Diagnosis of Primary Versus Secondary Achalasia: Reassessment of Clinical and Radiographic Criteria

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1 Courtney A. Woodfield 1 Marc S. Levine Stephen E. Rubesin Curtis P. Langlotz Igor Laufer Received January 14, 2000; accepted after revision February 16, All authors: Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce St., Philadelphia, PA Address correspondence to M. S. Levine. AJR 2000;175: X/00/ American Roentgen Ray Society Diagnosis of Primary Versus Secondary Achalasia: Reassessment of Clinical and Radiographic Criteria OBJECTIVE. Our purpose was to reassess the usefulness of barium studies and various clinical parameters for differentiating primary from secondary achalasia. MATERIALS AND METHODS. Radiology files from 1989 through 1999 revealed 29 patients with primary achalasia and 10 with secondary achalasia (caused by carcinoma of the esophagus in three, of the gastric cardia in three, of the lung in three, and of the uterus in one) who met our study criteria. The radiographs were reviewed to determine the morphologic features of the narrowed distal esophageal segment and gastric cardia and fundus. Medical records were also reviewed to determine the clinical presentation; endoscopic, manometric, and surgical findings; and treatment. RESULTS. The mean patient age was 53 years in primary achalasia versus 69 years in secondary achalasia ( p = 0.03). The mean duration of dysphagia was 4.5 years in primary achalasia versus 1.9 months in secondary achalasia ( p < ). The narrowed distal esophageal segment had a mean length of 1.9 cm in primary achalasia versus 4.4 cm in secondary achalasia ( p < ), and the esophagus had a mean diameter of 6.2 cm in primary achalasia versus 4.1 cm in secondary achalasia ( p < ). The narrowed segment was eccentric or nodular or had abrupt proximal borders in only four of 10 patients with secondary achalasia, and evidence of tumor was present in the gastric fundus in only three. CONCLUSION. When findings of achalasia are present on barium studies, a narrowed distal esophageal segment longer than 3.5 cm with little or no proximal dilatation in a patient with recent onset of dysphagia should be considered highly suggestive of secondary achalasia, even in the absence of other suspicious radiographic findings. A chalasia is a well-known esophageal motility disorder characterized by absent primary peristalsis and incomplete relaxation of the lower esophageal sphincter [1]. Most patients have primary (idiopathic) achalasia caused by loss of the ganglion cells in the esophageal myenteric plexuses [2, 3]. However, others have secondary achalasia (pseudoachalasia) caused by malignant tumor at the gastroesophageal junction [4 9] or, less commonly, by benign conditions such as Chagas disease [10]. Nearly 75% of patients with secondary achalasia are found to have underlying carcinoma of the cardia [6], but secondary achalasia may also be caused by carcinoma of the esophagus or by other malignant tumors that metastasize to the mediastinum or gastroesophageal junction, including carcinoma of the lung, breast, pancreas, uterus, and prostate gland [4, 7 9]. Primary achalasia is characterized on barium studies by absent primary peristalsis and smooth, tapered narrowing of the distal esophagus caused by incomplete relaxation of the lower esophageal sphincter [11]. However, in secondary achalasia, barium studies may also reveal eccentricity, nodularity, angulation, straightening, or proximal shouldering of the narrowed segment [4, 7, 8, 12, 13]. In one report, it was suggested that the narrowed segment may be longer in secondary than in primary achalasia [12]. Secondary achalasia should also be suspected if barium studies reveal tumor at the gastric cardia [4, 12, 13]. Nevertheless, little data are available about the usefulness of barium studies in differentiating primary from secondary achalasia. In the two largest series in the literature, it was possible to distinguish these conditions on barium studies in only six (46%) of 13 patients [6, 14]. We therefore performed a retrospective investigation of patients with primary and secondary achalasia to reassess AJR:175, September

