Capsule endoscopy--not just for the small bowel: a review.

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Capsule endoscopy – not just for the small bowel: a review Expert Rev. Gastroenterol. Hepatol. 9(1), 79–89 (2015)

Clare Elizabeth Parker*1, Christiano Spada2, Mark McAlindon3, Carolyn Davison4 and Simon Panter4 1 Department of Gastroenterology, South Tyneside NHS Foundation Trust, South Tyneside District Hospital Harton Lane, South Shields NE34 0PL, UK 2 European Endoscopy Training Centre, Largo A Gemelli, Rome 00168, Italy 3 Department of Gastroenterology, Sheffield Teaching Hospitals NHS Foundation Trust, Royal Hallamshire Hospital, Glossop Road, Sheffield S10 2JF, UK 4 Department of Gastroenterology, South Tyneside NHS Foundation Trust, South Tyneside District Hospital Harton Lane, South Shields NE34 0PL, UK *Author for correspondence: [email protected]

Video capsule endoscopy is being increasingly used to investigate the esophagus and colon as well as the small bowel. With the advancement of technology used in capsule endoscopy there have been marked improvements in diagnostic rates for colon capsule endoscopy in the detection of colonic polyps and colorectal cancer. It is also being increasingly used in the field if inflammatory bowel disease to investigate for mucosal inflammation and could potentially be used to assess mucosal healing. It also has role in completing the evaluation of colonic pathology in those in whom colonoscopy is incomplete. Esophageal capsule is preferred by patients over esophagogastroduodenoscopy (EGD) but as yet does not rival EGD in terms of diagnostic accuracy however the advent of magnetically steerable capsules may improve this. This review covers advances in the field of colon and esophageal capsule endoscopy; it covers diagnostic capabilities of these 2 tools as well as technical aspects of both procedures and preparation. KEYWORDS: Barrett’s oesophagus • bowel preparation • colon capsule • colorectal polyps • esophageal capsule • esophageal varices

Capsule endoscopy was first described in 2000 [1]. The first capsule endoscopy systems were initially developed for examination of the small bowel that is otherwise difficult to visualize, but demand for minimally invasive ways of visualizing other parts of the gastrointestinal tract has led to the development of capsules specifically designed for the analysis of the colon and the esophagus. In this review, we intend to cover the recent advances in the field of colon and esophageal capsule endoscopy (ECE) including the technology, diagnostic yields in comparison to the gold standard tests of gastroscopy and colonoscopy and also likely future developments in the fields of non-small-bowel capsule endoscopy. Colon capsule – technological aspects

The first generation of capsule with the ability to view the colon (PillCam Colon [CCE1] – Given Imaging, Israel) was on the market from 2006. More recently, a second-generation system has been developed (PillCam COLON 2 (CCE2) – Given Imaging, Israel), which is now US FDA approved. Colon capsule endoscopy 1 (CCE1) was a wireless capsule designed to evaluate the colon, it measured 31 11 mm and had dual cameras to acquire images from both ends with a viewing angle of 156˚ from informahealthcare.com

10.1586/17474124.2014.934357

each end. It recorded images at a rate of 4/s (two from each camera) and had a battery life of approximately 10 h. After the capsule was activated, it transmitted images for 3 min and then entered a sleep mode for 1 h and 45 min to save battery energy. After this hibernation period, it automatically reactivated the standard transmission mode. The timing of this delay enabled reactivation of transmission prior to the IC valve in 98% of the patients. The images transmitted were recorded to a portable external hard drive recorder specifically developed for colon capsule via sensors attached to the patients’ abdomen. After the examination was complete, the recorder was connected to a workstation for download of the images and subsequent reporting. To improve performance in detection of polyps and colorectal cancer (CRC), a secondgeneration colon capsule was developed. Significant improvements were made to the original capsule alongside developments to the data recorder and software for video processing and viewing. CCE2 is slightly larger in dimension, measuring 11.6 31.5 mm and the two imagers have a wider angle of view at 172˚, which allows for almost 360˚ coverage of the colon (see FIGURE 1). It has an adaptive frame rate to improve mucosal coverage and optimize

2015 Informa UK Ltd

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Parker, Spada, McAlindon, Davison & Panter

Figure 1. PillCam colon 2. Reproduced with permission from Given Imaging.

battery life, capturing images at a rate of 35/s when in motion and 4/s when stationary. It also transmits images via an antenna array to the data recorder, which is carried by the patient. CCE2 no longer enters a hibernation mode to conserve battery power. Instead, it employs a low work rate setting where it captures only 14 images per min until it automatically detects the small bowel mucosa, at which point it switches to the adaptive frame rate. A recent paper [2] reported sensitivity rates of 98.3% for automatic detection of small bowel by CCE2. The ability of the capsule to detect small bowel entry makes it possible to automatically alert the patient and medical staff at crucial points in the examination, such as the correct time to administer the first laxative booster, which is not effective until the capsule has passed out of the stomach. During the examination, the data recorder guides the patient and medical staff through the procedure. It buzzes, vibrates and displays instruction numbers on the display to alert the patient to ingest the booster or that the procedure has terminated. This also means that the procedure can be carried out at home. Transfer of recorded images to the workstation for review of videos with RAPID software is similar to that of the first-generation system (and similar to small bowel and esophageal capsule). The second generation of RAPID colon software also includes a tool for polyp size estimation. Preparation

