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Awareness of guidelines and trends in the management of suspected pancreatic cystic neoplasms: survey results among general gastroenterologists and EUS specialists
ORIGINAL ARTICLE: Clinical Endoscopy
Awareness of guidelines and trends in the management of suspected pancreatic cystic neoplasms: survey results among general gastroenterologists and EUS specialists Jonathan M. Buscaglia, MD, Eun Ji Shin, MD, Samuel A. Giday, MD, Sumit Kapoor, MBBS, MPH, Kerry B. Dunbar, MD, Mohamad A. Eloubeidi, MD, MHS, Marcia I. Canto, MD, MHS, Sanjay B. Jagannath, MD Baltimore, Maryland, Birmingham, Alabama, USA
Background: Although pancreatic cystic neoplasms are widely recognized, practice habits among physicians and awareness of consensus guidelines are currently unknown. Objectives: To assess the awareness of guidelines and describe variability in practice habits among 2 groups: (1) ‘‘general group’’ of gastroenterologists and surgeons and (2) ‘‘EUS group’’ of specialists in EUS. Design: An online survey was sent to randomly selected gastroenterologists and surgeons and e-mailed to members of the American Society for Gastrointestinal Endoscopy (ASGE) Special Interest Group in EUS (EUS-SIG). Results: Response rate for the general group was 8.8% (220/2500) and 9.7% for the EUS group (42/431). EUS specialists were mostly in academic practice (66.7% vs 36.3%, P ! .001) and reported seeing 21 to 50 cysts per year (54.8% vs 12.3%, P ! .001). The majority of the general group (64.1%) was unaware of any published practice guidelines, compared with 33.3% of EUS specialists (P! .001). Awareness of ASGE guidelines was more frequently reported than other guidelines in both groups and yet was still !50% for each group. Both demonstrated moderate consistency with the International Association of Pancreatology guidelines, appropriately answering 66.7% of the questions. For 9-mm lesions, only 25% of the questions were correctly answered in each group. EUS specialists were less likely to refer main-duct intraductal papillary mucinous neoplasms (IPMN) for surgery and more likely to opt for EUS-guided FNA (compared with high-resolution CT, MRCP, or surgery) for 9-mm, 22-mm, and 34-mm branch-duct IPMNs (P % .001). Limitations: Low response rate and recall bias. Conclusions: Awareness of practice guidelines about the management of suspected pancreatic cystic neoplasms is lower among general GI physicians compared with EUS specialists. Among all physicians, the greatest variability in practice is in small (!1 cm) lesions. (Gastrointest Endosc 2009;69:813-20.)
Pancreatic cysts are increasingly recognized because of the widespread use of cross-sectional imaging techniques, such as CT and magnetic resonance imaging (MRI). In a postmortem study, small cystic lesions of the pancreas
Copyright ª 2009 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 doi:10.1016/j.gie.2008.05.036
were discovered in nearly 50% of the 300 tissue samples examined.1 The concern about pancreatic cysts rests in the possibility of neoplasia within the lesion itself. Pancreatic cystic neoplasms account for 10% of all cysts, and the vast majority of these lesions (90%) are 1 of 3 types: intraductal papillary mucinous neoplasms (IPMNs), mucinous cystic neoplasms (MCNs), or serous cystadenomas.2,3 Although serous lesions are regarded as benign neoplasms, IPMNs and MCNs possess significant cancerous potential.4-16 In 2004, during the 11th Congress of the International Association of Pancreatology (IAP), Sendai, Japan, a set of expert consensus guidelines was drafted to aid clinicians in the management of mucinous cystic lesions of the pancreas (IPMNs and MCNs). The publication of these guidelines in 2006 has provided a thorough summary of the existing literature on this topic, and it outlines a concise
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Abbreviations: ASGE, American Society for Gastrointestinal Endoscopy; EUS-guided FNA, EUS-FNA; EUS-SIG, EUS special interest group; HR-CT, high-resolution CT; IAP, International Association of Pancreatology; IPMN, intraductal papillary mucinous neoplasm; MCN, mucinous cystic neoplasm; MRI, magnetic resonance imaging. DISCLOSURE: All authors disclosed no financial relationships relevant to this publication. This study was conducted in collaboration with Olympus America.
Management of suspected pancreatic cystic neoplasms
management strategy for IPMNs and MCNs of all sizes.4 Although many experts regard this publication as the criterion standard in practice guidelines for pancreatic cystic neoplasms, its publication in a non-American journal has limited its widespread endorsement from American professional societies. The aim of our study was to assess physician awareness of the IAP guidelines and other guidelines and to describe the variability in practice habits among 2 groups: (1) a group of U.S. gastroenterologists and GI surgeons (general group) and (2) a group of GI endoscopists who specialize in EUS (EUS group). The practice trends in both groups were then compared with the current set of recommendations put forth by the IAP.
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Capsule Summary What is already known on this topic d
What this study adds to our knowledge d
d
PATIENTS AND METHODS
The International Association of Pancreatology practice guidelines for pancreatic cystic neoplasms have met limited endorsement.
In a survey of gastroenterologists, surgeons, and members of the American Society for Gastrointestinal Endoscopy EUS Special Interest Group, awareness of practice guidelines for the management of suspected pancreatic cystic neoplasms was lower among general GI physicians than EUS specialists. Greatest variability in practice habits is in the management of small cystic lesions !1 cm in size.
Study participants This study was approved by the Johns Hopkins University School of Medicine Institutional Review Board. An Internet, Web-based survey was designed to address the different practice habits of 2 groups of physicians: (1) a general group of gastroenterologists and GI surgeons (general group) and (2) a group of EUS specialists (EUS group). General group members were contacted by e-mail on 2 occasions, between March and May 2006, alerting them to a Web site link that contained the online questionnaire. The e-mail address list of general GI practitioners was obtained from the Medical Marketing Service Corporation (Wood Dale, Ill). Addresses were extracted by Medical Marketing Service Corporation from a large, multimedical professional society database of physicians and other health care workers. Search terms used to create the address list were ‘‘gastroenterologist,’’ ‘‘general surgeon,’’ and ‘‘abdominal surgeon.’’ A total of 2500 e-mail solicitations were sent. EUS specialists participating in this study were members of the Endoscopic Ultrasound Special Interest Group (EUS-SIG) of the American Society for Gastrointestinal Endoscopy (ASGE). Participation was solicited through an advertisement in the February 2007 electronic newsletter that is sent via the Internet to all EUS-SIG members (total of 431 members). The Web-site link to the survey was directly accessible from the electronic newsletter. Individual e-mail addresses of the EUS-SIG members were not disclosed by the ASGE.
The survey was divided into 3 sections. The first section consisted of a series of questions regarding physician demographics. The second section was composed of different clinical vignettes designed to resemble medical board–like questions. The vignettes themselves were modeled around the algorithm for the management of branch-duct IPMNs, published within Figure 10 of the
IAP consensus guidelines by Tanaka et al.4 They described an asymptomatic 55-year-old woman incidentally found to have a small pancreatic cyst on a ‘‘screening whole-body CT scan.’’ This portion of the questionnaire was divided into 3 subsections; each described varying sizes of the cyst on a CT (9, 22, and 34 mm, respectively). In each scenario, participants were first asked their opinion on the next most appropriate test of choice. Then a series of questions followed regarding the management of each cyst. Participants were eventually told which subsequent MRI and/or MRCP imaging was most consistent with a branch-duct IPMN, and more questions then followed. Ultimately, in each of the 3 scenarios, there were 4 questions (12 total) designed to deliberately test participants’ knowledge of the current IAP guidelines on the management of mucinous cysts of the pancreas. The 4 questions in each clinical scenario were similar, yet the characteristics of the cyst and/or patient differed in each vignette. Question no. 1 assessed the need for cyst surveillance. Question nos. 2 and 3 addressed the appropriate time interval for surveillance (if any) and the methods used for surveillance when told the lesion most likely represented a branch-duct IPMN. Question no. 4 slightly altered the clinical vignette and asked participants to weigh their agreement or disagreement (scale 0-10) with a specific management strategy for that particular-sized branchduct IPMN. Participants in both groups were not notified as to the availability or publication of the IAP consensus guidelines before taking the survey. A copy of the survey can be viewed online (Appendix, available online at www.giejournal.org). The third and final section of the survey asked a series of questions on physician awareness of current practice guidelines on the management of cystic neoplasms of the pancreas. Furthermore, it probed the trends in clinical management of pancreatic cysts and presumed IPMNs. Questions ranged from physicians’ thoughts on the most
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The survey
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optimal imaging techniques, to evidence supporting cyst criteria for malignancy, to personal opinions on the publication of practice guidelines. This section of the questionnaire was modeled after a survey by Yusuf and Baron17 that examined physician practice trends on the endoscopic management of pancreatic pseudocysts. It was presented in a Likert scale format. The survey was posted on a Web site by Olympus America Inc (Center Valley, Pa). It was designed to be interactive and user-friendly, and it was structured such that it could be completed in approximately 10 to 15 minutes. The survey was electronically accessible for a 12-week period of time for both groups of participants. In the general group of gastroenterologists and surgeons, a reminder e-mail message was sent 4 weeks after the initial e-mail distribution. A reminder message was not sent to EUS-SIG members. All responses to the questionnaire were anonymous and were stored in a computerized database.
