Gastrointest Radiol 1,253
Gastrointestinal
261 (1976)
Radiology ~ by Springer-Verlag 1976
Esophago-Gastrie Invagination in Patients with Sliding Hiatus Hernia Gary G. Ghahremani and Phillip A. Collins Departments of Radiology, Virginia Commonwealth University - Medical College of Virginia Hospitals, Richmond, Virginia, U.S.A. and The University of Chicago Pritzker School of Medicine, Chicago, Illinois, U.S.A.
Abstract. Intussusception of t.he distal esophagus into a reducible hiatus hernia is described in nine female and three male patients. The main radiographic feature is demonstration of a lobulated fundal mass of changeable size and configuration surrounding the narrowed distal esophageal segment. This pseudotumor is produced by inversion of the hiatus hernia into the stomach, and may be mistaken for a neoplasm. Disinvagination invariably occurs when maneuvers directed toward demonstration of a sliding hernia are utilized during upper gastrointestinal fluoroscopy. It is emphasized that esophago-gastric invagination frequently accounts for masses shown in the cardia of older women with intermittent dysphagia and crampy epigastric pain. Key words: Esophagus, abnormalities - Cardioesophageal junction, diseases - Hernia, diaphragmatic - Stomach, neoplasm - Stomach, intussusception.
The diversity of intrinsic or extrinsic lesions and functional changes affecting the esophago-gastric junction continues to pose a diagnostic challenge to radiologists [1 6]. In this context the sliding hiatus hernia (SHH) has been thoroughly discussed in the literature but its presentation as a mass in the gastric cardia has received scant attention [2, 7-9]. The frequency of such occurrence, however, is reflected in a recent paper by Kaye and Stassa [2]. They reviewed a series of 40 patients with a mass in the cardia detected on upper gastrointestinal studies and found that 10 cases (25%) were due to SHH. The pseudotumors associated with S H H are produced by three commonly related mechanisms: Address reprint request.s to." G.G. Ghahremani, M.D., Department of Radiology, Evanston Hospital Northwestern University, Evanston, IL 60201, U.S.A.
1. Transmigration qf the Mucosa in the Esophago-Gastric Junction Similar to transpyloric prolapse of antral mucosa, the normal mucosa in the esophago-gastric junction can also slide in either cephalad or caudad direction [4, 5, 10 17]. During this transient phenomenon, the displaced mucosal folds may be visualized as a polypoid mass in the lower esophagus or in the cardia.
2. Incagination oJ the Distal Esophagus into the SHH In the initial stage of this process (Fig. 1 B), the herniated part of the stomach forms the intussuscipiens or sheath around the invaginated esophageal segment. Its radiographic appearance has been resembled to a "jack-in-the-pulpit" [9, 10, 18, 19]. With progressive prolapse of the esophagus, however, the S H H becomes inverted and eventually displaced through the hiatus (Fig. 1 C). It will then present as a lobulated mass in the cardia surrounding the tapered distal esophagus.
3. Spontaneous Reduction of SHH Beneath
the Diaphragm The laxity of phrenico-esophageal membrane, widening of the hiatus, and redundancy of the esophagus in older individuals permit the hiatus hernia to move distally and occupy the space between the fundus and the left crus of the diaphragm. This results in an extrinsic moon-shaped pressure defect upon the fundus [2, 8, 18]. When S H H is small it may merely produce a sharp notch-like deformity of the posterior fundal wall [7]. The above described phenomena can also occur successively or in combination. The narrowed distal
254
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
~
hagus
H rnia
Stomach
A
B
esophagus and the mass presented in the gastric cardia may closely resemble and be mistaken for manifestation of a malignancy [1 3, 6, 8, 9, 11, 14, 16, 18]. Because of not infrequent association of epigastric pain and/or dysphagia with these confusing radiographic and gastroscopic findings, the patients may be subjected to unnecessary surgery [2, 3, 6, 11]. Therefore, it seems appropriate to: (a) report our experience with pseudotumors resulting from esophago-gastric invagination in 12 patients with SHH; (b) describe their clinical symptomatology and characteristic roentgen presentations; and (c) provide technical guidelines for their radiographic evaluation and differentiation from other lesions.
Clinical Material and Method
C Fig. I A-C. Diagrammatic representation of anatomic relationships during the process of esophago-gastric invagination. A The usual relation of the lower esophagus to the sliding hiatus hernia. B Prolapse of the distal esophagus into the hernia producing a "jackin-the-pulpit" appearance. C Advanced stage of invagination whereby the inverted hernia presents as a lobulated fundal mass surrounding the narrowed distal esophagus
The series consists of 12 patients seen over a 3-year period at the hospitals of the Medical College of Virginia and The University of Chicago. In 7 patients the upper gastrointestinal series were obtained mainly because of dysphagia, epigastric pain and/or weight loss. Three other patients were referrals for further evaluation and possible gastric surgery because radiographs obtained elsewhere had shown findings consistent with a tumor in the cardia. In the remaining 2 cases detection of a mass in the air-filled fundus on chest or obdominal films had ted to further investigation. Prev-
Fig. 2. Case 1. Esophago-gastric invagination presenting as a large lobulated fundal mass which persists on prone, supine and upright views (A-C respectively)
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination ious radiographs were also available for comparison in 7 patients, 4 of whom had documented SHH. Nine of the patients were female, and 3 were male. The age at the time of diagnosis ranged from 44 to 81 years, with the majority in their 7th decade of life. The patients have been followed for a period of 8 m o n t h s to 4 years. Each case has had evaluation of the upper gastrointestinal tract by endoscopy and at least two barium studies. Thus
255 far, only five patients have undergone surgery which includcd hiatal hernia repair in three, and gastrectomy for the associated peptic ulcer or carcinoma in two, Seven others who have been treated conservatively are under further observation. From our clinical material, the following four case histories have been selected and are being presented to exemplify various problems encountered in the diagnosis of esophago-gastric invagination. Radiographs from three other cases will also be shown to complement the spectrum of the observed roentgen findings.