Adequate colon cleansing is a key requirement for CCE as the sensitivity for the detection of significant findings is significantly influenced by colon cleanliness [3] and even small amounts of residual stool may prevent accurate visualization of the mucosa. Washing of the mucosa is clearly not possible in any video capsule examination and as such is more of a ‘physiological’ examination. Standard colonoscopy preparation is not sufficient for CCE as a clear fluid-filled lumen is essential for CCE to work efficiently. Preliminary studies using the 80

same preparation as standard colonoscopy showed inadequate rates of capsule excretion and cleanliness [4]. A different preparation regimen is therefore required and the role of bowel preparation for CCE is threefold: to allow for adequate colonic mucosal visualization, to allow some colonic distension by filling the lumen with clear liquids and to precipitate progression of the capsule through the colon. Different preparation protocols have been described: they usually consist of high volume (~4 l) of polyethylene glycol (PEG) lavage solution combined with sodium phosphate (NaP) boosters plus up to 2 l of additional water. Current European Society of Gastrointestinal Endoscopy (ESGE) guidelines [5] recommend a liquid diet the day before the procedure and a total of 4 l of PEG to be administered in doses the day before and on the day of the examination. Two main split regimens of PEG have been proposed: 3+1 (i.e., 3 l of PEG on the day before and 1 l on the day of CCE) or 2 +2 (i.e., 2 l of PEG on the day before and 2 l on the day of CCE). Although no comparative study is available, the 2+2 regiimen seems to be more acceptable to patients and equally effective in terms of colon cleanliness. The majority of adverse events in the capsule literature are mild-to-moderate events, all related to the ingestion of bowel preparation and there have also been safety concerns about NaP preparations causing acute phosphate nephropathy [6]. In view of this, alternative preparation techniques and boosters have been studied using lower dose preparation, split-dose preparations as well as lower dose NaP boosters and alternative boosters. ESGE recommends avoiding phosphate boosters in those with an increased risk of NaP toxicity such as the elderly and those with hypovolemia, kidney disease, bowel obstruction, colitis and treatment with angiotensin-converting enzyme inhibitors [5]. Lower volume preparations have also been studied. Hartmann et al. [7] looked at low volume PEG and ascorbic acid preparation regimen. This had previously been used in colonoscopy and had been shown to reduce the volume patients need to drink without compromising the efficacy or safety of colonoscopy and is also more acceptable to patients [8]. It reported an adequate level of cleansing in 83% and a capsule excretion rate of 76%. A Japanese multicenter pilot study [9] has looked at reduced volume bowel preparation and compared a reduced volume regimen of 2 l PEG on the day of the procedure with 2 l the day before. They found excellent rates of adequate bowel cleanliness in both groups: 94% in the reduced volume group compared with 86% in the standard volume group. To meet the specific goals of bowel cleansing for CCE as described above, boosters after capsule ingestion have been added to PEG and diet recommendations. The role of boosters administered during capsule progression is not limited to improving colonic cleanliness but includes a propulsive effect by means of a volume effect, allowing the capsule to move in a watery environment. The cumulative dose of NaP booster adopted initially in CCE studies was 75 ml. In order to reduce Expert Rev. Gastroenterol. Hepatol. 9(1), (2015)


Capsule endoscopy

the risk of NaP side effects, a lower NaP dose (total 45 or 55 ml) has been used in the most recent studies on CCE2, with no apparent decrease in CCE excretion rate [10,11]. The use of low-dose NaP boosters is therefore recommended to enhance propulsion in those without contraindications [10,12]. This split-dose low NaP volume booster regimen of preparation seems to be effective in terms of cleansing level and excretion rate. The two most recent studies that evaluated CCE2 utilized the regimen of preparation recommended by the ESGE guidelines as described in TABLE 1 and achieved adequate cleansing in 78–85% of patients and a capsule excretion rate (within 8 h) of 81% [10,11]. Recently, in a large multicenter USA trial, 201 NaP was replaced with an oral solution of sodium sulfate, potassium sulfate and magnesium sulfate (Suprep, Braintree, USA). The authors reported adequate cleansing in 80% of patients and capsule excretion rate (within 10 h) of 91%. Magnesium citrate instead of a sodium phosphate booster has also been used [9]. It is thought that this may have safety benefits over NaP by causing less electrolyte imbalance, but the study had a capsule excretion rate of 71%, which questions the effectiveness of magnesium citrate. The same unsatisfactory results are also reported by Spada et al. [13] who looked at using PEG boosters instead of NaP and found an inferior capsule excretion rate. This study included 40 patients and found 63% sensitivity and 87% specificity, but adequate prep in only 43% with no significant difference between the groups (TABLE 2). As colon cleanliness is an important factor in the diagnostic accuracy of colon capsule, a four-point grading scale was devised [14] and the majority of subsequent trials have used this scale. It classifies the cleanliness level of the colon as poor, fair, good or excellent and was shown to have good interobserver agreement. More recently, it has been suggested that it could be just as effective to simplify this and use a two-grade system of adequate (good or excellent) versus

