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First published online August 2, 2006
British Journal of Radiology (2006) 79, 719-724
© 2006 British Institute of Radiology
doi: 10.1259/bjr/17000205
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Oesophageal dysmotility in systemic sclerosis: comparison of HRCT and scintigraphy

E H Pitrez, MD 1 M Bredemeier, MD, MSc 2 R M Xavier, MD, PhD 2 K G Capobianco, MD, MSc 2 V G Restelli, MD 2 M V Vieira, MD, PhD 1 D H C Ludwig, MD 3 J C T Brenol, MD, PhD 2 A P A Furtado, MD 1 L M B Fonseca, MD, PhD 4 and B Gutfilen, MD, PhD 4

1 Serviço de Radiologia, 2 Serviço de Reumatologia, 3 Serviço de Medicina Nuclear, Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos 2350, Porto Alegre, RS, Brazil, 90.035-003, 4 Departamento de Radiologia, Hospital Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, Brigadeiro Trompovsky, Ilha do Fundão, CEP 21941-590, Rio de Janeiro, RJ, Brazil


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Discussion
 References
 
The aim of this study was to compare oesophageal abnormalities observed in high-resolution CT with radionuclide transit in patients with systemic sclerosis. 76 patients with systemic sclerosis were evaluated by high-resolution CT and oesophageal transit scintigraphy. Residual activity ≥20% (in relation to peak activity) at 15 s after the beginning of the swallow of the labelled liquid (in supine position) was considered indicative of oesophageal dysfunction. Supra-aortic and infra-aortic oesophageal coronal diameters were measured in high-resolution CT. Oesophageal dilatation was deemed present when the diameters exceeded 10 mm. 19 patients (25%) had supra-aortic oesophageal dilatation and 48 patients (63.1%) had infra-aortic dilatation. The prevalence of radionuclide transit delay was 77.6%. All patients (19/19) with supra-aortic dilatation had oesophageal dysfunction, compared with 70.2% (40/57) of the patients with no supra-aortic dilatation (p = 0.004). Oesophageal dysfunction was present in 97.9% (47/48) of patients with infra-aortic dilatation, compared with 42.9% (12/28) in patients without it (p < 0.001). Receiver operating characteristic (ROC) curves have demonstrated that the supra-aortic and infra-aortic diameters had good discriminatory capacity for oesophageal dysfunction in systemic sclerosis (area under the curve, 95% confidence interval: 0.80, 0.70–0.89 and 0.92, 0.86–0.98, respectively). There is a clinically significant association between oesophageal dysmotility and high-resolution CT findings of oesophageal coronal dilatation. The evaluation of infra-aortic oesophageal coronal diameter can provide additional useful information about the functional and anatomic conditions of the oesophagus in systemic sclerosis.


   Introduction
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 Abstract
 Introduction
Material and methods
 Results
 Discussion
 References
 
Systemic sclerosis (SSc) is a connective tissue disease characterized by fibrosis in multiple organs, especially in the skin, lungs and gastrointestinal system [1, 2]. The oesophagus is the most frequently involved internal organ [3–5], and atrophy and fibrosis of the smooth muscle are probably responsible for the impaired oesophageal motility that is common in this disease [2, 5]. Diminished lower oesophageal sphincter pressure and associated gastro-oesophageal reflux (GER) occur frequently, leading to oesophagitis, strictures and ulcerations [4, 6]. Early recognition of the oesophageal dysfunction is important because patients may be asymptomatic for a long time despite the presence of oesophageal motor abnormalities [1, 3, 4].

Manometry has been considered the gold-standard examination to detect oesophageal dysfunction in early stages of SSc, but it gives no information on morphology and has low patient acceptance [1–3]. Radionuclide oesophageal scintigraphy (RES) stands out as a frequently used alternative to manometry, since it is a safe, non-invasive, and sensitive method that allows quantitative assessment [1, 2, 7–10].

