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Journal of Pediatric Gastroenterology & Nutrition:
doi: 10.1097/MPG.0b013e3182293d8c
Original Articles: Gastroenterology

Heterogeneity of Lower Esophageal Sphincter Function in Children With Achalasia

Morera, Claudio; Nurko, Samuel

Free Access
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Author Information

Center for Motility and Functional Gastrointestinal Disorders, Children's Hospital Boston, Boston, MA.

Address correspondence and reprint requests to Samuel Nurko, MD, MPH, Children's Hospital Boston, 300 Longwood Ave, Boston, MA 02115 (e-mail: samuel.nurko@childrens.harvard.edu).

Received 1 March, 2011

Accepted 18 May, 2011

The present study was supported in part by NIH grant K24-DK082792A (S.N.).

The authors report no conflicts of interest.

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Background and Aim: Achalasia is a rare esophageal motor disorder in children. The manometric hallmarks are esophageal body aperistalsis, lack of lower esophageal sphincter (LES) relaxation, and high LES pressure. However, LES relaxation and function may be heterogeneous, making the diagnosis difficult at times. The aim of the study was to describe LES function in children with achalasia.

Patients and Methods: The present study is a retrospective review of manometric tracings of pediatric patients with achalasia and controls. LES response after each swallow was evaluated. LES parameters were defined as homogeneous (normal or abnormal) if the same response was observed in >75% of swallows. Otherwise, the LES parameters were considered heterogeneous.

Results: Twenty-nine patients with achalasia and 16 control patients were included. All of the controls had normal LES pressure and relaxation in all of the wet swallows. In the achalasia group, some LES relaxation was present in 74% of swallows and 25% of swallows had normal relaxation. Depending on the parameter, a heterogeneous LES (resting pressure, relaxation, residual pressure, and duration of relaxation) was observed in 27.6% to 34.5% of patients with achalasia versus 0% of the controls (P < 0.001). The rest of the patients with achalasia had homogeneous abnormal responses versus homogeneous normal responses in 100% of control patients (P < 0.001).

Conclusions: The LES function in pediatric patients with achalasia is heterogeneous. The classic description of a nonrelaxing high-pressure LES in patients with achalasia is rarely found in children. Partial relaxations are common, and normal relaxations may be present.

Achalasia is a rare esophageal motor disorder particularly in children (1,2) that may be difficult to recognize because there may be an overlap with nonspecific symptoms that may include feeding aversion, failure to thrive, nonspecific regurgitation suggestive of gastroesophageal reflux, and respiratory symptoms (1,3–7).

The diagnosis is suspected based on clinical symptoms and an abnormal esophagogram, but the diagnosis is confirmed by esophageal manometry (1,5). In some cases, particularly early in the disease, there may be no radiographic abnormalities, so the diagnosis must rely only on the manometric findings. The hallmark for manometric diagnosis of achalasia is 100% aperistalsis during wet swallows (5,7). An abnormal relaxation of the lower esophageal sphincter (LES) is usually found. Other supporting findings include increased LES basal pressure and increased gastroesophageal gradient of pressure. There are, however, patients in whom the manometric findings are not clear, particularly because LES function and its response to swallows may appear normal at times, making the diagnosis difficult, particularly early in the disease or in young patients. LES heterogeneity with the possibility of having occasional normal LES relaxation after swallowing has been described in adults (8–10), but it has never been studied or described in children.

Few reports have studied the manometric characteristics of the LES in pediatric patients with achalasia. Most only describe the average resting pressure of the LES and the fact that the sphincter is nonrelaxing (1,11–13). No systematic studies of LES function in children with achalasia have been published. The aim of the present study was to establish the characteristics of LES function in pediatric patients with achalasia.

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This is a retrospective study in which manometric traces of pediatric patients with achalasia evaluated at the Center for Motility and Functional Gastrointestinal Disorders at Children's Hospital Boston were reviewed.

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All of the patients were younger than 18 years and had suggestive symptoms and typical radiologic findings of achalasia, which included abnormal peristalsis by barium study, delayed barium clearance after a 10-minute delayed film, and the characteristic “bird's beak” appearance in the distal esophagus. The diagnosis of achalasia was confirmed with esophageal manometry in which there was aperistalsis in 100% of wet swallows. All of the patients had upper endoscopy and biopsy, which excluded other causes of dysphagia such as eosinophilic or peptic esophagitis, as well as other enteropathies, or other anatomical causes such as rings or esophageal strictures and so on. All of the patients went on to have either pneumatic dilatation or surgical treatment.

