Abstract
Background
Early relapse after treatment of achalasia occurs in 10–32 % of patients. The best method to follow up these patients is not known. Symptoms often do not correlate with esophageal clearance: some patients are oligosymptomatic despite persistent esophageal stasis/dilatation.
Aim
The aim was to compare two methods of measurement of esophageal clearance (impedance manometry with barium swallow) in achalasia patients following treatment. Symptom assessment (Eckardt score/detailed dysphagia questions) was correlated with objective measurements of esophageal stasis (barium swallow and impedance manometry) in achalasia patients following treatment.
Methods
Post-treatment patients were followed up after median 38.4 months (median range 1–144 months). Symptoms were quantified using the Eckardt score and detailed dysphagia questions. Timed barium swallow quantified distal esophageal retention 0.5, 1, 3, and 5 minutes after oral contrast and impedance manometry assessed total and segmental esophageal clearance during water/viscous swallows and free drinking (200 mL).
Results
Thirty-two patients (7 women, age 48.3; range 20–74) completed all investigations. Bolus retention in the distal esophagus assessed by impedance correlated well with barium swallow. There were no differences in impedance and timed barium swallow parameters between patients with Eckardt score 0–2 points or ≥3 points. Nine (28%) patients had an Eckardt score ≥3 points and 21 (66%) had ≥1 point in the detailed dysphagia questions. Patients without any dysphagia history had lower barium column height and width at 3 and 5 minutes compared to those with ≥1 positive answer in the detailed dysphagia questions. Correlation between the Eckardt score and detailed dysphagia questions was moderately good (r = 0.546; p = 0.001).
Conclusion
A detailed history of esophageal dysphagia rather than the Eckardt score is more sensitive to detect oligosymptomatic patients with disturbed esophageal clearance. Impedance manometry correlates well with the timed-barium swallow examination and represents an alternative objective assessment as it avoids radiation exposure.
Keywords: Achalasia, impedance manometry, timed barium swallow, symptom assessment, questionnaire
Introduction
Achalasia is treated with balloon dilation or Heller myotomy, which both give good overall long-term treatment success.1–4 However, symptomatic relapse after treatment of achalasia occurs in 32% of patients after balloon dilation and in 10% of patients after Heller myotomy within the first year.5,6 In young patients the recurrence rate after 10 years may rise to as high as 72%.7 Symptoms often do not correlate with esophageal clearance: there are patients without symptoms but incomplete bolus clearance due to insufficient myotomy or dilation. On the other hand, patients may experience dysphagia without objective esophageal clearance impairment. Generally, patients present late for another treatment. This study was designed to compare two methods of esophageal clearance (esophageal manometry and timed barium swallow). We rated subjective symptoms using the Eckardt score.8 In addition, we asked detailed dysphagia questions on swallowing activities and compared them to the Eckardt score. Our questions were set to increase the patients’ awareness to early signs of relapse.
Currently the Eckardt score is worldwide the gold standard to assess achalasia patients pre and post treatment. Over the years we have observed, that the general questions in this score do not always picture the severity of incomplete esophageal bolus transit. With our clinical experience we composed several questions focusing on incomplete bolus transit as a sign of a relapse in achalasia.
The hypotheses were that (1) detailed dysphagia history with specific questions correlate better with the incomplete esophageal clearance in fluoroscopy than the Eckardt score and (2) that timed barium swallow and impedance manometry correlate in their assessment of bolus transit or retention.
Methods
Follow-up protocol
Our follow-up protocol includes an upper endoscopy with Lugol staining and clinical evaluation with questionnaires every three years. In the context of this study, patients were additionally asked to undergo impedance manometry and a timed barium swallow.
Patient selection
Thirty-two consecutive patients, who underwent treatment (pneumatic dilatation or Heller myotomy) for achalasia scheduled for routine follow-up exam in our outpatient clinic were asked to participate in this study comparing two methods of esophageal function testing (fluoroscopy and combined impedance manometry). If they agreed, they signed an informed consent form before the day of the exam. Three patients refused to participate. Participants could withdraw without any reason at any time from the study. The study was approved by the local ethic committee.