Thorax high-resolution computed tomography (HRCT) is the preferred radiological examination in the evaluation of interstitial lung disease in SSc [11]. Oesophageal abnormalities in thorax CT, including dilatation, air–fluid levels, and food retention have already been documented in SSc patients [12]. As far as we are aware, a comparison of the HRCT and RES results in the evaluation of oesophageal dysfunction has not yet been performed. Therefore, our objective in this study was to compare both methods and to test the utility of HRCT in the diagnosis of oesophageal dysfunction in SSc using RES as the gold standard.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Discussion
 References
 
Patients
76 patients with the diagnosis of SSc (made according to the clinical evaluation of experienced rheumatologists) were prospectively studied. The patients met the American College of Rheumatology criteria for SSc [13] or the criteria suggested by LeRoy and Medsger for diagnosis of early forms of SSc [14]. Patients with overlapping syndromes, active chronic or acute infections, insulin-dependent diabetes mellitus or with long-standing diabetes (more than 5 years since diagnosis) were excluded. Patients with definite diagnosis of SSc (according to the American College of Rheumatology criteria) who developed inflammatory myopathy were not excluded from the analysis. All patients signed written informed consent before entry in the study. The study was approved by the Research Ethics Committee of the Hospital de Clínicas de Porto Alegre.

Clinical evaluation
All patients were interviewed and examined by a rheumatologist (MB). The interview instrument was an extensive questionnaire directed to the evaluation of end-organ damage. Duration of disease was defined as the period of time between the onset of Raynaud's phenomenon or skin symptoms (whatever came first) and the moment of the interview [15].

The sample included 67 women and 9 men, and the age range varied from 26 years to 78 years (mean 51 years, standard deviation 11 years). The duration of symptoms ranged from 2–25 years (median 13 years).

Radionuclide oesophageal transit scintigraphy
All subjects were examined after 4 h of fasting. The study was performed in supine position with liquid ingestion. The liquid phase was prepared with 6 ml of water labelled with 1 mCi of 99mtechnetium-phytate for each swallow. Imaging was performed with a large field-of-view gamma camera (high sensitivity parallel-hole collimator, with the camera underneath. The field-of-view extended from the pharynx to the upper part of the stomach. A practice run with unlabelled water preceded the study. The labelled liquid was placed in the mouth and swallowed on command. The computer acquired a dynamic study at a rate of 1 s frame–1 for 60 s with a 64 x 64 matrix. No dry swallows were allowed. A region of interest over the whole oesophagus was defined and a time–activity curve was generated.

The percentage of emptying of the oesophagus was analysed in 15 s and 60 s after swallow. Residual activity ≥20% (in relation to peak activity) at 15 s after the beginning of the swallow in the supine liquid phase was considered abnormal and indicative of oesophageal dysfunction [16].

High-resolution CT
The HRCT was performed with an Elscint Twin scanner (Elscint, Haifa, Israel) and with a Somatom Plus 4 (Siemens Medical Systems, Iselin, NJ). HRCT scans were obtained in supine position during full inspiration, with the following parameters being used: 1-mm sections at 10-mm intervals, a high-spatial-frequency algorithm, 512 x 512 matrix, 140 kVp, and 150 mAs (Elscint), 140 kVp and 130 mAs (Siemens). The scanning time was 1.0 s and the examination was performed from the apices of the lungs to the lung bases. Prone scans were obtained whenever subpleural lesions were observed. HRCT was reviewed with lung (window width, 2000 H; window level, –700 H) and soft-tissue windows (window width, 400 H; window level, 40 H).

The thoracic oesophagus was divided in supra-aortic and infra-aortic levels (above and below the superior limit of aortic arch, respectively). The largest coronal diameters of the supra-aortic and infra-aortic levels observed in the HRCT pictures were measured and recorded, considering the internal limits of inner oesophageal mucosa (Figure 1Go). Oesophageal dilatation was diagnosed if the luminal coronal diameter of the oesophagus exceeded 10 mm, whatever the content (air, liquid or solid) [12].


Figure 1
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  		A schematic drawing of how the coronal oesophageal diameter was measured.

