Thorax (1067), 2±, ?3.

Anaemia and hiatus hernia: experience in 450 patientsCOLIN W. 0. WINDSOR AND J. LEIGH COLLIS

From the United Birmingham Hospitals

Since a correlation between hiatus hernia andanaemia was established in 1931 by Segal, numer-ous attempts have been made to elucidate itscause. Loss of blood may occur from the oeso-phagus or from associated peptic ulceration ofthe stomach or duodenum, but these sources donot account for the majority of cases presentingwith anaemia. In this paper it is suggested thatthe most common cause of blood loss is haemor-rhage from the area of the stomach which ridesover the crus at the neck of the hernial sac, andevidence is presented which substantiates thisview.

HISTORICAL REVIEW OF ANAEMIA ANDHIATUS HERNIA

The association of gastric ulceration and largediaphragmatic hernias is not a new one; Bright(1836) described a fatal case which died of respira-tory complications. Truesdale (1932) reviewed 17cases of gastric ulcer reported since 1904 inpatients with various types of diaphragmaticdefects. He points out that several authors men-tioned the complication of bleeding. from theulcer as well as perforation. Hiatus hernia as adistinct entity causing anaemia and often silentblood loss was recognized and reported by Segal(1931) and Bock, Dulin, and Brooke (1933). Sincethat time many attempts have been made toelucidate the aetiology.

Segal (1931), reviewing the situation, concludedthat anaemia was caused by bleeding from thestomach due to venous congestion, arterialobstruction, and inflammation. Weight was addedto this concept when Bock et al. (1933) foundintense venous congestion of the stomach in post-mortem material taken from patients with theassociated conditions. Harrington (1940), review-ing his own experience, put forward the view thathaemorrhage in hiatus hernia was due to ulcera-tion of either the oesophagus or the stomach nearto the cardia caused by the to and fro slidingmotion of this area in the hernial ring. He alsofelt that regurgitation of acid into the oesophagus

FP* 73

was a contributory factor. Agreeing with Harring-ton as to the site of the bleeding, small butrepeated blood losses were said to occur byMurphy and Hay (1943), who successfully treatedtheir patients by administering iron. Gastroscopywas used in an attempt to identify the bleedingsite by Sahler and Hampton (1943), who did notegastritis and erosions of mucosa in some anaemicpatients, but overall the findings were inconclu-sive. The litera-ture was reviewed again in 1949by Schwartz and Blumenthal, but no new con-clusions were reached. However, in the 20 newcases that they reported, all other probable bleed-ing sites were excluded and the hiatus hernia wasbeyond doubt incriminated as the cause of theanaemia.The significance of oesophageal ulceration, due

to reflux, as a prime cause of haemorrhage waschallenged by Clerf, Shallow, Putney, and Fry(1950). They demonstrated ulceration in 39 of 110patients with hiatus hernia, but found anaemia inonly nine. Following along similar lines, Phear(1957) found that reflux did not seem to causeanaemia unless it was associated with a hernia. Hecited 87 cases of hiatus hernia and 20 cases withreflux and no hernia; 33 were anaemic in thisgroup and all were found to be associated with ahernia. A case report by Roussak and Eden (1947)of a paraoesophageal hernia with anaemia seemedto be a prelude to observations based on thedifference between the types of hiatus herniawhere anaemia is concerned. Grimes and Stephens(1957) were aware that anaemia could be presentin patients with paraoesophageal hernias whichonly infrequently had gastro-oesophageal incom-petence. Later this point was amplified whenJohns and Clements (1961) noted that patients withthis type of hernia had a higher incidence ofanaemia than did those with the sliding variety.In listing possibilities, the same authors suggestediron-deficient diets and lack of 'gastric factors' asother probable causes of this syndrome. Againstthe trend in turning attention from the oesophagus,De Vito, Listerud, Nyhus, Merendino, and Harkins(1959) and Hood and McChesney (1962) presented

Colin W. 0. Windsor and J. Leigh Collis

good post-mortem and endoscopic findingsrespectively establishing a definite relationshipbetween haematemesis and oesophagitis. How-ever, Windsor (1964), investigating post-gastrec-tomy reflux, found this to be present in 40% ofhis patients, but found no increased incidence ofanaemia in this group.The need to eliminate other sites of gastro-

intestinal haemorrhage before incriminating thehiatus hernia is suggested by Palmer (1963), whofound a high incidence of duodenal and gastriculcer and oesophageal varices in his collection of500 cases having sliding hernias.