A control group was used for comparison. This group included patients in which esophageal manometry was done as part of their evaluation to exclude an esophageal motility disorder. Patients had either noncardiac chest pain or gastroesophageal reflux such as symptoms with a normal radiologic examination, normal esophagogastroduodenoscopy with biopsy, and normal 24-hour intraesophageal pH-metry. All of the control patients had an esophageal manometry reported as “normal” by presently accepted criteria. The study was approved by the institutional review board at Children's Hospital Boston.

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Esophageal Manometry

Esophageal manometry was performed with a continuously perfused low-compliance system following the recommendations of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition (14), American Gastroenterological Association (15), and other experts (3,16). Depending on the size of the patients, either a 4-port 5-cm spacing catheter or a 4-port 2.5-cm spacing catheter was used. With the patient in the supine position, after at least 4 hours of fasting and applying topical anesthesia in the nasal mucosa, a 4-channel pediatric esophageal manometry catheter was advanced until the 4 ports were in the stomach. After a few minutes in the adaptation period, intragastric pressure was considered the “zero” pressure. A slow pull-through was then performed until the LES high-pressure zone was found. The catheter was pulled until the lower transducer was left on the LES high-pressure zone. Ideally, 10 wet swallows with 3 to 5 mL of water were then performed. Given the different size of the pediatric patients, at times it was necessary to perform a further pull-through to study the upper part of the esophageal body, the upper esophageal sphincter (UES), and pharyngeal function.

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Manometric Analysis

Analysis of the manometric tracings was made in a blind fashion. The esophageal manometry was analyzed using standard accepted criteria (3,14,16,17). The results of each swallow were tabulated and averaged for each patient. The results from the control group were used for comparison using the 5th and 95th percentiles. The following parameters were analyzed in every manometric tracing.

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Resting or basal pressure was measured, as was sphincter response to swallows, by measuring the residual sphincter pressure postrelaxation, and percentage and duration of the relaxation.

Each LES parameter was then classified as follows using the control group results for comparison:

1. LES basal or resting pressure (measured at the end of expiration):

a. Hypertensive: >95th percentile of control

b. Normotensive: ≤95th percentile of control

c. We then calculated the percentage of measurements in which the LES was hypertensive or normotensive.

2. LES percentage of relaxation during swallowing:

a. Absent: 0% LES relaxation after a swallow

b. Present: any LES relaxation after a swallow

c. 100%: 100% LES relaxation after a swallow

d. Normal: LES relaxation ≥5th percentile value of controls

e. Abnormal: LES relaxation <5th percentile value of controls

f. We then calculated the percentage of swallows in which LES relaxation was absent, present, or 100%, and the percentage with normal or abnormal relaxation.

3. LES residual pressure after maximum relaxation after swallowing:

a. Normal: ≤95th percentile of controls

b. Abnormal: >95th percentile of controls

c. We then calculated the percentage of swallows in which there was normal or abnormal LES residual pressure during swallows.

4. LES dynamics: value that included basal pressure, percentage of relaxation, and residual pressure.

a. Normal LES dynamics, defined as the following: LES had a basal pressure between the 5th and 95th percentile of controls; LES relaxation was ≥5th percentile of controls; the LES residual pressure was ≤95th percentile of the controls. These values are shown in Table 1. Therefore, taking values from Table 1, the definition included an LES basal pressure between 8.34 and 32.0 mmHg, LES relaxation ≥80%, and a residual pressure after swallowing <4.25 mmHg.

Table 1
Table 1
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b. We then calculated the percentage of swallows that produce normal or abnormal LES dynamics.

5. Classification of patients as having homogeneous or heterogeneous LES function.

6. We arbitrarily used ≥75% of the same response as the cutoff for classification into either homogeneous (>75%) or heterogeneous (<75%).

7. Homogeneous function: The evaluated LES parameters were the same in ≥75% of swallows. Depending on whether the responses were normal or abnormal, LES function could be homogeneously normal or abnormal.

8. Heterogeneous function: A response was defined as heterogeneous if:

a. There was a mixture of normal and abnormal LES characteristics and neither response was present in at least 75% of swallows.

b. All of the LES characteristics and LES response to swallows were abnormal, but the same response was not present in >75% of swallows.

c. We then calculated the number of patients with homogeneity or heterogeneity for the following parameters: LES basal pressure, percentage of relaxation, residual pressure, and LES dynamics.