 
Intraobserver agreement for the oesophageal coronal diameter measurement in HRCT was tested in 30 examinations. The second reading was performed 12 months apart from the initial evaluation. There was a good agreement between the two observations for supra-aortic oesophageal coronal diameter (Fleiss weighted Kappa = 0.65) and a moderate agreement for infra-aortic oesophageal coronal diameter (Fleiss weighted Kappa = 0.56). Interobserver agreement for oesophageal coronal diameter measurement in HRCT was tested using another 30 examinations. The measurements obtained by another radiologist demonstrated a good agreement for the supra-aortic (Fleiss weighted Kappa = 0.64) and for the infra-aortic oesophageal coronal diameters (Fleiss weighted Kappa = 0.60).

All clinical, radiological, and scintigraphic examinations were performed within 6 months. No observer was informed about the clinical details of the SSc patients or about the results of the other examinations.

Statistical analysis
Data were analysed using EPI-INFO version 6 and SPSS for Windows version 11.0. Categorical variables were presented as numbers and proportions. Quantitative variables were tested graphically (with normal probability plots) and statistically (with Kolmogorov-Smirnov goodness-of-fit test) for the normality of distribution. Quantitative variable with normal distribution was presented as mean and standard deviation (SD). Non-normal quantitative variables were presented as median and interquartile range (IQR). The associations between categorical variables were tested using Fisher's exact test. Paired comparisons involving non-normal quantitative variables were performed with the Wilcoxon signed ranks test. A two-tailed p-value ≤ 0.05 was considered statistically significant.

Receiver operating characteristic (ROC) curves were used to test the ability of HRCT to differentiate patients with and without oesophageal radionuclide transit delay. The area under the ROC curve is a suitable measure to summarize the discrimination power of a diagnostic model (representing the accuracy of the model) and can range from 0.5 (no discrimination) to 1.0 (perfect discrimination). 95% confidence intervals for the areas under the curves were also calculated. Sensitivity and specificity values were estimated, along with 95% confidence intervals (95% CI).


   Results
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 Abstract
 Introduction
 Material and methods
 Results
Discussion
 References
 
59 out of 76 patients (77.6%) had scintigraphic evidence of oesophageal dysfunction. The prevalence of 20% or more retention of liquid in supine position at 60 s (75%) was similar to the evaluation at 15 s.

The thorax HRCT demonstrated ground-glass opacities or reticular pattern/honeycombing in 43 patients (56.6% of the sample). Out of these patients, 24 presented ground-glass opacities and reticular pattern/honeycombing, 6 presented reticular pattern/honeycombing without ground-glass opacities, and 13 presented only ground-glass opacities.

Supra-aortic oesophageal dilatation (Figure 2aGo) was present in 19 patients (25.0%). Infra-aortic oesophageal dilatation (Figure 2bGo) was detected in 48 patients (63.1%). Supra-aortic and infra-aortic oesophageal dilatations in HRCT were significantly associated with oesophageal dysmotility (GoTables 1 and 2Go, respectively). All oesophageal wall calibres were smaller than 3 mm (Figure 3Go).


Figure 2
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  		A 63-year-old man. High resolution CT demonstrates (a) supra-aortic oesophageal dilatation and (b) infra-aortic dilatation (black arrows). Note peripheral ground-glass opacities (white arrowheads).

 

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  		Table 1. Association between supra-aortic coronal oesophageal diameter and oesophageal dysmotility assessed by radionuclide oesophageal scintigraphy*

 

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  		Table 2. Association between infra-aortic coronal oesophageal diameter and oesophageal dysmotility assessed by radionuclide oesophageal scintigraphy

 

Figure 3
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  		A 55-year-old woman. Infra-aortic slice demonstrates patulous thin-wall (white arrow) oesophageal dilatation.

 
As the selection of cut-off values of coronal diameters is rather arbitrary, we additionally used ROC curves to test the ability of HRCT to discriminate patients with and without oesophageal dysfunction on scintigraphy. The areas under the ROC curves suggest that the oesophageal coronal diameters (particularly the infra-aortic) have good discriminatory ability for oesophageal dysmotility (Figure 4Go). An infra-aortic oesophageal diameter ≥9 mm would provide a sensitivity of 83.1% (95% CI: 71.0–91.5) and a specificity of 94.1% (95% CI: 71.2–99.0) for oesophageal dysmotility. Supra-aortic oesophageal diameter ≥4 mm would provide a sensitivity of 64.4% (95% CI: 50.9–76.4) and a specificity 94.1% (95% CI: 71.2–99.0) for oesophageal dysmotility.


