Journal of Pediatric Gastroenterology and Nutrition Publish Ahead of Print DIAGNOSTIC TESTS IN PEDIATRIC CONSTIPATION
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1 Journal of Pediatric Gastroenterology and Nutrition Publish Ahead of Print DOI: /MPG DIAGNOSTIC TESTS IN PEDIATRIC CONSTIPATION Renato Tambucci* 1,2, Paolo Quitadamo* 3,4, Nikhil Thapar 5, 6, Letizia Zenzeri 7, Tamara Caldaro 1, Annamaria Staiano 3, Alberto Verrotti 2, Osvaldo Borrelli 5 * Dr Tambucci and Dr Quitadamo equally contributed as First Authors 1 Digestive Endoscopy and Surgery Unit, Bambino Gesù Children s Hospital, IRCCS, Rome, Italy 2 Pediatric Unit, Department of Biotechnological and Applied Clinical Sciences, University of L Aquila, L Aquila, Italy 3 Department of Translational Medical Science, Section of Pediatrics, University Federico II, Naples, Italy 4 Department of Pediatrics, A.O.R.N. Santobono-Pausilipon, Naples, Italy 5 Division of Neurogastroenterology & Motility, Department of Pediatric Gastroenterology, Great Ormond Street Hospital, London, UK 6 Stem Cells and Regenerative Medicine, UCL Institute of Child Health, London, UK. 7 Department of Pediatrics, Santa Maria della Misericordia Hospital, University of Perugia, Perugia, Italy
2 Supportive foundations: This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict-of-interest statement: The authors declare no conflicts of interest. Correspondence to: Renato Tambucci, MD Digestive Endoscopy and Surgery Unit, Bambino Gesù Children s Hospital, IRCCS, Piazza Sant Onofrio 4, 00165, Rome, Italy Phone: , Fax: , renato.tambucci@gmail.com; renato.tambucci@opbg.net. Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal s Web site (
3 ABSTRACT Constipation is one of the most common gastrointestinal symptoms in children. With a median reported prevalence of 12%, it accounts for about 25% of all pediatric gastroenterology consultations. The majority of children suffers functional constipation and do not usually require any diagnostic testing. For those children not responding to conventional medical treatment or in the presence of a more significant clinical picture, however, an accurate instrumental assessment is usually recommended to evaluate either the underlying pathophysiologic mechanisms or a possible organic etiology. The present review analyzes the possible diagnostic investigations for severely constipated children, focusing on their actual indications and their utility in clinical practice. Over the last decade, there has been a remarkable increase in our knowledge of normal and abnormal colonic and anorectal motility in children, and a number of different techniques to measure transit and motility have been developed and are discussed in this narrative review. Key words: constipation; abdominal radiography; colonic transit studies; radiopaque marker test; colonic transit scintigraphy; anorectal manometry; colonic manometry; wireless motility capsule; rectal barostat.
4 WHAT IS KNOWN Constipation is one of the most common gastrointestinal complaints in children. Although most children do not require any diagnostic testing, a detailed assessment including the use of investigative tools is usually recommended in those children not meeting Rome criteria or unresponsive to conventional medical treatment. WHAT IS NEW Over the last decade, there has been a remarkable increase in our knowledge of colonic and anorectal motility, and different techniques to measure transit, motility and sensation have been developed. This review analyzes the possible diagnostic investigations for severely constipated children, focusing on their clinical indications and utility.
5 INTRODUCTION Constipation is one of the most common complaints in children with an estimated prevalence of 12% (1-3). Although several disorders might cause constipation, in more than 90% of children the underlying etiology is unrecognized and children labeled as having functional constipation (FC) (4). The diagnosis of FC is currently based on Rome IV criteria that define functional gastrointestinal disorders in children and have allowed symptom-based diagnosis, irrespective of invasive and expensive procedures (Supplemental Table 1, Supplemental Digital Content 1, (5). The majority of constipated children, indeed, do not require any diagnostic testing. However, almost one-third continue experiencing symptoms throughout adolescence despite medical treatment, giving importance to their early referral to specialized centers to evaluate the underlying pathophysiologic mechanisms or possible organic etiology and ultimately tailor effective treatment (6) (Supplemental Table 2, Supplemental Digital Content 2, Over the last decade, our knowledge of normal colonic and anorectal motility in children has improved remarkably and a number of techniques have been developed to evaluate intestinal sensory-motor function. ABDOMINAL RADIOGRAPHY TO ASSESS FAECAL LOADING A plain abdominal X-ray is often advocated as a first line non-invasive technique for evaluating the presence of fecal impaction, particularly in children with an unclear medical history or unremarkable physical examination. Three scoring systems have been
6 proposed to assess fecal loading severity based on fecal appearance on plain radiograph (Supplemental Table 3, Supplemental Digital Content 3, namely Barr et al, Blethyn et al and Leech et al (7, 8, 13). Conflicting results, however, have since been reported in terms of specificity, sensitivity and inter-observer agreement (9-12, 14). Van den Bosch et al reported good intra- and inter-observer agreement for all 3 scores, with the Leech score showing the highest reproducibility (15). Koh et al similarly suggested the superiority of the Leech score finding, in addition, that all systems scores positively correlated with CTT and negatively with the Bristol stool form scale (16). Conversely, Moylan et al reported poor inter-observer reliability across all available scoring systems (17) and Pensabene et al comparing CTT according to the Arhan method (18), Barr and Leech scores in children with FC or non-retentive fecal incontinence confirmed the limited value of plain abdominal X-rays (19). Two systematic reviews found large heterogeneity in terms of study design and conflicting data, concluding that there was insufficient evidence to support the correlation between symptoms of constipation and fecal loading on abdominal radiographs (20, 21). Based on this evidence, the recently published ESPGHAN and NASPGHAN guidelines concluded that abdominal radiography is not recommended for the diagnosis of FC (4). COLONIC TRANSIT TIME (CTT) STUDIES CTT measurement provides useful information, especially in children with severe and persisting symptoms. The most widely used method to determine CTT in clinical practice is the radiopaque marker (ROM) test (22). It is inexpensive, readily available and provides an accurate approximation of total and segmental CTT (23). Given excellent
