Anatomy and radiology ofthe areae gastricae

Gut, 1977, 18, 855-864

Anatomy and radiology of the areae gastricaeC. E. MACKINTOSH AND L. KREEL

From the Radiology Divisions of the Royal Free Hospital and the Clinical Research Centre,Northwick Park Hospital, Middlesex

SUMMARY The anatomy and radiology of the areae gastricae were studied in human and pigspecimens and it was shown that the double contrast barium meal demonstrates a true picture ofthe undulating gastric mucosa, which is distinctive in appearance in the antrum body and fundusof the pig stomach. The importance of the type of barium used and the thickness of barrier mucusin the demonstration of the areae pattern is emphasised and the high incidence of duodenal ulcerin the grade 4 pattern and the low incidence in the non-coater is described. A knowledge of theanatomy and radiology of the areae gastricae pattern is central to the interpretation of the doublecontrast barium meal.

The anatomy of the areae gastricae can be consideredfrom two points of view-that of the radiologist andof the anatomist. The object of this paper is tocombine the information from both disciplines insuch a way as to create a meaningful clinical pictureof the anatomy of the gastric mucosa for the rationalinterpretation of the double contrast barium meal.

Radiological appearance

The pattern of the areae gastricae as seen by theradiologist consists of a mosaic produced by bariumlying in the intervening grooves of the gastric mucosa(Fig. 1); the distance between the grooves variesfrom approximately 1 mm to 4-5 mm and the areaof gastric mucosa bound by the grooves is the so-called areae gastricae. While this pattern is startlinglyevident in a double contrast barium meal using thecorrect technique, it is to be noted that a groovepattern is seldom clearly visualised at gastroscopyin our experience while using an Olympus GIF 2Dpanendoscope. In this sense, the double contrastbarium meal resolves one aspect of mucosal anatomymore clearly than the endoscope and failure toappreciate this point can lead to confusion betweenendoscopists and radiologists. We have as yet failedto find a suitable dye to spray down the biopsychannel of the endoscope to highlight the areaepattern, although there is a report that they havebeen seen on endoscopy and on endoscopy im-mediately after a barium meal (Glanville, 1975).

Received for publication 8 April 1977

Anatomy

The anatomist's concept of the areae gastricae is wellillustrated in many textbooks of histology (Bloomand Fawcett, 1962; Elias and Pauly, 1966); basically,the gastric mucosa viewed en face looks like anirregularly ploughed field and the areas between thefurrows contain a multitude of holes (Fig. 2). Insection therefore the mucosa is 'perforated' by thegastric pits into which the gastric glands empty; thepits are lined principally by mucus secreting cells.The mucosa undulates in a fairly regular mannergiving a cobblestone effect-the bottom of eachgroove commonly being bounded by a relativelylarge gastric pit. This undulation of the gastricmucosa is a fundamental intrinsic feature of theanatomy and is not dependent on the state of con-traction of the muscularis mucosae and by definitionis unaltered by the degree of stretching or contractionof the stomach wall (Fig. 3).The first point to establish is whether the groove

pattern of the anatomist formed by the undulatinggastric mucosa 'perforated' by the gastric pits cor-responds with the barium groove pattern of theradiologist.

Correlation of anatomy and radiology

To ascertain this correlation a portion of the antrumof a human stomach was taken from a surgicallyresected specimen and coated with barium; this wasdone by taking the fixed specimen and gently runningbarium on to it from a syringe and pouring the excess

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C. E. Mackintosh and L. Kreel

Fig. 1 (a) Spot film of the fundus of the stomach taken at a routine double contrast barium meal, showing themnosaic areae gastricae patterii. (b) Humian gastric inucosa photographed en face at x JO (or-iginal) magnificationshowing the mosaic groove pattern.