Figure 4
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  		Receiver operating characteristic curves of(a) supra-aortic and (b) infra-aortic coronal diameters for oesophageal dysfunction detected in scintigraphy.

 

   Discussion
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 Abstract
 Introduction
 Material and methods
 Results
 Discussion
References
 
SSc affects the skin in the form of thickening, tightness, pitting oedema, digital ulcers and telangiectasias, but also affects visceral organs like the lungs, the kidneys and the gastrointestinal tract. Although skin changes are the most remarkable abnormalities, the visceral disease (especially pulmonary) is responsible for the prognosis [12].

The gastrointestinal tract is involved in up to 80–90% of SSc patients [12, 17–19], with the oesophagus being the internal organ most frequently involved (50–80%) in this disease [5, 6]. SSc leads to atrophy of smooth muscle, to impaired peristalsis, and to reduction of the lower oesophageal sphincter (LES) tone. Reduction in LES tone leads to gastro-oesophageal reflux and oesophagitis [5–7, 17]. Symptoms include dysphagia, odynophagia, heartburn and regurgitation [5, 7, 12, 17], but the absence of symptoms does not exclude advanced affliction of the oesophagus [6, 19–21]. The lower two-thirds of the oesophagus are usually affected, commonly appearing dilated, with absent peristalsis, and sometimes with strictures and mucosal changes due to oesophagitis [4–7, 12].

The sclerodermic oesophagus has been traditionally evaluated by different diagnostic methods, including manometry [1, 4, 22, 23], endoscopy [5], scintigraphy [1, 3, 4, 7, 9, 10, 16, 24–27], barium-oesophagogram [5, 19, 28], cine-oesophagography [23, 29], ultrasound [29] and oesophageal pH monitoring [30]. Since the introduction of the scintigraphic method in the oesophageal evaluation by Kazem, in 1972 [25], several authors have demonstrated that the radionuclide oesophageal transit examination is a safe and non-invasive method that could be used as an alternative to oesophageal manometry in SSc patients [1, 3, 4, 24, 26]. Oesophageal transit scintigraphy has been demonstrated to be sensitive (91–100%) and specific (88%) to detect motor function abnormalities diagnosed by manometry [1, 26, 31].

Although scintigraphy has been considered a good method for the evaluation of oesophageal motility disorders, there is not a uniformly accepted protocol to guide the execution and the interpretation of the examination. This compromises the applicability and reproducibility of the results obtained by different groups of researchers. To illustrate the variability in the methods used, Akesson et al [3] applied a single swallow protocol with the ingestion of a pineapple puree in sitting position, and oesophageal transit delay was defined as a transit time longer than 300 s. Carette et al [26] used a single swallow of 10 ml of labelled water in supine position, followed by a dry swallow 30 s later. Davidson et al [24] used a supine colloid ingestion protocol, defining RES abnormality as the retention of colloid ≥5% at 15 s after ingestion. In the present study, in which oesophageal transit was evaluated after a single swallow of labelled liquid in supine position, the prevalence of oesophageal dysfunction was 77.6%. In previous studies, the reported prevalence of oesophageal transit abnormalities on scintigraphy varied from 82% to 100% [1, 3, 7, 24, 26] what demonstrates a relative homogeneity of results despite methodological variations.

In the present report we used an evaluation of oesophageal transit after a single swallow. Previous studies have suggested that multiple swallows may be more appropriate in the evaluation of oesophageal dysfunction, since the variability observed in single swallow studies may be reduced [16]. However, as far as we are concerned, the diagnostic accuracy of single and multiple swallows (in relation to manometry) has not been directly compared in previous studies. Ham et al [32] suggested that the oesophageal transit patterns observed after multiple swallowing were different from those observed after a single swallow. Tolin et al [8] demonstrated that the oesophageal emptying may be incomplete in individuals with normal manometry after multiple swallows. Therefore, a definite answer about the ideal protocol to be used in RES has not yet been found.