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Esophageal Peristalsis and Esophageal Body

Gastroesophageal gradient (intraesophageal pressure), amplitude, duration, peristalsis, and speed of esophageal contractions were the variables evaluated. Based on the characteristics of the peristalsis, esophageal peristalsis in each patient was classified as follows:

1. Absence or presence of esophageal body contractions. Normal peristalsis was considered if there were >70% of peristaltic waves.

2. Vigorous achalasia was defined as when the amplitude of contractions was >40 mmHg (18,19).

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UES and Pharynx

Resting pressure, percentage of the relaxation, and pharyngo-UES coordination were the variables evaluated.

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Statistical Analysis

Values were reported as mean ± SD or percentage. The 5th and 95th percentiles of the results in the control group were calculated (mean ± 2 SD), and were used as upper and lower limits for comparisons and classifications. Results of the different parameters were compared between the achalasia and control groups. Chi-square analysis was used to analyze differences in categorical variables between groups. For continuous variables, a t test (if parametric) or a Wilcoxon signed rank test (if nonparametric) was used. Different subgroup analyses were also performed. Patients with achalasia were subclassified according to age of diagnosis (older or younger than average age group), evolution of symptoms (more or less than median evolution time), and those with hypertensive or normal LES basal pressure using the methods described above. SPSS (SPSS Inc, Chicago, IL) was the statistical software used.

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Forty-five patients were studied (29 with achalasia and 16 controls). Table 1 shows the results obtained from the control patients (mean age 13.13 ± 3.86 years). Table 2 shows the results from the patients with achalasia. The mean age at diagnosis was 11.45 ± 5.1 (0.9–18) years, with an average duration of symptoms of 12.9 ± 13.6 months (3–48, median 6).

Table 2
Table 2
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LES Evaluation

LES function could be evaluated in 181 swallows in the achalasia group and in 107 swallows in the control group. The results are shown in Table 2, and as evident, LES function was significantly different in all of the parameters when compared with controls. Figure 1 shows the average values observed for the different parameters of LES function. In general, the LES responses in the control group were homogeneous. The achalasia group response was heterogeneous and patients had diverse responses with large variability and some overlap with the controls. The only parameter in which there was no overlap between groups was the LES dynamics.

Figure 1
Figure 1
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In patients with achalasia, the overall LES response to swallows was abnormal in all of the patients. It was homogeneously abnormal in 86% of patients. All of the responses were homogeneously normal in the control group. These differences were statistically significant (P < 0.001) for all of the parameters. Figure 2 shows representative tracings of 1 control patient and 2 patients with achalasia, exemplifying homogeneous and heterogeneous responses.

Figure 2
Figure 2
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Resting Pressure

Patients with achalasia had significantly higher resting pressure as compared with the controls (Fig. 1). All of the control patients had homogeneous normal LES basal pressure. LES mean pressure was hypertensive in 69% (20/29) of patients with achalasia. Therefore, the average LES resting pressure was normal in only 31% (9/29) of the patients, although in those patients there was a combination between normal and abnormal pressure depending on the swallow. In fact, only 15% of patients had normal LES pressure in >75% of swallows, and only 9 patients (30%) had a hypertensive LES in >75% of swallows. Therefore, patients with achalasia had either a mixture of normal and abnormal resting pressure (heterogeneous) or mostly abnormal LES resting pressure (homogeneously abnormal).

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LES Relaxation

In the control group, LES relaxation was homogeneous and present in 100% of swallows. Patients with achalasia had a smaller percent of relaxation, higher LES residual pressure, and shorter duration of relaxation when compared with controls (Table 2, Fig. 1). Some LES relaxation was present in 74.2% of swallows, but it was >80% (5th percentile of control group) in only 25.6% and 100% in only 6% of swallows. No patients with achalasia had a homogeneously normal LES relaxation. Heterogeneous LES relaxation was observed in 34.5% (10/29) patients and the rest had homogeneous relaxations that were abnormal. Only 13.7% (4/29) of patients had no LES relaxation in 100% of swallows. Therefore, patients had either a mixture of normal and abnormal relaxations (heterogeneous) or mostly abnormal LES relaxations (homogeneously abnormal).

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Residual LES Pressure

As can be seen in Table 2 and Figure 1, all of the swallows produced a residual pressure <5 mmHg in the control group. In only 3.75% of the swallows in the controls, the residual pressure was between 4.25 (95th percentile) and 5 mmHg. All of the controls had a homogeneously normal LES residual pressure response to swallowing.