Statistical analysis All categorical variables that compared the physician demographics among the 2 groups were evaluated by using the Fisher exact test. Likert scale responses were treated as ordinal data and were analyzed by using the nonparametric Kruskal-Wallis test. All statistical analyses were performed by using Stata software, version 9.2 (StataCorp, College Station, Tex). Reported P values were 2-sided statistical tests with P ! .05 as the level of significance. In light of multiple testing of outcome data arising from individual respondents, it is noted that statistical significance would be removed by correction for multiple testing by using the Bonferroni method unless the nominal uncorrected P values have P ! .001. Each group’s responses to the clinical vignettes were compared with each other and to the current IAP guidelines. They were analyzed by assessing the number of ‘‘correct’’ responses. For each of the 12 questions, each group of respondents was scored a ‘‘1’’ if the majority of participants (O50%) answered the question in accordance with the guideline recommendations. A score of ‘‘0’’ was given if %50% of the participants in that group correctly responded to the question. The Fisher exact test was used to assess for statistical significance between both groups for each question. A P value !.05 was considered significant. The total number of correct responses (0-12) was tabulated for each group.
Management of suspected pancreatic cystic neoplasms
The characteristics of both groups of respondents are shown in Table 1. In the general group, 28.2% of respondents were GI surgeons compared with 4.8% in the EUS group (P ! .001). Both groups were predominantly men (P Z .59) and younger than 46 years of age (P Z .09). More EUS group members (88.1%) were within 15 years of fellowship training than general group members (65.9%, P Z .04). In terms of the practice setting, the general group of GI specialists was predominantly in private practice (59.5%), and EUS specialists were predominantly in full-time academic positions (54.8%); P ! .001. Two thirds of the EUS group reported some form of academic practice (full-time or part-time) compared with the general group in which only 36.3% reported academic involvement (Table 1). When assessing access to advanced endoscopic procedures, there was no significant difference between the 2 groups in terms of ERCP availability (96.8% vs 100%, P Z .60); however, only 83.6% of the general group reported access to EUS (P Z .01). The number of patients with pancreatic cysts seen annually among both groups is shown in Table 2. Nearly half of the respondents in the general group (49.5%) reported caring for fewer than 5 patients per year with pancreatic cysts. In the EUS group, the majority of respondents (54.8%) saw between 21 and 50 pancreatic cyst cases per year, and 14.3% saw more than 50 cysts per year. These differences were statistically significant (P ! .001).
Section 2: clinical vignettes
Questionnaire response rates were tabulated for both groups of participants. In the general group of GI specialists, 8.8% of the people who received the e-mail solicitation completed the survey (220/2500). In the EUS group, 9.7% of EUS-SIG members responded (42/431).
In each clinical vignette, all participants were initially asked for the most appropriate ‘‘next best test of choice’’ when discovering an incidentally found lesion of 9 mm, 22 mm, and 34 mm in size. In the 9-mm vignette, 78.6% of the EUS group respondents opted for direct referral to EUS-guided FNA compared with only 31.4% in the general group (Fig. 1A). According to the IAP guidelines, high-resolution CT (HR-CT) or MRCP is the initially preferred tests when faced with a lesion of this size. In addition, 13.2% of general group members chose to do no further testing, as opposed to only 2.4% in the EUS group. General group members opted for MRCP (25.9%) or HR-CT (22.7%) more frequently overall than EUS group members (9.5% and 2.4%, respectively). These differences across both groups were statistically significant (P! .001). In the 22-mm vignette, a similar trend was seen (Fig. 1B). Again, EUS group members were much more likely to choose EUS-FNA as the next appropriate test (83.3%) compared with members of the general group (46.4%). Furthermore, the desire to first perform MRCP or HR-CT was more common in the general group than the EUS group (25.5% vs 7.1% and 14.6% vs 4.8%, respectively). The IAP guidelines recommend EUS and MRCP (or ERCP) for lesions 1 to 3 cm in size. The differences between the 2 groups were statistically significant (P Z .001).
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RESULTS Section 1: respondent demographics
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TABLE 1. General characteristics of respondents No. total responses
TABLE 1 (continued )
Response ratio (%)
No. total responses
General EUS General EUS P group group group group value Specialty Gastroenterologist
38
60.9
GI surgeon
62
2
28.2
4.8
Other
24
2
10.9
4.8
Total
220
42
90.5 !.001
195
39
88.6
92.9
25
3
11.4
7.1
26-35 y
30
9
13.6
21.4
36-45 y
95
24
43.2
57.1
46-55 y
63
8
28.6
19.0
56-65 y
32
1
14.5
2.4
O65 y
0
0
!1
15
4
6.8
9.5
1-5
53
17
24.1
40.5
6-10
44
6
20.0
14.3
11-15
33
10
15.0
23.8
16-20
29
2
13.2
4.8
21-30
40
2
18.2
4.8
O30
6
1
2.7
2.4
131
9
59.5
21.4 !.001
Full-time academic
61
23
27.7
54.8
Part-time academic
19
5
8.6
11.9
9
5
4.1
11.9
Yes
99
34
45.0
81.0 !.001
No
121
8
55.0
19.0
Yes
213
42
96.8
100
No
7
0
3.2
0
.09
41
19.5
97.6 !.001
No
177
1
80.5
2.4
Yes
184
41
83.6
97.6
No
36
1
16.4
2.4
.01
TABLE 2. Number of patients seen per year with pancreatic cysts No. patients (%) Cysts/y
Years since training .04
Type of practice
Other
43
.59
Age
Private
Yes
Access to EUS
Sex
Women
General EUS General EUS P group group group group value Perform EUS
134
Men
Response ratio (%)
Perform ERCP
Access to ERCP .60
(continued on next page)
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General group
EUS group
P value
%5
109 (49.5)
3 (7.1)
!.001
6-10
56 (25.5)
4 (9.5)
11-20
19 (8.6)
6 (14.3)
21-50
27 (12.3)
23 (54.8)
O50
9 (4.1)
6 (14.3)
The responses for the 34-mm cyst vignette are highlighted in Figure 1C. Guidelines recommend that lesions of this size should be referred for surgical resection. When compared with the 9-mm and 22-mm cyst vignettes, the 34-mm cyst vignette had the greatest proportion of general group members who initially opted for EUS-FNA (48.2% vs the 22-mm and 9-mm scenarios, 46.4% and 31.4%, respectively). However, within the 34-mm vignette, the difference compared with EUS group members for choosing EUS-FNA as the ‘‘next best test of choice’’ was still statistically significant (83.3% vs 48.2%, P ! .001). General group members, however, were more likely to opt for surgery versus the EUS group (11.4% vs 4.8%) and were more likely to choose MRCP (21.4% vs 4.8%) or HR-CT (11.4% vs 2.4%) when managing these larger pancreatic lesions (P! .001). Both groups of respondents were more likely to choose surgery in the 34-mm vignette (general group, 11.4% and EUS group, 4.8%) compared with the 22-mm vignette (general group, 3.6% and EUS group, 2.4%) and the 9-mm vignette (general group, 0% and EUS group, 0%). The ‘‘correct’’ responses to those questions in each clinical vignette designed to compare practice habits with the published IAP guidelines are reported in Table 3. www.giejournal.org
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Management of suspected pancreatic cystic neoplasms
TABLE 3. Scoring sheet for the 4 questions in the 3 different clinical vignettes Score (% correct)* Question no.
General EUS P group group value
9-mm cyst 1 (need for surveillance)
1 (92.3) 1 (97.6) .32
2 (time interval of surveillance)
0 (20.4) 0 (30.9) .24
3 (method of surveillance for branch-duct PMN)
0 (4.1)
4 (agree with management strategy)
0 (42.8) 0 (35.7) .71
0 (2.4)
.67
22-mm cyst 1 (need for surveillance)
1 (89.6) 1 (97.6) .14
2 (time interval of surveillance) 1 (54.0) 1 (59.4) .59
Figure 1. A, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 9-mm pancreatic cyst (P ! .001). B, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 22-mm pancreatic cyst (P Z .001). C, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 34-mm pancreatic cyst (P ! .001).
