1):5–19.
32. Shah SB, Pickham D, Araya H, et al. Prevalence of anal dysplasia in patients with inflamma-
tory bowel disease. Clin Gastroenterol Hepatol. 2015;13(11):1955–61 e1951.
33. Pineda CE, Berry JM, Jay N, Palefsky JM, Welton ML. High-resolution anoscopy targeted
surgical destruction of anal high-grade squamous intraepithelial lesions: a ten-year experience.
Dis Colon Rectum. 2008;51(6):829–35; discussion 835–27.
34. Pineda CE, Berry JM, Jay N, Palefsky JM, Welton ML. High resolution anoscopy in the
planned staged treatment of anal squamous intraepithelial lesions in HIV-negative patients.
J Gastrointest Surg. 2007;11(11):1410–5; discussion 1415–16.
35. Goldstone RN, Goldstone AB, Russ J, Goldstone SE. Long-term follow-up of infrared coagu-
lator ablation of anal high-grade dysplasia in men who have sex with men. Dis Colon Rectum.
2011;54(10):1284–92.
36. Marchesa P, Fazio VW, Oliart S, Goldblum JR, Lavery IC. Perianal Bowen’s disease: a clini-
copathologic study of 47 patients. Dis Colon Rectum. 1997;40(11):1286–93.
37. Stier EA, Goldstone SE, Berry JM, et al. Infrared coagulator treatment of high-grade anal
dysplasia in HIV-infected individuals: an AIDS malignancy consortium pilot study. J Acquir
Immune Defic Syndr. 2008;47(1):56–61.
38. van der Snoek EM, den Hollander JC, van der Ende ME. Imiquimod 5 % cream for five con-
secutive days a week in an HIV-infected observational cohort up to 32 weeks in the treatment
of high-grade squamous intraepithelial lesions. Sex Transm Infect. 2015;91(4):245–7.
39. Singh JC, Kuohung V, Palefsky JM. Efficacy of trichloroacetic acid in the treatment of anal
intraepithelial neoplasia in HIV-positive and HIV-negative men who have sex with men.
J Acquir Immune Defic Syndr. 2009;52(4):474–9.
23 Anal Dysplasia/Cancer: Management of Patients with AIN 3
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267© Springer International Publishing Switzerland 2017
N. Hyman, K. Umanskiy (eds.), Difficult Decisions in Colorectal Surgery,
Difficult Decisions in Surgery: An Evidence-Based Approach,
DOI 10.1007/978-3-319-40223-9_24
Chapter 24
Management of the Abnormal Pap Smear
in HIV Positive Patients
Brad Champagne
Introduction
Condylomaacuminata, anal intraepithelial neoplasia and anal cancer are diseases
that commonly afflict men who have sex with men (MSM). The disease process may
often be complicated by a coexisting infection with the Human Immunodeficiency
Virus (HIV). Other than patients with HIV and MSM populations, transplant recipi-
ents on immunosuppression or other immunosuppressed states, and women with a
history of genital cancers are at increased risk [1, 2] High risk populations have been
encouraged to undergo screening with anal pap smear with increasing frequency and
intensity over recent years. However, the appropriate follow-up, diagnostic work-up
and treatment modality for patients with a positive smear remains nebulous.
Although anal squamous cell carcinoma (ASCC) represents only approximately
2 % of all GI cancers, its incidence has steadily risen over the past decade [1, 3, 4].
This increase is particularly remarkable in specific populations, such as individuals
infected with HIV, and even more so among men who have sex with men (MSM),
which makes this patient group a primary focus for screening [5]. It has long been
recognized that, much like cervical cancer, there is a strong, causal relationship
between anal cancer and human papilloma virus (HPV) infection [6, 7]. Anal
intraepithelial neoplasia (AIN), HPV-related dysplastic changes in the cells at the
anal transition zone, is the presumed precursor lesion for ASCC [1, 8]. Anal intraep-
ithelial neoplasia is classified into three grades, corresponding to low-grade (AIN I),
moderate grade (AIN II), and high-grade dysplasia (AIN III). The terms low-grade
(LGAIN) and high grade (HGAIN) have been used to refer to AIN I/II and AIN III,
B. Champagne
Lerner College of Medicine, Cleveland Clinic, Cleveland, OH, USA
Cleveland Clinic, Fairview Hospital, Cleveland, OH, USA
e-mail: brad.champagne@uhhospitals.org
268
respectively [1]. The epithelium in both the cervix and anus may contain atypical
squamous cells of undetermined significance, low grade squamous intraepithelial
lesions, and high grade squamous intraepithelial lesions. It is fairly well established
that high grade squamous intraepithelial lesions represent the precursor to cervical
SCC [9]. Given the similarities between cervical and anal intraepithelial lesions and
the association with anogenital HPV, this precursor pathway is similarly applied to
concepts of progression to anal SCC [10]. Therefore, recognizing its effectiveness
in relation to cervical cancer, anal Pap smear cytology has been adapted as one of
the first steps in screening for AIN [2, 11]. There is little debate that the destruction
of AIN is paramount in the prevention of progression to ASCC [1–3].