Fig. 3. Case l. A - C Radiographs from a subsequent hypotonic upper gastrointestinal series reveal a large sliding hiatal hernia, and the disappearance of the fundal mass after disinvagination
Fig. 4. Case 2. A and B Radiographs demonstrate narrowing of the distal esophagus and marked deformity of the fundus suggestive of an infiltrative malignancy. Note the esophageal diverticuli and the "jet-effect" produced by passage of barium into the fundus. C Spot film after application o f abdominal compression shows cephalad displacement of the sliding hernia and esophageal stricture
256
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
Fig. 5. Case 3. A and B Spot films of the fundus in PA and lateral projection demonstrate a large mass covered by normal-appearing mucosa. C and D Two consecutive spot films obtained during spontaneous disinvagination show the sliding l)iatus hernia Case Reports Case 1: This 61-year-old w o m a n had previously undergone bilateral mastectomy for intraductal carcinoma. Five years later a recurrent t u m o r in the chest wall was resected and bilateral oophorectomy and adrenalectomy were performed. She was placed on steroid substitution therapy and felt well for the next 2 years. Her referral to the hospital was prompted by recent episodes of dysphagia, vomiting, epigastric pain, and weakness. Furthermore, a routine upright chest film obtained a few days earlier had shown a small pneumoperitoneum. This finding was not present on her admission 2 days later, but she appeared dehydrated and hypotensive. An upper gastrointestinal series demonstrated a persistent large lobulated mass in the gastric cardia. There was narrowing of the distal esophageal lumen, and marked deformity of the fundus
(Fig. 2 A C). The diagnosis entertained was most likely primary gastric neoplasm. Gastroscopy showed normal mucosa of the esophagus and stomach; however, the suggestion of a submucosal mass was made due to deformity of the posterior fnndal wall and flattening of its rugal folds. The laboratory data and other radiologic studies including liver and spleen scan were normal. L a p a r o t o m y revealed a small healing antral ulcer. A 7-cm gastrotomy incision was made in the body of the stomach. However, inspection and three biopsies from the cardioesophageal region disclosed no abnormality. A pyloroplasty without vagotomy was carried out and the patient recovered uneventfully. A barium study 1 m o n t h later re-demonstrated the fundal mass, though slightly smaller than on previous examination. To clarify this observation the patient was reexamined after i.m. injection of 30 mg of Pro-Banthine and use of effervescent agents. During this study there was gradual disappearance of the apparent mass with concur-
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
257
Fig. 6. Case 4. A Close-up view of the mass projecting into the fundus as seen on the upright chest film. B Spotfilm from a barium study shows the lobulated margin of the t u m o r which appears to be entirely within the stomach. C and D Two consecutive spot films with patient prone demonstrate gradual cephalad displacement of a sliding hernia which harbors the superficially ulcerated carcinoma
rent development of a large sliding hernia (Fig. 3A C). The latter finding was not recognized on two previous radiologic studies, or at gastroscopy and surgical exploration. Case 2." This 51-year-old alcoholic w o m a n had an 8-month history of dysphagia and substernal pain. The s y m p t o m s had been progressive recently leading to difficulty in swallowing solid food, regurgitation of undigested material, and about 7 kg weight loss. Her admission 3 years earlier was because of colonic hemorrhage from diverticulosis and an a d e n o m a t o u s polyp of the sigmoid. The upper gastrointestinal series at that time had shown an epiphrenic diverticulum, small sliding hernia, and transpyloric antral mucosal prolapse. A barium study of the upper gastrointestinal tract revealed two diverticula in the lower esophagus. The distal, 3 4 cm of the esophagus was narrowed so that the passage of barium produced
a "jet-effect." The rugal folds in the markedly deformed fundus also appeared distorted (Fig. 4 A and B). The findings suggested presence of an infiltrative malignancy. However, on review of radiographs obtained 3 years earlier it became apparent that a mass projecting into the air-filled fundus had been present on the upright chest film. Furthermore, the previously documented S H H was not visible on the current study. Because of our similar experience with other cases ofesophago-gastric invagination the barium examination was repeated. With application of abdominal compression the fundal mass completely disappeared when the hernia projected upward through the hiatus. At this time, marked narrowing of the distal esophagus was also recognized (Fig. 4C). Subsequent esophagoscopy confirmed the presence of diverticula, and chronic esophagitis proximal to the stricture. The instrument could not be advanced into the narrowed segment but obtained esophageal brushing specimens failed to reveal any malig-
258 nant ceils. Dilation of the benign stricture was then carried out on two separate occasions. Subsequently, the patient's condition further improved under conservative management, and clinical or radiographic findings of invagination have not recurred. Case 3." This 74-year-old w o m a n was referred to the hospital with the diagnosis o f a I u m o r in the gastric fundus. For nearly 3 m o n t h s she had had intermittent retrosternal and epigastric pain which usually developed during meals. An upper gastrointestinal series done elsewhere had demonstrated tertiary contractions in the esophagus and a persistent mass in the fundus covered by normalappearing mucosa (Fig. 5A and B). On admission the physical examination and laboratory data were unremarkable. A repeat upper gastrointestinal series intitially showed a deformity of the fundus suggestive of an extrinsic compression. During the course of the study, however, the lesion decreased in size and eventually disappeared when a large sliding hernia became visible above the diaphragm (Fig. 5C and D). The patient was kept in the recumbent position, and abdominal compression was applied. A transient prolapse of the lower esophageal segment into the hernia was noted to follow passage of each bolus of barium, thereby causing a "jack-in-the-pulpit" appearance. Elevation of the patient to the vertical position resulted in redevelopment of an infradiaphragmatic mass deforming the fundus when the hernia itself was no longer recognizable. Although evidence for reflux esophagitis and hiatal hernia was obtained on a subsequent esophagoscopy, the patient has not yet submitted to corrective surgery. However, the radiographic findings of intermittent esophago-gastric invagination have remained unchanged on two follow-up studies over the past 2 years. Case 4: A 67-year-old m a n visited the out-patient clinic complaining of severe back pain radiating to both flanks. This s y m p t o m of 2 days duration was preceded by 1-month history of experiencing epigastric pain, decreased appetite, and some loss of weight. Physical examination revealed an enlarged firm liver and marked tenderness on percussion of the lumbar vertebrae. The stool was positive for occult blood. A radiograph of the a b d o m e n showed lytic destruction of the right pedicle of L-3 surrounded by a faintly calcified soft tissue mass of about 4 cm in diameter. Upright chest films demonstrated diffuse pulmonary interstitial infiltrates. Furthermore, a large lobulated mass projecting into the air-filled fundus was clearly visible (Fig. 6A). These findings led to provisional radiologic diagnosis of a gastric malignancy with metastases to the lungs and the lumbar spine. An upper gastrointestinal series showed a large mass of changeable size and s m o o t h margin protruding into the cardia (Fig. 6B). Serial spot films of air-contrast-filled fundus were obtained in prone oblique positions while applying abdominal compression. These radiographs demonstrated extensive superficial ulceration of the lesion which actually infiltrated the wall of a sliding hiatal hernia (Fig. 6C and D). The distal esophagus and the hernia prolapsed readily into the stomach, and accounted for presentation of a mass of variable size in the cardia. The subsequent evaluation by fiberoptic esophagoscopy and " i n v e r s i o n " gastroscopy using retroflexion of the distal tip of the instrument to visualize the fundus confirmed the radiologic observations. The obtained biopsy material revealed presence of an adenocarcinoma. Emergency laparotomy was then performed because of a gastric perforation complicating the endoscopic procedures. The patient died a few days later due to peritonitis and bilateral pneumonia.