Overall, both groups had an identical number of correct responses (8/12 [66.7%]). In addition, both groups answered the same questions correctly. In the 9-mm cyst vignette, only 1 of 4 questions (25%) were answered correctly by both groups. However, in the 22-mm and 34-mm vignettes, 4 of 4 (100%) and 3 of 4 (75%) questions were correctly answered, respectively. In question no. 3 of the 22-mm cyst vignette, when participants were told MRI and/or MRCP findings highly suggested a branch-duct IPMN, 78.6% of respondents in the EUS group correctly chose EUS as the ‘‘next best test of choice’’ compared with 59.1% of general group respondents. Although both groups were scored ‘‘correct’’ in answering this questions, the difference between the 2 was statistically significant, P Z .02.
3 (method of surveillance for branch-duct PMN)
1 (59.1) 1 (78.6) .02
4 (agree with management strategy)
1 (69.6) 1 (69.1) .33
34-mm cyst 1 (need for surveillance)
1 (76.4) 1 (88.1) .11
2 (time interval of surveillance) 1 (80.8) 1 (81.6) .93 3 (method of surveillance for branch-duct PMN) 4 (agree with management strategy) Total
0 (41.8) 0 (28.6) .12 1 (58.2) 1 (64.4) .52 8/12
8/12
*Score: 1, if O50% of respondents answered correctly; 0, if %50% of respondents answered correctly.
Both groups of respondents were queried on their opinions regarding the general concept of consensusderived practice guidelines. The overwhelming majority of members agreed with the publication of such guidelines and felt them to be useful for clinical practice (95% general vs 100% EUS, P Z .22). However, only 26.2% of
EUS specialists and 9.6% of the general group reported awareness of the practice guidelines put forth by the IAP (P Z .01). A small proportion of respondents in both groups reported knowledge of practice guidelines published by the American Gastroenterological Association (13.6% general group and 23.8% EUS group, P Z .11), American College of Gastroenterology (13.2% general group and 9.5% EUS group, P Z .62), and the American Pancreatic Association (11.4% general group and 14.3% EUS group, P Z .61). Awareness of the ASGE guidelines was more frequently reported than other guidelines in both groups (47.6% EUS group and 25.5% general group, P Z .01), but this still comprised less than half of respondents in each group. A significant proportion was unsure whether any guideline existed at all (33.3% EUS group and 64.1% general group, P ! .001).
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Section 3: guideline awareness and management questions
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decision regarding the need for surgery versus continued surveillance. Both groups thought strongly that cyst size was an important characteristic (90.5% EUS group vs 91.4% general group, P Z .77). Conversely, EUS specialists more often agreed with the guidelines and thought that large pancreatic-duct diameter (64.3% EUS group vs 42.3% general group, P Z .01), the presence of a mural nodule (85.7% EUS group vs 66.4% general group, P Z .02), and patient symptoms (71.4% EUS group vs 54.1% general group, P Z .04) were strong factors in the risk for malignancy, thus influencing their decision for surgery or surveillance.
DISCUSSION
The differences in responses to 6 key questions that probe the opinions of physicians on the management of pancreatic cysts and IPMNs are shown in Figure 2. In question no. 1 (bottom of Fig. 2), when asked to weigh their agreement with the guidelines that all main-duct IPMNs be referred for surgical resection, 69.2% of the general group agreed with plans for surgery unless there was a specific contraindication. Only 52.4% of EUS specialists agreed with surgical resection when confronted with a presumed main-duct IPMN; this difference was statistically significant (P Z .03). In question no. 2, 49.6% of the general group agreed that the medical literature supports the surveillance of branch-duct IPMNs that do not exhibit features that are a concern for malignancy (true statement according to the guidelines) versus 26.3% of EUS specialists (P ! .001). A similar proportion of general and EUS group members in question no. 3 agreed that cyst size is the most important factor when making a referral for surgery for a suspected IPMN (P Z .06); however, only 35% of general practitioners agreed that there are clear indications in the medical literature for surgical resection (question no. 4) versus 71.5% of EUS group members (P ! .001). When asked if EUS, HR-CT, and MRCP are equivalent in terms of their ability to detect small cystic lesions of the pancreas (question no. 5), EUS specialists more often agreed in the nonsuperiority of these 3 studies (66.7% vs 36.4%, P ! .001). In question no. 6, roughly the same proportion of general group and EUS group agreed that all cysts smaller than 1 cm in size should be evaluated by EUS (39.1% and 40.4%, respectively, P Z .69). Also, to predict the likelihood of cyst malignancy, respondents were asked to choose which characteristics or criteria were most important in making a management
Noninflammatory pancreatic cysts are increasingly discovered with the expanding use of modern-day CTscanners and MRI machines.18,19 Often, patients are incidentally found to have a small cystic lesion in their pancreas on a CT done for the evaluation of renal calculi or another benign disease. After discussion with their primary care physician, they are frequently referred to a gastroenterologist or a GI surgeon for guidance regarding the management of such lesions. The specialist is then forced to make a decision as to which additional tests to order (if any) and whether or not surgical resection of the pancreas should be considered based on the perceived risk of malignancy within the cyst. The difficulties in managing this clinical scenario are many. First, there is a relative lack of strong medical evidence delineating those morphologic features of the cyst that are most suggestive of malignancy. Furthermore, there are scant data regarding which of the currently available noninvasive imaging techniques is most accurate in detecting cyst progression from a benign lesion to a malignant one. Previously published series on the natural history of these noninflammatory cysts mostly come from retrospective studies with small numbers of patients.4-16 Although such studies are useful, they limit the conclusions that may be drawn because of suboptimal design and the introduction of biases. Also, the availability of certain technologic advances, eg, HR-CT (pancreas protocol) and MRCP, or easy referral to an experienced endoscopist who performs EUS may substantially vary depending upon one’s geographical location. Overall, these factors often create difficulty in trying to make management decisions for patients regarding disease surveillance or definitive therapy. During the 11th Congress of the IAP, an expert panel of physicians and surgeons drafted a set of consensus guidelines for the management of IPMNs and MCNs of the pancreas.4 This document has a list of clinical questions regarding the definition and classification of these lesions, the indications for resection, the steps involved in the preoperative evaluation, the method of resection, the
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Figure 2. Responses to 6 key questions regarding the management of pancreatic cysts and IPMNs.