In contrast, in the achalasia group, the mean value of the residual pressure was >20 mmHg with great variability. It was >4.25 mmHg in 80% of swallows, and most of the patients (28/29) had either a heterogeneous residual pressure or a homogeneously abnormal LES residual pressure after swallowing.

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Duration of Relaxation

The duration of LES relaxation after swallowing was longer than 5 seconds (5th percentile) and homogeneous in all of the controls. In contrast, only 60% of swallows in the patients with achalasia had a duration of relaxation >5 seconds, and in almost 40%, the duration of LES relaxation was heterogeneous.

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LES Dynamics

In the control group, LES dynamics were normal in 96% of swallows. Four controls had a total of 5 swallows with abnormal LES dynamics. In these swallows, the LES relaxation was between 74% and 85%.

In the achalasia group, LES dynamics were normal in only 7.7% of swallows. No individual patient with achalasia had >75% of swallows with normal LES dynamics (Fig. 1). The LES relaxation dynamics seemed to be homogeneous in both groups. It was homogeneously normal in the control and homogeneously abnormal in patients with achalasia.

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LES Function Among Achalasia Subgroups
Age at Diagnosis

There was no difference in any of the LES function parameters when comparing patients according to age at diagnosis (data not shown).

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Duration of Achalasia Symptoms Before Diagnosis

The average duration of symptoms was 12.84 months, with a median of 6 months. The LES parameters of those with symptoms shorter or longer than 6 months are shown in Table 3. Patients with symptom duration <6 months seemed to have more normal LES responses to swallows than those with longer duration. Although the differences are not statistically significant, longer evolution times seem to be associated with more homogeneously abnormal LES response.

Table 3
Table 3
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Comparison Between Patients With Achalasia With Hypertensive or Normotensive LES

The normotensive group had shorter duration of symptoms before diagnosis: 5 ± 1.5 months (median 5 months) versus 18.4 ± 15.8 months (median 12 months, P < 0.03) for patients with hypertensive LES. Patients with normotensive LES had lower LES residual pressure (10.3 vs 25.7 mmHg, P < 0.001), more percentage of swallows with normal LES dynamics (21 vs 1.5 mmHg, P < 0.001), and more patients with heterogeneous LES than the hypertensive group (44.44 vs 0 mmHg, P < 0.005). There were no patients in the hypertensive group with heterogeneous LES response; all of them had a homogeneously abnormal response.

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Esophageal Body Peristalsis

In the achalasia group, the esophagogastric gradient pressure was 4.69 ± 4.68  mmHg as compared with −5.95 ± 4.29 mmHg in controls (P < 0.05). No patient had normal peristaltic waves and most had tertiary peristalsis. In only 5 of 29 patients, some swallows did not generate any contractions. Only 1 patient had vigorous achalasia and the average esophageal contraction pressure in that patient was 44.4 ± 13.7 mmHg.

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UES Evaluation

As can be seen in Table 2, the UES pressure of patients with achalasia was significantly lower. There were no differences in UES function or pharyngeo-UES coordination between patients and controls.

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The present study is the first study that systematically describes LES function in a well-defined population of children with achalasia. Contrary to previous reports in which it was stressed that there is a lack of LES relaxation (1,7,20), we have shown that in children with achalasia, there is evidence of LES relaxation after some wet swallows; however, LES relaxation characteristics are abnormal and LES function in children with achalasia is heterogeneous. These observations may facilitate the diagnosis of achalasia in children and may allow an earlier diagnosis in patients with suspected achalasia in whom there is some degree of LES relaxation (7,21).