THREE DIMENSIONAL DIAGRAMOF THE GASTRIC MUCOSAAND STOMACH WALL Fig. 2 Three-dimensional

diagrammatic representationof the gastric mucosa with arepresentative antral andfundic type gland showing thedifference in relative depthbetween the antral andfundicpits.

off (Kreel et al., 1974). The specimen was then photo-graphed and radiographed and a fine mosaic bariumgroove pattern was demonstrated. A second speci-men was taken from the anatomical body of thestomach and coated with barium; again a mosaicbarium groove pattern was demonstrated, morecoarse than in the case of the antrum. The specimenwas photographed and radiographed and two small

areas were identified in the specimen and films-onewith four parallel barium grooves and one with aY-shaped groove. These two portions were cut outof the specimens and serial sections cut at rightangles to the grooves were prepared. It was clearlydemonstrated that the barium grooves correspondedwith anatomical grooves in the gastric mucosa(Fig. 4).

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RELAXED STOMACH WALL

identicalmuscularis mucosae areae gastricae

L}m-muscle coat

CONTRACTED STOMACH WALLWITH RUGAL FOLD

Fig. 3 Diagrammaticrepresentation of a micro-scopic section of the gastricwall showing the repetitiveundulation of the mucosatypical of the antral mucosaand the lack of alteration inthe areae gastricae whetherthe stomach is stretched orcontracted.

relatively thickmuscle coat

C

Fig. 4 1: Radiograph, 2: photograph (x 3 original magnification) of a portion ofhuman stomach, body, coatedwith barium. The two portions removed for serial sections shown in the marked rectangle with four grooves andsquare with the Y-shaped groove: (a) and (b) are microscopic sections across the stem and arms of the Y-shapedgroove, and (c) is a section of the upper rectangle with four grooves. In each case a groove is marked with a blackarrow head.



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Because of the difficulty of obtaining specimensof the human stomach it was decided to use the pigstomach for the continued study of the areaegastricae anatomy. The pig stomach is a good modelfor the human, the main difference being the exten-sion of the stratified squamous epithelium of theoesophagus down the lesser curve to abut on theantral type of mucosa. The areae gastricae patternof the fresh isolated pig stomach is clearly visible tothe naked eye and also when coated with barium asin the human specimen. After photography andradiography a clear mosaic areae gastricae patterncan be demonstrated (Fig. 5). The mosaic pattern inthe antrum is relatively fine with a short distancebetween the grooves and, on occasion in the mag-nified image, there is an impression of a punctatepattern between the grooves themselves. A histo-logical section shows the regular repetitive undula-tions of the mucosa giving the groove pattern withthe multiple 'perforations' of the gastric pits; theseare commonly large at the bottom of the groovesand shallower over the 'tufts' forming the areaegastricae. In the anatomical body of the stomachcontaining the fundic glands the grooves are muchwider and further apart with a coarse mosaic quitedifferent from the antral mucosa and a punctatepattern between the grooves is not clearly seen(Fig. 6). The anatomical fundus has a groove patternintermediate in coarseness-that is, average distancebetween the grooves-between the antrum and body

of the stomach. An 'intermediate' zone is notedbetween the antrum and body. This zone is quitenarrow and shows the grooves becoming wider thanin the anatomical antrum and merges into the coarsemosaic of the body 'acid-producing' mucosa. Theantral pits in the pig and human are deeper than thefundic type and one might expect them to producea more pronounced pattern between the grooves onthese grounds. Histological sections taken throughthe site where the barium grooves are visible alsoshow anatomical grooves, while the sections cutbetween the barium grooves in the body of thestomach show no anatomical grooves.We have therefore demonstrated that the barium

groove pattern corresponds with an anatomicalgroove pattern in the human and pig and that thispattern is distinctive in the anatomical antrum, body,and fundus (Fig. 7). This is easily and clearly repro-duceable in double contrast barium meals performedin the isolated freshly fixed pig stomach in which thestratified squamous epithelium in the stomach canalso be distinguished because of its characteristic'wavy' barium groove pattern.

Mucus layer

It was noted that the longer the pig stomach wasleft after the surgical removal the more copious andtenacious was the layer of 'barrier' mucus over it.The work to date on both the human and the pig

Fig. 5 Double contrast bariummeal performed on the intact pigstomach (Kreel and Sandin,1974b); d: duodenum with corkand tube inserted for barium andair insufflation; a: antrum;b: body; f: fundus; 0:oesophagus tied off.