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Management of suspected pancreatic cystic neoplasms
_histologic questions, and the method of follow-up. Each question is answered by reviewing the existing medical literature and then by providing the consensus opinion of the expert panel of IAP members. It has served as a useful document in guiding clinicians with the management of patients who have pancreatic cystic neoplasms, and it is currently considered the criterion standard by several international experts in terms of practice guidelines involving this disease. At the time of this survey, only the ASGE had published similar guidelines to those of the IAP, albeit, the focus of the ASGE guidelines is mainly on the role of endoscopy in the diagnosis and management of cystic lesions of the pancreas.20 The problem with the guidelines from the IAP, however, is that their publication and endorsement by a nonAmerican professional society has limited the widespread dissemination within the United States. This translates into reduced awareness among American practitioners and increases the likelihood of variability in practice. The objective of this study was to assess the awareness of the IAP guidelines and other guidelines, and to describe the variability in practice habits among U.S. gastroenterologists and GI surgeons. These trends were then compared with a group of physicians who, based on their practice of EUS, ‘‘specialize’’ in pancreatic cysts. EUS specialists who participated in this questionnaire study were predominantly full-time academicians who see more than 20 patients per year with pancreatic cysts. Compared with general GI practitioners, this group of physicians reported increased awareness of the current practice guidelines put forth by the IAP. Overall, the greatest variability in practice among EUS specialists and the general group was in their management of small (!1 cm) cystic lesions of the pancreas. Although most agreed that surveillance is necessary, there were differences in terms of the recommended time interval, the appropriate method to be used, and how to manage small branchduct IPMNs (ie, when is the optimal time for surgical resection). In addition, EUS specialists were much more likely to evaluate a pancreatic cyst of any size with EUSFNA as the test of choice, and their chances of referring even a large lesion for surgical resection without prior EUS examination was lower. Different noninvasive imaging techniques, such as MRCP or HR-CT, were also used less often by EUS specialists. Furthermore, EUS specialists demonstrated a smaller proportion of respondents who agreed that suspected main-duct IPMNs, lesions with a reported prevalence of malignancy of 57% to 92%,4 should be referred for surgical resection provided there is no significant operative contraindication. This group was also less likely to acknowledge the body of existing medical literature that supports the surveillance of some branch-duct IPMNs with other noninvasive means, such as HR-CT and MRI and/or MRCP. Why do these differences in practice habits exist? The reason for this is not entirely clear but may be related to
the availability of EUS and a physician’s preference for the trade he or she practices. EUS specialists first favor EUS in the evaluation and management of pancreatic cysts because this is the skill they possess. Reliance on FNA results, or the ability to detect certain ‘‘concerning features’’ by EUS (eg, mural nodule), may afford an endosonographer confidence in the decision to delay surgical referral or continue with EUS surveillance. Conversely, for those physicians who are less familiar with the capabilities of EUS or who practice in an area in which EUS is less accessible, they may be more likely to rely upon other imaging modalities or their local surgical expertise to manage such lesions of the pancreas. Despite these differences, both groups of respondents demonstrated similar consistency with the guidelines, each answering two thirds of questions correctly when deliberately tested on many of their key points. This is somewhat unexpected, because only a small minority of general GI practitioners even reported awareness of the IAP practice guidelines, and most (64.1%) had no knowledge that any guidelines had even been published. One explanation for this perceived lack of awareness may be that physicians are more familiar with position statements and recommendations published by larger, more well-known societies. Practice guidelines put forth by the ASGE20 were reported as the most widely recognized recommendations by both groups of respondents in this study. The evidence that supports the ASGE guidelines on the management of cystic lesions of the pancreas is similar to that used by the IAP in creating their set of recommendations, and familiarity with any formal position statements on this topic may be enough to ‘‘correctly’’ manage pancreatic cysts. Nonetheless, a significant number of participants in both groups (approximately one-third EUS specialists and approximately two-thirds general group) admitted to having no knowledge of any recently published guidelines on this topic, yet their trends in management were both moderately aligned with what is currently recommended by the IAP. This inconsistency may be because of commonsense clinical management of pancreatic cysts or rather a physician’s ability to assimilate evidence-based management strategies from other media sources besides officially published practice guidelines. Medical and surgical symposia, journal article editorials, and electronic newsletter publications are all alternative sources of information that highlight position statements and practice guidelines recommended by national and international societies. This study has several limitations. Like all survey studies, it is subject to recall bias on the part of the respondents. This usually causes some degree of overestimation or underestimation in the number of cases seen per year, success rates in clinical management, and familiarity (or lack of familiarity) with certain practice guidelines. Furthermore, each real-life clinical scenario is different from the next, and what may be considered the appropriate course of management for one patient may
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Management of suspected pancreatic cystic neoplasms
not be true for another. As such, artificial clinical vignettes and test questions tend to pigeonhole participants into only 1 or 2 possible response options, and this may skew actual trends in practice management. Also, although the survey response rate in this study was similar to those previously published,17 the relatively low rate (8.8% general group, 9.7% EUS group) makes it difficult to apply broad generalizability to our findings, and this may account for some of the similarities noted between the 2 groups. In conclusion, awareness of published guidelines on the management of cystic neoplasms of the pancreas was low among both general GI practitioners and EUS specialists. In particular, awareness of the current set of consensus guidelines published by the IAP was only 26.2% among endosonographers and 9.6% among generalists. However, both groups of physicians demonstrated moderate consistency with the IAP guidelines when deliberately tested on several of their key points. The greatest variability in practice between the 2 groups was seen in the management of small cystic lesions !1 cm. Overall, EUS specialists were less likely to refer all main-duct IPMNs for surgery and were more likely to opt for EUS-FNA (compared with HR-CT, MRCP, or surgery) for suspected 9-mm, 22-mm, and 34-mm branch-duct IPMNs.
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7. 8.
9.
10.
11.
12.
13.
14.
15.
16.
ACKNOWLEDGMENTS 17.
We thank James Harper and the Internet technology team of Olympus America for assistance. We appreciate their support in designing the survey Web site and for maintaining the data collection.
18. 19. 20.
REFERENCES 1. Kimura W, Nagai H, Kuroda A, et al. Analysis of small cystic lesions of the pancreas. Int J Pancreatol 1995;18:197-206. 2. Fernandez-del Castillo C, Targarona J, Thayer SP, et al. Incidental pancreatic cysts: clinicopathologic characteristics and comparison with symptomatic patients. Arch Surg 2003;138:427-34. 3. Adsay NV, Klimstra DS, Compton CC. Cystic lesions of the pancreas: introduction. Semin Diagn Pathol 2000;17:1-6. 4. Tanaka M, Chari S, Adsay V, et al. International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology 2006;6: 17-32. 5. Kobari M, Egawa S, Shibuya K, et al. Intraductal papillary mucinous tumors of the pancreas comprise 2 clinical subtypes: differences in clinical characteristics and surgical management. Arch Surg 1999;134:1131-6. 6. Terris B, Ponsot P, Paye F, et al. Intraductal papillary mucinous tumors of the pancreas confined to secondary ducts show less aggressive
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pathologic features as compared with those involving the main pancreatic duct. Am J Surg Pathol 2000;24:1372-7. Doi R, Fujimoto K, Wada M, et al. Surgical management of intraductal papillary mucinous tumor of the pancreas. Surgery 2002;132:80-5. Matsumoto T, Aramaki M, Yada K, et al. Optimal management of the branch duct type intraductal papillary mucinous neoplasms of the pancreas. J Clin Gastroenterol 2003;36:261-5. Choi BS, Kim TK, Kim AY, et al. Differential diagnosis of benign and malignant intraductal papillary mucinous tumors of the pancreas: MR cholangio-pancreatography and MR angiography. Korean J Radiol 2003;4:157-62. Kitagawa Y, Unger TA, Taylor S, et al. Mucus is a predictor of better prognosis and survival in patients with intraductal papillary mucinous tumor of the pancreas. J Gastrointest Surg 2003;7:12-9. Sugiyama M, Izumisato Y, Abe N, et al. Predictive factors for malignancy in intraductal papillary-mucinous tumors of the pancreas. Br J Surg 2003;90:1244-9. Sohn TA, Yeo CJ, Cameron JL, et al. Intraductal papillary mucinous neoplasms of the pancreas: an updated experience. Ann Surg 2004;239:788-99. Salvia R, Ferna´ndez-del Castillo C, Bassi C, et al. Main duct intraductal papillary mucinous neoplasms of the pancreas: clinical predictors of malignancy and long-term survival following resection. Ann Surg 2004;239:678-707. Reddy RP, Smyrk TC, Zapiach M, et al. Pancreatic mucinous cystic neoplasm defined by ovarian stroma: demographics, clinical features, and prevalence of cancer. Clin Gastroenterol Hepatol 2004;2:1026-31. Zamboni G, Scarpa A, Bogina G, et al. Mucinous cystic tumors of the pancreas: clinicopathological features, prognosis, and relationship to other mucinous cystic tumors. Am J Surg Pathol 1999;23:410-22. Thompson LD, Becker RC, Przygodzki RM, et al. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low-grade potential) of the pancreas: a clinicopathological study of 130 cases. Am J Surg Pathol 1999;23:1-16. Yusuf TE, Baron TH. Endoscopic transmural drainage of pancreatic pseudocysts: results of a national and international survey of ASGE members. Gastrointest Endosc 2006;63:223-7. Yeo CJ, Sarr MG. Cystic and pseudocystic diseases of the pancreas. Curr Probl Surg 1994;31:165-243. Brugge WR, Lauwers GY, Sahani D, et al. Cystic neoplasms of the pancreas. N Engl J Med 2004;351:1218-26. Jacobson BC, Baron TH, Adler DG, et al. ASGE guideline: the role of endoscopy in the diagnosis and the management of cystic lesions and inflammatory fluid collections of the pancreas. Gastrointest Endosc 2005;61:363-70.
Received November 12, 2007. Accepted May 12, 2008. Current affiliations: Division of Gastroenterology and Hepatology (J.M.B., E.J.S., S.A.G., S.K., K.B.D., M.I.C., S.B.J.), Johns Hopkins University School of Medicine, Johns Hopkins Hospital, Baltimore, Maryland, Division of Gastroenterology and Hepatology (M.A.E.), University of Alabama at Birmingham School of Medicine, University Hospital, Birmingham, Alabama, USA. Reprint requests: Jonathan M. Buscaglia, MD, Johns Hopkins Hospital, 1830 E. Monument St, Rm 7100-A, Baltimore, MD 21205. If you want to chat with an author of this article, you may contact him at [email protected].