Symptom assessment
Dysphagia was assessed using the Eckardt score (severity of dysphagia, chest pain, regurgitation, and weight loss). Additionally, detailed dysphagia questions (Figure 1) were asked to assess eating difficulties associated with achalasia. These six questions addressed (1) slow eating (when compared to earlier times and other people), (2) prolonged chewing, (3) forced swallowing, (4) water flush between swallows of solid food, (5) peeling apples, and (6) problems toward the end of a meal (dysphagia, retrosternal pressure). In the Eckardt score, a maximum of 12 points could be achieved (4 questions with grades 0–3 for each answer). The detailed dysphagia questions scored maximal 6 points. These questions were put to eight asymptomatic volunteers with normal EGD and manometry. All of them scored 0 points; thus we defined a score ≥1 as indicative for dysphagia. As we focused on dysphagia, we defined symptomatic relapse as Eckardt score ≥3, according to currently used criteria in a large European treatment study.9
Figure 1.
Detailed dysphagia questionnaire.
Combined impedance-manometry testing
The combined manometry and impedance testing catheter is a specially designed solid-state catheter system (Sandhill Scientific Inc., Highlands Ranch, CO, USA). The catheter includes five pairs of impedance sensors separated by 5 cm intervals and five manometric sensors spaced 5 cm apart. The pressure/impedance catheter was passed transnasally to a distance of 60 cm from the nares. The length and proximal position of the lower esophageal sphincter were determined via a station pull-through technique. Then the catheter was positioned such that the distal manometric transducer was positioned in the high-pressure zone of the lower esophageal sphincter. When the probe was correctly positioned subjects underwent a short period of accommodation and all measured pressures were referenced to end expiratory intragastric pressure. A series of 10 swallows of 5 mL liquid (0.9% saline solution) and 10 swallows of 5 mL viscous (apple sauce, Hero®, Lenzburg, Switzerland) were performed in the 45° position, with swallows separated by intervals of at least 20 s. At the end, free drinking in the upright position of 200 mL of water showed possible obstruction at the lower esophageal sphincter (LES). Data were recorded and analyzed with dedicated software (Bioview Analysis 5.5.4.1, Sandhill Scientific Inc., Highlands Ranch, CO, USA).
Bolus retention in a given segment (incomplete clearance) was defined as the failure of impedance to recover back to 50% difference between baseline and nadir values.
Timed barium swallow
After the visit to our laboratory, patients proceeded to the radiology department for a timed barium swallow procedure. X-rays were taken at 0.5, 1, 3, and 5 minutes after swallowing 50 mL barium solution (Micropaque® Susp. 1 g/mL, Guerbet AG). The height and width of the barium column was measured in centimeters scaled on the radiographic picture.
Analyzed parameters are summarized in Table 1.
Table 1.
Parameters recorded and analyzed
| Symptom data | Eckardt score Detailed dysphagia history with specific questions |
| Manometric data | Lower esophageal sphincter basal pressure (LESP) Lower esophageal sphincter relaxation pressure (LESRP) during liquid and viscous swallows |
| Impedance data | Total and segmental clearance (at 20, 15, 10, 5 cm above the LES) of liquid and viscous material and free drinking (200 mL of liquid) Bolus transit time |
| Timed barium swallow | Height and width of barium column at 0.5, 1, 3, and 5 minutes |
Statistical analyses
Descriptive statistics were calculated using Microsoft Excel and SPSS Version 12.0. Normally distributed continuous parameters were compared using a two-tailed student t-test, but non-normal distributed continuous parameters using a Mann–Whitney test. Correlations between Eckardt score and the detailed dysphagia history with specific questions were assessed using Pearson correlation coefficient; p values less than 0.05 were considered statistically significant.
Adjustments for multiple comparisons were performed as required.