Discussion The difficulty in radiological diagnosis of carcinoma or other lesions of the gastric cardia becomes a for-
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric lnvagination
midable problem in older patients because the usually concurrent SHH further distorts the anatomic landmarks [2, 3, 6]. Furthermore, the prolapsing mucosal folds of the cardio-esophageal junction and intermittent invagination of the lower esophagus into SHH can themselves mimic findings of a malignancy [2 5, 9, 14 17]. In this regard, Ruzicka and Rigler [16] stated in 1951 that " t h e experience of reporting a mass in this region and the finding of no lesion whatsoever at surgery undoubtedly befalls every radiologist sooner or later." Many examples of pseudotumors produced by mucosal prolapse and/or esophago-gastric invagination in patients who were often submitted to unnecessary surgery have since been encountered [2, 3, 6, 11]. If one is familiar with these entities and their modes of presentation, however, the correct radiologic diagnosis and differentiation from other more significant lesions becomes a simple task. Antegrade prolapse of the distal esophageal mucosa as it is often visualized during upper gastrointestinal fluoroscopy probably represents a physiologic phenomenon [9-11, 13, 14, 19]. Its frequency of occurrence was determined by Aldridge among 2100 cases [10]. Of patients with SHH, 22.7% and of those without demonstrable hiatal hernia, 1.9% showed variable degrees of antegrade mucosal prolapse of the lower esophagus. Its concurrent association with transpyloric antral mucosal prolapse was also noted in 24 (10.3%) of 232 patients. Indeed, radiographic features of these two conditions are strikingly similar since the mobile redundant mucosa of the distal esophagus may also present as a polypoid mass of changeable configuration on serial spot films [3, 4, 10, 11, 14, 19]. This transient phenomenon commonly accounts for the so-called "jack-in-the-pulpit" appearance of the associated SHH [9, 10, 18, 19]. With rare exceptions such a finding has no definite clinical importance [10, 11, 13-15, 17]. However, it probably represents a precursor or the early, stage in the development of esophago-gastric invagination. The latter condition as illustrated in our patients obviously involves more than just the distal esophageal mucosa, though it is hardly possible to determine the actual extent of esophageal wall participating in the process. In 1956 Klinefelter reported 3 patients and reviewed 11 previously published cases in whom invagination of the lower esophagus into SHH was radiographically and/or surgically documented [18]. The series of patients encountered by us and others [9, 18, 19] indicates that this condition is certainly not so rare as one may suspect due to lack of its description in many current textbooks. Therefore, the clinical and radiologic manifestations of esophago-gastric invagination should be clarified so that the potentiality
G.G. Ghahremani and P.A. Collins: Esophago-Gastric Invagination
259
Figs. 7-9. Representative radiographs of three different cases of esophago-gastric invagination in its various forms
Fig. 7. Prolapse of the distal esophagus into the sliding hernia presenting a "jack-in-the pulpit" appearance Fig. 8. A large lobulated pseudotumor which disappeared when the associated sliding hernia was fully displaced above the diaphragm. This patient presented with burning epigastric pain and blood stained vomitus 3 years after a Billroth I gastroduodenostomy for peptic ulcer. The sliding hiatus hernia and hemorrhagic gastritis were documented on endoscopy Fig, 9. This well-defined fundal mass which simulates a leiomyoma was produced by invagination of the distal esophagus into a small reducible hiatus hernia
of misinterpretation of the findings is further diminished. Esophago-gastric invagination usually occurs in individuals beyond their 5th decade of life. An elongated redundant esophagus and a rather large S H H are invariably present and appear to be the necessary predisposing elements. To our knowledge the condition has not been reported to occur with paraesophageal hernia, in children, and is rare in adults who do not have SHH. F r o m a total of 36 cases studied by us and two other authors, 28 (78%) have been females [9, 18, 19]. In most instances a history suggestive of long-standing S H H with reflux esophagitis, e.g., frequent episodes of regurgigation and heartburn, could be elicited. As in four of our patients availability of previous radiographs showing an S H H would be of enormous value. Thus disappearance of such hernia and concurrent development of a mass in the cardia are highly suggestive of invagination. Intermittent dysphagia and epigastric pain are the c o m m o n symptoms in patients with narrowing of the invaginated distal esophagus by the surrounding mass of reduced and inverted hernia. According to Klinefelter [18], dysphagia occurs in over 50% of the cases
of invagination as compared with 8 % in patients with uncomplicated sliding hernia. Spontaneous relief of symptoms after eructation and regurgitation was experienced by several of our patients. Their subjective feeling correlated closely with fluoroscopic observation of disinvagination occurring following reflux of air and barium from the stomach. The correct diagnosis of esophago-gastric invagination depends on fluoroscopic spot filming performed with the patient in recumbent and upright positions. The mucosal prolapse at the cardio-esophageal junction and minimal invagination of the distal esophagus into a sliding hernia still above the diaphragm are easily recognized due to their very transient nature [4, 5, 10 19]. The presentation as "jack-in-thep u l p i t " appearance (Fig. 7) is best seen with the patient in a recumbent position [9, 10, 18, 19]. The usual inferior descent and reduction of S H H in the upright position readily explains the disappearance of radiographic findings following spontaneous disinvagination. Considerable difficulty m a y be encountered when invagination has occurred into a reducible hernia resulting in its inversion into the gastric fundus (Figs. 2,
260
3, 6, and 8). The radiographic presentation of this condition may then closely resemble the appearance noted after Nissen's fundoplication procedure [20]. Of course, previous history of SHH without subsequent corrective surgery is significant information. However, the combination of the following findings is characteristic of esophago-gastric invagination: a) A lobulated mass in the gastric cardia showing intact mucosa with variation in size and configuration depending on position of the patient. As a rule the pseudotumor becomes smaller when the esophagus is filled with barium and attains its largest size on an upright view of the fundus. b) The distal esophagus surrounded by a mass shows tapered narrowing of the lumen but without obstruction or any mucosal abnormality. Furthermore, the length of this apparent intra-abdominal portion of the esophagus appears unusually long. Spontaneous disinvagination occurs almost invariably during a carefully performed upper gastrointestinal examination [2, 9, 18, 19]. Application of abdominal compression with the patient prone often facilitates this process [18]. It is also helpful to administer effervescent agents or a larger quantity of barium. The full distention of the fundus will then provide additional force for displacing an inverted hernia above the diaphragm and will aid in reducing the prolapsed distal esophagus. It is of interest to note that in two of our patients complete disinvagination occurred only after i.m. injection of 30 mg of ProBanthine (Fig. 3). The spasmolytic effect of the drug on smooth muscles resulting in relaxation of the cardia and lower esophageal sphincter probably accounted for induction of gastro-esophageal reflux and cephalad displacement of the SHH [21]. The mass in the gastric cardia produced by esophagogastric invagination may occasionally persist throughout an upper gastrointestinal examination performed without the above recommended modifications (Fig. 2A C). This is probably due to tonic spasm of the cardia prohibiting cephalad mobility of the prolapsed esophagus and the inverted hernia [11, 18, 19]. The visible lesion (Figs. 2, 4, 8, and 9) may then be mistaken for a true tumor such as carcinoma or leiomyoma on both radiologic and gastroscopic studies [2, 3, 6, 9, 14]. The serious consequences of such misinterpretation can be avoided by careful performance of the upper gastrointestinal series, keeping in mind that about 25% of masses in the cardia are due to mucosal prolapse of the esophagus and/or its invagination into a reducible hernia [2, 3, 6 9, 16, 18, 19]. Therefore, it is most important that every effort be made to ascertain the presence or absence of SHH before labeling a mass in the cardia as a true tumor.