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APPENDIX
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Awareness of guidelines and trends in the management of suspected pancreatic cystic neoplasms: survey results among general gastroenterologists and EUS specialists Jonathan M. Buscaglia, MD, Eun Ji Shin, MD, Samuel A. Giday, MD, Sumit Kapoor, MBBS, MPH, Kerry B. Dunbar, MD, Mohamad A. Eloubeidi, MD, MHS, Marcia I. Canto, MD, MHS, Sanjay B. Jagannath, MD Baltimore, Maryland, Birmingham, Alabama, USA
Background: Although pancreatic cystic neoplasms are widely recognized, practice habits among physicians and awareness of consensus guidelines are currently unknown. Objectives: To assess the awareness of guidelines and describe variability in practice habits among 2 groups: (1) ‘‘general group’’ of gastroenterologists and surgeons and (2) ‘‘EUS group’’ of specialists in EUS. Design: An online survey was sent to randomly selected gastroenterologists and surgeons and e-mailed to members of the American Society for Gastrointestinal Endoscopy (ASGE) Special Interest Group in EUS (EUS-SIG). Results: Response rate for the general group was 8.8% (220/2500) and 9.7% for the EUS group (42/431). EUS specialists were mostly in academic practice (66.7% vs 36.3%, P ! .001) and reported seeing 21 to 50 cysts per year (54.8% vs 12.3%, P ! .001). The majority of the general group (64.1%) was unaware of any published practice guidelines, compared with 33.3% of EUS specialists (P! .001). Awareness of ASGE guidelines was more frequently reported than other guidelines in both groups and yet was still !50% for each group. Both demonstrated moderate consistency with the International Association of Pancreatology guidelines, appropriately answering 66.7% of the questions. For 9-mm lesions, only 25% of the questions were correctly answered in each group. EUS specialists were less likely to refer main-duct intraductal papillary mucinous neoplasms (IPMN) for surgery and more likely to opt for EUS-guided FNA (compared with high-resolution CT, MRCP, or surgery) for 9-mm, 22-mm, and 34-mm branch-duct IPMNs (P % .001). Limitations: Low response rate and recall bias. Conclusions: Awareness of practice guidelines about the management of suspected pancreatic cystic neoplasms is lower among general GI physicians compared with EUS specialists. Among all physicians, the greatest variability in practice is in small (!1 cm) lesions. (Gastrointest Endosc 2009;69:813-20.)
Pancreatic cysts are increasingly recognized because of the widespread use of cross-sectional imaging techniques, such as CT and magnetic resonance imaging (MRI). In a postmortem study, small cystic lesions of the pancreas
Copyright ª 2009 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 doi:10.1016/j.gie.2008.05.036
were discovered in nearly 50% of the 300 tissue samples examined.1 The concern about pancreatic cysts rests in the possibility of neoplasia within the lesion itself. Pancreatic cystic neoplasms account for 10% of all cysts, and the vast majority of these lesions (90%) are 1 of 3 types: intraductal papillary mucinous neoplasms (IPMNs), mucinous cystic neoplasms (MCNs), or serous cystadenomas.2,3 Although serous lesions are regarded as benign neoplasms, IPMNs and MCNs possess significant cancerous potential.4-16 In 2004, during the 11th Congress of the International Association of Pancreatology (IAP), Sendai, Japan, a set of expert consensus guidelines was drafted to aid clinicians in the management of mucinous cystic lesions of the pancreas (IPMNs and MCNs). The publication of these guidelines in 2006 has provided a thorough summary of the existing literature on this topic, and it outlines a concise
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Abbreviations: ASGE, American Society for Gastrointestinal Endoscopy; EUS-guided FNA, EUS-FNA; EUS-SIG, EUS special interest group; HR-CT, high-resolution CT; IAP, International Association of Pancreatology; IPMN, intraductal papillary mucinous neoplasm; MCN, mucinous cystic neoplasm; MRI, magnetic resonance imaging. DISCLOSURE: All authors disclosed no financial relationships relevant to this publication. This study was conducted in collaboration with Olympus America.
Management of suspected pancreatic cystic neoplasms
management strategy for IPMNs and MCNs of all sizes.4 Although many experts regard this publication as the criterion standard in practice guidelines for pancreatic cystic neoplasms, its publication in a non-American journal has limited its widespread endorsement from American professional societies. The aim of our study was to assess physician awareness of the IAP guidelines and other guidelines and to describe the variability in practice habits among 2 groups: (1) a group of U.S. gastroenterologists and GI surgeons (general group) and (2) a group of GI endoscopists who specialize in EUS (EUS group). The practice trends in both groups were then compared with the current set of recommendations put forth by the IAP.
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Capsule Summary What is already known on this topic d
What this study adds to our knowledge d
d
PATIENTS AND METHODS
The International Association of Pancreatology practice guidelines for pancreatic cystic neoplasms have met limited endorsement.
In a survey of gastroenterologists, surgeons, and members of the American Society for Gastrointestinal Endoscopy EUS Special Interest Group, awareness of practice guidelines for the management of suspected pancreatic cystic neoplasms was lower among general GI physicians than EUS specialists. Greatest variability in practice habits is in the management of small cystic lesions !1 cm in size.
Study participants This study was approved by the Johns Hopkins University School of Medicine Institutional Review Board. An Internet, Web-based survey was designed to address the different practice habits of 2 groups of physicians: (1) a general group of gastroenterologists and GI surgeons (general group) and (2) a group of EUS specialists (EUS group). General group members were contacted by e-mail on 2 occasions, between March and May 2006, alerting them to a Web site link that contained the online questionnaire. The e-mail address list of general GI practitioners was obtained from the Medical Marketing Service Corporation (Wood Dale, Ill). Addresses were extracted by Medical Marketing Service Corporation from a large, multimedical professional society database of physicians and other health care workers. Search terms used to create the address list were ‘‘gastroenterologist,’’ ‘‘general surgeon,’’ and ‘‘abdominal surgeon.’’ A total of 2500 e-mail solicitations were sent. EUS specialists participating in this study were members of the Endoscopic Ultrasound Special Interest Group (EUS-SIG) of the American Society for Gastrointestinal Endoscopy (ASGE). Participation was solicited through an advertisement in the February 2007 electronic newsletter that is sent via the Internet to all EUS-SIG members (total of 431 members). The Web-site link to the survey was directly accessible from the electronic newsletter. Individual e-mail addresses of the EUS-SIG members were not disclosed by the ASGE.
The survey was divided into 3 sections. The first section consisted of a series of questions regarding physician demographics. The second section was composed of different clinical vignettes designed to resemble medical board–like questions. The vignettes themselves were modeled around the algorithm for the management of branch-duct IPMNs, published within Figure 10 of the
IAP consensus guidelines by Tanaka et al.4 They described an asymptomatic 55-year-old woman incidentally found to have a small pancreatic cyst on a ‘‘screening whole-body CT scan.’’ This portion of the questionnaire was divided into 3 subsections; each described varying sizes of the cyst on a CT (9, 22, and 34 mm, respectively). In each scenario, participants were first asked their opinion on the next most appropriate test of choice. Then a series of questions followed regarding the management of each cyst. Participants were eventually told which subsequent MRI and/or MRCP imaging was most consistent with a branch-duct IPMN, and more questions then followed. Ultimately, in each of the 3 scenarios, there were 4 questions (12 total) designed to deliberately test participants’ knowledge of the current IAP guidelines on the management of mucinous cysts of the pancreas. The 4 questions in each clinical scenario were similar, yet the characteristics of the cyst and/or patient differed in each vignette. Question no. 1 assessed the need for cyst surveillance. Question nos. 2 and 3 addressed the appropriate time interval for surveillance (if any) and the methods used for surveillance when told the lesion most likely represented a branch-duct IPMN. Question no. 4 slightly altered the clinical vignette and asked participants to weigh their agreement or disagreement (scale 0-10) with a specific management strategy for that particular-sized branchduct IPMN. Participants in both groups were not notified as to the availability or publication of the IAP consensus guidelines before taking the survey. A copy of the survey can be viewed online (Appendix, available online at www.giejournal.org). The third and final section of the survey asked a series of questions on physician awareness of current practice guidelines on the management of cystic neoplasms of the pancreas. Furthermore, it probed the trends in clinical management of pancreatic cysts and presumed IPMNs. Questions ranged from physicians’ thoughts on the most
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optimal imaging techniques, to evidence supporting cyst criteria for malignancy, to personal opinions on the publication of practice guidelines. This section of the questionnaire was modeled after a survey by Yusuf and Baron17 that examined physician practice trends on the endoscopic management of pancreatic pseudocysts. It was presented in a Likert scale format. The survey was posted on a Web site by Olympus America Inc (Center Valley, Pa). It was designed to be interactive and user-friendly, and it was structured such that it could be completed in approximately 10 to 15 minutes. The survey was electronically accessible for a 12-week period of time for both groups of participants. In the general group of gastroenterologists and surgeons, a reminder e-mail message was sent 4 weeks after the initial e-mail distribution. A reminder message was not sent to EUS-SIG members. All responses to the questionnaire were anonymous and were stored in a computerized database.