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Table 1. European society of gastrointestinal endoscopy recommended bowel preparation for PillCam colon 2. ESGE recommended bowel preparation for CCE2 Day 1 All day

Clear liquid diet

Evening

2l PEG

Examination day Morning

2l PEG

PillCam colon ingestion† SB detection

First booster of NaP 30 mls

3 h later

Second booster of NaP 25 mls

2 h later

Suppository if CCE not excreted

†

Domperidone 20 mg tablet if capsule is still in stomach after 2 h. CCE: PillCam colon; ESGE: European society of gastrointestinal endoscopy; NaP: Sodium phosphate; PEG: Polyethylene glycol.

inadequate (fair or poor) [15]. A cleanliness grade of good or excellent is considered adequate for the detection of >5 mm polyps [16]. Thus, in conclusion, the data currently support a preparation of 4 l of PEG administered in a split regimen between the day before and on the day of the examination. Boosters also need to be administered during the procedure to improve CCE excretion rate and complete visualization of the colonic mucosa. In patients without contraindications to NaP, low-dose NaP boosters should be used to achieve adequate CCE excretion rate and should be preferred over higher NaP doses. The use of a prokinetic (usually domperidone) is not routinely recommended unless the capsule stays in the stomach for longer than 1 h.

Table 2. Preparation and capsule excretion rates. Ref.

Study (year)

Preparation (total amount litres)

Booster used (amount, mls)

Capsule excretion rate (%)

Adequate preparation (%)

Eliakim et al. (2006)

PEG (3)

Sodium phosphate (30 + 15)

78

84.4

[23]

Schoofs (2006)

PEG (4)


84

88

[75]

Van Gossum et al. (2009)

PEG (4)


92.8

72

[3]

Eliakim et al. (2009)

PEG (4)

Sodium phosphate (30 + 15–25)

81

78

[10]

Pilz (2010)

PEG (4)


64

81

[76]

Sacher-Huvelin et al. (2010)

PEG (5)


91

55

[24]

Spada et al. (2011)

PEG (4)

Sodium phosphate (30 + 15–25)

85

81

[11]

Spada et al. (2011)

PEG (4)

PEG

75

42.5

[11]

Hartmann et al. (2012)

PEG (2)

PEG

76

83

[12]

Kakagawa et al. (2012)

PEG (2)

Magnesium citrate

71

94

[9]

Kakagawa et al. (2012)

PEG (3)

Magnesium citrate

55

86

[9]

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Contraindications

Contraindications are similar to small bowel capsule, which are few and most of which are relative; for example, swallowing disorders or cardiac pacemaker or defibrillator. Absolute contraindications include suspected or known obstruction, pseudoobstruction, pregnancy and impending MRI [17].The main risk as with small bowel capsule is that of capsule retention. No small bowel retentions of CCE have occurred in published studies so far (the rate of SB retention for SB capsule is 1.4–16% depending on the indication) [18,19] and the same contraindications apply. There has been a case of ‘impaction’ of colon capsule on a large colonic tumor which was detected by real-time viewing and subsequently removed by colonoscopy within hours of capsule ingestion, without causing any obstructive symptoms [20]. CCE1 studies – polyps & CRC

The results of studies using the previous, first generation of colon capsule have been summarized in two meta-analyses [21,22]. They have reported a sensitivity ranging between 71 and 73% for polyps of any size and a specificity of 75 and 89%. For significant CCE findings as defined using the ESGE consensus (polyps of equal or greater than 6 mm in size or more than three polyps of any size), sensitivities were 68 and 69% and specificities 82 and 86%. CCE1 showed an inferior sensitivity for the detection of CRC, diagnosing a total of 20 out of 27 patients diagnosed with CRC at colonoscopy. In the largest trial, it only diagnosed 14 of 19 cancers [3,23,24]. CCE2 studies