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
It should be pointed out that esophago-gastric invagination may occasionally be associated with peptic esophagitis, a polyp or carcinoma of the distal esophagus, or with tumors arising within the hernia itself [6, 11, 17, 19, 22]. As illustrated in Cases 2 and 4, evaluation of the mucosa of the fundus, the hernia and distal esophagus is important for detection of an associated inflammatory or neoplastic process and its extent. Amory has reported production of "'gastric inlet j e t " by passage of barium through the esophagogastric junction narrowed by a malignancy [23]. We observed this phenomenon in Case 2, who had a benign stricture of the distal esophagus. (Fig. 4A), but not in any of the remaining patients. Thus we can reasonably state that, in the absence of an inflammatory or neoplastic stricture, the passage of barium through the narrowed distal esophagus involved in invagination would not cause a "'jet-effect.'" In patients with esophago-gastric invagination included here and in previous reports, spontaneous disinvagination occurred without complication [2, 9, 18, 19]. Since the process is often recurrent, the symptoms such as dysphagia and epigastric pain are also experienced intermittently [1 l, 17, 18]. This clinical history, particularly in patients with known SHH, should always alert one to the possibility of invagination [18]. The symptomatic relief noted in several patients after medication of anticholinergic-spasmolytic agents, tranquilizers, antacids, and with dietary measures suggests effectiveness of the conservative therapy [11, 14, 18]. Therefore, surgical intervention may not be necessary unless the associated sliding hernia is further complicated by chronic peptic esophagitis or a neoplasm. References l. Calenoff L. Sparberg M: Gastric pseudolesions: roentgenographic-gastrophotographic correlation. Am J RoeHtgenol 113.139 146, 1971 2. Kaye JJ. Stassa G: Mimicry and deception in the diagnosis of tumors of the gastric cardia. Am J Roentgenol 110. 295 303, 1970 3. Lame EL: The gastric cardia and fundus. Extrinsic and benign tissues simulating gastric cancer. Radiology 75.'703 711, 1960 4. Rosenkranz W, Bryk D: Pseudotumors in large hiatus hernias. Am J RoentgelTol 116:289 292, 1972 5. Rudnick JP, Ferrucci JT Jr, Eaton SB Jr, e t a l : Esophageal pseudotumor: Retrograde prolapse of gastric mucosa into the esophagus. Am J Roenlgenol 115.'253 256, 1972 6. Wohl GT, Shore L : Lesions of the cardiac end of the stomach simulating carcinoma. Am J Roentgenol 82.1048 1057, 1959 7. Isard, HJ : An infradiaphragmatic clue to the diagnosis of hiatus hernia. Br J Radiol 41.'354 358, 1968 8. Kalokerinos J: The moon-shaped fundal defect of hiatus hernia: A new radiological sign. Report of nine cases. ,4u.~'trala.~ Radio/ 13.'96 102, 1969
G.G. Ghahremani and P.A. Collins: Esophago-Gastric Invagination 9. Walker BQ: The variable roentgenographic appearance of invagination of the esophagus. Based on thirteen cases. Cleceland Clin Q 33.'35 37, I966 10. Aldridge NH : Transmigration of the lower esophageal mucosa. Radiolow 79:962 968, 1962 11. de Lorimier AA, Warren JP: Prolapse of the mucosa at the esophagogastric j unction. A m J Roen lgeno184 : 1061-1069, 1960 12. Eeldman M: Retrograde extrusion or prolapse of the gastric mucosa into the esophagus. A m e r J Med Sci 222.54 60, 1951 13. Palmer ED: An attempt to localize the normal esophagogastric junction. Radiolog'y 60 : 825-83 l, 1953 14. Palmer ED: Mucosal prolapse at the esophagogastric junction. Ant J Gastroenterol 23: 530-537, 1955 15. Poirer A, Poirer B: Invagination de l'oesophage dans la bernie diaphragmatic de l'estomac. Arch Mal App Digest 43.'610 612, 1954 16. Ruzicka FF Jr, Rigler LG: Inflation of the stomach with double contrast. A roentgen study. J A M A 145.'696 702, 195l 17. Sarasin R, Hoch A: Die lnvagination der Oesophagusschleim-
261
I8. 19. 20. 21.
22. 23.
haut in den Magen. Sehweiz M e d Wochenschr 81.'1207 1209, 1951 Klinefelter EW: Invagination of the esophagus in hiatus hernia. Radiology 67." 562 568, 1956 Odegaard H: Invagination of the esophagus in hiatus hernia. Aeta Radiol 51.'443 448. 1959 Feigin DS, James AE Jr, Stitik FP, et al: The radiological appearance of hiatal hernia repairs. Radiology 110.'71 77, 1974 Longin F: Pharmakoradiographische Untersuchungen der oesophago-gastrischen Ubergangsregion zum Nachweis der kleinen Hiatushernie. Fortschr Geb Roentgenstr Nuklearmed 104.'389 398, 1966 Sarasin R, Hoch A: Les invaginations oesophagogastriques. Arch Mal App D~ge.s't 41.'434M-41, I952 A m o r y HI: The gastric inlet jet. Am J Roentgenol 101.'450 452, 1967
Received: September 20, 1976," accepted." October 15, 1976
Gastrointestinal
261 (1976)
Radiology ~ by Springer-Verlag 1976
Esophago-Gastrie Invagination in Patients with Sliding Hiatus Hernia Gary G. Ghahremani and Phillip A. Collins Departments of Radiology, Virginia Commonwealth University - Medical College of Virginia Hospitals, Richmond, Virginia, U.S.A. and The University of Chicago Pritzker School of Medicine, Chicago, Illinois, U.S.A.