Statistical analysis All categorical variables that compared the physician demographics among the 2 groups were evaluated by using the Fisher exact test. Likert scale responses were treated as ordinal data and were analyzed by using the nonparametric Kruskal-Wallis test. All statistical analyses were performed by using Stata software, version 9.2 (StataCorp, College Station, Tex). Reported P values were 2-sided statistical tests with P ! .05 as the level of significance. In light of multiple testing of outcome data arising from individual respondents, it is noted that statistical significance would be removed by correction for multiple testing by using the Bonferroni method unless the nominal uncorrected P values have P ! .001. Each group’s responses to the clinical vignettes were compared with each other and to the current IAP guidelines. They were analyzed by assessing the number of ‘‘correct’’ responses. For each of the 12 questions, each group of respondents was scored a ‘‘1’’ if the majority of participants (O50%) answered the question in accordance with the guideline recommendations. A score of ‘‘0’’ was given if %50% of the participants in that group correctly responded to the question. The Fisher exact test was used to assess for statistical significance between both groups for each question. A P value !.05 was considered significant. The total number of correct responses (0-12) was tabulated for each group.
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The characteristics of both groups of respondents are shown in Table 1. In the general group, 28.2% of respondents were GI surgeons compared with 4.8% in the EUS group (P ! .001). Both groups were predominantly men (P Z .59) and younger than 46 years of age (P Z .09). More EUS group members (88.1%) were within 15 years of fellowship training than general group members (65.9%, P Z .04). In terms of the practice setting, the general group of GI specialists was predominantly in private practice (59.5%), and EUS specialists were predominantly in full-time academic positions (54.8%); P ! .001. Two thirds of the EUS group reported some form of academic practice (full-time or part-time) compared with the general group in which only 36.3% reported academic involvement (Table 1). When assessing access to advanced endoscopic procedures, there was no significant difference between the 2 groups in terms of ERCP availability (96.8% vs 100%, P Z .60); however, only 83.6% of the general group reported access to EUS (P Z .01). The number of patients with pancreatic cysts seen annually among both groups is shown in Table 2. Nearly half of the respondents in the general group (49.5%) reported caring for fewer than 5 patients per year with pancreatic cysts. In the EUS group, the majority of respondents (54.8%) saw between 21 and 50 pancreatic cyst cases per year, and 14.3% saw more than 50 cysts per year. These differences were statistically significant (P ! .001).
Section 2: clinical vignettes
Questionnaire response rates were tabulated for both groups of participants. In the general group of GI specialists, 8.8% of the people who received the e-mail solicitation completed the survey (220/2500). In the EUS group, 9.7% of EUS-SIG members responded (42/431).
In each clinical vignette, all participants were initially asked for the most appropriate ‘‘next best test of choice’’ when discovering an incidentally found lesion of 9 mm, 22 mm, and 34 mm in size. In the 9-mm vignette, 78.6% of the EUS group respondents opted for direct referral to EUS-guided FNA compared with only 31.4% in the general group (Fig. 1A). According to the IAP guidelines, high-resolution CT (HR-CT) or MRCP is the initially preferred tests when faced with a lesion of this size. In addition, 13.2% of general group members chose to do no further testing, as opposed to only 2.4% in the EUS group. General group members opted for MRCP (25.9%) or HR-CT (22.7%) more frequently overall than EUS group members (9.5% and 2.4%, respectively). These differences across both groups were statistically significant (P! .001). In the 22-mm vignette, a similar trend was seen (Fig. 1B). Again, EUS group members were much more likely to choose EUS-FNA as the next appropriate test (83.3%) compared with members of the general group (46.4%). Furthermore, the desire to first perform MRCP or HR-CT was more common in the general group than the EUS group (25.5% vs 7.1% and 14.6% vs 4.8%, respectively). The IAP guidelines recommend EUS and MRCP (or ERCP) for lesions 1 to 3 cm in size. The differences between the 2 groups were statistically significant (P Z .001).
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RESULTS Section 1: respondent demographics
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TABLE 1. General characteristics of respondents No. total responses
TABLE 1 (continued )
Response ratio (%)
No. total responses
General EUS General EUS P group group group group value Specialty Gastroenterologist
38
60.9
GI surgeon
62
2
28.2
4.8
Other
24
2
10.9
4.8
Total
220
42
90.5 !.001
195
39
88.6
92.9
25
3
11.4
7.1
26-35 y
30
9
13.6
21.4
36-45 y
95
24
43.2
57.1
46-55 y
63
8
28.6
19.0
56-65 y
32
1
14.5
2.4
O65 y
0
0
!1
15
4
6.8
9.5
1-5
53
17
24.1
40.5
6-10
44
6
20.0
14.3
11-15
33
10
15.0
23.8
16-20
29
2
13.2
4.8
21-30
40
2
18.2
4.8
O30
6
1
2.7
2.4
131
9
59.5
21.4 !.001
Full-time academic
61
23
27.7
54.8
Part-time academic
19
5
8.6
11.9
9
5
4.1
11.9
Yes
99
34
45.0
81.0 !.001
No
121
8
55.0
19.0
Yes
213
42
96.8
100
No
7
0
3.2
0
.09
41
19.5
97.6 !.001
No
177
1
80.5
2.4
Yes
184
41
83.6
97.6
No
36
1
16.4
2.4
.01
TABLE 2. Number of patients seen per year with pancreatic cysts No. patients (%) Cysts/y
Years since training .04
Type of practice
Other
43
.59
Age
Private
Yes
Access to EUS
Sex
Women
General EUS General EUS P group group group group value Perform EUS
134
Men
Response ratio (%)
Perform ERCP
Access to ERCP .60
(continued on next page)
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General group
EUS group
P value
%5
109 (49.5)
3 (7.1)
!.001
6-10
56 (25.5)
4 (9.5)
11-20
19 (8.6)
6 (14.3)
21-50
27 (12.3)
23 (54.8)
O50
9 (4.1)
6 (14.3)
The responses for the 34-mm cyst vignette are highlighted in Figure 1C. Guidelines recommend that lesions of this size should be referred for surgical resection. When compared with the 9-mm and 22-mm cyst vignettes, the 34-mm cyst vignette had the greatest proportion of general group members who initially opted for EUS-FNA (48.2% vs the 22-mm and 9-mm scenarios, 46.4% and 31.4%, respectively). However, within the 34-mm vignette, the difference compared with EUS group members for choosing EUS-FNA as the ‘‘next best test of choice’’ was still statistically significant (83.3% vs 48.2%, P ! .001). General group members, however, were more likely to opt for surgery versus the EUS group (11.4% vs 4.8%) and were more likely to choose MRCP (21.4% vs 4.8%) or HR-CT (11.4% vs 2.4%) when managing these larger pancreatic lesions (P! .001). Both groups of respondents were more likely to choose surgery in the 34-mm vignette (general group, 11.4% and EUS group, 4.8%) compared with the 22-mm vignette (general group, 3.6% and EUS group, 2.4%) and the 9-mm vignette (general group, 0% and EUS group, 0%). The ‘‘correct’’ responses to those questions in each clinical vignette designed to compare practice habits with the published IAP guidelines are reported in Table 3. www.giejournal.org
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TABLE 3. Scoring sheet for the 4 questions in the 3 different clinical vignettes Score (% correct)* Question no.
General EUS P group group value
9-mm cyst 1 (need for surveillance)
1 (92.3) 1 (97.6) .32
2 (time interval of surveillance)
0 (20.4) 0 (30.9) .24
3 (method of surveillance for branch-duct PMN)
0 (4.1)
4 (agree with management strategy)
0 (42.8) 0 (35.7) .71
0 (2.4)
.67
22-mm cyst 1 (need for surveillance)
1 (89.6) 1 (97.6) .14
2 (time interval of surveillance) 1 (54.0) 1 (59.4) .59
Figure 1. A, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 9-mm pancreatic cyst (P ! .001). B, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 22-mm pancreatic cyst (P Z .001). C, Percentage of responses in each group for the ‘‘next best test of choice’’ when faced with an incidentally found 34-mm pancreatic cyst (P ! .001).