However, once AIN has been identified, there is considerable debate on the opti-
mal protocol for management and surveillance of these lesions, specifically in high
risk populations [12]. This controversy is largely centered on recommendations of
routine high-resolution Anoscopy (HRA) in all patients with suspected AIN versus
clinical follow-up with expectant management (EM). High resolution anoscopy
(HRA) is similar to colposcopy, wherein the anal canal and transition zone are
inspected under a high resolution microscope with the addition of acetic acid and/or
Lugol’s iodine solution to identify areas of dysplasia, which are then biopsied [13–
17]. Expectant management includes regular office-based examination, operative
fulguration of larger lesions, and treatment of dysplasia with imiquimod [18]. With
this debate in mind, we set out to analyze the literature in an effort to answer the ques-
tion regarding optimal follow up of HIV patients with an abnormal anal Pap smear.
Methods
Our search strategy involved a Pubmed search with the following keywords: High
Resolution Anoscopy (HRA), Anal Intraepithelial Neoplasia (AIN), Papanicolaou
(pap) smear, cost, and screening. We limited our search from the year 1995 to pres-
ent. The evidence is analyzed, described, and placed in tabular form.
Patient population (P) Intervention (I) Comparator (C) Outcome studied (O)
HIV pts with abnormal
pap smear
High resolution
anoscopy (HRA)
Clinical
follow-up
Cancer prevention,
cost
Results
Screening HIV-infected MSM with annual anal cytology has been shown to be cost-
effective, with an incremental cost-effectiveness ratio compared to no screening of
$16,600 per quality –adjusted life year (QALY) saved, which is similar to other
accepted screening test such as colorectal cancer screening [10].
B. Champagne
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269
Currently, there are no randomized controlled trials comparing the efficacy of
HRA versus clinical follow-up with regards to ASCC prevention. We are thus left
with observational studies and retrospective reviews. A meta-analysis of published
studies suggests that the pooled prevalence of histological high grade AIN in MSM
with HIV was 29.1 % [7], with incidences of 8.5 % and 15.4 % per year respectively
in two estimates [19, 20]. The pooled anal cancer incidence was 45.9 per 100,000
men [7]. This number is corroborated by a pilot study which found that high grade
AIN (AIN II and III) was found on histological analysis after HRA in approxi-
mately 32 % of asymptomatic MSM living with HIV. In this population of 368
asymptomatic MSM, 1.4 % developed invasive anal cancer at a median follow up of
4.2 years after HRA. All patients had high grade AIN at initial HRA screening.
Additionally, during this study, the cumulative risk of anal cancer following HSIL
diagnosis was 0.6 % at 5 years [14]. It is clear from this and other studies that AIN
II-III represents a significant risk factor for development of ASCC.
However, does the incidence of ASCC support the widespread usage of HRA,
and does the cost outweigh the benefit? A recent large retrospective review addresses
the utility of routinely performing HRA. Crawshaw et al performed a single institu-
tion retrospective analysis of 424 patients from 2007 to 2013 comparing HRA to
clinical follow-up. Surgeons in the group differed in their views on this controversy
and their use of HRA, creating a natural experiment of sorts. 220 patients underwent
HRA after abnormal pap smear, and 204 patients underwent clinical follow-up. The
authors found no significant difference in progression to ASCC among the two
groups [12]. It is important to note, however, that the surgeons in the clinical follow-
up group performed mapping biopsies, ablated all visible lesions, and readily used
imiquimod. Therefore, the only real difference between the groups was the use of
HRA. HRA was not associated with prevention of ASCC when compared to the non
HRA arm.
A recent Markov model analysis suggests that surveillance strategies after treat-
ment for HGAIN that included HRA at 6 and 12 month intervals, with or without
anal cytology testing, were more effective than using HRA only for confirmatory
testing of abnormal anal cytology testing. However, a combined strategy of HRA
and anal cytology extended life expectancy and quality-adjusted life expectancy
(QALE) while remaining below the commonly-cited threshold of 100,000/QALY
gained [21]. Similarly, Lam et al built a decision analytic model, and found that of
18 screening strategies, the direct use of HRA was the most cost-effective approach
for the detection of high grade AIN [22]. However, neither of these analyses com-
pare HRA to that of clinical follow-up.