7 correlation with scintigraphic techniques, it may be considered the first-line investigation tool in children with refractory constipation (24, 25). Current indications include the discrimination between constipation-related fecal incontinence and non-retentive fecal incontinence as well as between slow-transit constipation (STC) and rectal outlet obstruction. This understanding allows for the tailoring and evaluation of medical and surgical treatments and selection of those children who may benefit from more invasive motility investigations (26). Several ROM test protocols have been suggested, ranging from a single or multiple capsule ingestion followed by single or multiple abdominal X-rays including at fixed times (4 th day or 4 th and 7 th day) (18, 27-31). Amongst these protocols, the most common are the Abrahamsson s (ingestion of 3 sets of distinctive pellets on 3 consecutive days followed by an X-ray on day 7) and Metcalf (X-ray on day 4) methods (23). As the single-radiograph technique allows significant reduction in radiation exposure and provides excellent correlation with other protocols requiring daily radiographs, it is now recognized as the most suitable for children (31). The ROM test can be performed in children as young as 2 years of age (18, 32) Overall CTT is calculated by counting the total number of markers on the plain X- Ray, whereas segmental CTT is based on the number of retained markers in 3 colonic segments, namely right colon, left colon and rectosigmoid region (as described by Arhan et al) (18, 27). The modified Metcalf formula is used to calculate segmental transit time (23, 27). The number of markers per segment has to be multiplied by 1.2, a constant representing the ratio between the period during which the exam is performed (72 hours) and the number of markers ingested (#60), expressed in hours. Patients are considered as
8 having slow CTT when there is a delay in transit with the pellets spread throughout the colon. When the delay occurs in the rectosigmoid, with more than 50% of the markers lying in this area, children are labeled as having rectal outlet obstruction. Normal transit time has been defined as a CTT less than 36 hours (33) (Figure 1). Recently, it has been reported that colonic filling state may considerably influence CTT measurement and the presence of fecal masses might bias CTT results, mimicking colonic inertia. Therefore, bowel disimpaction prior to ROM studies is helpful in avoiding this type of bias (34). SCINTIGRAPHY Colonic scintigraphy is a safe and noninvasive alternative investigation able to evaluate total and regional colonic transit (35-37). The main disadvantages are represented by the need for multiple image acquisition over consecutive days and limited availability due to high costs and need for specialized equipment (36). As images are captured on a g-camera, the radiation burden, comparable to that of two X-rays, does not increase with the number of acquired images (38). Although its comparison with ROM test remains difficult due to the different test dynamics, the administration of radiolabeled meals appears more physiological than the administration of solid indigestible pellets, therefore allowing more reliable measurement of colonic transit (26, 36). 111 In-DTPA (2.8-day half-life) is the most common isotope used for labeling the liquid phase of colonic transit studies, although 99m Tc (6 hours half-life) is also frequently used for labeling the solid test feed, also allowing the assessment of gastric emptying (37-39). The isotopes can be given orally in a non-absorbable form with a test meal [ 99m Tc or 67 Ga (3.2-day half-life)], in water ( 111 In or 67 Ga) or in a capsule coated with a ph
9 sensitive material, which dissolves in the colon or terminal ileum ( 111 In) (40, 41). Theoretically, as 111 In-DTPA can be administered in water, colonic scintigraphy can be performed at any age. Interpretation of scintigraphic colon transit studies requires both analysis of quantitative parameters as well as visual inspection of the images (42). Data analysis and its presentation differ between studies and several reporting methods have been used. Results can be expressed as transit time in hours (T½), percentage of radioactivity retained (%RET), proximal colonic emptying (PCE) or center of mass (25). The geometric center (GC), which has been proposed as a measure of the progression of colon radiotracer activity across the duration of the study, is the weighted average of radioactivity over specific regions of interest (ROI) drawn around bowel segments. A variable number of ROIs, from 5 to 8, has been used across studies and the most commonly used are based on the Mayo Clinic (#5) and Temple University (#7) methods (38, 43, 44) (Supplemental Figure 1, Supplemental Digital Content 4, The GC is calculated by multiplying the fraction of counts in each ROI by the ROI number and summing the products: a low GC value indicates that the center of activity is in the proximal colon, whereas a high GC value indicates that the center of activity is in the rectosigmoid or has already been excreted (46). The GC can be determined for every time point that colon images are acquired. It has been suggested that the time points of greatest interest are 24, 48 and 72 hours (45) (Figure 2). Since healthy individuals typically show complete colon evacuation by 72 hours, some authors suggest imaging only up to 48 hours. However, scans at 72 hours may be required to diagnose functional outlet obstruction or localize segmental abnormalities (37, 38). Since CTT measured by ROM is comparable in children and
10 young adults, it seems reasonable to use scintigraphic reference values derived from adults, although some normative data have been published in children (Supplemental Table 4, Supplemental Digital Content 5, (25). Cook et al performed colonic scintigraphy in 101 constipated children and showed it allows the accurate assessment of segmental colonic transit in children with FC and, by also assessing gastric and small bowel transit in the same study, it might help in identifying children with previously unrecognized pan-intestinal motility disorders (46). Sutcliffe et al, using both visual and quantitative analysis, identified 3 main patterns of transit: normal transit, anorectal hold-up and slow colonic transit. The latter group was further subdivided into pan-colonic delay, discrete hold-up in the transverse colon, and abnormal small and large bowel transit (39). Whether these groups, however, are truly distinct requires further investigation (47). Mugie et al evaluated 26 children with severe constipation who underwent both colonic manometry and colonic scintigraphy showing fair agreement between the two modalities in the categorization of constipation, confirming that scintigraphy should be part of the management of refractory constipation (48). In 2005, a task force committee stated "the scintigraphic method is the only one that reliably allows the determination of both total and regional transit times" (36). In a position paper published in 2011, the American and European Neurogastroenterology and Motility Societies recommended the use of colonic scintigraphy for assessing colonic transit in patients with constipation, despite its limited availability (49). In summary, despite the disadvantages related to the lack of standardization, the wide range of normal values and its limited availability, colonic scintigraphy should be