The first published literature on CCE2 was an Israeli prospective study published in 2009 [10]. A total of 104 patients were recruited who were scheduled to undergo colonoscopy for either known or suspected colonic disease. The upper age limit of those recruited was 57 years due to concerns about the use of NaP boosters. The preparation regimen used was similar to previous CCE1 studies. A total of 98 patients were included in the final data analysis. Colonic cleanliness was deemed adequate (good or excellent rating) in 78% and capsule excretion occurred within 8 h in 81% of patients. Sensitivities for polyp detection were 87% for >6 mm polyps and 88% for >10 mm polyps. Specificities were 76% for >6 mm polyps and 89% for >10 mm polyps. CCE2 reported >10 mm polyps in 10 patients who had different findings at colonoscopy. In two cases, this was due to size mismatch with the polyp reported as 6–9 mm on colonoscopy. In one patient, a lesion identified as a polyp on CCE was reported as a hemangioma on colonoscopy. Two other patients underwent a further colonoscopy and in one, the polyp identified on CCE was confirmed. In the second case, the polyp was again confirmed on subsequent colonoscopy but was sized at 8 mm. The other five patients were awaiting repeat colonoscopy at the time the paper was published. The second published study was only slightly larger and was a prospective European multicenter trial published in 2011 [11]. 82

A total of 117 patients were randomized, and data from 109 were analyzed. Colon cleansing was adequate in 81% of cases and 88% excreted the capsule after 10 h. In three cases, the capsule impacted against a tumor and was removed at colonoscopy or surgery. Again, the patients selected were those scheduled to undergo colonoscopy for known or suspected colonic disease. Sensitivities were 84% for polyps >6 mm and 88% for polyps >10 mm. Specificities were lower at 64% for >6 mm polyps and 95% for >10 mm polyps. It also picked up three of three colorectal malignancies. There were seven false-negative cases; three were due to size mismatch, that is, polyp measured 6 mm polyps was due to size mismatch, that is, a 10 mm polyp at CCE, this occurred in 20 of 25 cases. No polyp was detected at colonoscopy in the other five cases (CCE detected a >6 mm polyp). The largest study so far of CCE2 by Rex et al. [25] has recently had initial results presented at DDW 2013. This multicenter trial aimed to assess accuracy of CCE compared with colonoscopy for detection of lesions >6 mm. A total of 884 patients were enrolled who underwent CCE and then colonoscopy 4–6 weeks later. If a lesion was found on CCE not detected by initial colonoscopy, then a repeat procedure was performed. A total of 689 patients were included in the final analysis; those with inadequate bowel cleansing were excluded. Overall excretion rate was 91%, and 80% had adequate bowel preparation. Reported sensitivities were 88% for over 6 mm polyps and 92% for over 10 mm polyps, and specificities were 82 and 95%, respectively. There were concerns reported about the pickup of CCE for serrated colonic lesions as a disproportionate number of false negatives had serrated lesions on colonoscopy. Four of four cancers were picked up by CCE2. In conclusion, although three major studies have a different design and methodology, and include different populations, they showed comparable results meaning that potentially this is the accuracy and performance that we might expect to see from CCE2. It should be borne in mind that CCE is being compared to colonoscopy as the gold standard test, but this test does not have a 100% pick-up rate. The pooled miss rate for polyps in colonoscopy studies using back-to-back design was 22% for all adenomas, 2% for >10 mm adenomas, 13% for 5–10 mm and 28% for polyps measuring 1–5 mm [26]. CCE: other indications Inflammatory bowel disease

More recently, there has been increasing interest in the use of CCE for the assessment of inflammatory bowel disease as these patients often undergo repeat procedures, and there is increasing Expert Rev. Gastroenterol. Hepatol. 9(1), (2015)


Capsule endoscopy

importance being placed on mucosal healing as a target for therapy for ulcerative colitis (UC). CCE seems a good option for assessment of disease without the invasiveness of colonoscopy. There have been a few recently published trials of the use of CCE1 to accurately assess inflammatory grading and mucosal damage in UC. The numbers of patients so far are small, 26, 13 and 96 patients, respectively [27–29]. The studies looked at grade of disease activity based on the appearance of the colonic mucosa. Ye et al. [27] showed good agreement with a kappa score of 0.751 for the assessment of degree of inflammation, but only fair agreement with a kappa score of 0.522 for the assessment of extent of disease. Meister et al. [29] showed that colonoscopy was significantly better for detection of mucosal damage than CCE. Sung et al. [28] in the largest study looked at the accuracy of CCE in assessing colonic inflammation and had a sensitivity of 89% to detect active colonic inflammation and a specificity of 75%. These trials have found CCE to be safe in UC but not accurate enough to recommend it to replace colonoscopy without further assessment. It may be that trials with CCE2 may have a better accuracy; however, its utility will always be limited by the inability to obtain histology. Incomplete colonoscopy