2 Woodfield et al. the usefulness of barium studies and various clinical parameters for differentiating these conditions. Materials and Methods Computerized radiology files at our university hospital from 1989 through 1999 and radiology logs at our affiliated Veterans Affairs medical center from 1995 through 1999 revealed 150 patients with a diagnosis of achalasia on barium studies. Seventy-two of these 150 patients were excluded from our analysis because of known treatment for achalasia (e.g., pneumatic dilatation, botulinum toxin injection, or surgical myotomy) before undergoing any barium studies at our hospital, and 39 were excluded because medical records were unavailable (36 patients) or clinical follow-up was inadequate to establish the diagnosis (three patients). The remaining 39 patients constituted our study group. On the basis of the endoscopic, manometric, CT, and surgical findings, 29 patients (74%) had a final diagnosis of primary achalasia, and 10 (26%) had a final diagnosis of secondary achalasia caused by carcinoma of the esophagus in three patients, carcinoma of the gastric cardia in three, and metastases to the mediastinum or gastroesophageal junction from carcinoma of the lung in three and from carcinoma of the uterus in one. All 39 patients underwent barium studies, including double-contrast esophagography in 11, single-contrast esophagography in five, doublecontrast upper gastrointestinal examinations in 17, and single-contrast upper gastrointestinal examinations in six. In all 39 patients, the radiographic reports described absent primary peristalsis in the esophagus on fluoroscopy and a segment of distal esophageal narrowing that extended to the gastroesophageal junction. The correct diagnosis was suggested on the original radiology reports in all 10 patients with secondary achalasia. The radiographs from these 39 studies were reviewed in a blinded fashion to determine the degree of esophageal dilatation at its widest point and to evaluate the morphologic features of the narrowed distal esophageal segment, including symmetry (symmetric versus eccentric), contour (smooth versus nodular or ulcerated), proximal borders (tapered versus abrupt or shouldered), and length (measured from the proximal border of the narrowed segment to the gastroesophageal junction, not accounting for radiographic magnification). When sufficient barium entered the stomach, the gastric cardia and fundus were also evaluated for evidence of tumor in this region. Medical, radiologic, and endoscopic records were also reviewed to determine the clinical presentation as well as the endoscopic, manometric, CT, and surgical findings. Univariate statistical analysis was performed on all major study variables. Wilcoxon s rank sum test was performed using JMP statistical analysis software (SAS Institute, Cary, NC) to determine whether the patient s age, the duration of dysphagia, the length of the narrowed distal esophageal segment, or the diameter of the proximal esophagus was significantly associated with achalasia etiology (i.e., primary versus secondary achalasia). Results Clinical Findings Primary achalasia. Sixteen of the 29 patients with primary achalasia were women and 13 were men. The mean age was 53 years (range, years); 11 patients (38%) were more than 60 years old. All 29 patients presented with dysphagia, which had a mean duration of 4.5 years (range, years); 28 patients (97%) had dysphagia for 1 year or longer. Five patients had weight loss, with a mean loss of 8.2 kg (range, kg) over a mean period of 13 months (range, 2 36 months). Secondary achalasia. Nine of the 10 patients with secondary achalasia were men and one was a woman. The mean age was 69 years (range, years); eight patients (80%) were more than 60 years old. All 10 patients presented with dysphagia, which had a mean duration of 1.9 months (range, months). Patients with secondary achalasia were significantly more likely to be older ( p = 0.03) and to have a shorter duration of dysphagia ( p < ) than patients with primary achalasia (Table 1). Seven patients had weight loss, with a mean loss of 10.5 kg (range, kg) over a mean period of 5 months (range, months). Radiographic Findings Primary achalasia. In all 29 patients with primary achalasia, barium studies revealed smooth symmetric, tapered narrowing of the distal esophagus that extended to the gastroesophageal junction (Figs. 1 and 2). The narrowed segment had a mean length of 1.9 cm (range, cm). The esophagus above the narrowed segment had a mean diameter of 6.2 cm (range, 4 10 cm) and was greater than 4 cm in diameter in 26 patients TABLE 1 (90%). In two patients, the distal esophagus had a tortuous (i.e., sigmoid) configuration. The gastric cardia and fundus appeared normal in 10 patients (34%) but could not be adequately evaluated because of delayed emptying of barium from the esophagus in the remaining 19 patients (66%). Secondary achalasia. In six (60%) of 10 patients with secondary achalasia, barium studies revealed smooth symmetric, tapered narrowing of the distal esophagus (Figs. 3 and 4). The remaining four patients (40%) had eccentric narrowing of the distal esophagus (Fig. 5A), with abrupt proximal borders in one, nodularity in one, and straightening in one. The narrowed segment had a mean length of 4.4 cm (range, cm) and was longer than 3.5 cm in eight patients (80%) (Figs. 3 5). The esophagus above the narrowed segment had a mean diameter of 4.1 cm (range, cm) and was 4 cm or less in diameter in eight patients (80%). Patients