Results
Drop out, follow-up results
Between October 2008 and July 2010, 32 patients (7 women, age 48.3; range 20–74) underwent symptom assessment, combined impedance-manometry testing, and timed barium swallow recordings. One patient had to be excluded from the study after the follow-up intervention because of a misdiagnosis (hypertensive LES with regained peristalsis). There were no dropouts due to technical problems. The median follow-up interval from the last procedure was 38.4 months (1–144 months). Twenty-seven patients have been treated with pneumatic dilation and five patients have been treated with Heller myotomy. According to the Eckardt score and to the timed barium swallow we recommended eight patients to have further treatment done. Treatment suggestion was also discussed if only symptom score or timed barium swallow were abnormal. Seven patients underwent a successful procedure. One single patient underwent a myotomy, six had another dilation performed. All seven patients had a significant reduction in the Eckardt score as well as in the detailed dysphagia questions.
Dysphagia scores/subjective symptoms
Twenty-one (65%) patients had ≥1 point in the detailed dysphagia questions and nine (28%) patients had ≥3 points in the Eckardt score. During 5 mL water swallows administered for esophageal manometry, only one patient reported some sensation of dysphagia; this patient had a normal Eckardt and no points in the detailed dysphagia questions. During 5 mL viscous swallows, six patients reported perception of incomplete bolus clearance during the test. Four (66%) of these patients had ≥1 point in the detailed dysphagia questions, whereas only three (50%) had an abnormal Eckardt score.
Twenty-six (81%) patients reported no dysphagia sensation with free drinking of 200 mL water, while five out of six (83%) symptomatic patients on manometry had a ≥1point in the detailed dysphagia questions compared to a pathological Eckardt score in three of them (50%).
Assessment of esophageal clearance
Timed barium swallow
An impaired esophageal clearance with a detectable barium column at 3 min was observed in 18/32 (56%) of patients. Of these 18 patients, 9 (50%) had an Eckardt score ≥3 point and 15 (83%) ≥1 point in the detailed dysphagia questions. There was no differences between patients with an Eckardt score of 0–2 points or ≥3 points regarding the retention of barium at all times measured.
On the other hand, detailed dysphagia questions could discriminate patients with different column width at 3 and 5 minutes (p = 0.04).
Impedance manometry
LES basal pressure
The average LES basal pressure was similar in both groups of patients, as assessed by the Eckardt score (18.9 vs. 20.0 mmHg, p = 0.83) and detailed dysphagia questions (16.7 vs. 21.1 mmHg, p = 0.31). The LES basal pressure was numerically higher in dysphagia score positive patients, but not of statistical significance.
Combined impedance manometry
None of the achalasia patients showed any propulsive peristalsis on manometry tracing. Bolus clearance assessed by impedance (Table 2 and 3) found that segmental clearance worsened from the proximal to the distal esophagus. Clearance moreover deteriorated with increased consistency (viscous applesauce) and increasing volume (free drinking of 200 mL water). There were no differences between patients with Eckardt score 0–1 point or ≥2 points in the percentage of swallows with segmental and total bolus clearance. Asking the detailed dysphagia questions there was a trend (at a p-level of 0.05) to discriminate patients according to their percentage of swallows with impaired or normal segmental and total bolus clearance as measured by impedance manometry.
Table 2.