There has also been literature describing the use of CCE following failed or incomplete colonoscopy. Spada reported a case in 2008 where CCE allowed complete visualization of the colon following an incomplete colonoscopy secondary to a stricture [30]. This was performed on a patient already enrolled in a CCE trial and therefore had CCE and colonoscopy on the same day. The colonoscopy was incomplete due to a stricture and CCE showed polyps and ulcerations/narrowing. A retrospective series by Triantafyllou et al. reported the use of CCE1 after incomplete colonoscopy and did not find it to be especially helpful [31]. Only 12 patients agreed to undergo CCE, 6 of these were cases of obstructing left-sided tumor and 6 were incomplete due to technical difficulties. They all underwent CCE 4–10 days after colonoscopy, but only one CCE was complete, that is, with visualization of the rectum. In six cases, the capsule stopped recording before the area seen at colonoscopy was reached. Overall, CCE added information in only four cases, polyps in two and diverticular disease in two. A further trial by Triantafyllou et al. [32] published in 2014 looked further at whether CCE was feasible following a failed colonoscopy. This was a prospective follow-up study that followed consecutive outpatients after a colonoscopy failure over 1 year. A total of 75 patients were recruited, one-third had CCE on the day of the failed colonoscopy and the rest were rescheduled due to patient choice and in ability of department to fit in the procedure. This study found that CCE is technically feasible after incomplete colonoscopy in the majority (96%). Additional findings were detected in 36% of same day CCE and 48% of rescheduled CCE; all the findings were located in the previously nonvisualized segment of colon. A study of 34 patients with an incomplete colonoscopy had a completion CCE, which enabled examination of the informahealthcare.com

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nonvisualized part of the colon in 86% of cases, and the findings facilitated a medical decision making resulting in a specific treatment plan in 60% of patients [33]. There has been a small study looking at CCE in comparison with colonoscopy and virtual colonography published only as an abstract [34]. This found that CCE was slightly superior to virtual colonography detecting 63.5% of significant findings compared to 54.5% for colonography and 82% for colonoscopy. More recently, CCE has been compared to CT colonography (CTC) in evaluation of patients with an incomplete colonoscopy. Both procedures were able to complete the examination in 98% of patients and detected a significant finding in 20% of these but the diagnostic yield was significantly higher for significant polyps (>6 mm) in CCE compared with CTC [35]. Limitations/adverse events

Preparation is one limitation as ingestion of high volumes of fluid is required and there are concerns about the nephrotoxic effects of NaP and the majority of reported adverse events in the trials are related to bowel preparation. Adequate preparation is essential for CCE and limits the applicability of colon capsule to some patient groups, for example, the elderly. Currently, only approximately 80% of the patients are reported to have adequate preparation in the studies, further limiting its accuracy, although this is similar to the preparation for colonoscopy with trials demonstrating suboptimal bowel preparation in more than 20% of all colonoscopic examinations [36–38]. The noninferiority of lower volumes of preparation has been demonstrated and this may extend the applicability of CCE. The sensitivity for polyp detection for CCE2 is much improved but is still not sufficient to recommend its routine use over colonoscopy. Further limitations to be considered are the cost of the procedure and the amount of time that is required for capsule reporting, as well as the current lack of guidance for capsule endoscopy training and accreditation. Clearly, the capsule lacks the functionality to obtain histology; however, this limitation may be mitigated against in the future if the current interest in optical diagnosis for colonoscopy is proved to be sensitive and specific and is translatable to capsule studies. Esophageal capsule

The gold standard method of investigating the esophagus is currently esophagogastroduodenoscopy (EGD), and this also allows biopsies and therapeutics as this is an invasive technique with measurable risks. Cardiopulmonary adverse events related to sedation account for up to 60% of adverse events occurring around the time of EGD [39–43], and perforation rates of between 1 in 2500 and 1 in 11,000 are reported [42,44]. It is also expensive and is not always well tolerated by patients. Alternative methods of investigation are needed which should be safe, less invasive, accurate and less expensive than EGD. The first-generation ECE – PillCam esophageal capsule (ESO) (Given Imaging, Israel) was approved by the FDA in 2004 and allowed visualization of the esophagus without sedation and 83


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was better tolerated by the majority of patients [45–48]. PillCam ESO measured 11 26 mm similar dimensions to the small bowel capsule. It had cameras at both ends to acquire images at a rate of 7 frames per s (fps) from each camera, and the battery life was approximately 20 min. Subsequent to this, second- and third-generation ECEs have been developed. PillCam ESO 2 was approved in 2007 and had improved image quality, a 169˚ field of view and an increased capture rate of 18 fps. PillCam ESO 3 was cleared by the FDA in 2011; it has a wider field of view and a capture rate of 35 fps as well as a longer battery life of 30 min. It utilizes the new version of reading software and a new data recorder that has an integrated real-time viewer. PillCam ESO is also equipped with flexible spectral imaging color enhancement (FICE) – a post image acquisition image modification algorithm and may improve lesion detection by enhancing vascular and mucosal patterns. ECE has been used to study patients with a variety of conditions including gastroesophageal reflux disease and esophageal carcinoma. It has been assessed for use as a screening tool in patients at high risk of esophageal squamous cell carcinoma but was not sensitive enough to diagnose neoplastic lesions in comparison to EGD [49]. It has mainly been evaluated in two specific indications: screening for Barrett’s esophagus (BE) and screening for esophageal varices (EVs) Procedure