Abstract. Intussusception of t.he distal esophagus into a reducible hiatus hernia is described in nine female and three male patients. The main radiographic feature is demonstration of a lobulated fundal mass of changeable size and configuration surrounding the narrowed distal esophageal segment. This pseudotumor is produced by inversion of the hiatus hernia into the stomach, and may be mistaken for a neoplasm. Disinvagination invariably occurs when maneuvers directed toward demonstration of a sliding hernia are utilized during upper gastrointestinal fluoroscopy. It is emphasized that esophago-gastric invagination frequently accounts for masses shown in the cardia of older women with intermittent dysphagia and crampy epigastric pain. Key words: Esophagus, abnormalities - Cardioesophageal junction, diseases - Hernia, diaphragmatic - Stomach, neoplasm - Stomach, intussusception.
The diversity of intrinsic or extrinsic lesions and functional changes affecting the esophago-gastric junction continues to pose a diagnostic challenge to radiologists [1 6]. In this context the sliding hiatus hernia (SHH) has been thoroughly discussed in the literature but its presentation as a mass in the gastric cardia has received scant attention [2, 7-9]. The frequency of such occurrence, however, is reflected in a recent paper by Kaye and Stassa [2]. They reviewed a series of 40 patients with a mass in the cardia detected on upper gastrointestinal studies and found that 10 cases (25%) were due to SHH. The pseudotumors associated with S H H are produced by three commonly related mechanisms: Address reprint request.s to." G.G. Ghahremani, M.D., Department of Radiology, Evanston Hospital Northwestern University, Evanston, IL 60201, U.S.A.
1. Transmigration qf the Mucosa in the Esophago-Gastric Junction Similar to transpyloric prolapse of antral mucosa, the normal mucosa in the esophago-gastric junction can also slide in either cephalad or caudad direction [4, 5, 10 17]. During this transient phenomenon, the displaced mucosal folds may be visualized as a polypoid mass in the lower esophagus or in the cardia.
2. Incagination oJ the Distal Esophagus into the SHH In the initial stage of this process (Fig. 1 B), the herniated part of the stomach forms the intussuscipiens or sheath around the invaginated esophageal segment. Its radiographic appearance has been resembled to a "jack-in-the-pulpit" [9, 10, 18, 19]. With progressive prolapse of the esophagus, however, the S H H becomes inverted and eventually displaced through the hiatus (Fig. 1 C). It will then present as a lobulated mass in the cardia surrounding the tapered distal esophagus.
3. Spontaneous Reduction of SHH Beneath
the Diaphragm The laxity of phrenico-esophageal membrane, widening of the hiatus, and redundancy of the esophagus in older individuals permit the hiatus hernia to move distally and occupy the space between the fundus and the left crus of the diaphragm. This results in an extrinsic moon-shaped pressure defect upon the fundus [2, 8, 18]. When S H H is small it may merely produce a sharp notch-like deformity of the posterior fundal wall [7]. The above described phenomena can also occur successively or in combination. The narrowed distal
254
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
~
hagus
H rnia
Stomach
A
B
esophagus and the mass presented in the gastric cardia may closely resemble and be mistaken for manifestation of a malignancy [1 3, 6, 8, 9, 11, 14, 16, 18]. Because of not infrequent association of epigastric pain and/or dysphagia with these confusing radiographic and gastroscopic findings, the patients may be subjected to unnecessary surgery [2, 3, 6, 11]. Therefore, it seems appropriate to: (a) report our experience with pseudotumors resulting from esophago-gastric invagination in 12 patients with SHH; (b) describe their clinical symptomatology and characteristic roentgen presentations; and (c) provide technical guidelines for their radiographic evaluation and differentiation from other lesions.
Clinical Material and Method
C Fig. I A-C. Diagrammatic representation of anatomic relationships during the process of esophago-gastric invagination. A The usual relation of the lower esophagus to the sliding hiatus hernia. B Prolapse of the distal esophagus into the hernia producing a "jackin-the-pulpit" appearance. C Advanced stage of invagination whereby the inverted hernia presents as a lobulated fundal mass surrounding the narrowed distal esophagus
The series consists of 12 patients seen over a 3-year period at the hospitals of the Medical College of Virginia and The University of Chicago. In 7 patients the upper gastrointestinal series were obtained mainly because of dysphagia, epigastric pain and/or weight loss. Three other patients were referrals for further evaluation and possible gastric surgery because radiographs obtained elsewhere had shown findings consistent with a tumor in the cardia. In the remaining 2 cases detection of a mass in the air-filled fundus on chest or obdominal films had ted to further investigation. Prev-
Fig. 2. Case 1. Esophago-gastric invagination presenting as a large lobulated fundal mass which persists on prone, supine and upright views (A-C respectively)
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination ious radiographs were also available for comparison in 7 patients, 4 of whom had documented SHH. Nine of the patients were female, and 3 were male. The age at the time of diagnosis ranged from 44 to 81 years, with the majority in their 7th decade of life. The patients have been followed for a period of 8 m o n t h s to 4 years. Each case has had evaluation of the upper gastrointestinal tract by endoscopy and at least two barium studies. Thus
255 far, only five patients have undergone surgery which includcd hiatal hernia repair in three, and gastrectomy for the associated peptic ulcer or carcinoma in two, Seven others who have been treated conservatively are under further observation. From our clinical material, the following four case histories have been selected and are being presented to exemplify various problems encountered in the diagnosis of esophago-gastric invagination. Radiographs from three other cases will also be shown to complement the spectrum of the observed roentgen findings.