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Anatomy and radiology of the areae gastricae

Fig. 6 Pig stomach shown in Fig. S divided along the greater curve and opened out and radiographed.0: oesophagus; F: fundus; B: body; A: antrum; D: duodenum; wavy stratified squamous epithelium shown belowthe oesophagus. The insert on the left shows photomicrograph (low power) of typical antral mucosa with two adjacentgrooves marked. The insert on the right shows photomicrograph of typical body mucosa with two grooves just joining*narked.

Fig. 7 Typical fine antral areae pattern in the pig ( x S) on the left with punctate pattern between and the coarseareae pattern of the 'acid-producing' body mucosa on the right.

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B

Fig. 8 (A) Pig antral mucosa (PAS stain) showing the barium on top of the mucus and the typical antral undulation.(B) Typical large body groove with barium 'pooling' in it. A Barium. A Mucus.

stomach had been done with specimens fixed withformol saline and washed 'clean'. The bariumcoated specimen may have had its coating of mucusand gastric secretions removed or significantly

altered and in this respect it may not have repre-sented the living state. To elucidate the bariumgroove pattern in a state as close to the living aspossible pig specimens were used which were not

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Anatomy and radiology of the areae gastricae

washed in any way. The isolated pig stomach wastaken and opened along the greater curve and gentlyspread out. Large particles of food matter werepicked off the gastric mucosa and the specimen thencoated with barium and radiographed. Grooveswhich were demonstrated were then removed andsectioned as before but on this occasion the speci-mens were stained for mucus with the PAS tech-nique. In this way it was shown that the bariumlies on top of the mucus layer and in no way perco-lates through it (Fig. 8). Where good coating isobtained the barium layer follows the relativelynalTow mucus layer as it outlines the undulations ofthe gastric mucosa and gives an 'image' of thegastric mucosa in this way, the barium layer 'pooling'in the grooves and being thin over the 'tufts' whichform the typical areae gastricae pattern in thestomach. When coating fails-that is, no groovepattern is shown-this is explained in some speci-mens by the thick mucus layer which 'irons out' theundulations of the gastric mucosa forming anentirely new 'relief map' which in its turn is outlinedby the barium but bears no relation to underlyingmucosal anatomy (Fig. 9). While varying thicknessin the barrier mucus is important in the success ofbarium coating to show the areae gastricae so alsois the thickness of the barium coat itself (Fig. 10).

Areae gastricae on barium meal examination

The radiologist's areae gastricae pattern reflects a

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true anatomical mucosal relief pattern which in thepig is distinctive in certain areas of the stomach. In272 double contrast barium meals in humans theantral areae pattern was graded from 1-4-that is,average distance between grooves 1, 2, 3, or 4 mmand non-visualisation graded as 0. It was found that35% of the duodenal ulcer cases had a grade 4pattern in the antrum and less than 3% of theduodenal ulcers occurred in the 'non-visualised'group (Fig. 11). This may reflect many factors suchas grade 4 pattern in the antrum being associatedwith a high parietal cell mass but it also serves todraw our attention to the question of the gastricmucus layer which may be a decisive feature not onlyin the success or failure of the double contrastbarium meal as an anatomical parameter of thesituation but it may be that the double contrast mealtechnique is reflecting in some way the 'protectivecapability' of the mucus layer, the 'non-coater'having a low duodenal ulcer incidence, and theintense coater having a high incidence.

Conclusion

Radiological demonstration of the areae gastricaedepends on a number of factors some of which areclearly evident. The type of barium is of centralimportance, some preparations giving good demon-stration significantly more often than others (Kreelet al., 1974); the barium used in the present studylay. exclusively on top of the 'barrier' mucus layerd'~~~~~~~~~~~~~~~~~~~T.~~0,f

Fig. 9 Gastric mucosa (PAS stain) with excess mucus (A) layer (appears black) and thin coat of overlyingbarium (A).