11 considered as the most sensitive noninvasive method for the evaluation of colonic motility disorders. ANORECTAL MANOMETRY Anorectal manometry (ARM) is a commonly performed test in infants and children with defecation disorders providing an assessment of sensorimotor activity of the rectum and anal region (50). ARM allows direct measurement of anal resting pressures, anal relaxation upon balloon distension (recto-anal inhibitory reflex, RAIR) and squeeze pressures, which predominantly reflect internal and external anal sphincter function respectively. It also indirectly assesses defecation dynamics by measuring the recto-anal pressure gradient during straining and by the rectal balloon expulsion test. ARM is best conducted in a lab with the necessary technical and interpretative expertise. Anal resting pressure and RAIR should be always assessed and can be performed either awake or under sedation, during the test. Squeeze pressure and the recto-anal pressure changes during defecation attempt should also be evaluated when an evacuation disorder is suspected, but they require the child s active participation (Supplemental Table 5, Supplemental Digital Content 6, Indications for ARM include exclusion of Hirschsprung s disease (HD), characterized by a non-relaxing internal anal sphincter (Supplemental Figure 2,, Supplemental Digital Content 7, assessment of fecal incontinence or conversely rectal outlet obstruction as well as the post-surgical assessment of anorectal motility in persistently symptomatic children previously operated for HD or imperforate anus. ARM may also help guide anal treatments, such as the botulinum toxin injection in children with a hypertensive or poorly relaxing anal sphincter (51). In children >1 year, ARM
12 shows similar a diagnostic accuracy to suction rectal biopsy in the diagnosis of HD with a sensitivity of 91% and specificity of 94%. In infants (<1 year of age), however, it is less reliable with an error rate up to 26%, making a rectal biopsy mandatory (52, 53). Although ARM can be done in children of any age, older children (usually >5 years) are typically able to cooperate with the sensory testing and dynamic components of the test (squeeze and bear-down maneuvers). Thus, for younger patients, ARM analysis is usually limited to anal sphincter resting pressure and RAIR assessment. Patients are usually encouraged to defecate prior to the study. If fecal impaction is suspected, an enema or suppository is used to prevent stool interference. Typically, as infants have soft stool no preparation is necessary, stressing again the limited utilization of this test in this age group. Recent years have witnessed considerable advancements in ARM technology, with conventional water-perfused systems gradually being replaced by high-resolution (HRARM) and 3D high-definition manometry (HDARM). Water-perfusion system consists of a flexible PVC catheter (diameter mm) with 4-12 side holes circumferentially/spirally arranged and a central channel for balloon inflation, connected to perfusion apparatus with a pneumo-hydraulic pump. Newer solidstate manometric systems use high-resolution catheters with multiple closely spaced sensors (usually 36 sensors spaced at 0.5 to 1 cm intervals) allowing radial acquisition of pressure data. Data from HRARM can be displayed as topographical plot of intraluminal pressure rather than overlapping line traces (54). Given that catheters with outer diameters <5mm are available, HRARM can, in theory, be done at any age.
13 In adults, the recent advent of HDARM has allowed for the first-time detailed assessment of pressure distribution in the anal canal (55). HDARM has 256 microtransducers distributed circumferentially 3 mm apart, and provides topographical and three-dimensional (3D) pressure gradient representation of the anal canal. In adults, HDARM measurements correlate with anatomic structures defined by MRI or 3Dultrasound (56). Therefore, HDARM allows better definition of the contribution of different components of the anal canal including the puborectalis muscle and the external and internal anal sphincters. Moreover, it evaluates the radial asymmetry of the anal canal, which could not be detected with 2D HRM. This highly integrated method therefore allows for 3D dynamic representation of pressure changes within the anal canal both radially and longitudinally (56). These observations could have a major impact on the future evaluation of patients with incontinence, and may provide a better data and disease classification to inform optimal therapeutic options. Currently, 3DHRAM uses a catheter with an outer diameter of almost 11 mm, which in theory could be used in infants. The linear relationship between catheter outer diameter and intraluminal anal pressure reading (Laplace's law), however, may result in the anal resting pressure being overestimated and anal canal dynamics upon balloon distension being misinterpreted. Although 3DHRAM has been used in children aged 2 years the technology is still in its infancy and likely to become more refined with time including the development of tools specifically designed for young children. Despite its extensive use in clinical practice, validated and reproducible ARM values for children are lacking. A number of different studies involving healthy subjects from varying pediatric age groups have provided baseline data on ARM (Table 1) (57-