Proponents of clinical management without HRA cite the increased morbidity as
well as the additional cost incurred with repeated procedures often seen with HRA,
as well as the low rate of disease progression to ASCC in compliant patients [1].
However, whilst HRA has been shown to be more effective in the detection of AIN
than standard anoscopy with biopsies, this has failed to translate into lower rates of
disease progression to ASCC [14, 16, 17]. The purpose of cancer screening is to
reduce cancer-related mortality; there is a paucity of high quality evidence to make
clear recommendations regarding the true benefit of HRA.
24 Management of the Abnormal Pap Smear in HIV Positive Patients
270
Recommendations Based on the Data
MSM with HIV are consistently more affected by HPV and HPV related abnormali-
ties than are HIV-negative MSM. Furthermore, longitudinal data suggests a very
high annual incidence of high grade AIN in HIV-positive men. Therefore, we
strongly recommend based on high and moderate quality evidence that HIV positive
MSM undergo screening with anal pap. In regards to treatment, the absence of data
from randomized and longitudinal trials showing that treatment of high-grade AIN
reduces the incidence of anal cancer and the morbidity associated with treatment
needs to be considered. Therefore, the recommendation that approaches to cervical
cancer prevention and treatment can be extrapolated to anal cancer are weak and
based on very low quality evidence.
High-resolution anoscopy is costly, time consuming and technically demanding
when compared to colposcopy for cervical cancer or to clinical follow-up with map-
ping biopsies in patients with a positive pap. The recommendation that HRA is
superior to clinical follow-up or expectant management is weak with very low qual-
ity evidence. In addition, the low progression rates of high grade AIN to anal cancer
also question the real value of repeated surgical treatments in this patient popula-
tion. Therefore, the recommendation that aggressive and repeated treatments are
warranted in patients with AIN to prevent anal cancer is weak and based on very
low quality evidence. Lastly, the argument that the cost of HRA is nominal when
compared to the cost savings achieved with cancer progression is not substantiated
by high quality data. Therefore, the recommendation that HRA is cost-effective
when applied to HIV positive MSM is weak with low quality data.
A Personal View of the Data
There is little debate that the destruction of AIN is paramount in the prevention of
progression to ASCC. Thus, identification of, and surveillance for the presence of
AIN is a key step in any screening protocol. While HRA has been shown to be more
effective in the detection of AIN than standard anoscopy with biopsies, there has not
been definitive proof that its utilization results in lower progression to ASCC than
more traditional expectant management. Recent studies at our institution, as out-
lined above, showed that there was no progression to ASCC in patients regardless
of their treatment protocol (HRA vs EM), if they were compliant with therapy.
The majority of our patients now follow the expectant management (EM)
algorithm.
All patients are initially evaluated in the office with DRE and anoscopy. If they
had a positive anal pap smear or visible condyloma they are brought to the operating
room for evaluation. During surgery, all visible abnormal areas are both biopsied
and ablated. Furthermore, representative biopsies are performed from every quad-
rant in the anal canal and the anal margin in areas with no identifiable lesions.
B. Champagne
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271
Postoperatively, patients with anal intraepithelial neoplasia are treated with imiqui-
mod and followed. Recurrent lesions amendable to office-based therapy with acetic
acid and or podophyllin are not brought back to the operating room for ablation
unless the disease persists for 3 months after treatment.
. Overall, in our recently published data, we found that patients with anal intraep-
ithelial neoplasia rarely progress to squamous cell cancer after ablation when fol-
lowed with expectant management or high-resolution anoscopy. Our results support
the concept that physicians treating these diseases should utilize the technique that
they are most comfortable with. The cost, morbidity and value of high-resolution
anoscopy should be further critically evaluated before it is regarded as the gold
standard in anal cancer screening.
Questions Utility/sens/spec of abnormal pap smears, cost of HRA, sens/spec of
HRA, increased incidence with HIV positivity, cost of pap smears
References
1. Steele SR, Varma MG, Melton GB, et al. Practice parameters for anal squamous neoplasms.
Dis Colon Rectum. 2012;55(7):735–49.
2. Smyczek P, Singh AE, Romanowski B. Anal intraepithelial neoplasia: review and recommen-
dations for screening and management. Int J STD AIDS. 2013;24(11):843–51.
3. Goldstone SE, Johnstone AA, Moshier EL. Long-term outcome of ablation of anal high-grade
squamous intraepithelial lesions: recurrence and incidence of cancer. Dis Colon Rectum.
2014;57(3):316–23.
4. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):
11–30.
