In patients with Hirschsprung disease (HSCR), resection of the affected aganglionic bowel segment with pull-through of the normal proximal colon to the rectum is the accepted treatment. Fecal soiling is a frequent, “expected” outcome after surgical correction. Most patients are misdiagnosed as having functional constipation with overflow incontinence. They are treated with laxatives, often with poor outcomes. Fecal incontinence has a significant effect on the quality of life and can be physically, emotionally, and psychologically disabling. In a retrospective study, quality of life was found to correlate directly with fecal continence, and Antao et al did not find any correlation between age and fecal continence (1). This challenged the long-standing myth that fecal incontinence resolves with time (2,3). In addition, fecal incontinence in children with HSCR is frequently underreported by clinicians; incontinence was reported more commonly on patient questionnaires and diaries than in the medical record (4).
There are essentially 2 types of normal colonic motor activities: low-amplitude tonic and phasic contractions, which mix luminal contents; and high-amplitude propagated contractions (HAPCs), which propel stool from the right side of the colon toward the sigmoid colon. HAPCs end in the sigmoid colon and do not traverse through the rectum. The rectal reservoir therefore serves as a “break” to the passage of an HAPC's propelling stool down from the sigmoid colon. Colonic motility increases after a meal (gastrocolonic response) and on awakening (orthocolonic response) (5). Typically, healthy adults have 6 to 12 HAPCs per day, whereas children have several more (6–13). Ethical considerations preclude us from gathering normative manometric data from healthy children. The historical controls have been children who had colonic manometry for a history of constipation.
Di Lorenzo et al (14) reported fecal soiling in 65% of children who had persistent defecatory problems after surgery for HSCR. In children with fecal soiling after surgery for HSCR, 2 physiologically distinct groups were described. In 1 group, HAPCs were found to propagate all the way to the rectum. In the absence of the rectal reservoir, the anal sphincter was insufficient to resist the amplitude of the HAPC, resulting in soiling. In the rest, soiling was thought to be related to overflow incontinence resulting from retained fecal mass. In both groups, colonic motility testing was considered normal. The frequency of HAPCs was not reported in the present study. Although the present study explains the pathophysiology of the individual soiling, the study does not explain why the subset of children after surgery for HSCR has multiple episodes of fecal soiling rather than infrequent episodes. The frequency of HAPCs in the subset of children with multiple soiling episodes may explain this phenomenon.
The hypothesis for this multicenter study was that increased numbers of HAPCs, in the absence of a rectal reservoir, led to daily, multiple episodes of fecal soiling in a subset of patients after surgery for HSCR.
PATIENTS AND METHODS
The present retrospective study was conducted in 2003 at 4 pediatric motility centers in the United States: Cincinnati Children's Hospital, Children's Hospital of Pittsburgh, Tufts University Medical Center, and Kansas University Medical Center. Approval was obtained from the institutional review boards by all of the participating centers. We reviewed records of 59 children who had undergone pull-through surgery for nonsyndromic HSCR and who had both colonic and anorectal manometry studies when they presented with complaints of daily, multiple episodes of fecal soiling. All of the children with soiling had been treated with a variety of laxatives, with persistence of symptoms. None had evidence for a retained aganglionic segment or colitis on repeat rectal biopsies. Anorectal manometry was performed in all of the subjects and showed normal basal anal pressure. None had botulinum toxin injection to the anal sphincters within at least 3 months of the colonic manometry study. We also investigated 25 controls, which included children who were referred for evaluation for chronic constipation, were found to have normal colonic manometry, and were eventually diagnosed as having functional constipation.
Water-perfused manometry catheters were used at all of the centers and were placed with the aid of colonoscopy and fluoroscopy with the tip in the right colon (ascending colon). Manometric methods used were similar at all 4 centers and complied with published standards (15). Recordings were performed during fasting and postprandial states. Bisacodyl was given only if no spontaneous or meal-induced HAPCs were noted.
HAPCs were defined as colonic contractions with amplitudes > 80 mmHg, propagating aborally for a minimum of 30 cm and lasting >10 seconds. The term “colonic inertia” was used to describe an adynamic colon with no HAPCs in the fasting and postprandial states and no response to bisacodyl administration. We did not study the motility index in the fasting and postprandial states because only HAPCs have been shown to be associated with bowel movements (16). The total number of HAPCs was counted manually during fasting and postprandial phases and this number was divided by the number of minutes of recording during each phase to obtain the mean number of HAPCs per minute. Children who had HSCR were categorized a priori based on the absence or presence of HAPCs (Hirschsprung disease group 1 [HD1]: absence of HAPCs in the fasting and postprandial periods; Hirschsprung disease group 2 [HD2]: presence of at least 1 HAPC either spontaneous or meal-induced).
The 2-tailed Student t test was used to compare HAPCs/min in fasting and postprandial states in both groups. Significance was achieved with P < 0.05.