Fig. 3. Case l. A - C Radiographs from a subsequent hypotonic upper gastrointestinal series reveal a large sliding hiatal hernia, and the disappearance of the fundal mass after disinvagination
Fig. 4. Case 2. A and B Radiographs demonstrate narrowing of the distal esophagus and marked deformity of the fundus suggestive of an infiltrative malignancy. Note the esophageal diverticuli and the "jet-effect" produced by passage of barium into the fundus. C Spot film after application o f abdominal compression shows cephalad displacement of the sliding hernia and esophageal stricture
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G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
Fig. 5. Case 3. A and B Spot films of the fundus in PA and lateral projection demonstrate a large mass covered by normal-appearing mucosa. C and D Two consecutive spot films obtained during spontaneous disinvagination show the sliding l)iatus hernia Case Reports Case 1: This 61-year-old w o m a n had previously undergone bilateral mastectomy for intraductal carcinoma. Five years later a recurrent t u m o r in the chest wall was resected and bilateral oophorectomy and adrenalectomy were performed. She was placed on steroid substitution therapy and felt well for the next 2 years. Her referral to the hospital was prompted by recent episodes of dysphagia, vomiting, epigastric pain, and weakness. Furthermore, a routine upright chest film obtained a few days earlier had shown a small pneumoperitoneum. This finding was not present on her admission 2 days later, but she appeared dehydrated and hypotensive. An upper gastrointestinal series demonstrated a persistent large lobulated mass in the gastric cardia. There was narrowing of the distal esophageal lumen, and marked deformity of the fundus
(Fig. 2 A C). The diagnosis entertained was most likely primary gastric neoplasm. Gastroscopy showed normal mucosa of the esophagus and stomach; however, the suggestion of a submucosal mass was made due to deformity of the posterior fnndal wall and flattening of its rugal folds. The laboratory data and other radiologic studies including liver and spleen scan were normal. L a p a r o t o m y revealed a small healing antral ulcer. A 7-cm gastrotomy incision was made in the body of the stomach. However, inspection and three biopsies from the cardioesophageal region disclosed no abnormality. A pyloroplasty without vagotomy was carried out and the patient recovered uneventfully. A barium study 1 m o n t h later re-demonstrated the fundal mass, though slightly smaller than on previous examination. To clarify this observation the patient was reexamined after i.m. injection of 30 mg of Pro-Banthine and use of effervescent agents. During this study there was gradual disappearance of the apparent mass with concur-
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Fig. 6. Case 4. A Close-up view of the mass projecting into the fundus as seen on the upright chest film. B Spotfilm from a barium study shows the lobulated margin of the t u m o r which appears to be entirely within the stomach. C and D Two consecutive spot films with patient prone demonstrate gradual cephalad displacement of a sliding hernia which harbors the superficially ulcerated carcinoma
rent development of a large sliding hernia (Fig. 3A C). The latter finding was not recognized on two previous radiologic studies, or at gastroscopy and surgical exploration. Case 2." This 51-year-old alcoholic w o m a n had an 8-month history of dysphagia and substernal pain. The s y m p t o m s had been progressive recently leading to difficulty in swallowing solid food, regurgitation of undigested material, and about 7 kg weight loss. Her admission 3 years earlier was because of colonic hemorrhage from diverticulosis and an a d e n o m a t o u s polyp of the sigmoid. The upper gastrointestinal series at that time had shown an epiphrenic diverticulum, small sliding hernia, and transpyloric antral mucosal prolapse. A barium study of the upper gastrointestinal tract revealed two diverticula in the lower esophagus. The distal, 3 4 cm of the esophagus was narrowed so that the passage of barium produced
a "jet-effect." The rugal folds in the markedly deformed fundus also appeared distorted (Fig. 4 A and B). The findings suggested presence of an infiltrative malignancy. However, on review of radiographs obtained 3 years earlier it became apparent that a mass projecting into the air-filled fundus had been present on the upright chest film. Furthermore, the previously documented S H H was not visible on the current study. Because of our similar experience with other cases ofesophago-gastric invagination the barium examination was repeated. With application of abdominal compression the fundal mass completely disappeared when the hernia projected upward through the hiatus. At this time, marked narrowing of the distal esophagus was also recognized (Fig. 4C). Subsequent esophagoscopy confirmed the presence of diverticula, and chronic esophagitis proximal to the stricture. The instrument could not be advanced into the narrowed segment but obtained esophageal brushing specimens failed to reveal any malig-
258 nant ceils. Dilation of the benign stricture was then carried out on two separate occasions. Subsequently, the patient's condition further improved under conservative management, and clinical or radiographic findings of invagination have not recurred. Case 3." This 74-year-old w o m a n was referred to the hospital with the diagnosis o f a I u m o r in the gastric fundus. For nearly 3 m o n t h s she had had intermittent retrosternal and epigastric pain which usually developed during meals. An upper gastrointestinal series done elsewhere had demonstrated tertiary contractions in the esophagus and a persistent mass in the fundus covered by normalappearing mucosa (Fig. 5A and B). On admission the physical examination and laboratory data were unremarkable. A repeat upper gastrointestinal series intitially showed a deformity of the fundus suggestive of an extrinsic compression. During the course of the study, however, the lesion decreased in size and eventually disappeared when a large sliding hernia became visible above the diaphragm (Fig. 5C and D). The patient was kept in the recumbent position, and abdominal compression was applied. A transient prolapse of the lower esophageal segment into the hernia was noted to follow passage of each bolus of barium, thereby causing a "jack-in-the-pulpit" appearance. Elevation of the patient to the vertical position resulted in redevelopment of an infradiaphragmatic mass deforming the fundus when the hernia itself was no longer recognizable. Although evidence for reflux esophagitis and hiatal hernia was obtained on a subsequent esophagoscopy, the patient has not yet submitted to corrective surgery. However, the radiographic findings of intermittent esophago-gastric invagination have remained unchanged on two follow-up studies over the past 2 years. Case 4: A 67-year-old m a n visited the out-patient clinic complaining of severe back pain radiating to both flanks. This s y m p t o m of 2 days duration was preceded by 1-month history of experiencing epigastric pain, decreased appetite, and some loss of weight. Physical examination revealed an enlarged firm liver and marked tenderness on percussion of the lumbar vertebrae. The stool was positive for occult blood. A radiograph of the a b d o m e n showed lytic destruction of the right pedicle of L-3 surrounded by a faintly calcified soft tissue mass of about 4 cm in diameter. Upright chest films demonstrated diffuse pulmonary interstitial infiltrates. Furthermore, a large lobulated mass projecting into the air-filled fundus was clearly visible (Fig. 6A). These findings led to provisional radiologic diagnosis of a gastric malignancy with metastases to the lungs and the lumbar spine. An upper gastrointestinal series showed a large mass of changeable size and s m o o t h margin protruding into the cardia (Fig. 6B). Serial spot films of air-contrast-filled fundus were obtained in prone oblique positions while applying abdominal compression. These radiographs demonstrated extensive superficial ulceration of the lesion which actually infiltrated the wall of a sliding hiatal hernia (Fig. 6C and D). The distal esophagus and the hernia prolapsed readily into the stomach, and accounted for presentation of a mass of variable size in the cardia. The subsequent evaluation by fiberoptic esophagoscopy and " i n v e r s i o n " gastroscopy using retroflexion of the distal tip of the instrument to visualize the fundus confirmed the radiologic observations. The obtained biopsy material revealed presence of an adenocarcinoma. Emergency laparotomy was then performed because of a gastric perforation complicating the endoscopic procedures. The patient died a few days later due to peritonitis and bilateral pneumonia.