5. Sendagorta E, Herranz P, Guadalajara H, et al. Prevalence of abnormal anal cytology and high-
grade squamous intraepithelial lesions among a cohort of HIV-infected men who have sex with
men. Dis Colon Rectum. 2014;57(4):475–81.
6. Frisch M, Glimelius B, van den Brule AJ, et al. Sexually transmitted infection as a cause of
anal cancer. N Engl J Med. 1997;337(19):1350–8.
Specific Recommendations
1. HIV positive men who have sex with men (MSM) should undergo routine
screening with anal pap (Grade: High. Recommendation: Strong)
2. Approaches to cervical cancer prevention and treatment can be extrapo-
lated to anal cancer. (Grade: Low. Recommendation Weak)
3. HRA is superior to clinical follow-up or expectant management for AIN.
(Grade: Low. Recommendation: Weak)
4. Aggressive and repeated treatments with HRA are warranted in patients
with AIN to prevent anal cancer. (Grade: Low. Recommendation: Weak.)
5. HRA is a cost-effective strategy to prevent anal cancer in HIV positive
MSM. (Grade: Low. Recommendation: Weak).
24 Management of the Abnormal Pap Smear in HIV Positive Patients
272
7. Machalek DA, Poynten M, Jin F, et al. Anal human papillomavirus infection and associated
neoplastic lesions in men who have sex with men: a systematic review and meta-analysis.
Lancet Oncol. 2012;13(5):487–500.
8. Berry JM, Jay N, Cranston RD, et al. Progression of anal high-grade squamous intraepithelial
lesions to invasive anal cancer among HIV-infected men who have sex with men. Int J Cancer.
2014;134(5):1147–55.
9. Palefsky JM, Holly EA. Molecular virology and epidemiology of human papillomavirus and
cervical cancer. Cancer Epidemiol Biomarkers Prev. 1995;4(4):415–28.
10. Goldie SJ, Kuntz KM, Weinstein MC, Freedberg KA, Welton ML, Palefsky JM. The clinical
effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in
homosexual and bisexual HIV-positive men. JAMA. 1999;281(19):1822–9.
11. Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer
Cytopathol. 2011;119(1):5–19.
12. Crawshaw BP, Russ AJ, Stein SL, et al. High-resolution anoscopy or expectant management
for anal intraepithelial neoplasia for the prevention of anal cancer: is there really a difference?
Dis Colon Rectum. 2015;58(1):53–9.
13. Goldstone SE. High-resolution anoscopy is a crucial component of anal dysplasia screening.
Dis Colon Rectum. 2010;53(3):364–5.
14. Dalla Pria A, Alfa-Wali M, Fox P, et al. High-resolution anoscopy screening of HIV-positive
MSM: longitudinal results from a pilot study. AIDS. 2014;28(6):861–7.
15. Richel O, Hallensleben ND, Kreuter A, van Noesel CJ, Prins JM, de Vries HJ. High-resolution
anoscopy: clinical features of anal intraepithelial neoplasia in HIV-positive men. Dis Colon
Rectum. 2013;56(11):1237–42.
16. Silvera R, Gaisa MM, Goldstone SE. Random biopsy during high-resolution anoscopy
increases diagnosis of anal high-grade squamous intraepithelial lesions. J Acquir Immune
Defic Syndr. 2014;65(1):65–71.
17. Gimenez F, Costa-e-Silva IT, Daumas A, Araújo J, Medeiros SG, Ferreira L. The value of
high-resolution anoscopy in the diagnosis of anal cancer precursor lesions in HIV-positive
patients. Arq Gastroenterol. 2011;48(2):136–45.
18. Devaraj B, Cosman BC. Expectant management of anal squamous dysplasia in patients with
HIV. Dis Colon Rectum. 2006;49(1):36–40.
19. de Pokomandy A, Rouleau D, Ghattas G, et al. HAART and progression to high-grade anal
intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect
Dis. 2011;52(9):1174–81.
20. Palefsky JM, Holly EA, Ralston ML, Jay N, Berry JM, Darragh TM. High incidence of anal
high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homo-
sexual and bisexual men. AIDS. 1998;12(5):495–503.
21. Assoumou SA, Mayer KH, Panther L, Linas BP, Kim J. Cost-effectiveness of surveillance
strategies after treatment for high-grade anal dysplasia in high-risk patients. Sex Transm Dis.
2013;40(4):298–303.
22. Lam JM, Hoch JS, Tinmouth J, Sano M, Raboud J, Salit IE. Cost-effectiveness of screening for
anal precancers in HIV-positive men. AIDS. 2011;25(5):635–42.