Bolus clearance parameters (impedance and timed barium swallow) in patients with Eckardt score 0–2 points and patients with Eckardt score ≥3 points cm above LES (impedance manometry) and time after bolus ingestion (barium swallow)
| Parameter | Eckardt 0–2 (N = 23) | Eckardt ≥3 (N = 9) | |
|---|---|---|---|
| % swallows with complete | 20 cm | 92.6 ± 1.6 | 94.4 ± 1.0 |
| segmental clearance | 15 cm | 79.1 ± 2.3 | 81.1 ± 2.0 |
| during liquid swallows | 10 cm | 77.8 ± 2.4 | 72.2 ± 2.8 |
| 5 cm | 67.0 ± 2.6 | 54.4 ± 3.7 | |
| % swallows with complete | 20 cm | 79.6 ± 5.7 | 90.0 ± 4.1 |
| segmental clearance | 15 cm | 50.4 ± 6.4 | 64.4 ± 7.3 |
| during viscous swallows | 10 cm | 43.5 ± 7.0 | 48.9 ± 11.3 |
| 5 cm | 38.7 ± 6.7 | 47.8 ± 12.0 | |
| % swallows with complete | 20 cm | 87.0 ± 3.4 | 78.0 ± 4.4 |
| segmental clearance | 15 cm | 65.0 ± 4.9 | 67.0 ± 5.0 |
| during free drinking | 10 cm | 43.0 ± 5.1 | 44.0 ± 5.3 |
| (200 mL) | 5 cm | 30.0 ± 4.7 | 33.0 ± 5.0 |
| % swallows with | water | 57.0 ± 2.3 | 47.8 ± 3.1 |
| complete bolus transit | viscous | 25.7 ± 2.3 | 35.6 ± 2.9 |
| % patients with barium | 30 seconds | 69.7 ± 4.7 | 55.6 ± 5.2 |
| column at | 1 minute | 65.2 ± 4.9 | 55.6 ± 5.2 |
| 3 minutes | 56.5 ± 5.1 | 55.6 ± 5.2 | |
| 5 minutes | 39.1 ± 5.0 | 44.4 ± 5.2 | |
| Timed barium swallow | 30 seconds | 5.0 ± 1.2 | 3.2 ± 4.1 |
| (column height in cm) | 1 minute | 4.5 ± 1.1 | 3.1 ± 1.4 |
| 3 minutes | 4.1 ± 1.1 | 2.9 ± 1.4 | |
| 5 minutes | 2.7 ± 0.9 | 3.9 ± 2.7 | |
| Timed barium swallow | 30 seconds | 1.3 ± 0.4 | 1.5 ± 0.3 |
| (column width in cm) | 1 minute | 1.5 ± 0.4 | 1.5 ± 0.3 |
| 3 minutes | 0.8 ± 0.3 | 1.1 ± 0.3 | |
| 5 minutes | 0.6 ± 0.3 | 0.8 ± 0.2 |
Table 3.
Bolus clearance parameters (impedance and timed barium swallow) in patients without dysphagia (0 points) and with ≥1 points in the detailed dysphagia questions
| Parameter | Dysphagia 0 (N = 11) | Dysphagia ≥1 (N = 21) | |
|---|---|---|---|
| % swallows with complete | 20 cm | 98.2 ± 1.2 | 90.5 ± 3.8 |
| segmental clearance | 15 cm | 87.3 ± 3.6 | 75.7 ± 5.5 |
| during liquid swallows | 10 cm | 83.6 ± 4.1 | 72.4 ± 6.2 |
| 5 cm | 75.5 ± 5.5 | 57.1 ± 5.0 | |
| % swallows with complete | 20 cm | 85.5 ± 6.4 | 81.0 ± 5.7 |
| segmental clearance | 15 cm | 63.6 ± 6.6 | 49.5 ± 6.8 |
| during viscous swallows | 10 cm | 51.8 ± 9.1 | 41.4 ± 7.6 |
| 5 cm | 42.7 ± 8.5 | 40.5 ± 7.8 | |
| % swallows with complete | 20 cm | 90.9 ± 9.1 | 81.0 ± 8.8 |
| segmental clearance | 15 cm | 63.6 ± 15.2 | 66.7 ± 10.5 |
| during free drinking | 10 cm | 54.6 ± 15.7 | 38.1 ± 10.9 |
| (200 mL) | 5 cm | 45.5 ± 15.7 | 23.8 ± 9.5 |
| % swallows with | water | 62.7 ± 4.9 | 50.0 ± 6.3 |
| complete bolus transit | viscous | 29.1 ± 7.2 | 28.1 ± 5.5 |
| % patients with barium | 30 seconds | 54.6 ± 15.7 | 71.4 ± 10.1 |
| column at | 1 minute | 45.5 ± 15.7 | 71.4 ± 10.1 |
| 3 minutes | 27.3 ± 14.1*A | 71.4 ± 10.1 | |
| 5 minutes | 18.2 ± 12.2*B | 52.4 ± 11.2 | |
| Timed barium swallow | 30 seconds | 2.6 ± 1.0 | 5.6 ± 1.3 |
| (column height in cm) | 1 minute | 2.3 ± 1.0 | 5.1 ± 1.2 |
| 3 minutes | 1.6 ± 1.0 | 5.0 ± 1.2 | |
| 5 minutes | 1.2 ± 0.9 | 4.0 ± 1.4 | |
| Timed barium swallow | 30 seconds | 1.0 ± 0.4 | 1.6 ± 0.3 |
| (column width in cm) | 1 minute | 1.1 ± 0.3 | 1.7 ± 0.3 |
| 3 minutes | 0.5 ± 0.2*C | 1.3 ± 0.3 | |
| 5 minutes | 0.2 ± 0.1*D | 1.1 ± 0.3 |
A, p = 0.019; *B, p = 0.049; *C, p = 0.015; *D, p = 0.005.