Originally, the patient required a 6 h fast prior to capsule ingestion. The patient then drank 100 ml of water quickly while standing (to clear bubbles and saliva). Then the capsule was swallowed in the supine position with approximately 10 ml of water, the patient remained supine for 2 min and then the incline of the bed was increased to 30˚ for 2 min, followed by a further increase to 60˚. After 1 min, the patient drank another 10 ml of water, then sat upright and had another 10 ml of water. Following this, they were allowed to get up and walk around until the batteries expired. On completion of the procedure, the images are downloaded. Gralnek et al. have since demonstrated a revised method of ingestion, the Simplified Ingestion Procedure (SIP) significantly improves visualization of the Z line [47]. This has also been confirmed in a subsequent study [48], and SIP has now been adopted as standard of practice. SIP involves fasting for at least 2 h prior to the procedure. While standing, the patient ingests 100 ml of water and is then asked to lie on their right hand side and swallow the PillCam ESO with a sip of water. While remaining on the right hand side, the patient drinks 15 ml of water every 30 s for 7 min. After 7 min, the patient sits upright and drinks another sip of water, waiting a further 30 s, the procedure is then complete. Use of ECE in reflux & screening for BE

BE is a condition with increased risk of esophageal malignancy with a risk of 0.5% of adenocarcinoma per patient-year and may be present in up to 10% of patients with chronic 84

reflux [50]. International guidelines recommend consideration of screening patients with gastro esophageal reflux or other risk factors for the presence of BE [51]. The cost-effectiveness of this strategy remains controversial due to limitations of cost and invasiveness. The first published article on ECE [52] used small bowel capsule to evaluate the esophagus and found that none of the procedures had 100% visualization of the Z line. Ramirez et al. then developed a technique using small bowel capsules attached to strings to attempt to delay transit through the esophagus [53]. Using this technique, they looked at accuracy for the diagnosis of BE (in known BE patients) and found that as a result of longer mean recording times, BE was successfully detected in all 50 patients. Following the development of PillCam ESO 1, an initial pilot feasibility study of 17 patients [45] was conducted and showed that ECE could image the esophagus clearly as well as detect esophagitis. A subsequent multicenter study of 106 patients reported good performance for detecting BE in patients with chronic esophageal reflux disease with sensitivity and specificity of 97 and 99%, respectively, as well as good results (89% sensitivity and 99% specificity) for erosive esophagitis. ECE was found to be much preferred over EGD in these studies [46]. Koslowsky in 2006 evaluated a new device with a higher frame rate of 14 fps in those with known gastroesophageal reflux disease and BE and found a greater sensitivity (100%) than in 4 fps devices [54]. Two subsequent and similar studies both used 14 fps devices and prospectively randomized both chronic reflux patient and those undergoing surveillance for BE. Lin et al. [55] found identical sensitivity (67%) for BE and reflux patients and specificity of 84%. There was no difference in the pickup of long versus short segment BE. Sharma et al. [56] reported a similar sensitivity of 67% and specificity of 87% for BE in reflux patients, but had an improved sensitivity of 79% for known BE patients although specificity was still similar at 78%. Further small studies have found varying results for sensitivity and specificity in the diagnosis of BE in reflux disease [47,48]. Gralnek in 2008 found sensitivity of 100% for BE and specificity of 74%. De Jonge et al. in their comparison of original versus SIP found a sensitivity of 96% and specificity 91% for BE overall. Patients also preferred ECE over EGD with less discomfort and pain during ECE. These data are supported by findings from a meta-analysis (2009) that looked at data from nine studies with a total of 618 patients. The pooled sensitivity was 78% and specificity was 86% [57]. A more recent publication by Mussetto et al. [58] looked at screening for BE in first-degree relatives with reflux symptoms of those with known BE and reported the sensitivity and specificity of ECE as 100 and 70%, respectively, although there were very small numbers analyzed (n = 18) (TABLE 3). In summary, although ECE has moderately high sensitivity and accuracy in diagnosis and surveillance of BE, it is not accurate enough to be recommended as a replacement for EGD. Expert Rev. Gastroenterol. Hepatol. 9(1), (2015)