Discussion The difficulty in radiological diagnosis of carcinoma or other lesions of the gastric cardia becomes a for-
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric lnvagination
midable problem in older patients because the usually concurrent SHH further distorts the anatomic landmarks [2, 3, 6]. Furthermore, the prolapsing mucosal folds of the cardio-esophageal junction and intermittent invagination of the lower esophagus into SHH can themselves mimic findings of a malignancy [2 5, 9, 14 17]. In this regard, Ruzicka and Rigler [16] stated in 1951 that " t h e experience of reporting a mass in this region and the finding of no lesion whatsoever at surgery undoubtedly befalls every radiologist sooner or later." Many examples of pseudotumors produced by mucosal prolapse and/or esophago-gastric invagination in patients who were often submitted to unnecessary surgery have since been encountered [2, 3, 6, 11]. If one is familiar with these entities and their modes of presentation, however, the correct radiologic diagnosis and differentiation from other more significant lesions becomes a simple task. Antegrade prolapse of the distal esophageal mucosa as it is often visualized during upper gastrointestinal fluoroscopy probably represents a physiologic phenomenon [9-11, 13, 14, 19]. Its frequency of occurrence was determined by Aldridge among 2100 cases [10]. Of patients with SHH, 22.7% and of those without demonstrable hiatal hernia, 1.9% showed variable degrees of antegrade mucosal prolapse of the lower esophagus. Its concurrent association with transpyloric antral mucosal prolapse was also noted in 24 (10.3%) of 232 patients. Indeed, radiographic features of these two conditions are strikingly similar since the mobile redundant mucosa of the distal esophagus may also present as a polypoid mass of changeable configuration on serial spot films [3, 4, 10, 11, 14, 19]. This transient phenomenon commonly accounts for the so-called "jack-in-the-pulpit" appearance of the associated SHH [9, 10, 18, 19]. With rare exceptions such a finding has no definite clinical importance [10, 11, 13-15, 17]. However, it probably represents a precursor or the early, stage in the development of esophago-gastric invagination. The latter condition as illustrated in our patients obviously involves more than just the distal esophageal mucosa, though it is hardly possible to determine the actual extent of esophageal wall participating in the process. In 1956 Klinefelter reported 3 patients and reviewed 11 previously published cases in whom invagination of the lower esophagus into SHH was radiographically and/or surgically documented [18]. The series of patients encountered by us and others [9, 18, 19] indicates that this condition is certainly not so rare as one may suspect due to lack of its description in many current textbooks. Therefore, the clinical and radiologic manifestations of esophago-gastric invagination should be clarified so that the potentiality
G.G. Ghahremani and P.A. Collins: Esophago-Gastric Invagination
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Figs. 7-9. Representative radiographs of three different cases of esophago-gastric invagination in its various forms
Fig. 7. Prolapse of the distal esophagus into the sliding hernia presenting a "jack-in-the pulpit" appearance Fig. 8. A large lobulated pseudotumor which disappeared when the associated sliding hernia was fully displaced above the diaphragm. This patient presented with burning epigastric pain and blood stained vomitus 3 years after a Billroth I gastroduodenostomy for peptic ulcer. The sliding hiatus hernia and hemorrhagic gastritis were documented on endoscopy Fig, 9. This well-defined fundal mass which simulates a leiomyoma was produced by invagination of the distal esophagus into a small reducible hiatus hernia
of misinterpretation of the findings is further diminished. Esophago-gastric invagination usually occurs in individuals beyond their 5th decade of life. An elongated redundant esophagus and a rather large S H H are invariably present and appear to be the necessary predisposing elements. To our knowledge the condition has not been reported to occur with paraesophageal hernia, in children, and is rare in adults who do not have SHH. F r o m a total of 36 cases studied by us and two other authors, 28 (78%) have been females [9, 18, 19]. In most instances a history suggestive of long-standing S H H with reflux esophagitis, e.g., frequent episodes of regurgigation and heartburn, could be elicited. As in four of our patients availability of previous radiographs showing an S H H would be of enormous value. Thus disappearance of such hernia and concurrent development of a mass in the cardia are highly suggestive of invagination. Intermittent dysphagia and epigastric pain are the c o m m o n symptoms in patients with narrowing of the invaginated distal esophagus by the surrounding mass of reduced and inverted hernia. According to Klinefelter [18], dysphagia occurs in over 50% of the cases
of invagination as compared with 8 % in patients with uncomplicated sliding hernia. Spontaneous relief of symptoms after eructation and regurgitation was experienced by several of our patients. Their subjective feeling correlated closely with fluoroscopic observation of disinvagination occurring following reflux of air and barium from the stomach. The correct diagnosis of esophago-gastric invagination depends on fluoroscopic spot filming performed with the patient in recumbent and upright positions. The mucosal prolapse at the cardio-esophageal junction and minimal invagination of the distal esophagus into a sliding hernia still above the diaphragm are easily recognized due to their very transient nature [4, 5, 10 19]. The presentation as "jack-in-thep u l p i t " appearance (Fig. 7) is best seen with the patient in a recumbent position [9, 10, 18, 19]. The usual inferior descent and reduction of S H H in the upright position readily explains the disappearance of radiographic findings following spontaneous disinvagination. Considerable difficulty m a y be encountered when invagination has occurred into a reducible hernia resulting in its inversion into the gastric fundus (Figs. 2,
260
3, 6, and 8). The radiographic presentation of this condition may then closely resemble the appearance noted after Nissen's fundoplication procedure [20]. Of course, previous history of SHH without subsequent corrective surgery is significant information. However, the combination of the following findings is characteristic of esophago-gastric invagination: a) A lobulated mass in the gastric cardia showing intact mucosa with variation in size and configuration depending on position of the patient. As a rule the pseudotumor becomes smaller when the esophagus is filled with barium and attains its largest size on an upright view of the fundus. b) The distal esophagus surrounded by a mass shows tapered narrowing of the lumen but without obstruction or any mucosal abnormality. Furthermore, the length of this apparent intra-abdominal portion of the esophagus appears unusually long. Spontaneous disinvagination occurs almost invariably during a carefully performed upper gastrointestinal examination [2, 9, 18, 19]. Application of abdominal compression with the patient prone often facilitates this process [18]. It is also helpful to administer effervescent agents or a larger quantity of barium. The full distention of the fundus will then provide additional force for displacing an inverted hernia above the diaphragm and will aid in reducing the prolapsed distal esophagus. It is of interest to note that in two of our patients complete disinvagination occurred only after i.m. injection of 30 mg of ProBanthine (Fig. 3). The spasmolytic effect of the drug on smooth muscles resulting in relaxation of the cardia and lower esophageal sphincter probably accounted for induction of gastro-esophageal reflux and cephalad displacement of the SHH [21]. The mass in the gastric cardia produced by esophagogastric invagination may occasionally persist throughout an upper gastrointestinal examination performed without the above recommended modifications (Fig. 2A C). This is probably due to tonic spasm of the cardia prohibiting cephalad mobility of the prolapsed esophagus and the inverted hernia [11, 18, 19]. The visible lesion (Figs. 2, 4, 8, and 9) may then be mistaken for a true tumor such as carcinoma or leiomyoma on both radiologic and gastroscopic studies [2, 3, 6, 9, 14]. The serious consequences of such misinterpretation can be avoided by careful performance of the upper gastrointestinal series, keeping in mind that about 25% of masses in the cardia are due to mucosal prolapse of the esophagus and/or its invagination into a reducible hernia [2, 3, 6 9, 16, 18, 19]. Therefore, it is most important that every effort be made to ascertain the presence or absence of SHH before labeling a mass in the cardia as a true tumor.