Correlation
Eckardt vs. detailed dysphagia questions
Nine (28%) patients had an Eckardt score ≥3 points. There was no difference in the Eckardt score regarding the mode of treatment (Eckardt myotomy vs. dilation; 66% vs. 73%, p = 0.55 Fisher exact test). Twenty-one (65%) patients had at least one positive answer in the detailed dysphagia questions (myotomy vs. dilatation 67 vs. 65%, p = 0.67 Fisher exact). There was only a moderate correlation between the Eckardt score and the detailed dysphagia questions (r = 0.55, p < 0.001).
Correlation of impedance and timed barium swallow measurements
Impedance testing correlated well with barium swallow directly above the LES and decreased to the proximal esophagus (cf. Table 4). We found no correlation between the Eckardt score and the percentage of swallows with bolus retention during liquid/viscous swallow or barium retention. On the other hand, the detailed dysphagia questions correlated with the percentage of swallows with liquid retention at 5 cm (r = 0.598; p = 0.001), 10 cm (r = 0.482; p < 0.001), 15 cm (r = 0.521; p = 0.015), and 20 cm above LES (r = 0.421; p = 0.015) and with the width of barium column measured at 3 min (r = 0.422; p = 0.016) and 5 min (r = 0.407; p = 0.021) after ingestion of barium.
Discussion
In our study focusing on patients who have been treated for achalasia, we compared two methods of esophageal clearance (impedance manometry vs. timed barium swallow), and we also compared a composition of detailed dysphagia questions with the established Eckardt score in the same patient group. The Eckardt score evaluates four symptoms of achalasia (dysphagia, regurgitation, chest pain, weight loss) but includes only limited differentiation of each symptom. The current new set of questions focuses more on rating the components of difficult swallowing, the sum of “yes” answers offers an additional grading of dysphagia.
We found that a detailed history of dysphagia pictures incomplete bolus transit better than the broader questions of the Eckardt score.
There were no differences between Eckardt score patients with <3 vs. ≥3 points in the percentage of swallows with complete segmental and total bolus clearance and of patients with barium retention at 0.5, 1, 3, and 5 minutes. In contrast, patients with at least one pathological answer in the detailed dysphagia questions showed a significant difference in the barium column at 3 and 5 minutes.
Neither of the standardized tests as liquid/viscous swallows measured by impedance manometry nor the barium retention correlated with symptom severity assessed by the Eckardt score. On the other hand, the detailed dysphagia questions correlated with the swallows with liquid retention at 5 cm, 10 cm, 15 cm, and 20 cm above LES (and with the width of barium column measured at 3 min and 5 min) after ingestion of barium. Many of our patients were asymptomatic when assessed by the Eckardt score and later showed pathologic findings on impedance manometry or timed barium swallow. This reflects the limited clinical utility of the Eckardt symptom score. The Eckardt score did not correlate with objectively assessed esophageal clearance as measured by impedance manometry and timed barium swallow. More detailed questions show promise to identify those patients who may benefit from functional esophageal testing to decide on further management.