14 65). Recently, Banasiuk et al determined normative values from HDARM analysis in a prospective study on 61 healthy children (mean age: 8.28 years, range: 2-17 years) (65). However, the small sample size and heterogeneity in equipment and methodology used in the various studies do not allow for reliable normative data for children. Moreover, it is always important to correlate the findings with symptom presentation. Overall, ARM has been found to be a safe test with rare side effects. A small risk of colonic perforation exists; therefore, care should be taken in the placement and removal of probes. To minimize this risk, ARM should not be performed in children with significant bleeding and severe distal colonic/anorectal inflammatory disorders. COLONIC MANOMETRY Colonic manometry (CM) provides both a qualitative and quantitative assessment of colonic motor function by measuring intraluminal pressures and coordination of colonic muscle pressure activity (50, 66). The 2008 consensus statement from the American Neurogastroenterology and Motility Society recommended the use colonic manometry in children and adults with intractable constipation with evidence of STC in the absence of an evacuatory disorder (67). Moreover, the latest joint ESPGHAN and NASPGHAN guidelines suggest that CM may be indicated in patients with intractable constipation before considering surgical intervention (4). An updated overview about technique, interpretation and indications in children has recently been published by NASPGHAN (50). Nonetheless, the use of CM is far from routine and remains limited to few specialized centers around the world (68). Over the last decade, manometric techniques have sensibly improved from few pressure-recording channels to the development of high-resolution manometry (HRM),
15 enabling more detailed definition of colonic segments and pressure data to be presented as color topographical maps (68). The catheter type, number of recording sites and spacing between sensors differs amongst centers. Currently, there are 2 different types of CM catheters available on the market: water-perfused and solid-state catheters (Supplemental Table 6, Supplemental Digital Content 8, Under anesthesia, the catheter is placed into the colon either endoscopically or utilizing fluoroscopic guidance. During endoscopic placement, the catheter tip may be fixed to the right colon wall using one/two hemostatic clips to minimize catheter dislodgment. A plain X-ray is ideally performed at the beginning and end of the recording to confirm the position of catheter. The recording is usually started 2-4 hours after the placement, when the patient is fully awake. However, recent data suggests that in children with abnormal results on the day of catheter placement the test should repeated the following day given what appear to be significant effects on colonic function and therefore overall interpretation of the study presumably secondary to the anaesthetic and/or instrumentation (69). With regards to the actual procedure the CM recording is usually carried out 1 hour before and after a combined semisolid test meal (20 kcal/kg), and 1 hour after the delivery of 1 or 2 pharmacologic stimuli into the colon. High amplitude propagated contractions (HAPCs) are the most distinctive and best-studied components of colonic motor activity (70). HAPCs are defined as colonic contractions greater than 75 mmhg in amplitude (from 50 to 116 mmhg according to different studies) migrating ab-orally for at least 15 cm (60-74). HAPCs do not to propagate beyond the distal sigmoid colon and often associated with anal relaxation (colo-anal reflex) (74). They may occur spontaneously or in response to a meal, to
16 pharmacological stimulation (bisacodyl, neostigmine or other colonic irritants) or colonic distention (70, 75, 76). HAPCs have been considered the most important marker of colonic neuromuscular integrity and their absence after stimulation taken to imply significant dysfunction of colonic motility. Based on their propagation HAPCs are classified as fully propagated (reach the sigmoid colon; Figure 3 A-B), partially propagated (do not progress beyond the splenic flexure or descending colon; Figure 3 C- D) or absent (no contractions recorded along the whole colon; Figure 3 E-F) (74-78). HAPCs can be also classified as normal and abnormal based on the morphology of the pressure waves within sequences (71). Interestingly, in children with refractory constipation Koppen et al found that the progression of HAPCs is inversely correlated to the diameter of colonic segments, and segmental colonic dilation was associated with premature ending of HAPCs (79). Pharmacologic provocation during CM has become a routine tool for assessing colonic neuromuscular integrity (80-82). It is usually performed with bisacodyl, which is intraluminally infused either into the proximal colon through the central channel of the catheter (or via an ostomy opening if present), or into the rectum. Despite the attempts to define standard protocols, the ideal dose of bisacodyl is still undetermined and the test is usually performed with a dose of 0.2 mg/kg (max 10 mg). However, recent data suggested that in children with STC a double dose of bisacodyl (0.4 mg/kg, max 20 mg) increased the number of HAPCs, improved their propagation toward the distal colon and sharpened their morphology, suggesting that higher doses may be more useful in definitively assessing colonic residual motor function (83).
17 Upon neural and hormonal stimulation, normal colonic activity increases throughout the colon within few minutes after the meal and continues for up to 2½ hours depending on meal composition and caloric content (50). The absence of this gastrocolonic response to a meal could be indicative of abnormalities of the enteric nervous system (50). Another colonic motor pattern, characterized by a less vigorous propulsive activity (amplitude less than 45 mmhg) are low-amplitude propagating contractions (LAPCs), occurring times per day, more often during the daytime after meals and upon waking (70, 84). However, their function as well as the significance of other colonic motor patterns, such as the absence of motor quiescence between bisacodyl-induced HAPSs, antegrade and retrograde cyclic propagating motor patterns, short single antegrade and retrograde events, and pre- and post-prandial long-single contractions is still unknown (70, 84-86). In clinical practice, CM has been proven to have a significant impact on the diagnosis and management of constipation in children. Indeed, the identification and location of colonic motor dysfunction may provide useful information for therapeutic decision-making (50, 80). CM is useful in discriminating between functional constipation and intrinsic colonic dysmotility, in helping to plan surgical interventions in selected patients with constipation refractory to medical therapy, in determining whether a diverted colon may be re-anastomosed, in assessing improvement of colonic dysmotility after long-term use of antegrade colonic enemas (ACE), and in evaluating persistent symptoms following surgery, specifically for HD and anorectal malformations (81, 87-91).