The lungs are the second most commonly affected internal organ in scleroderma. The patients often have diffuse interstitial lung disease (fibrosing alveolitis), which is clinically and prognostically relevant. Thorax HRCT is the established non-invasive gold-standard technique for the diagnosis of fibrosing alveolitis [11]. HRCT abnormalities in scleroderma lung disease are well documented: ground-glass opacification in isolation or with reticular patterns are associated with inflammatory alveolitis and a reticular pattern – with or without honeycomb changes – is associated with a fibrotic histology [11, 12]. Further than diagnosis, patients with scleroderma are also evaluated with HRCT to assess the activity and progression of pulmonary disease.

Thorax CT has been previously used to evaluate the oesophagus in SSc patients. Bhalla et al [12] demonstrated oesophageal asymptomatic dilatation (12–40 mm) in 20/25 patients (80%) with SSc. The authors suggested that oesophageal evaluation by CT could be used to narrow the differential diagnosis of patients with interstitial lung disease. In the present study, infra-aortic and supra-aortic dilatation (≥10 mm) were observed in 63.1% and 25% of the cases, respectively. The predominance of dilatation in the infra-aortic region (lower two-thirds) has been largely demonstrated [3, 6, 7, 12] and is related to the greater amount of smooth muscle fibres in the inferior portions of the oesophagus. These fibres are affected by extensive fibrosis and atrophy [7], leading to impaired peristalsis, dilatation, pouches of air–liquid, and even to solid contents in the oesophagus (Figure 5Go).


Figure 5
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  		A 61-year-old woman. Dilated infra-aortic oesophagus after overnight fasting demonstrates ingested contents (black arrow).

 
There are a few studies reporting supra-aortic oesophageal dilatation in SSc patients [21, 33]. Proximal oesophageal dilatation can be explained examining the anatomic variability of the distribution of the smooth musculature in the oesophageal wall. Post-mortem studies have shown that the level of the transition zone between striated and smooth muscle is quite variable, sometimes occurring as proximally as the thoracic inlet or even in the cervical oesophagus [33]. Therefore, patients with a higher transition zone would probably have a greater likelihood of presenting supra-aortic dilatation.

As far as we are aware, there have been no previous studies trying to relate the coronal oesophageal diameters with the oesophageal dysfunction in SSc. Our study demonstrated that oesophageal dilatation (particularly at the infra-aortic level) is highly associated to radionuclide transit delay. Additionally, our results also suggest that the infra-aortic coronal diameter may be useful in the diagnosis of oesophageal dysmotility, as suggested by the ROC curve analysis. Therefore, besides the routine evaluation of interstitial lung disease on HRCT, the measurement of coronal oesophageal diameters could provide useful and easily attainable information about the oesophageal motility status in SSc.

In the present study we had no control group or patients with other causes of oesophageal dysfunction to compare with SSc patients. Therefore, our results apply exclusively to patients with SSc. It would be interesting to compare HRCT and RES in other diseases characterized by oesophageal dysmotility or structural abnormalities.

In no patient of this study the oesophageal wall thickness exceeded the reported normal value of 3 mm. This has been also described in a previous report [34] and probably reflects that, although histopathological oesophageal abnormalities (fibrosis and atrophy) may be striking, these findings do not correlate with oesophageal wall thickening, not even in patients with long lasting disease.

Considering the results presented here, we conclude that the measurement of oesophageal coronal diameters in thorax HRCT (directed primarily to the evaluation of interstitial lung disease) provide useful information about the functional status of the oesophagus in SSc patients.


   Acknowledgments
 
We acknowledge Drs Raquel Faccioni, Marcus Franck, Tatiana Freitas Tourinho, Marcelo Maltchick, Paulo Sérgio Thys, Patrícia Minuzzi da Motta, Max Brenner, Tamara Mucenic, Adriano Barbiero, Tatiana Karenini Müller, Carmen Both Schenatto, Charles Lubianca Kohem, Lilian Scussel-Lonzetti, Claiton Viegas Brenol, Sandra Helena Machado, and Ilóite Scheibel on their valuable support. We also thank to Juliana Bredemeier for the English review of this manuscript.

Received for publication November 7, 2005. Revision received January 4, 2006. Accepted for publication January 30, 2006.


   References
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 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 

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