Overall, both groups had an identical number of correct responses (8/12 [66.7%]). In addition, both groups answered the same questions correctly. In the 9-mm cyst vignette, only 1 of 4 questions (25%) were answered correctly by both groups. However, in the 22-mm and 34-mm vignettes, 4 of 4 (100%) and 3 of 4 (75%) questions were correctly answered, respectively. In question no. 3 of the 22-mm cyst vignette, when participants were told MRI and/or MRCP findings highly suggested a branch-duct IPMN, 78.6% of respondents in the EUS group correctly chose EUS as the ‘‘next best test of choice’’ compared with 59.1% of general group respondents. Although both groups were scored ‘‘correct’’ in answering this questions, the difference between the 2 was statistically significant, P Z .02.
3 (method of surveillance for branch-duct PMN)
1 (59.1) 1 (78.6) .02
4 (agree with management strategy)
1 (69.6) 1 (69.1) .33
34-mm cyst 1 (need for surveillance)
1 (76.4) 1 (88.1) .11
2 (time interval of surveillance) 1 (80.8) 1 (81.6) .93 3 (method of surveillance for branch-duct PMN) 4 (agree with management strategy) Total
0 (41.8) 0 (28.6) .12 1 (58.2) 1 (64.4) .52 8/12
8/12
*Score: 1, if O50% of respondents answered correctly; 0, if %50% of respondents answered correctly.
Both groups of respondents were queried on their opinions regarding the general concept of consensusderived practice guidelines. The overwhelming majority of members agreed with the publication of such guidelines and felt them to be useful for clinical practice (95% general vs 100% EUS, P Z .22). However, only 26.2% of
EUS specialists and 9.6% of the general group reported awareness of the practice guidelines put forth by the IAP (P Z .01). A small proportion of respondents in both groups reported knowledge of practice guidelines published by the American Gastroenterological Association (13.6% general group and 23.8% EUS group, P Z .11), American College of Gastroenterology (13.2% general group and 9.5% EUS group, P Z .62), and the American Pancreatic Association (11.4% general group and 14.3% EUS group, P Z .61). Awareness of the ASGE guidelines was more frequently reported than other guidelines in both groups (47.6% EUS group and 25.5% general group, P Z .01), but this still comprised less than half of respondents in each group. A significant proportion was unsure whether any guideline existed at all (33.3% EUS group and 64.1% general group, P ! .001).
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decision regarding the need for surgery versus continued surveillance. Both groups thought strongly that cyst size was an important characteristic (90.5% EUS group vs 91.4% general group, P Z .77). Conversely, EUS specialists more often agreed with the guidelines and thought that large pancreatic-duct diameter (64.3% EUS group vs 42.3% general group, P Z .01), the presence of a mural nodule (85.7% EUS group vs 66.4% general group, P Z .02), and patient symptoms (71.4% EUS group vs 54.1% general group, P Z .04) were strong factors in the risk for malignancy, thus influencing their decision for surgery or surveillance.
DISCUSSION
The differences in responses to 6 key questions that probe the opinions of physicians on the management of pancreatic cysts and IPMNs are shown in Figure 2. In question no. 1 (bottom of Fig. 2), when asked to weigh their agreement with the guidelines that all main-duct IPMNs be referred for surgical resection, 69.2% of the general group agreed with plans for surgery unless there was a specific contraindication. Only 52.4% of EUS specialists agreed with surgical resection when confronted with a presumed main-duct IPMN; this difference was statistically significant (P Z .03). In question no. 2, 49.6% of the general group agreed that the medical literature supports the surveillance of branch-duct IPMNs that do not exhibit features that are a concern for malignancy (true statement according to the guidelines) versus 26.3% of EUS specialists (P ! .001). A similar proportion of general and EUS group members in question no. 3 agreed that cyst size is the most important factor when making a referral for surgery for a suspected IPMN (P Z .06); however, only 35% of general practitioners agreed that there are clear indications in the medical literature for surgical resection (question no. 4) versus 71.5% of EUS group members (P ! .001). When asked if EUS, HR-CT, and MRCP are equivalent in terms of their ability to detect small cystic lesions of the pancreas (question no. 5), EUS specialists more often agreed in the nonsuperiority of these 3 studies (66.7% vs 36.4%, P ! .001). In question no. 6, roughly the same proportion of general group and EUS group agreed that all cysts smaller than 1 cm in size should be evaluated by EUS (39.1% and 40.4%, respectively, P Z .69). Also, to predict the likelihood of cyst malignancy, respondents were asked to choose which characteristics or criteria were most important in making a management
Noninflammatory pancreatic cysts are increasingly discovered with the expanding use of modern-day CTscanners and MRI machines.18,19 Often, patients are incidentally found to have a small cystic lesion in their pancreas on a CT done for the evaluation of renal calculi or another benign disease. After discussion with their primary care physician, they are frequently referred to a gastroenterologist or a GI surgeon for guidance regarding the management of such lesions. The specialist is then forced to make a decision as to which additional tests to order (if any) and whether or not surgical resection of the pancreas should be considered based on the perceived risk of malignancy within the cyst. The difficulties in managing this clinical scenario are many. First, there is a relative lack of strong medical evidence delineating those morphologic features of the cyst that are most suggestive of malignancy. Furthermore, there are scant data regarding which of the currently available noninvasive imaging techniques is most accurate in detecting cyst progression from a benign lesion to a malignant one. Previously published series on the natural history of these noninflammatory cysts mostly come from retrospective studies with small numbers of patients.4-16 Although such studies are useful, they limit the conclusions that may be drawn because of suboptimal design and the introduction of biases. Also, the availability of certain technologic advances, eg, HR-CT (pancreas protocol) and MRCP, or easy referral to an experienced endoscopist who performs EUS may substantially vary depending upon one’s geographical location. Overall, these factors often create difficulty in trying to make management decisions for patients regarding disease surveillance or definitive therapy. During the 11th Congress of the IAP, an expert panel of physicians and surgeons drafted a set of consensus guidelines for the management of IPMNs and MCNs of the pancreas.4 This document has a list of clinical questions regarding the definition and classification of these lesions, the indications for resection, the steps involved in the preoperative evaluation, the method of resection, the
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Figure 2. Responses to 6 key questions regarding the management of pancreatic cysts and IPMNs.