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Fig. 10 (A) Section showing suitable thin layer of barium (A) and mucus (A) from the body of a pig stomach; thesection does not cross any groove (PAS stain). (B) Section showing not only a thick mucus layer but also an excessivelythick barium layer.

and in no way percolated through the mucus. The that it allows the barium coating to reflect the under-thickness of the mucus layer is of basic importance, lying mucosal relief pattern. In studies of the relation-as a thick layer will efface the undulations in the ship of barium to the gastric mucosa after coatinggastric mucosa which produce the areae pattern; the the role played by mucus becomes evident only iflayer of barrier mucus should be of such a thickness specific stains for mucus are employed. From the

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Anatomy and radiology of the areae gastricae 863

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Fig. 11 Review of 272 double contrast barium meals in which the antral areae gastricae pattern has been graded(I to 4 mm in diameter and grade 0 for 'non-coaters'). Distribution ofgrading shown in diagram on the left; on the rigthdistribution of duodenal ulcer cases shown (in %) according to the areae grading. Note high incidence in grade 4and low in grade 0.

series of 272 double contrast meals reviewed it canbe put forward that when a grade 4 areae gastricaepattern is visualised the likelihood of a duodenalulcer being present is relatively high and when noareae pattern is visualised the incidence is low. Theinference is that the non-coater has a thick barriermucus layer and a low duodenal ulcer incidence,which is in keeping with experimental work on ratsshowing that drugs which promote ulcer healingsuch as carbenoxolone increase mucus secretion(Parke and Lindup, 1973) and ulcerogenic steroidsexperimentally reduce the amount of barrier mucuspresent (Corne et al., 1974). When a thick layer ofmucus is present a characteristic radiological 'wavy'interference pattern is shown on barium coating asopposed to the areae pattern (Kreel, 1975). It seemsclear that in clinical practice in the future histo-logical examination of the gastric mucosa will needto be accompanied by an assessment of the mucuspresent.

Special thanks are due to Mrs. B. Sandin for radio-graphy and Mr. C. Gilson of the Department ofMedical Photography, Royal Free Hospital, and his

staff for prints. The project was made possible by thesupply of pig stomachs by Professor K. Hobbs,Professor of Surgery, Royal Free Hospital, and hiscolleagues during the liver transplantation researchprogramme being undertaken at the MedicalResearch Council unit at Northwick Park Hospital.Also thanks are due to Dr. Ashley Price, ConsultantHistopathologist, Northwick Park Hospital. Theslides showing barium and mucus stained werepossible due to the expertise of Mr. ChristopherSowter, Chief Technician, Department ofPhysiology,Medical Research Council Unit, Northwick ParkHospital.

References

Bloom, W., and Fawcett, D. W. (1962). Textbook ofHistology,8th ed. Saunders: Philadelphia.

Corne, S. J., Morrissey, S. M., and Woods, R. J. (1974).A method for the quantative estimation of gastric barriermucus. Journal of Physiology (London), 242, 116-117.

Elias, H., and Pauly, J. E. (1966). Human Microanatomy, 3rdedition. Davis: Philadelphia.

Glanville, J. N., (1975). Areae gastricae and the endoscopist,in The Double Contrast Barium Meal. A Discussion Day inLeeds, 11 October 1975. pp 23-26. Sponsored by ConceptPharmaceuticals Ltd.



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864 C. E. Mackintosh and L. Kreel

Kreel, L. (1975). The surface pattern of the stomach. Pro-ceedings of the Royal Society of Medicine, 68, 111-114.

Kreel, L., Herlinger, H., Sandin, B., and France, C. (1974).A technique for the in vitro testing of barium preparations.Radiography, 40, 51-55.

Kreel, L., and Sandin, B. (1974). Personal communication.Parke, D. V., and Lindup, W. E. (1973). Quantitative and

qualitative aspects of the plasma protein binding ofcarbenoxolone, an ulcer healing drug. Annals of NemwYork Academy of Sciences, 226, 200-213.



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Anatomy and radiology ofthe areae gastricae