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The sensitivity of ECE for BE is variable Table 3. Sensitivity and specificity of esophageal capsule for Barrett’s between studies although part of this may oesophagus. be explained by the heterogeneity of the Study (year) Number Sensitivity (%) Specificity (%) Ref. studies in terms of design, especially Eliakim et al. (2005) 106 97 99 [46] regarding selection of patients and interpretation of results, for example, one of Gralnek et al. (2006) 24 100 74 [47] the studies had an adjudication panel. Lin et al. (2007) 90 67 84 [55] There have been studies which suggest Sharma et al. (2008) 94 67 87 [56] that ECE is not cost-effective in comparison to EGD; however, neither study took De Jonge et al. (2008) 30 96 91 [48] into account the tolerability and accept18 100 70 [58] ability of either procedure and any impact Mussetto et al. (2013) this may have. It may also be that if capsule endoscopy becomes more widely available, then this will 50 patients with cirrhosis [66]. They found only moderate agreement with a kappa score of 0.56, and ECE was only accurate have an impact on the cost [59,60]. enough to allow a decision on prophylaxis in 74% of patients. The other Pena et al. was again a small study of only Esophageal varices Screening for EVs in cirrhosis is recommended by AASLD, 20 patients, which identified 9 of 10 patients with grade 2 or BSG ESGE guidelines, and the current gold standard screening larger varices, and of the six patients where ECE had been test for varices is EGD [61,62]. Screening is recommended to unable to diagnose varices; 5 of these were grade 1 [67]. The 2009 study was a multicenter study [68] and graded variallow primary and secondary prophylaxis for EV with either band ligation or b-blockers, the aim being to reduce mortality ces as to whether there would be an indication for a b-blocker due to variceal bleeding. Repeat endoscopy is recommended on or band ligation. About 113 underwent ECE and sensitivity a 1–3 year basis depending on the findings from the baseline was 77%, specificity 86%, with a PPV of 69% and NPV of endoscopy. Adherence to the guidelines can result in multiple 90%. The esophageal recording time was less than 2 min in procedures and can result in reduced compliance and therefore 47% of patients, and it is likely that this will have had an effect effectiveness of screening programs. As a consequence, ECE is on accuracy; however, all patients were adequately classified for being looked to as a potential alternative because trials have indication of b-blocker treatment or band ligation depending suggested much improved patient tolerance that may have a on larger than grade 1 varices or red signs. All patients preferred ECE over EGD. positive effect on uptake. A meta-analysis [69] has also been published, which showed Several studies have looked at PillCam ESO in comparison to EGD for screening of EVs. The initial study in 2006 [63] a pooled sensitivity of 83% and pooled specificity of 85% from three-site pilot study of 32 patients had promising results with a total of nine studies and 631 patients (TABLE 4). In summary, ECE is safe with minimal reported adverse a reported 96.9% overall concordance between ECE and EGD for varices and 90.6% for portal hypertensive gastropathy. events; in the largest study, there were two cases of vomiting of A further pilot study again had only small numbers of patients the capsule due to previously undiagnosed esophageal strictures. (n = 21) and reported sensitivity of 81% with a specificity of It also has greater patient preference than EGD; however, the literature suggests that ECE struggles to adequately diagnose 100% [64]. Subsequently, there have also been larger multicenter trials, small, grade 1, varices but has better diagnostic accuracy for three published in 2008 and one in 2009. The largest of these large varices, although it is not yet comparable to the gold stanwas de Franchis et al. which compared ECE with EGD in dard test of EGD. It may be that for screening purposes, 290 patients with portal hypertension, which demonstrated sensitivity and speciTable 4. Sensitivity and specificity of esophageal capsule for ficity of 84 and 88% [65]. The majority esophageal varices. of cases where varices were missed on ECE were small with only 1.4% of Study (year) Number Sensitivity (%) Specificity (%) Ref. medium or large varices being missed by 32 100 89 [63] ECE. Overall, the agreement between the Eisen et al. (2006) Lapalus et al. (2006) 21 81 100 [64] two tests was deemed to be good with a kappa value of 0.68. However, the overall de Franchis et al. (2008) 288 84 88 [65] recommendation was that EGD be conFrenette et al. (2008) 50 63 82 [66] tinued to be used for screening for EV. Of the smaller studies the first, Pena et al. (2008) 20 68 100 [67] Frenette et al. assessed the utility of ECE Lapalus et al. (2009) 120 77 86 [68] to diagnose and grade varices in informahealthcare.com

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identification of those who require further treatment/ prophylaxis is adequate, and its benefits in terms of uptake would make up for this in a screening program.


Limitations

The main limitations currently are lack of diagnostic accuracy in comparison to EGD. Some of this is likely due to rapid transit through the esophagus, and there is lack of visualization of the stomach, which limits its use for the diagnosis of gastric varices and gastric portal hypertension. The other main limitation is the lack of ability to get histological samples, which is especially an issue for BE cases (surveillance) and its ability to perform therapy for EV meaning the likelihood of a further procedure. The lack of air insufflation means that the existing grading system used for varices diagnosed with EGD is less meaningful in ECE and perhaps, the development of a specific grading system for EV diagnosed by ECE may be helpful. Expert commentary

Of the non-small-bowel capsules currently available, it is colon capsule that currently presents the greatest potential. It is feasible and safe with a low rate of technical failure of 3%, a high rate of capsule excretion and few adverse events. With improved preparation regimens, better optics and field of view, its diagnostic yield has reached acceptable levels especially if one considers that colonoscopy although the ‘gold standard’ has a significant miss rate. However, a major limitation is the inability to remove polyps if found. Currently, ECE is not accurate enough to be recommended as a replacement for the gold standard test of EGD especially for BE; however, this may change if there is ever the introduction of a population-based screening programme due to likely improvements in uptake, given significant patient preference for ECE. It may be that future developments in nonwhite light technology, for example, FICE may bring improvements in ECE for the diagnosis if dysplasia or malignancy in BE as a first-step tool but given the lack of histology, it is unlikely to replace EGD. In terms of EV, which tends to be observational rather than requiring any histology, ECE may well have a role in the future as again its strength lies in it being preferred over EGD as a test. The diagnostic accuracy needs to improve and perhaps, methods to slow esophageal transit may improve diagnostic rates as well as technological advances which will give improved images. ECE has some way to go to find its role in routine clinical practice, but steerable capsule raises exciting possibilities.