B. Champagne
www.ebook3000.com
Part V
Benign Colon Disease
275© Springer International Publishing Switzerland 2017
N. Hyman, K. Umanskiy (eds.), Difficult Decisions in Colorectal Surgery,
Difficult Decisions in Surgery: An Evidence-Based Approach,
DOI 10.1007/978-3-319-40223-9_25
Chapter 25
Indications for Surgery in Patients with Severe
Clostridium Difficile Colitis
Vikram Reddy and Walter Longo
Introduction
Clostridium difficile colitis (CDC) is the leading cause of nosocomial diarrhea in
the United States, with a broad spectrum of symptoms ranging from mild diarrhea
to fulminant colitis which can lead to multisystem organ failure and death. For the
majority of cases, surgical therapy is unnecessary as CDC responds to antibiotic
therapy. Medically refractory colitis carries a high morbidity and mortality, and
often necessitates surgical intervention which may also be associated with poor
outcomes. The timing of surgery in the setting of CDC is critical; surgical interven-
tion early in the course of disease may lead to an unnecessary colectomy with ileos-
tomy when medical therapy may have been sufficient, but delaying surgical therapy
in fulminant colitis commonly leads to a fatal outcome.
Recommendations for intervention requires is based on the severity of disease.
Mild disease is characterized by diarrhea without any systemic symptoms.
Endoscopic findings in mild disease show non-specific diffuse or patchy erythema-
tous colitis, and pseudomembranes are usually not found. Imaging shows no evi-
dence of colitis. Moderate disease is associated with more severe diarrhea, and mild
systemic signs such as fever, leukocytosis, nausea and general malaise. Pseudo-
membranes, though not specific for CDC, are likely to be noted on endoscopy.
Severe disease is progressively worsening CDC with hypoalbuminema (<3 g/dL) in
the setting of worsening leukocytosis (>15,000 cells/mm
3
) or abdominal tenderness.
Fulminant colitis is a rare but life-threatening progression of severe CDC character-
ized by segmental or total colonic distention with signs of systemic toxicity (fever,
V. Reddy, MD, PhD • W. Longo, MD, MBA (*)
Department of Surgery, Yale University School of Medicine, New Haven, CT 06510, USA
e-mail: walter.longo@yale.edu
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276
leukocytosis, distention, tenderness, hemodynamic instability, and organ dysfunc-
tion) and clinical deterioration with peritonitis and sepsis. Unfortunately, a clear
algorithmic approach to surgical management is difficult as the ability to categorize
the severity of the disease is challenging. Most of the studies addressing indications
for surgery are limited by small sample sizes, retrospective analysis, and inconsis-
tent criteria in distinguishing severe from fulminant colitis.
Non-surgical options include treatment with antibiotics, fecal microbiota trans-
plant (FMT) and intravenous immunoglobulin (IVIG) transfers. Antibiotic therapy
includes single agent therapy with oral metronidazole or vancomycin for mild to
moderate disease, and dual coverage with metronidazole and vancomycin for severe
disease. Nitazoxanide and fidaxomicin have also been used, but their utility in
severe CDC needs to be more fully addressed. FMT is the transfer of stool from a
heathy donor to a patient with CDC to remedy the decreased colonic diversity that
is thought to drive CDC [1]. Instillation can be done by colonoscopy, upper endos-
copy, per nasogastric tube, or by retention enemas. Lower GI tract instillations are
associated with better outcomes.
Surgical options for the management of fulminant colitis include segmental col-
ectomy, total or subtotal abdominal colectomy (TAC) with a stoma, or a diverting
stoma with lavage of the distal bowel [2]. Of these, TAC with end ileostomy is the
gold standard [3] which eliminates the diseased colon while avoiding the added
morbidity of a pelvic dissection. Diverting stoma and lavage of the distal bowel
markedly decreases the magnitude of the surgical procedure and diminishes the
likelihood of a permanent ileostomy.
Search Strategy
The MEDLINE database was searched using the following MeSH headings:
“Clostridium difficile”, “surgery”, and “outcome.” The time interval of the retreived
articles was limited to 2005–2015. Non-english language publications were excluded.
Information obtained was graded according to published GRADE guidelines. In gen-
eral, the strength of the evidence is moderate to low, as it has been difficult to initiate
large randomized controlled trials to evaluate the role of surgery in severe Clostridium
difficile colitis. Meta-analyses, case reports, and reviews not containing original data
were also excluded (Table 25.1).
Table 25.1 PICO table
P (patient population) I (intervention)
C
(comparator) O (key outcomes)
Patients with severe
Clostridium difficile colitis
Surgery No surgery Morbidity, mortality,
quality of life
V. Reddy and W. Longo