The correlation of dysphagia symptoms assessed with the detailed dysphagia questions and esophageal retention as measured by either impedance testing or barium fluoroscopy was moderately good (r = 0.402–0.598). We interpreted this as an advantage compared to the Eckardt score in clinical assessment of post-treatment patients.
Regarding follow up of achalasia patients with impedance manometry in comparison to timed barium swallow: As the combined impedance-manometry is a new technique there is so far a dearth of data about its use in testing people with treated achalasia or its value in comparison to fluoroscopy. Conchillo and Smout acknowledged in a review article that impedance monitoring can be used to assess the clearance of a swallowed bolus.10 Tatum et al. have used impedance manometry in patients treated for achalasia to measure esophageal clearance and peristalsis.11 They have found, that bolus clearance improved and peristalsis partially restored after any treatment. In contrast, we could not detect post treatment peristaltic contraction in our achalasia patient. A possible explanation may be that patients with distal esophageal spasms and incomplete LES relaxation were included in the study by Tatum et al. and therefore propulsive contraction returned after disruption of the LES.
Impedance manometry correlated to fluoroscopy regarding the degree of esophageal clearance in the lower, but not in the upper part of the esophagus. Fluoroscopy and in particular timed barium swallow are considered to be the best currently available tool to quantify esophageal dysfunction following achalasia treatment.12 While timed barium swallows documents esophageal retention in the distal to mid esophagus impedance-manometry dissects the characteristics of retention quantifying bolus retention at distinct levels in the esophagus. Although both techniques are aimed a quantifying bolus transit/retention they provide information on different processes. Timed barium swallow quantifies how long a radio-opaque substance remains in the esophagus, impedance manometry quantifies esophageal transit (or lack of transit) of small amounts (i.e. 5–10 mL) of liquids and viscous substances. Thus, the degree of correlation 0.4–0.6 is, although statistically only moderately good, clinically important. One has to recognize that interpreting impedance recordings in patients with achalasia is difficult due to fluid retention in the distal esophagus and/or air entrapment in the proximal esophagus.13,14 The poor correlation between symptoms recorded during swallowing and symptom scores is not surprising. Neither duration of bolus retention (assessed by timed barium swallow) nor bolus retention of small volumes (assessed by impedance manometry) necessarily reproduce symptoms provoked by progressive accumulating boluses in the distal esophagus in daily life.
Re-intervention was recommended if timed barium swallow alone or in combination with the dysphagia score was abnormal. Our experience tells us, that most achalasia patients have adapted to the feeling of incomplete clearance without disabling symptoms. Post intervention usually shows an improvement in quality of life especially in esophageal sensation during meal intake. Incomplete clearance and therefore possible increased risk of carcinogenesis in patients with achalasia is in debate. Studies to prove a significant correlation are lacking because it would need a very long follow up of decades.
This study has some limitations. First of all, we had a small patient collective with 32 patients. Moreover the time between intervention and follow up differed widely and there were two different types of interventions (pneumatic dilation vs. myotomy). Because of the small number, we could not perform a subgroup analysis. Though the dysphagia questions picture a detailed history, it is not validated and remains to be further validated in different dysphagia groups and volunteers. In addition the specificity is low: 21/32 (66%) had a ≥1 point in the detailed dysphagia questions. Nevertheless current data underscore that a detailed history of daily dysphagia symptoms is a more sensitive clinical tool to predict bolus retention after achalasia treatment than the Eckardt score.
In conclusion, classical available questionnaires (Eckardt) and intraluminal measurements for quantifying esophageal clearance (impedance manometry) correlate poorly with esophageal clearance assessed by barium swallow. Objective parameters to support the clinical assessment in deciding further treatment for symptomatic relapse of achalasia should base on a more detailed dysphagia history as proposed by the six dysphagia questions.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Conflict of interest
Claudia Krieger-Grübel and Jan Borovicka have no conflicts of interest or financial ties to disclose.
Radu Tutuian is a consultant and contributes to scientific programs of Sandhill Scientific Inc. and MMS International.
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