The control group had 25 children (age 6.7 ± 3.5 years; range 17 months–16 years, 12 boys). Eighty-four percent of the children had HAPCs in the fasting state, whereas 92% demonstrated HAPCs in the postprandial state.
The 59 patients with HSCR (age 6.5 ± 3.5 yr; range 16 months–15 years, 48 boys) were divided into 2 groups based on the absence (HD1) or presence (HD2) of HAPCs. HD1 included 21 subjects (35% of all studied) who had no HAPCs in the fasting or postprandial periods. Of these, 13 (22% of all studied) had colonic inertia and the remaining 8 responded to bisacodyl. HD2 included 38 subjects who had significantly more HAPCs/min during the fasting (P = 0.04) and postprandial phases (P < 0.001) when compared with the control group (Table 1). There was a significant increase in HAPC frequency from fasting to the postprandial phase for children in the HD2 group (P = 0.01) but not in controls (P = 0.37). If we consider 2 SD above the mean frequency of HAPCs in the control group as hyperactivity (≥ 0.11 HAPCs/min), then 15 of 38 in HD2 had colonic hyperactivity (Fig. 1) and only 3 in the control group (P = 0.02). Additionally, in HD2 the HAPCs almost always started in the right colon and traversed the entire length of the remaining colon up to the anus (Fig. 2).
Fecal soiling after pull-through surgery for HSCR is a challenging problem in some children. A previous study on children with this problem demonstrated that colonic manometry could show normal findings (majority), complete absence of HAPCs (inertia), or segmental dysmotility of the colon in a minority (14). The authors, however, did not count the frequency of HAPCs to detect colonic hyperactivity as an abnormal finding, and hence these children were included with those with “normal” colonic manometry. On the basis of this evidence, the standard practice in managing these children has been to address fecal impaction, if present, and then treat with laxatives. There is, however, a subset of children within this group that does worse on laxatives. The results of this multicenter study reveal a novel finding that has a significant effect on the understanding and management of this particular cohort. In the HD2 subset, the number of HAPCs in the fasting and postprandial phases were greater than that in controls. Within this group, the increase in HAPCs from the fasting to the postprandial phase was also significant. This hyperactivity of the colon in a cohort of patients after pull-through surgery for HSCR is a new finding. This observation assumes added significance because our controls had higher numbers of HAPCs (fasting and postprandial) compared with historical controls.
Studies in healthy adults note that the total number of HAPCs varies from 6 to 12 times per day (up to 0.008 HAPCs/min), but not all result in a bowel movement (6–12). Di Lorenzo et al (13) reported an inverse correlation of the number of HAPCs and age, such that younger children have more frequent HAPCs than adults, up to several times each hour in infants, resulting in more frequent bowel movements. In healthy adult controls HAPCs in the fasting state are rare and HAPC-like activity after meals has been reported in only 19% to 25% (9,11). The underlying physiological basis for this transition in colonic motor activity from infancy (high) to adulthood (low) has not been elucidated and is a potential area for additional research.
Being a relatively large, nonfunded, multicenter study removes several biases and provides some legitimacy to these results. The major drawback of this study is the control population, which included children with functional constipation, and therefore the data may not truly reflect the norm. Performing invasive studies such as colonic manometry on healthy children has ethical connotations, and it is therefore difficult to obtain normative data.
The pathophysiological basis for colonic hyperactivity observed in some children in the present study is unclear. It is possible that the hyperactivity exists even before surgery and reflects an imbalance in the excitatory and inhibitory neuronal control of colonic motor activity. The only way to address this issue would be to perform manometry before pull-through surgery, which would be rather impractical in the setting of a potentially life-threatening disease. If the hyperactivity noted is a result of surgical resection of the aganglionic bowel, it is possible that inadvertent severance of an inhibitory nerve or neuronal circuitry that travels aborally from the rectum results in removal of an inhibitory influence, thereby causing hyperactivity. Detailed histological examination of full-thickness colonic biopsies may provide helpful information to explain the colonic hyperactivity observed. Although we do not have information on the frequency of enterocolitis in the HD2, it is likely that multiple episodes of inflammation could have altered the neural control of colonic motor function, resulting in hyperactivity. Another interesting possibility is that children who have this phenotype on manometry may have a specific genotype, raising another potential hypothesis for research.
In summary, we describe a novel and distinct manometric feature to explain daily, frequent soiling in some children after pull-through surgery for HSCR. They typically do not present with a history of withholding, and rectal examination is unremarkable with soft stool in a nondilated neorectum with an intact dentate line. Abdominal x-ray or contrast enema usually shows a nondilated colon, with no caliber change and without excessive fecal load. It is imperative that distinction be made between those with colonic hyperactivity and those without because the management strategies are completely different in the 2 conditions: 1 group requiring laxatives and the other avoidance of laxatives.
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