18 In conclusion, CM has become a routine diagnostic test in children with defecatory disorders with clear indications and standardized interpretation, and the advent of high resolution technology is allowing physicians achieve a more in-depth understanding of the physiology/pathophysiology of colonic motor disorders. MAGNETIC RESONANCE IMAGING Magnetic resonance imaging (MRI) might be used to rule out the presence of lumbosacral spine (LSS) abnormalities. Few studies have been performed to quantify the incidence of spinal malformations in children with defecation disorders. In a retrospective study, Rosen et al found LSS malformations in 9% of children with intractable constipation not associated with major neurologic symptoms (92). Later, Bekkali et al prospectively evaluated 130 children with intractable constipation and 28 with nonretentive fecal incontinence undergoing MRI and found LSS malformations in only 3% of children, none of which had clinical neurological features (93). MRI should not be included in the routine workup of children with chronic constipation, whereas it should only be considered when there is strong suspicion of neurologic disorders, such as neurological findings in the lower extremity and midline defects in the skin over the lower back and gluteal cleft manifestations. In conclusion, no evidence supports the use of spinal MRI in patients with intractable constipation without other neurologic abnormalities (4). WIRELESS MOTILITY CAPSULE The wireless motility capsule (WMC) is a novel radiation-free device that provides a comprehensive assessment of gastrointestinal transit and motor function. It
19 allows simultaneous measurements of intraluminal ph, pressure and temperature throughout the entire GI tract (94). The WMC system (Smartpill ) consists of a single-use capsule ( mm), a receiver, and data processing software. The patient ingests the capsule just before a standardized meal and is then discharged wearing the recording device for 3-5 days or until the capsule is excreted. Characteristic patterns of temperature and ph are used to track the capsule throughout the GI tract (time of arrival into the stomach, small intestine, cecum, and eventual exit from the body). This information allows the determination of gastric emptying time (GET), small bowel transit time (SBTT), colonic transit time (CTT) and whole gut transit time (WGTT). In adults, normative values for these parameters have been determined to be 2-5 hours (GET), 2-6 hours (SBTT), hours (CTT) and hours (WGTT) (95). Clinical trials in adults have shown that CTT assessed with WMC is comparable with that assessed by ROM tests in both healthy and constipated subjects (96, 97). In a study on 10 healthy adults who underwent simultaneous whole gut scintigraphy and WMC, good correlation was reported in both GET and WGTT (98). Although WMC has been used to measure contractility pressures in different segments of the gastrointestinal tract in constipated adults (99), its utility in measuring the contractile activity is limited by the presence of a single pressure sensor. Only one study has explored the feasibility of WMC in children referred for gastric scintigraphy and antroduodenal manometry for severe upper gastrointestinal symptoms. The WMC test was found being highly sensitive in detecting gastroparesis and more sensitive than antroduodenal manometry in detecting
20 motor abnormalities (100). To date, no studies have been conducted on constipated children. Although WMC could be considered an alternative tool in evaluating whole gut transit and colonic transit, its role in the routine clinical evaluation and management of children presenting with possible colonic dysmotility is still undetermined. The main drawback of WMC in children could be the practical difficulty of getting them to swallow the capsule as well as the possibility of capsule retention, especially in young children. BAROSTAT The rectal barostat is a valuable tool for assessing rectal muscle tone, pressurevolume relationships, and sensory thresholds (101). It is an electromechanical computerdriven air pump connected to a highly compliant balloon placed in the rectum and its principle relies in maintaining a constant pressure within an air-filled bag placed in the rectum. When the rectum contracts, the barostat aspirates air to maintain a constant intrabag pressure and when the rectum relaxes, air is injected into the barostat bag. The volume of air entering or leaving the bag is an indirect measurement of rectal tone changes. By using a pressure-controlled distending protocol, thresholds for sensation (first sensation, urge to defecate and pain) can be determined. Different protocols have been used to determine visceral sensory threshold, with the ascending method being the most applied in children. It consists of delivering phasic intermittent stimuli of progressively increasing pressures (2-4 mmhg per step) until perceived by the subject. This method may be influenced by psychological bias (fear of pain) because the stimuli are predictable to the subject. To overcome this limit, further distension pressure
21 sequences can be randomly delivered depending on the response of the previous distension (tracking technique). Although the tracking technique is less prone to psychological bias and allows multiple determinations rectal sensitivity threshold, it may transmit multiple painful stimuli that are less acceptable in children (102, 103). Although it was hypothesized that constipated children required higher threshold to trigger rectal sensation, more recent data using the barostat show that only a small proportion of patients have true rectal hyposensitivity (103, 104). The barostat can also be used to assess rectal tone and compliance, which is defined as the ability to stretch (expand) in response to an imposed force and expressed as a pressure-volume relationship (ml/mmhg). It has been shown that although rectal compliance is higher in constipated adolescents compared to those who recovered from constipation, almost half of recovered subjects still had increased rectal compliance (105). Moreover, constipated children with significant increases in rectal compliance have more severe symptoms, and emptying the rectum by a regular use of enemas does not appear to improve rectal compliance (104). Although the use of the barostat has increased our knowledge of the role of rectal sensitivity and compliance in the pathophysiology of defecatory disorders, its use is still limited to the research setting. CONCLUSIONS Considerable progress in assessing colonic and anorectal sensory-motor function has been achieved in the last decades. Although the majority of children with constipation do not require any diagnostic testing, the use some of the tests described above should be
22 considered mainly for those children who are refractory to conventional treatment, as their judicious use might provide invaluable insight into underlying physiopathology and in turn help inform optimal management of these challenging conditions.