with secondary achalasia were significantly more likely to have a longer segment of narrowing (p < ) and to have a less dilated proximal esophagus (p < ) than patients with primary achalasia (Table 1). One patient also had an annular lesion with abrupt shelflike borders in the upper esophagus caused by esophageal carcinoma (Fig. 5B). Secondary achalasia in this patient presumably resulted from the spread of tumor via lymphatics in the esophageal wall to the gastroesophageal junction. The gastric cardia and fundus appeared abnormal in three patients (30%) with secondary achalasia. Two had carcinoma of the cardia; barium studies revealed lobulated fundal folds in one and encasement of the fundus by tumor in the other. In one patient with esophageal carcinoma, a barium study revealed nodularity of the gastric fundus. In two other patients, barium studies revealed a normal-appearing cardia and fundus. In the remaining five patients (including one with carcinoma of the cardia), the cardia and fundus could not be adequately evaluated because of delayed emptying of barium from the esophagus. Major Variables of Primary and Secondary Achalasia in 30 Patients Variable Primary Achalasia (20 Patients) Secondary Achalasia (10 Patients) Age (years) 53 ± ± Duration of dysphagia (months) 54 ± ± 1.2 < Length of narrowing (cm) 1.9 ± ± 0.88 < Diameter of proximal esophagus (cm) 6.2 ± ± 0.76 < p 728 AJR:175, September 2000

3 Radiography of Primary Versus Secondary Achalasia Fig year-old man with primary achalasia. Spot radiograph from doublecontrast barium study shows 1-cm-long smooth, tapered narrowing (straight arrow ) of distal esophagus with esophageal diameter proximally of 6 cm. Note standing column of barium (curved arrow ) on this upright view. Short length of narrowed segment is characteristic of primary achalasia. Endoscopic, Manometric, CT, and Surgical Findings Primary achalasia. Twenty-five of the 29 patients with primary achalasia had typical findings of achalasia on manometry [1, 15]. In all 29 patients, endoscopy revealed a closed lower esophageal sphincter that opened in response to the advancing endoscope, allowing it to pass into the gastric fundus [15]. Secondary achalasia. Eight of the 10 patients with secondary achalasia underwent endoscopy, which revealed a closed lower esophageal sphincter in all cases; the endoscope could not be advanced into the stomach in four of these patients, a finding that has been associated with secondary achalasia [6, 15 17]. Three patients had esophageal carcinoma at endoscopy, with infiltrative lesions in the distal esophagus in two and in the upper esophagus in one; endoscopic biopsy specimens revealed squamous cell carcinoma in all three patients. Three other patients had carcinoma of the cardia on endoscopy, with polypoid masses in the gastric Fig year-old woman with primary achalasia. Spot radiograph from double-contrast barium study shows 3.5-cmlong, gradually tapered segment of narrowing (straight arrows) in distal esophagus with esophageal diameter proximally of 7 cm and standing column of barium (curved arrow ). This was longest segment of narrowing shown on radiography in a patient with primary achalasia. fundus; endoscopic biopsy specimens revealed carcinoma of the cardia in two of these patients. The third had carcinoma of the cardia at surgery. In three patients with lung carcinoma, chest CT scans revealed mediastinal adenopathy and mediastinal invasion by tumor. In the remaining patient with endometrial carcinoma, an abdominal CT scan revealed widespread intraperitoneal metastases, and a bone scan revealed diffuse osseous metastases. Although this patient did not have a chest CT scan, she was presumed to have secondary achalasia because of her widely disseminated endometrial carcinoma, advanced age (87 years), and short duration of dysphagia (3 months). Discussion In our study, barium studies revealed classic findings of secondary achalasia with an eccentric, nodular, or shouldered segment of distal esophageal narrowing (Fig. 5A) in only 40% of Fig year-old man with secondary achalasia caused by lung carcinoma. Spot radiograph from single-contrast barium study shows 5-cm-long symmetric, tapered narrowing (arrows) of distal esophagus with esophageal diameter proximally of 6 cm. Note fine irregularity of contour of distal esophagus above narrowed segment caused by superimposed infection with Candida esophagitis organisms proven on endoscopy. patients with this condition. In the remaining 60%, the narrowed segment was smooth and symmetric with tapered proximal borders (Figs. 3 and 4). Therefore, secondary achalasia would not be suspected in most cases solely on the basis of classic radiologic criteria. However, the narrowed distal esophageal segment was longer than 3.5 cm in 80% of patients with secondary achalasia, and an unusually long segment of narrowing was the only suspicious finding in 40% (Figs. 3 and 4). In contrast, the narrowed segment was 3.5 cm or shorter in all patients with primary achalasia (Figs. 1 and 2). Therefore, the length of the narrowed distal esophageal segment was a useful and statistically significant criterion for differentiating secondary achalasia from primary achalasia on barium studies (p < ). In our series, the degree of esophageal dilatation above the narrowed segment was also a statistically significant criterion for differentiating secondary achalasia from primary achalasia AJR:175, September