acceptance is superior, then this may well mean that CCE has a superior uptake for bowel screening which would make it more cost-effective [70]. It has been used following incomplete colonoscopies and has been shown to be safe and feasible: there is increasing literature on the use of CCE as an alternative to radiological procedures after incomplete colonoscopy, and there is emerging evidence that it may be superior to CTC for the detection of significant polyps. It may be that CCE becomes the tool of choice to complete examination of the colon in those with incomplete colonoscopies. It is unlikely to replace CTC in those referred to avoid preparation with fecal tagging but may be used to replace CTC in those who choose it as they do not wish to undergo colonoscopy. A recent development in capsule technology is the Mirocam Navi system which using magnetic control enables maneuver of a capsule throughout an entire replica colon. The preliminary results of this suggest that it may be feasible to magnetically guide a capsule endoscope in the human colon [71]. Further developments in this field could potentially result in further improvement in the yield of CCE for optical diagnosis which is likely to be where its niche lies. ECE

Improvements in technology and software are likely to mean that ECE will expand in its role as a screening tool especially for the assessment of EV. A string system has previously been used to slow esophageal transit times, and recently the feasibility of using remote magnetic control of wireless capsules in patients has been established [72]. Keller et al. recently used a prototype of a magnetic maneuverable capsule which is a modification of the standard colon capsule with magnetic discs inserted into one dome. It is then controlled by an external magnetic paddle. It did show ability to slow transit through the esophagus. This will allow more detailed assessment of the esophageal mucosa and may well improve diagnostic yield. The use of FICE (Oka et al.) [73] with ECE to help diagnose esophageal malignancy has also been studied, and technological improvements in this may help to diagnose and assess BE and possible esophageal dysplasia. One other role for ECE in the future settings may include the use for risk stratification in the assessment of patients with an upper gastrointestinal bleed to clarify those at low risk of further bleeding who could wait for an EGD. It is currently not ready to be used as a triage tool due to lack of duodenal visualization but again technological advances may improve this [74].

Five-year view CCE

Financial & competing interests disclosure

Given the limitations of CCE, it is unlikely to replace colonoscopy as the gold standard; however, it has been shown to be have very good patient acceptance, suggesting that the main potential for use maybe as a screening tool. Currently, it is suggested that CCE is no more cost-effective than colonoscopy if equal uptake of each test is presumed; however, if patient

C Parker had a previous research post funded by Aquilant. C Spada is a paid consultant for Given Imaging. M McAlindon is supported by Given to attend conferences and has received honoraria from Intromedic Ltd and CapsoVision Ltd for delivering lectures. C Davison has received honoraria in the past as a speaker from Given and Diagmed Healthcare- for past consultancy on national CE nurse training. S Panter is an educational

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Capsule endoscopy

supervisor for Aquilant funded research post as well as being faculty on capsule training course supported by Given imaging and Diagmed. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict

Review

with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the production of this manuscript.


Key issues • PillCam colon capsule endoscopy (CCE) and esophageal capsule endoscopy (ECE) are alternative methods of investigating the colon and esophagus which are both feasible, safe and have benefits in terms of patient preference. • Preparation is a key requirement of CCE. Current recommendations are to use a split-dosing regimen of a total of 4 l of PEG solution plus low-dose phosphate boosters. This achieves an acceptable level of colonic cleanliness and adequate rates of capsule excretion. • CCE1 has an inferior sensitivity for colorectal polyp and cancer detection. Advancements in technology with CCE2 have resulted in much improved diagnostic yield. The three major trials reported sensitivities of 84–88% for 6–9 mm polyps and 88–92% for >10 mm polyps. Reported specificities are 64–82% for 6–9 mm polyps and 89–95% for >10 mm polyps. • CCE is also increasingly being used in the field of inflammatory bowel disease to assess mucosal inflammation although its performance does not yet rival colonoscopy. It is also being looked at as an alternative to CT colonography in patients with a failed colonoscopy, and initial results are promising. • ECE had been evaluated mainly as a screening tool for Barrett’s esophagus and esophageal varices. It has a moderately high sensitivity and accuracy for diagnosis and surveillance of Barrett’s esophagus, but not enough to recommend it as a replacement of EGD. • In varices screening, ECE has a greater patient preference than EGD; however, the literature suggest that ECE is not yet accurate enough to diagnose small, grade 1 varices but has better accuracy for large varices although it is still not comparable to EGD. • Further technological advances with the advent of magnetically maneuverable capsules are currently under evaluation and may well have a positive impact on the diagnostic yield of both ECE and CCE.

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