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_histologic questions, and the method of follow-up. Each question is answered by reviewing the existing medical literature and then by providing the consensus opinion of the expert panel of IAP members. It has served as a useful document in guiding clinicians with the management of patients who have pancreatic cystic neoplasms, and it is currently considered the criterion standard by several international experts in terms of practice guidelines involving this disease. At the time of this survey, only the ASGE had published similar guidelines to those of the IAP, albeit, the focus of the ASGE guidelines is mainly on the role of endoscopy in the diagnosis and management of cystic lesions of the pancreas.20 The problem with the guidelines from the IAP, however, is that their publication and endorsement by a nonAmerican professional society has limited the widespread dissemination within the United States. This translates into reduced awareness among American practitioners and increases the likelihood of variability in practice. The objective of this study was to assess the awareness of the IAP guidelines and other guidelines, and to describe the variability in practice habits among U.S. gastroenterologists and GI surgeons. These trends were then compared with a group of physicians who, based on their practice of EUS, ‘‘specialize’’ in pancreatic cysts. EUS specialists who participated in this questionnaire study were predominantly full-time academicians who see more than 20 patients per year with pancreatic cysts. Compared with general GI practitioners, this group of physicians reported increased awareness of the current practice guidelines put forth by the IAP. Overall, the greatest variability in practice among EUS specialists and the general group was in their management of small (!1 cm) cystic lesions of the pancreas. Although most agreed that surveillance is necessary, there were differences in terms of the recommended time interval, the appropriate method to be used, and how to manage small branchduct IPMNs (ie, when is the optimal time for surgical resection). In addition, EUS specialists were much more likely to evaluate a pancreatic cyst of any size with EUSFNA as the test of choice, and their chances of referring even a large lesion for surgical resection without prior EUS examination was lower. Different noninvasive imaging techniques, such as MRCP or HR-CT, were also used less often by EUS specialists. Furthermore, EUS specialists demonstrated a smaller proportion of respondents who agreed that suspected main-duct IPMNs, lesions with a reported prevalence of malignancy of 57% to 92%,4 should be referred for surgical resection provided there is no significant operative contraindication. This group was also less likely to acknowledge the body of existing medical literature that supports the surveillance of some branch-duct IPMNs with other noninvasive means, such as HR-CT and MRI and/or MRCP. Why do these differences in practice habits exist? The reason for this is not entirely clear but may be related to
the availability of EUS and a physician’s preference for the trade he or she practices. EUS specialists first favor EUS in the evaluation and management of pancreatic cysts because this is the skill they possess. Reliance on FNA results, or the ability to detect certain ‘‘concerning features’’ by EUS (eg, mural nodule), may afford an endosonographer confidence in the decision to delay surgical referral or continue with EUS surveillance. Conversely, for those physicians who are less familiar with the capabilities of EUS or who practice in an area in which EUS is less accessible, they may be more likely to rely upon other imaging modalities or their local surgical expertise to manage such lesions of the pancreas. Despite these differences, both groups of respondents demonstrated similar consistency with the guidelines, each answering two thirds of questions correctly when deliberately tested on many of their key points. This is somewhat unexpected, because only a small minority of general GI practitioners even reported awareness of the IAP practice guidelines, and most (64.1%) had no knowledge that any guidelines had even been published. One explanation for this perceived lack of awareness may be that physicians are more familiar with position statements and recommendations published by larger, more well-known societies. Practice guidelines put forth by the ASGE20 were reported as the most widely recognized recommendations by both groups of respondents in this study. The evidence that supports the ASGE guidelines on the management of cystic lesions of the pancreas is similar to that used by the IAP in creating their set of recommendations, and familiarity with any formal position statements on this topic may be enough to ‘‘correctly’’ manage pancreatic cysts. Nonetheless, a significant number of participants in both groups (approximately one-third EUS specialists and approximately two-thirds general group) admitted to having no knowledge of any recently published guidelines on this topic, yet their trends in management were both moderately aligned with what is currently recommended by the IAP. This inconsistency may be because of commonsense clinical management of pancreatic cysts or rather a physician’s ability to assimilate evidence-based management strategies from other media sources besides officially published practice guidelines. Medical and surgical symposia, journal article editorials, and electronic newsletter publications are all alternative sources of information that highlight position statements and practice guidelines recommended by national and international societies. This study has several limitations. Like all survey studies, it is subject to recall bias on the part of the respondents. This usually causes some degree of overestimation or underestimation in the number of cases seen per year, success rates in clinical management, and familiarity (or lack of familiarity) with certain practice guidelines. Furthermore, each real-life clinical scenario is different from the next, and what may be considered the appropriate course of management for one patient may
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not be true for another. As such, artificial clinical vignettes and test questions tend to pigeonhole participants into only 1 or 2 possible response options, and this may skew actual trends in practice management. Also, although the survey response rate in this study was similar to those previously published,17 the relatively low rate (8.8% general group, 9.7% EUS group) makes it difficult to apply broad generalizability to our findings, and this may account for some of the similarities noted between the 2 groups. In conclusion, awareness of published guidelines on the management of cystic neoplasms of the pancreas was low among both general GI practitioners and EUS specialists. In particular, awareness of the current set of consensus guidelines published by the IAP was only 26.2% among endosonographers and 9.6% among generalists. However, both groups of physicians demonstrated moderate consistency with the IAP guidelines when deliberately tested on several of their key points. The greatest variability in practice between the 2 groups was seen in the management of small cystic lesions !1 cm. Overall, EUS specialists were less likely to refer all main-duct IPMNs for surgery and were more likely to opt for EUS-FNA (compared with HR-CT, MRCP, or surgery) for suspected 9-mm, 22-mm, and 34-mm branch-duct IPMNs.
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7. 8.
9.
10.
11.
12.
13.
14.
15.
16.
ACKNOWLEDGMENTS 17.
We thank James Harper and the Internet technology team of Olympus America for assistance. We appreciate their support in designing the survey Web site and for maintaining the data collection.
18. 19. 20.
REFERENCES 1. Kimura W, Nagai H, Kuroda A, et al. Analysis of small cystic lesions of the pancreas. Int J Pancreatol 1995;18:197-206. 2. Fernandez-del Castillo C, Targarona J, Thayer SP, et al. Incidental pancreatic cysts: clinicopathologic characteristics and comparison with symptomatic patients. Arch Surg 2003;138:427-34. 3. Adsay NV, Klimstra DS, Compton CC. Cystic lesions of the pancreas: introduction. Semin Diagn Pathol 2000;17:1-6. 4. Tanaka M, Chari S, Adsay V, et al. International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology 2006;6: 17-32. 5. Kobari M, Egawa S, Shibuya K, et al. Intraductal papillary mucinous tumors of the pancreas comprise 2 clinical subtypes: differences in clinical characteristics and surgical management. Arch Surg 1999;134:1131-6. 6. Terris B, Ponsot P, Paye F, et al. Intraductal papillary mucinous tumors of the pancreas confined to secondary ducts show less aggressive
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pathologic features as compared with those involving the main pancreatic duct. Am J Surg Pathol 2000;24:1372-7. Doi R, Fujimoto K, Wada M, et al. Surgical management of intraductal papillary mucinous tumor of the pancreas. Surgery 2002;132:80-5. Matsumoto T, Aramaki M, Yada K, et al. Optimal management of the branch duct type intraductal papillary mucinous neoplasms of the pancreas. J Clin Gastroenterol 2003;36:261-5. Choi BS, Kim TK, Kim AY, et al. Differential diagnosis of benign and malignant intraductal papillary mucinous tumors of the pancreas: MR cholangio-pancreatography and MR angiography. Korean J Radiol 2003;4:157-62. Kitagawa Y, Unger TA, Taylor S, et al. Mucus is a predictor of better prognosis and survival in patients with intraductal papillary mucinous tumor of the pancreas. J Gastrointest Surg 2003;7:12-9. Sugiyama M, Izumisato Y, Abe N, et al. Predictive factors for malignancy in intraductal papillary-mucinous tumors of the pancreas. Br J Surg 2003;90:1244-9. Sohn TA, Yeo CJ, Cameron JL, et al. Intraductal papillary mucinous neoplasms of the pancreas: an updated experience. Ann Surg 2004;239:788-99. Salvia R, Ferna´ndez-del Castillo C, Bassi C, et al. Main duct intraductal papillary mucinous neoplasms of the pancreas: clinical predictors of malignancy and long-term survival following resection. Ann Surg 2004;239:678-707. Reddy RP, Smyrk TC, Zapiach M, et al. Pancreatic mucinous cystic neoplasm defined by ovarian stroma: demographics, clinical features, and prevalence of cancer. Clin Gastroenterol Hepatol 2004;2:1026-31. Zamboni G, Scarpa A, Bogina G, et al. Mucinous cystic tumors of the pancreas: clinicopathological features, prognosis, and relationship to other mucinous cystic tumors. Am J Surg Pathol 1999;23:410-22. Thompson LD, Becker RC, Przygodzki RM, et al. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low-grade potential) of the pancreas: a clinicopathological study of 130 cases. Am J Surg Pathol 1999;23:1-16. Yusuf TE, Baron TH. Endoscopic transmural drainage of pancreatic pseudocysts: results of a national and international survey of ASGE members. Gastrointest Endosc 2006;63:223-7. Yeo CJ, Sarr MG. Cystic and pseudocystic diseases of the pancreas. Curr Probl Surg 1994;31:165-243. Brugge WR, Lauwers GY, Sahani D, et al. Cystic neoplasms of the pancreas. N Engl J Med 2004;351:1218-26. Jacobson BC, Baron TH, Adler DG, et al. ASGE guideline: the role of endoscopy in the diagnosis and the management of cystic lesions and inflammatory fluid collections of the pancreas. Gastrointest Endosc 2005;61:363-70.
Received November 12, 2007. Accepted May 12, 2008. Current affiliations: Division of Gastroenterology and Hepatology (J.M.B., E.J.S., S.A.G., S.K., K.B.D., M.I.C., S.B.J.), Johns Hopkins University School of Medicine, Johns Hopkins Hospital, Baltimore, Maryland, Division of Gastroenterology and Hepatology (M.A.E.), University of Alabama at Birmingham School of Medicine, University Hospital, Birmingham, Alabama, USA. Reprint requests: Jonathan M. Buscaglia, MD, Johns Hopkins Hospital, 1830 E. Monument St, Rm 7100-A, Baltimore, MD 21205. If you want to chat with an author of this article, you may contact him at [email protected].
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APPENDIX
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