4 Woodfield et al. A Fig year-old woman with secondary achalasia caused by carcinoma of uterus. Spot radiograph from double-contrast barium study shows 4-cm-long smooth, tapered narrowing (arrows) of distal esophagus with esophageal diameter proximally of 3.5 cm. As in Figure 3, a narrowed segment longer than 3.5 cm should be considered highly suggestive of secondary achalasia, even lacking other suspicious radiographic findings. (p < ). The diameter of the esophagus at its widest point was 4 cm or less in 80% of patients with secondary achalasia, whereas the diameter of the esophagus was greater than 4 cm in 90% of patients with primary achalasia. The greater degree of esophageal dilatation in patients with primary achalasia was presumably related to the more gradual course of the disease that allowed the esophagus to progressively dilate over a period of years. In fact, both patients who had a tortuous (i.e., sigmoid) distal esophagus were found to have primary achalasia with relatively long-standing disease. A limitation of our study is the variable effect of magnification on our radiographic measurements of the narrowed distal esophageal segment or dilated proximal esophagus in patients with primary or secondary achalasia, depending on the height of the fluoroscopic tower above the examining table. This variable could create a potential bias if greater magnification occurred primarily in one group or the other. However, the degree of magnification was in no way related to patient selection, so this variable should not have had a significant effect on our findings. When findings of achalasia are present on barium studies, it is important to evaluate the gastric cardia and fundus to rule out an underlying malignant tumor at the gastroesophageal junction as the cause of these findings [4, 6, 13, B Fig year-old man with secondary achalasia caused by carcinoma of esophagus. A, Spot radiograph from double-contrast barium study shows 4-cm-long eccentric, tapered narrowing (arrows) of distal esophagus with esophageal diameter proximally of 4 cm. B, Additional spot radiograph shows annular carcinoma with relatively abrupt, shelflike margins (arrows) in upper thoracic esophagus. 730 AJR:175, September 2000

5 Radiography of Primary Versus Secondary Achalasia 18]. In our series, however, the cardia and fundus could not be adequately evaluated radiographically in 66% of patients with primary achalasia and in 50% with secondary achalasia because of delayed emptying of barium from the esophagus. Therefore, it is important to be aware of the limitations of barium studies in evaluating the cardia and fundus in patients with suspected achalasia. In the past, some investigators have advocated amyl nitrite inhalation as a simple test for differentiating primary and secondary achalasia on barium studies. It has been shown that inhalation of amyl nitrite, a smooth-muscle relaxant, has no effect on the narrowed distal esophageal segment in secondary achalasia but causes a measurable increase of 2 mm or more in the caliber of this segment in primary achalasia [19]. Nevertheless, this technique has not gained widespread acceptance. Although our investigation focused on the usefulness of barium studies for differentiating the two forms of achalasia, CT may also be useful in these patients. CT typically reveals little or no esophageal wall thickening and no evidence of a mass at the cardia in patients with primary achalasia [20 22]. In some cases, however, CT may reveal a pseudomass at the cardia in patients without tumor because of inadequate distention of this region [23]. In contrast, CT may show asymmetric thickening of the distal esophageal wall, a soft-tissue mass at the cardia, or mediastinal adenopathy in patients with secondary achalasia [21]. CT may also be helpful for identifying the site of the primary tumor in patients with secondary achalasia caused by remote tumors. Various clinical parameters are also purported to be useful for differentiating primary achalasia from secondary achalasia, including the age of the patient, the duration of dysphagia, and substantial weight loss. Primary achalasia is more likely to occur in younger patients (<50 years old) with longstanding dysphagia (>1 year) and little or no weight loss (<7 kg) [15, 