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25 17. Moylan S, Armstrong J, Diaz-Saldano D, et al. Are abdominal x-rays a reliable way to assess for constipation? J Urol 2010;184: Arhan P, Devroede G, Jehannin B, et al. Segmental colonic transit time. Dis Colon Rectum 1981;24: Pensabene L, Buonomo C, Fishman L, et al. Lack of utility of abdominal x-rays in the evaluation of children with constipation: comparison of different scoring methods. J Pediatr Gastroenterol Nutr 2010;51: Reuchlin-Vroklage LM, Bierma-Zeinstra S, Benninga MA, et al. Diagnostic value of abdominal radiography in constipated children: a systematic review. Arch Pediatr Adolesc Med 2005;159: Berger MY, Tabbers MM, Kurver MJ, et al. Value of abdominal radiography, colonic transit time, and rectal ultrasound scanning in the diagnosis of idiopathic constipation in children: a systematic review. J Pediatr 2012;161: Hinton JM, Lennard-Jones JE, Young AC. A new method for studying gut transit times using radioopaque markers. Gut 1969;10: Metcalf AM, Phillips SF, Zinsmeister AR, et al. Simplified assessment of segmental colonic transit. Gastroenterology 1987;92: Lundin E, Graf W, Garske U, et al. Segmental colonic transit studies: comparison of a radiological and a scintigraphic method. Colorectal Dis 2007;9: Southwell BR, Clarke MC, Sutcliffe J, et al. Colonic transit studies: normal values for adults and children with comparison of radiological and scintigraphic methods. Pediatr Surg Int 2009;25:
26 26. Tipnis NA, El-Chammas KI, Rudolph CD, et al. Do oro-anal transit markers predict which children would benefit from colonic manometry studies? J Pediatr Gastroenterol Nutr 2012;54: Abrahamsson H, Antov S. Accuracy in assessment of colonic transit time with particles: how many markers should be used? Neurogastroenterol Motil 2010;22: Bouchoucha M, Devroede G, Arhan P, et al. What is the meaning of colorectal transit time measurement? Dis Colon Rectum 1992;35: De Lorijn F, Van Wijk MP, Reitsma JB, et al. Prognosis of constipation: clinical factors and colonic transit time. Arch Dis Child 2004;89: Abrahamsson H, Antov S, Bosaeus I. Gastrointestinal and segmental colonic transit time evaluated by a single abdominal x-ray in healthy subjects and constipated patients. Scand J Gastroenterol 1998;32: Zaslavsky C, da Silveira TR, Maguilnik J. Total and segmental colonic transit time with radio-opaque markers in adolescents with functional constipation. J Pediatr Gastroenterol Nutr 1998;27: Gutiérrez C, Marco A, Nogales A, et al. Total and segmental colonic transit time and anorectal manometry in children with chronic idiopathic constipation. J Pediatr Gastroenterol Nutr 2002;35: Bautista Casasnovas A, Varela Cives R, Villanueva Jeremias A, et al. Measurement of colonic transit time in children. J Pediatr Gastroenterol Nutr 1991;13:42-5.
27 34. Quitadamo P, Thapar N, Staiano A, et al. Effect of Bowel Cleansing on Colonic Transit Time Measurement in Children with Chronic Constipation. J Pediatr 2015;167: Van der Sijp JR, Kamm MA, Nightingale JM, et al. Radioisotope determination of regional colonic transit in severe constipation: comparison with radio opaque markers. Gut 1993;34: Lin HC, Prather C, Fisher RS, et al. Measurement of gastrointestinal transit. Dig Dis Sci 2005;50: Bonapace ES, Maurer AH, Davidoff S, et al. Whole gut transit scintigraphy in the clinical evaluation of patients with upper and lower gastrointestinal symptoms. Am J Gastroenterol 2000;95: Sutcliffe JR, King S, Hutson JM, et al. What is new in radiology and pathology of motility disorders in children? Semin Pediatr Surg 2010;19: Sutcliffe JR, King SK, Hutson JM, et al. Gastrointestinal transit in children with chronic idiopathic constipation. Pediatr Surg Int 2009;25: Burton DD, Camilleri M, Mullan BP, et al. Colonic transit scintigraphy labeled activated charcoal compared with ion exchange pellets. J Nucl Med 1997;38: Stubbs JB, Valenzuela GA, Stubbs CC, et al. A noninvasive scintigraphic assessment of the colonic transit of nondigestible solids in man. J Nucl Med 1991;32: Maurer AH, Camilleri M, Donohoe K, et al. The SNMMI and EANM practice guideline for small-bowel and colon transit 1.0. J Nucl Med 2013;54:
28 43. Camilleri M, Zinsmeister AR. Towards a relatively inexpensive, noninvasive, accurate test for colonic motility disorders. Gastroenterology 1992;103: Szarka LA, Camilleri M. Methods for the assessment of small-bowel and colonic transit. Semin Nucl Med 2012;42: Krevsky B, Malmud LS, D'Ercole F, et al. Colonic transit scintigraphy. A physiologic approach to the quantitative measurement of colonic transit in humans. Gastroenterology 1986;91: Cook BJ, Lim E, Cook D, et al. Radionuclear transit to assess sites of delay in large bowel transit in children with chronic idiopathic constipation. J Pediatr Surg 2005;40: Belkind-Gerson J, Tran K, Di Lorenzo C. Novel techniques to study colonic motor function in children. Curr Gastroenterol Rep 2013;15: Mugie SM, Perez ME, Burgers R, et al. Colonic manometry and colonic scintigraphy as a diagnostic tool for children with severe constipation. J Pediatr Gastroenterol Nutr 2013;57: Rao SS, Camilleri M, Hasler WL, et al. Evaluation of gastrointestinal transit in clinical practice: position paper of the American and European Neurogastroenterology and Motility Societies. Neurogastroenterol Motil 2011;23: Rodriguez L, Sood M, Di Lorenzo C, et al. An ANMS-NASPGHAN consensus document on anorectal and colonic manometry in children. Neurogastroenterol Motil 2017;29.