Attempts to correlate microscopic changes inthe mucosa of the herniated stomach with anaemiawere made by Forstner and Bogoch (1963). Theyraised the possibility that macroscopically un-recognized sites of bleeding may be present in thestomach when they found changes in the laminapropria associated with anaemia. Dagradi, Killeen,and Schindler (1958) also studied the herniatedstomach and were able to detect by gastroscopymacroscopic changes of gastritis in 45% of hiatushernia patients.

Defective absorption of iron in patients withhiatus hernia is suggested by Michaelides andPhilis (1959) and Loeper, Rameix, and Moges(1963) as being a common cause of anaemia. Theformer cites a single case in which he found thatferric iron was not absorbed unless administeredwith ascorbic acid or intrinsic factor. Loeper et al.(1963) investigated 12 patients and found that thelow serum iron levels in six did not rise as aresult of the ingestion of iron during the six hoursof his test. These are interesting observations, aspointed out in a leading article in the BritishMedical Journal (1964), but it is not felt that thefindings warrant the drawing of any generalizedconclusions.These are some of the thoughts and trends in

the understanding of the relationship betweenhiatus hernia and anaemia over the past 40 years.Table I gives some collected data on the incidenceof anaemia encountered.

MATERIAL

Four hundred consecutive cases of hiatus hernia,selected only because they had symptoms severeen,ough to require operative treatment, form thebasis for this study. Additional information wasobtained from a further consecutive series of 50cases with a short oesophagus and stricture.

Special follow-up was reserved for 59 patientswho either were anaemic or had bled from theupper gastro-intestinal tract at the time of admis-sion to hospital. Bleeding from a duodenal or low

TABLE IINCIDENCE OF ANAEMIA AND HIATUS HERNIA

Author No. of Cases IAnaemia(o)Harrington (1940) 198 1 tSahler & Hampton (1943) . . 221 14Clerf et al. (1950) 110 8Blades & Hall (1956) . 66 33Phear (1957) ..87 37Grimes & Stephens (1957) . 113 42Johns & Clements (1961) t.110 34This study (1966) .. 400 15

gastric ulcer excluded them from this follow-up;other possible sites of blood loss were investigatedand not found to play a significant role in thecause of anaemia in this group. Of the 59 patientsasked to attend hospital, eight were dead and threeuntraced at the time of review, which variedbetween one and 13 years post-operatively. On100 non-anaemic patients with sliding hernia takenfrom the original 400, certain special studies werecarried out.

FINDINGS

GENERAL The arbitrary level of haemoglobinconsidered to indicate anaemia was below 11 5g./100 ml. in females and 13 5 g./100 ml. in males.These figures may appear to be high, but the meanhaemoglobin in the anaemic group was 8-5g./100 ml. All of the haematological data showedan iron-deficiency type of anaemia and it wasassumed that this was the result of blood loss.Dietary deficiencies could be a cause of anaemia,but only nine patients were found to be taking adiet poor in iron before surgery and four of thesepresented with haematemesis. Diet does not seemto be a significant causative factor in the anaemicpatients reported in this series.The overall incidence of anaemia and symptoms

of haemorrhage in the 400 patients was 15%.Some patients presenting with haematemesis ormelaena were not anaemic at the time of admis-sion to hospital but are included in this investiga-tion.RESULTS OF OPERATION As a result of operativetreatment in the anaemic group (Collis, 1961), thehernia was controlled in all but two cases andreflux in all but four. There was no recurrence ofmelaena or haematemesis and the mean rise ofhaemoglobin was 5-4 g./100 ml. (range 0 to 1114g./100 ml.).