The diagnosis of achalasia is based on manometric abnormalities and must include a lack of esophageal peristalsis, which is the hallmark of the diagnosis (7). Also, a lack of LES relaxation is described; in fact, the term achalasia derives from the Greek word “αχαλασíα,” “a” meaning failure or absence and “chalasis” meaning relaxation, combining to mean “failure of relaxation or lack of relaxation.” These manometric findings have been described in children with achalasia, and the few published reports describing the manometric characteristics of pediatric patients with achalasia mention a lack of esophageal peristalsis and a nonrelaxing LES (1,11–13); however, no specific descriptions of LES function have been provided children with achalasia. In our series, contrary to what has been reported, only 4 of 29 patients had no LES relaxation in all of the swallows, and we found that children with achalasia have as heterogeneous LES function, with some intermittent degrees of LES relaxation including some occasional normal relaxations. This LES heterogeneity was present when comparing not only between different patients with achalasia but also within each patient. This is an important observation because throughout the manometric study, the LES response consisted of a mixture of mostly abnormal swallows, intermixed with occasional normal LES responses. This heterogeneity highlights the importance of analyzing multiple wet swallows during esophageal manometry in children. This LES heterogeneity has not been described in children with achalasia; however, it has been reported in adults (8–10). Katz et al (9), in a series of 23 patients with achalasia, noted that 7 of 23 (30%) patients had normal mean LES relaxation. Manometric LES heterogeneous response has also been demonstrated by studying the response to deglutitive inhibition in patients with achalasia (22). Also, recent data obtained from studies using high-resolution manometry (HRM) have also suggested that there is heterogeneity in the type of manometric abnormalities seen in adults with achalasia (17,23).

The cause of this variability in LES function is unclear. It could be a reflection of various degrees of neural damage to the LES. It has been suggested that the different manometric findings may correlate with well-defined neuronal abnormalities, as well as with duration of the disease (8,24), with those patients that still show evidence of LES relaxation having a shorter duration of symptoms than the patients with more classical findings (9,25). In our series, we also found that patients with shorter evolution had more normal LES responses and a significant lower LES basal and residual pressure.

In adults with achalasia, age at diagnosis has also been suggested as an influencing parameter in LES function (26). In our series, we found no statistically significant difference in the manometric parameters between our younger and older patients, suggesting that in pediatrics, the duration of illness has a greater effect than age.

The presence of LES relaxation in patients with achalasia does not mean that esophageal function and emptying is normal or not impaired. Nuclear medicine and radiologic studies have shown delayed esophageal emptying even in patients with apparent normal LES relaxation (9,27,28). We confirmed in all our patients that there was delayed passage of barium from the esophagus to the stomach after 10 minutes of ingestion. This abnormal transit is probably related to not only a lack of peristalsis in the presence of an abnormally relaxing sphincter but also additional mechanisms. It has been suggested that an increased LES residual pressure during swallowing may be a contributing factor, and that LES compliance is abnormal, thereby contributing to an increased resistance to flow through gastroesophageal junction (28,29). Therefore, the apparent LES relaxation is functionally inadequate (28,29). Combined manometry and impedance studies have also shown that as the residual LES pressure increases, the bolus clearance is less effective (30). Based on these findings, it has been suggested that residual LES pressure during swallowing is the most reliable measure to identify the presence of achalasia (8,21). In our series, we found that the residual LES pressure during swallowing was abnormal in most swallows. Given the variability in LES manometric characteristics among patients with achalasia, the finding of high LES residual pressure during swallowing may be another good manometric indicator of achalasia in children.

Another important contribution of the present study is that we are providing esophageal stationary manometry measurements for 16 control patients that can be used as reference values when perfused stationary esophageal manometry is performed.

One of the major limitations of the present study is that our esophageal motility testing was not performed with a sleeve catheter. It has been suggested that the appearance of LES relaxation in achalasia may be related to catheter migration. We think it is unlikely that our findings are a result of catheter movement. First, our unit is experienced in the performance of esophageal manometry in children, and we always monitor for manometric evidence of movement. Second, we did not find this LES heterogeneity in our control patients. Furthermore, adult studies that have examined LES heterogeneity in achalasia with the use of sleeve sensors have shown that in patients with achalasia, the role of LES displacement seems to be lower (excluding “apparent complete relaxation”) and is not a factor (8,10). Our findings are also similar to previous adult studies (21). Finally, recent studies with HRM in adults have also demonstrated that some degree of true LES relaxation, although impaired, does exist in patients with achalasia with minimal axial displacement (17,31,32). These results support that the finding of some degree of LES relaxation in conventional manometry is a true phenomenon. Even though HRM has an advantage over conventional manometry in that it eliminates the possible displacement factor, it is a new technology that has not been validated in children. It is also expensive and not readily available to most pediatric motility centers around the world, which must continue to rely on conventional manometry.

In conclusion, we have shown that LES function in children with achalasia is heterogeneous, although LES relaxation is abnormal most of the time in all patients. It is possible that sphincter function varies with time and may look more “normal” in early stages of the disease. Our findings are important because they provide some guidance about LES function in children with achalasia.

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achalasia; esophageal manometry; lower esophageal sphincter; children; esophageal motility

Copyright 2012 by ESPGHAN and NASPGHAN


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