29 51. Koivusalo AI, Pakarinen MP, Rintala RJ. Botox injection treatment for anal outlet obstruction in patients with internal anal sphincter achalasia and Hirschsprung's disease. Pediatr Surg Int 2009;25: De Lorijn F, Kremer LC, Reitsma JB, et al. Diagnostic tests in Hirschsprung disease: a systematic review. J Pediatr Gastroenterol Nutr 2006;42: Meunier P, Marechal JM, Mollard P. Accuracy of the manometric diagnosis of Hirschsprung s disease. J Pediatr Surg 1978;13: Zar-Kessler C, Belkind-Gerson J. Anorectal Manometry. In: Faure C, Thapar N, Di Lorenzo C. Pediatric Neurogastroenterology, Gastrointestinal Motility and Functional Disorders in Children. 2th ed. Springer International Publishing Switzerland, 2017: Raizada V, Bhargava V, Karsten A, et al. Functional morphology of anal sphincter complex unveiled by high definition anal manometery and three dimensional ultrasound imaging. Neurogastroenterol Motil 2011;23: Ambartsumyan L, Rodriguez L, Morera C, et al. Longitudinal and radial characteristics of intra-anal pressures in children using 3D high-definition anorectal manometry: new observations. Am J Gastroenterol 2013;108: Benninga MA, Wijers OB, van der Hoeven CW, et al. Manometry, profilometry, and endosonography: normal physiology and anatomy of the anal canal in healthy children. J Pediatr Gastroenterol Nutr 1994;18: Sutphen J, Borowitz S, Ling W, et al. Anorectal manometric examination in encopretic-constipated children. Dis Colon Rectum 1997;40:
30 59. Benninga MA, Omari TI, Haslam RR, et al. Characterization of anorectal pressure and the anorectal inhibitory reflex in healthy preterm and term infants. J Pediatr 2001;139: de Lorijn F, Omari TI, Kok JH, et al. Maturation of the rectoanal inhibitory reflex in very premature infants. J Pediatr 2003;143: Hyman PE, Milla PJ, Benninga MA, et al. Childhood functional gastrointestinal disorders: neonate/toddler. Gastroenterology 2006;130: Li ZH, Dong M, Wang ZF. Functional constipation in children: investigation and management of anorectal motility. World J Pediatr 2008;4: Kumar S, Ramadan S, Gupta V, et al. Manometric tests of anorectal function in 90 healthy children: a clinical study from Kuwait. J Pediatr Surg 2009;44: Tang YF, Chen JG, An HJ, et al. High-resolution anorectal manometry in newborns: normative values and diagnostic utility in Hirschsprung disease. Neurogastroenterol Motil 2014;26: Banasiuk M, Banaszkiewicz A, Dziekiewicz M, et al. Values From Threedimensional High-resolution Anorectal Manometry Analysis of Children Without Lower Gastrointestinal Symptoms. Clin Gastroenterol Hepatol 2016;14: e Rao SS, Sadeghi P, Beaty J, et al. Ambulatory 24-h colonic manometry in healthy humans. Am J Physiol Gastrointest Liver Physiol 2001;280:
31 67. Camilleri M, Bharucha AE, di Lorenzo C, et al. American Neurogastroenterology and Motility Society consensus statement on intraluminal measurement of gastrointestinal and colonic motility in clinical practice. Neurogastroenterol Motil 2008;20: Dinning PG, Carrington EV, Scott SM. The use of colonic and anorectal highresolution manometry and its place in clinical work and in research. Neurogastroenterol Motil 2015;7: Arbizu RA, Nurko S, Heinz N, et al. Prospective evaluation of same day versus next day colon manometry results in children with medical refractory constipation. Neurogastroenterol Motil 2017; Scott SM. Manometric techniques for the evaluation of colonic motor activity: current status. Neurogastroenterol Motil 2003;15: Di Lorenzo C, Flores AF, Reddy SN, et al. Use of colonic manometry to differentiate causes of intractable constipation in children. J Pediatr 1992;120: Di Lorenzo C, Flores AF, Reddy SN et al., Colonic manometry in children with chronic intestinal pseudo-obstruction. Gut 1993;34: Di Lorenzo C, Solzi GF, Flores AF, et al. Colonic motility after surgery for Hirschsprung's disease. Am J Gastroenterol 2000;95: Rodriguez, L., A. Siddiqui, and S. Nurko, Internal anal sphincter relaxation associated with bisacodyl-induced colonic high amplitude propagating contractions in children with constipation: a colo-anal reflex? Neurogastroenterol Motil 2012; 24:1023-e545.
32 75. Liem O, van den Berg MM, Mousa HM, et al. Distention of the colon is associated with initiation of propagated contractions in children. Neurogastroenterol Motil 2010;22: Gomez R, Mousa H, Liem O, et al. How do antegrade enemas work? Colonic motility in response to administration of normal saline solution into the proximal colon. J Pediatr Gastroenterol Nutr 2010;51: van den Berg MM, Hogan M, Caniano DA et al. Colonic manometry as predictor of cecostomy success in children with defecation disorders. J Pediatr Surg 2006;41: Aspirot A, Fernandez S, Di Lorenzo C et al Antegrade enemas for defecation disorders: do they improve the colonic motility? J Pediatr Surg 2009;44: Koppen IJN, Thompson BP, Ambeba EJ, et al. Segmental colonic dilation is associated with premature termination of high-amplitude propagating contractions in children with intractable functional constipation. Neurogastroenterol Motil 2017; 29: Dinning PG, Di Lorenzo C. Colonic dysmotility in constipation. Best Pract Res Clin Gastroenterol 2011;25: Pensabene L, Youssef NN, Griffiths JM, et al. Colonic manometry in children with defecatory disorders. role in diagnosis and management. Am J Gastroenterol 2003;98: Hamid SA, Di Lorenzo C, Reddy SN, et al. Bisacodyl and high-amplitudepropagating colonic contractions in children. J Pediatr Gastroenterol Nutr 1998;27:
33 83. Borrelli O, Pescarin M, Saliakellis E, et al. Sequential incremental doses of bisacodyl increase the diagnostic accuracy of colonic manometry. Neurogastroenterol Motil 2016;28: Bassotti G, Clementi M, Antonelli E, et al. Low amplitude propagated contractile waves: a relevant propulsive mechanism of human colon. Dig Liver Dis 2001;33: Giorgio V, Borrelli O, Smith VV, et al. High-resolution colonic manometry accurately predicts colonic neuromuscular pathological phenotype in pediatric slow transit constipation. Neurogastroenterol Motil 2013;25: Wessel S, Koppen IJ, Wiklendt L, et al. Characterizing colonic motility in children with chronic intractable constipation: a look beyond high-amplitude propagating sequences. Neurogastroenterol Motil 2016;28: Martin MJ, Steele SR, Mullenix PS, et al. A pilot study using total colonic manometry in the surgical evaluation of pediatric functional colonic obstruction. J Pediatr Surg 2004;39: Van den Berg MM, Hogan M, Caniano DA, et al. Colonic manometry as predictor of cecostomy success in children with defecation disorders. J Pediatr Surg 2006;41: Tan YW, Borrelli O, Lindley K, et al. Duhamel operation for children with distal colonic dysmotility. Pediatr Surg Int 2017;33: Villarreal J, Sood M, Zangen T, et al. Colonic diversion for intractable constipation in children: colonic manometry helps guide clinical decisions. J Pediatr Gastroenterol Nutr 2001;33:
34 91. Di Lorenzo C, Solzi GF, Flores AF, et al. Colonic motility after surgery for Hirschsprung's disease. Am J Gastroenterol 2000;95: Rosen R, Buonomo C, Andrade R, et al. Incidence of spinal cord lesions in patients with intractable constipation. J Pediatr 2004;145: Bekkali NL, Hagebeuk EE, Bongers ME, et al. Magnetic resonance imaging of the lumbosacral spine in children with chronic constipation or non-retentive fecal incontinence: a prospective study. J Pediatr 2010; 156: Saad RJ. The Wireless Motility Capsule: a One-Stop Shop for the Evaluation of GI Motility Disorders. Curr Gastroenterol Rep 2016;18: Lee YY, Erdogan A, Rao SS. How to assess regional and whole gut transit time with wireless motility capsule. J Neurogastroenterol Motil 2014;20: Rao SS, Kuo B, McCallum RW, et al. Investigation of colonic and whole-gut transit with wireless motility capsule and radiopaque markers in constipation. Clin Gastroenterol Hepatol 2009;7: Camilleri M, Thorne NK, Ringel Y, et al. Wireless ph-motility capsule for colonic transit: prospective comparison with radiopaque markers in chronic constipation. Neurogastroenterol Motil 2010;22: Maqbool S, Parkman HP, Friedenberg FK. Wireless capsule motility: comparison of the SmartPill GI monitoring system with scintigraphy for measuring whole gut transit. Dig Dis Sci 2009;54: Hasler WL, Saad RJ, Rao SS, et al. Heightened colon motor activity measured by a wireless capsule in patients with constipation: relation to colon transit and IBS. Am J Physiol Gastrointest Liver Physiol 2009;297:G
35 100. Green AD, Belkind-Gerson J, Surjanhata BC, et al. Wireless motility capsule test in children with upper gastrointestinal symptoms. J Pediatr 2013;162: Whitehead WE, Delvaux M. Standardization of barostat procedures for testing smooth muscle tone and sensory thresholds in the gastrointestinal tract. The Working Team of Glaxo-Wellcome Research, UK. Dig Dis Sci 1997;42: Faure C. Barostat and Other Sensitivity Tests. In: Faure C, Thapar N, Di Lorenzo C. Pediatric Neurogastroenterology, Gastrointestinal Motility and Functional Disorders in Children. 2th ed. Springer International Publishing Switzerland, 2017: Voskuijl WP, van Ginkel R, Benninga MA, et al. New insight into rectal function in pediatric defecation disorders: disturbed rectal compliance is an essential mechanism in pediatric constipation. J Pediatr 2006;148: Van den Berg MM, Bongers ME, Voskuijl WP, et al. No role for increased rectal compliance in pediatric functional constipation. Gastroenterology 2009;137: Van den Berg MM, Voskuijl WP, Boeckxstaens GE, et al. Rectal compliance and rectal sensation in constipated adolescents, recovered adolescents and healthy volunteers. Gut 2008;57:
36 FIGURE 1 Example of radio-opaque marker (ROM) study in a patient with normal colonic transit time showing only few pellets in the right colon (A), in a patient with rectal outlet obstruction showing more than 50% of the markers lying within the rectosigmoid (B) and in a patient with slow colonic transit showing the pellets spread throughout the colon (C). FIGURE 2 Examples of colonic transit scintigraphy studies performed with 67 Gallium given orally with a standard meal. Patient with slow colonic transit showing abnormal retention of radioisotope throughout the colon with failure of the activity to progress beyond the sigmoid colon at 48 and 72 hours (A). Patient with rectosigmoid outlet obstruction showing normal progression from right to left colon with radioisotope retention into the rectosigmoid colon at 72 hours (B). Patient with normal colonic transit time showing nearly complete rectal emptying at 72 hours (C).
37 FIGURE 3 Examples of conventional (A-C-E) and spatiotemporal plots (B-D-F) in a subject with normal colonic motor activity (A-B), in a subject with left colonic dysmotility (C-D) and in a subject with pan-colonic dysmotility (E-F). In the first patient, upon stimulation with bisacodyl there are thre fully propagated HAPCs throughout the colon into the sigmoid-rectum seen in both (A) conventional manometry (B) spatiotemporal plots. HAPCs sequences show normal propagation, amplitude and morphology. It is also possible to appreciate the presence of the colo-anal reflex, defined as the relaxation of IAS during the occurrence of an HAPC. In the patient with left colonic dysmotility, upon bisacodyl stimulation there are three partially propagated HAPCs stopping at the level of mid descending colon seen in both (C) conventional manometry (D) spatiotemporal plots. Both HAPCs sequences show abnormal propagation, amplitude and morphology. In the left colon, HAPCs followed by a synchronous pressurization with no propagative activity associated with the IAS relaxation (colon-anal reflex). In the patient with pancolonic dymotility, upon stimulation with bisacodyl there is an absence of HAPSs in both (E) conventional manometry (F) spatiotemporal plots. HAPCs = high amplitude propagating contractions, IAS = internal anal sphincter.
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