DETAILED FINDINGS

A comparison of the paraoesophageal and slidinghernia groups revealed certain features significantin the aetiology of the anaemia. Where relevantthe additional facts obtained from the non-

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Aniaemia and hiatus hernia: exper-ience in 450 patients

anaemic group and the short oesophagus groupare discussed in relation to the conclusions drawn.Of the 400 patients, 326 had sliding hernias, 59paraoesophageal, and 15 mixed hernias. Forsimplicity, the mixed hernias have been consideredwith the paraoesophageal ones throughout thispaper.Table II shows that anaemia is nearly three

times more common in the paraoesophagealhernia patients than in those with a sliding hernia.The incidence of anaemia in the patients with ashort oesophagus and hiatus hernia is midwaybetween the two.

TABLE IIINCIDENCE OF ANAEMIA

Total No. AnaemicType of Hernia of Patients No. %

Paraoesophageal andmixed.74 22 30

Sliding.326 37 11Fixed with stricture 50 9 18

Radiological reflux was present in all of thesliding hernia group and in one of the para-oesophageal group, where it was associated witha mixed-type hernia (Table III).

TABLE IIIINCIDENCE OF RADIOLOGICAL REFLUX IN ANAEMIC

PATIENTS

No. withTypeofHernia Total No. Radio- IncidenceType of H4ernia of Patients logical (n c

Reflux

Paraoesophageal andmixed. 22 1 5

Sliding.37 37 100

In all but six patients, pre-operative oeso-

phagoscopy was carried out. The findings were

graded as follows:

Grade I Mild oesophagitis, indicating a redden-ing of the mucosa;

Grade II Moderate oesophagitis, indicating a redmucosa which bled readily as a resultof mild trauma but not spontaneously;

Grade Ill Severe oesophagitis, indicating frankulceration often with spontaneousbleeding taking place.

The findings are shown in Table IV.

TABLE IVOESOPHAGOSCOPY FINDINGS

T No. of Grade of Oesophagitis(0,)Type of 1-fernia Patients I I

Paraoesophagealand mixed .. 22 0 5 5

Sliding (anaemic)i 37 14-5 11-6 5-8Fixed with

stricture .. 50 16 20 42Sliding (non-

anaemic) .. 100 13 16 13

It is clear that reflux oesophagitis is very un-common in patients with paraoesophageal hernia,and that only about 17% of patients havinganaemia and a sliding hernia have significantoesophagitis.

Further evidence that oesophagitis has littleinfluence on the incidence of anaemia is providedby the additional information found in Tables IIand IV. Patients with fixed hernias, with grossoesophagitis in 42% of cases and stricture forma-tion in 80%, have a lower incidence of anaemiathan patients with no reflux at all. In the 100cases of hernia without anaemia the pattern ofoesophagitis is almost identical to that in theanaemic group.

HERNIA SIZE AND RIDING ULCERS IN ANAEMICPATIENTS Twenty of the total 59 anaemic patientsare recorded in their operation note as having hadhuge hiatus hernias. Five patients had high gastriculcers occurring at the site where the stomachcrossed the right crus; three of these ulcersoccurred in the paraoesophageal group and two,high on the lesser curve, in the sliding group. Inaddition, changes varying from hyperaemia topetechial haemorrhages on the serosal surface ofthe stomach were found in several patients at sitescorresponding to the neck of the hernial sac.These findings suggest that local trauma causedby the crura is associated with bleeding andanaemia.

ASYMPTOMATIC HERNIA WITH ANAEMIA All thepatients operated on for sliding hiatus hernia hadsymptoms of reflux oesophagitis except for fivepatients whose only complaint was of weaknessand malaise. These patients were in the anaemicgroup and had radiological confirmation of hiatushernia with a mild degree of reflux but did notcomplain of heartburn. After careful investiga-tion, the hernia was found to be the only possiblecause for the anaemia. Despite the absence ofoesophageal symptoms, surgical repair was carriedout and in all cases the anaemia was cured. Reduc-

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Colin W. 0. Windsor and J. Leigh Collis

tion of the stomach into the abdomen was theonly change effected in these patients. Thismanceuvre stopped loss of blood from the uppergastro-intestinal tract and it is therefore con-sidered likely that the site of the haemorrhage wasin that portion of the stomach reduced byoperation.