18], whereas secondary achalasia is more likely to occur in older patients (>60 years old) with recent onset of dysphagia (<6 months) and substantial weight loss (>7 kg) [14]. Nevertheless, overlap in the clinical presentation has been reported for all these parameters [17, 24]. In our series, the duration of dysphagia was a statistically significant clinical criterion for differentiating secondary achalasia from primary achalasia ( p < ); all patients with secondary achalasia had dysphagia for 4 months or less, whereas 97% of patients with primary achalasia had dysphagia for 1 year or more. The age of the patient was also a statistically significant but somewhat less useful criterion for differentiating these conditions ( p = 0.03); 80% of patients with secondary achalasia and 38% with primary achalasia were more than 60 years old. In two previously published series, 28 30% of patients with primary achalasia were also found to be more than 60 years old [17, 24], limiting the usefulness of this criterion. In conclusion, only 40% of patients in our series had classic radiographic features of secondary achalasia such as eccentricity, nodularity, or shouldering of the narrowed distal esophageal segment, or suspicious findings in the region of the gastric cardia or fundus. Instead, the most useful criteria for differentiating secondary from primary achalasia were the length of the narrowed segment and the degree of proximal dilatation, and the most useful clinical criterion was the duration of dysphagia. When findings of achalasia are present on barium studies, a narrowed distal esophageal segment longer than 3.5 cm with little or no proximal dilatation in a patient with recent onset of dysphagia should be considered highly suggestive of secondary achalasia, even in the absence of other suspicious radiographic findings. References 1. Katz PO, Castell DO. Review: esophageal motility disorders. Am J Med Sci 1985;290: Cassella RR, Brown AL, Sayre GP, Ellis FH. Achalasia of the esophagus: pathologic and etiologic considerations. Ann Surg 1964;160: Csendes A, Smok G, Braghetto I, Ramirez C, Velasco N, Henriquez A. Gastroesophageal sphincter pressure and histological changes in distal esophagus in patients with achalasia of the esophagus. Dig Dis Sci 1985;30: Lawson TL, Dodds WJ. Infiltrating carcinoma simulating achalasia. Gastrointest Radiol 1976;1: McCallum RW. Esophageal achalasia secondary to gastric carcinoma: report of a case and review of the literature. Am J Gastroenterol 1979;71: Kahrilas PJ, Kishk SM, Helm JF, Dodds WJ, Harig JM, Hogan WJ. Comparison of pseudoachalasia and achalasia. Am J Med 1987;82: Feczko PJ, Halpert RD. Achalasia secondary to nongastrointestinal malignancies. Gastrointest Radiol 1985;10: Joffe N. Right-angled narrowing of the distal oesophagus secondary to carcinoma of the tail of the pancreas. Clin Radiol 1979;30: Eaves R, Lambert J, Rees J, King RWF. Achalasia secondary to carcinoma of the prostate. Dig Dis Sci 1983;28: Ferreira-Santos R. Aperistalsis of the esophagus and colon etiologically related to Chagas disease. Am J Dig Dis 1961;6: Ott DJ. Motility disorders. In: Gore RM, Levine MS, Laufer I, eds. Textbook of gastrointestinal radiology. Philadelphia: Saunders, 1994: Seaman WB, Wells J, Flood CA. Diagnostic problems of esophageal cancer: relationship to achalasia and hiatus hernia. AJR 1963;90: Marshak RH, Eliasoph J. Cardiospasm or carcinoma? The roentgen findings. Am J Dig Dis 1957; 2: Tucker HJ, Snape WJ, Cohen S. Achalasia secondary to carcinoma: manometric and clinical features. Ann Intern Med 1978;89: Reynolds JC, Parkman HP. Achalasia. Gastroenterol Clin North Am 1989;18: Rozman RW, Achkar E. Features distinguishing secondary achalasia from primary achalasia. Am J Gastroenterol 1990;85: Tracey JP, Traube M. Difficulties in the diagnosis of pseudoachalasia. Am J Gastroenterol 1994; 89: Levine MS. Other malignant tumors. In: Gore RM, Levine MS, Laufer I, eds. Textbook of gastrointestinal radiology. Philadelphia: Saunders, 1994: Dodds WJ, Stewart ET, Kishk SM, Kahrilas PJ, Hogan WJ. Radiologic amyl nitrite test for distinguishing pseudoachalasia from idiopathic achalasia. AJR 1986;146: Rabushka LS, Fishman EK, Kuhlman JE. CT evaluation of achalasia. J Comput Assist Tomogr 1991; 15: Carter M, Deckmann RC, Smith RC, Burrell MI, Traube M. Differentiation of achalasia from pseudoachalasia by computed tomography. Am J Gastroenterol 1997;92: Tishler JM, Shin MS, Stanley RJ, Koehler RE. CT of the thorax in patients with achalasia. Dig Dis Sci 1983;28: Marks WM, Callen PW, Moss AA. Gastroesophageal region: source of confusion on CT. AJR 1981; 136: Sandler RS, Bozymski EM, Orlando RC. Failure of clinical criteria to distinguish between primary achalasia and achalasia secondary to tumor. Dig Dis Sci 1982;27: AJR:175, September

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