G.G. G h a h r e m a n i and P.A. Collins: Esophago-Gastric Invagination
It should be pointed out that esophago-gastric invagination may occasionally be associated with peptic esophagitis, a polyp or carcinoma of the distal esophagus, or with tumors arising within the hernia itself [6, 11, 17, 19, 22]. As illustrated in Cases 2 and 4, evaluation of the mucosa of the fundus, the hernia and distal esophagus is important for detection of an associated inflammatory or neoplastic process and its extent. Amory has reported production of "'gastric inlet j e t " by passage of barium through the esophagogastric junction narrowed by a malignancy [23]. We observed this phenomenon in Case 2, who had a benign stricture of the distal esophagus. (Fig. 4A), but not in any of the remaining patients. Thus we can reasonably state that, in the absence of an inflammatory or neoplastic stricture, the passage of barium through the narrowed distal esophagus involved in invagination would not cause a "'jet-effect.'" In patients with esophago-gastric invagination included here and in previous reports, spontaneous disinvagination occurred without complication [2, 9, 18, 19]. Since the process is often recurrent, the symptoms such as dysphagia and epigastric pain are also experienced intermittently [1 l, 17, 18]. This clinical history, particularly in patients with known SHH, should always alert one to the possibility of invagination [18]. The symptomatic relief noted in several patients after medication of anticholinergic-spasmolytic agents, tranquilizers, antacids, and with dietary measures suggests effectiveness of the conservative therapy [11, 14, 18]. Therefore, surgical intervention may not be necessary unless the associated sliding hernia is further complicated by chronic peptic esophagitis or a neoplasm. References l. Calenoff L. Sparberg M: Gastric pseudolesions: roentgenographic-gastrophotographic correlation. Am J RoeHtgenol 113.139 146, 1971 2. Kaye JJ. Stassa G: Mimicry and deception in the diagnosis of tumors of the gastric cardia. Am J Roentgenol 110. 295 303, 1970 3. Lame EL: The gastric cardia and fundus. Extrinsic and benign tissues simulating gastric cancer. Radiology 75.'703 711, 1960 4. Rosenkranz W, Bryk D: Pseudotumors in large hiatus hernias. Am J RoentgelTol 116:289 292, 1972 5. Rudnick JP, Ferrucci JT Jr, Eaton SB Jr, e t a l : Esophageal pseudotumor: Retrograde prolapse of gastric mucosa into the esophagus. Am J Roenlgenol 115.'253 256, 1972 6. Wohl GT, Shore L : Lesions of the cardiac end of the stomach simulating carcinoma. Am J Roentgenol 82.1048 1057, 1959 7. Isard, HJ : An infradiaphragmatic clue to the diagnosis of hiatus hernia. Br J Radiol 41.'354 358, 1968 8. Kalokerinos J: The moon-shaped fundal defect of hiatus hernia: A new radiological sign. Report of nine cases. ,4u.~'trala.~ Radio/ 13.'96 102, 1969
G.G. Ghahremani and P.A. Collins: Esophago-Gastric Invagination 9. Walker BQ: The variable roentgenographic appearance of invagination of the esophagus. Based on thirteen cases. Cleceland Clin Q 33.'35 37, I966 10. Aldridge NH : Transmigration of the lower esophageal mucosa. Radiolow 79:962 968, 1962 11. de Lorimier AA, Warren JP: Prolapse of the mucosa at the esophagogastric j unction. A m J Roen lgeno184 : 1061-1069, 1960 12. Eeldman M: Retrograde extrusion or prolapse of the gastric mucosa into the esophagus. A m e r J Med Sci 222.54 60, 1951 13. Palmer ED: An attempt to localize the normal esophagogastric junction. Radiolog'y 60 : 825-83 l, 1953 14. Palmer ED: Mucosal prolapse at the esophagogastric junction. Ant J Gastroenterol 23: 530-537, 1955 15. Poirer A, Poirer B: Invagination de l'oesophage dans la bernie diaphragmatic de l'estomac. Arch Mal App Digest 43.'610 612, 1954 16. Ruzicka FF Jr, Rigler LG: Inflation of the stomach with double contrast. A roentgen study. J A M A 145.'696 702, 195l 17. Sarasin R, Hoch A: Die lnvagination der Oesophagusschleim-
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I8. 19. 20. 21.
22. 23.
haut in den Magen. Sehweiz M e d Wochenschr 81.'1207 1209, 1951 Klinefelter EW: Invagination of the esophagus in hiatus hernia. Radiology 67." 562 568, 1956 Odegaard H: Invagination of the esophagus in hiatus hernia. Aeta Radiol 51.'443 448. 1959 Feigin DS, James AE Jr, Stitik FP, et al: The radiological appearance of hiatal hernia repairs. Radiology 110.'71 77, 1974 Longin F: Pharmakoradiographische Untersuchungen der oesophago-gastrischen Ubergangsregion zum Nachweis der kleinen Hiatushernie. Fortschr Geb Roentgenstr Nuklearmed 104.'389 398, 1966 Sarasin R, Hoch A: Les invaginations oesophagogastriques. Arch Mal App D~ge.s't 41.'434M-41, I952 A m o r y HI: The gastric inlet jet. Am J Roentgenol 101.'450 452, 1967
Received: September 20, 1976," accepted." October 15, 1976