DISCUSSION

From the results of this investigation it is possibleto exclude certain factors as likely causes ofanaemia and to emphasize others as beingsignificant.The lower oesophagus damaged by oesophagitis

is often said to be the site of blood loss inpatients presenting with anaemia and hiatushernia. From the findings in this series, oeso-phagitis seems to be an unlikely cause ofanaemia. In patients with paraoesophageal hiatushernia, which does not cause reflux or oeso-phagitis (Tables III and IV), there is a 30%incidence of anaemia. In patients with the slidingtype hernia, with 100% radiological reflux, thereis an 11 % incidence of anaemia. These facts suggesta lack of correlation between oesophagitis andanaemia which is emphasized by two additionalfindings. Patients with hiatus hernia and a shortoesophagus (Table IV) having gross bleedingoesophagitis (42%) have a significantly lowerincidence of anaemia (18%) than the para-oesophageal cases. Also the oesophagoscopyfindings (Table IV) show that the pattern ofoesophagitis in the 100 non-anaemic cases withsliding hernia is almost identical to that in the 37with anaemia. These highly significant findingssuggest that there is little correlation betweenthe state of the lower oesophagus and theincidence of anaemia and, furthermore, thatbleeding from the lower oesophagus is unlikely toresult in anaemia.

Other causes of blood loss which may be asso-ciated with hiatus hernia, such as low gastric ulcerand duodenal ulcer, have been deliberately ex-cluded from this series. Bleeding from haemor-rhoids and heavy menstrual losses have been foundto be possible complicating factors in only threeof the 59 patients; it is therefore reasonable toassume that the hiatus hernia has been the solecause of anaemia in the majority of cases. It hasbeen suggested (Johns and Clements, 1961) thatpatients with symptoms of hiatus hernia may takea diet deficient in iron. In nine of the cases re-ported here dietary restriction was significant, butfour of these patients presented with haemat-

emesis, which is considered to be a far more likelycause of the anaemia. This leaves five in whomdiet could be a factor; the importance of this isreduced if consideration is given to the group witha sliding hernia and short Gesophagus, 80 of whompresented with dysphagia and were undoubtedlyon very poor iron-containing diets, who did notsuffer from a high incidence of iron-deficiencyanaemia. These findings seem to exclude asso-ciated diseases or deficient diet as significantfactors in the causation of anaemia.

Acceptance of the negative findings leads tothe conclusion that bleeding is associated withthe herniated stomach. A factor common to allcases is the to and fro riding movement duringrespiration of the stomach over the crura at theneck of the hernial sac. Large hernias, in whichthe force of this movement is thought likely tobe greatest, have been found in 20 of the 59patients in the series, and have been noted pre-viously as being associated with a bleeding ten-dency by Sahler and Hampton (1943) and Flood(1960). Paraoesophageal hernias are probably*more liable to this type of movement because theclosed herniated stomach is subjected to a strongtraction force on respiration (Fig. 1).

FIG. 1. Forces acting to damage the stomach mucosa atthe neck of the sac during inspiration. A, negative intra-thoracic pressure; B, crural muscle movement; C', slidingmovement of the stomach.

Ulceration of the stomach at the point whereit crosses the crus has been encountered in fivepatients in this series, and this gross change was

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Anaemia and hiatus hernia: experience in 450 patients

associated with profound anaemia in threepatients. Gastric ulceration, except in this area ofthe stomach, is an uncommon finding in associa-tion with hiatus hernia and would seem to becaused by some local factor such as the onealready mentioned. The term 'riding ulcer' hasbeen introduced to indicate the special nature ofthis type of gastric ulcer. Recently a carefulexamination of this area of the stomach has beenmade at operation and petechial subserosalhaemorrhages have been demonstrated in five outof six cases (Fig. 2). It is thought that thesechanges represent the first stage of a series leadingto frank ulceration of the mucosa at this site andthat there is likely to be considerable trauma tothe mucosa sufficient to result in haemorrhagebefore these late changes occur.The dramatic effect of operation in the cure of

anaemia and prevention of further haematemesisand melaena in all cases is a significant feature.

This further rules out associated disease as acontributory factor in the causation of anaemiasince in no case was an additional procedure otherthan hiatus hernia repair (Collis, 1961) under-taken. Some of the patients who presented withweakness and anaemia had no other symptomsfrom the hiatus hernia; replacement of thestomach into the abdomen at operation was suffi-cient to reverse the iron-deficiency anaemia.Two other possible causes of anaemia must be

considered in this discussion, but it is not con-sidered that they are very common contributor)factors. Arterial and venous obstruction, mentionedby both Segal (1931) and Bock et al. (1933), lead-ing to oedema and haemorrhage from the gastricmucosa may be encountered when the hernia isstrangulated. In this series of 400 cases none ofthe anaemic group presented with symptoms ofstrangulation, neither were any of them found tohave evidence of this at operation. This compli-

FIG. 2. Photograph taken during the operative repair of a paraoesophageal hiatus hernia. The stomach has beenreduced from the sac. Gentle rubbing with gauze has produced petechiae in a band across the stomach in thearea in which it has been in contact with the crura at the mouth of the sac. In this band there is also oedemaof the stomach wall. These changes are in contrast to the state of the stomach in the sac above and the rest of thestomach in the abdomen below.

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C'olit W. 0. Witidsori and J. Leigh Collis

cationl was, however, noticed in several non-anaemic patients. The second possible factor is theeffect of trapped gastric secretions in the stomachpouch on the mucosa of the herniated stomach.This has been referred to by Johns and Clements(1961) as a probable cause of mucosal damage;however, it is thought that some gastric ulcerswould have been found in the fundus of thestomach if this were so rather than at the neckof the hernia, as is described in this paper. Ageneralized gastritis could conceivably causebleeding in some patients, but this probabilityneeds further evaluation.

In conclusion, an attempt has been made topinpoint the likely site of blood loss in patientswith hiatus hernia. Mechanical trauma at the neckof the sac where the stomach rides to and froover the crus during respiration is a factor com-mon to all cases. Changes in this area varyingfrom subserosal haemorrhages to frank gastriculcer have been encountered in this series andhave been associated with anaemia. It is consideredlikely that this is the commonest cause of anaemiain patients with hiatus hernia.

SUMMARY

Four hundred patients with hiatus hernia werestudied and a 15', overall incidence of anaemia,melaena, or haematemesis was found. Anaemiawas three times as common in the patients withparaoesophageal hernia as in those with a slidinghernia, 30%,/ and 11 % respectively. No correlationbetween this symptom and confirmed oesophagitiswas found, neither was there any evidence that adeficient diet or associated disease played any partin the syndrome. Local trauma to the stomach atthe site where it rides to and fro in the hiatusduring respiration is thought to be the likelycause of the bleeding encountered, and argumentsfor this theory are put forward. The term 'ridingulcer' is used to describe the particular type ofgastric ulcer found in some of these cases. A

review of the literature on the association betweenhiatus hernia and anaemia is also presented.Our thanks are due to Dr. W. Trevor Cooke and

his colleague Dr. Ann Benn for their advice and helpin the preparation of this paper.

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Bright, R. (1836). Account of a remarkable misplacement of thestomach. GuY'S Hosp. Rep., 1, 598.

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Loeper, J., Rameix, P., and Moges, J. (1963). Contribution a letudede l'anrmie des hernies diaphragmatiques. Presse med., 71, 2775.

Michaelides, G. J.. and Philis, H. C. (1959). Pathogenesis and treat-ment of the anaemia associated with hiatus hernia. Lancet, 1, 552.

Murphy, W. P., and Hay, W. E. (1943). Symptoms and incidence ofanemia in hernia at the esophageal hiatus. Arch. intern. Med., 72,58.

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Amer. J. Roentgenol., 49, 433.Schwartz, S. O., and Blumenthal, S. A. (1949). Diaphragmatic hiatus

hernia with severe iron-deficient anemia. Amer. J. Med., 7, 501.Segal, H. L. (1931). Secondary anemia associated with diaphragmatic

hernia. N. Y. St. J. Med., 31, 692.Truesdale, P. E. (1932). Gastric ulcer associated with diaphragmatic

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