CLINICAL GASTROENTEROLOGY

Campylobacter pylori detection in gastric mucosa: Association

with gastritis

ALAIN PARADIS. MD. MARIE GOURDEAU. M D, FRCPC, SU/ANNE LAMBERT, MD, FRCPC,

SYLVAIN LAVOIE, MD, FRCPC, SU7ANNE LEMIRE. MD, FRCPC, CLAUOE PARENT, MD. FRCPC,

REJcAN CANTIN, MD, FRCPC

ABSTRACT: ln order to cvalu;ne the association between Camfrylobacier pylon· and gastritis. two hiopsics were taken from the duodenal bulb, antrum, hody and fund us (and from lesions if there were any) in 100 consecutive patients referred to this gastro~copic clin ic For each ~ite, one hiopsy was for histology and C pylon de tection by Warthin-Starry stain ing, ;,nd the second biopsy wns for culcu re. In addition, for each patient a gas tric h rushing was Gram sta ined. Twen ty-one patients were excluded from the study. Among the rl'maining, 13 patient~ had po:,i tivc biopsy cu lture for C f1ylon and, uf these , 30 (9 1 "i, ) had gastri tis (including 23 wi th active chronic gastritis). Thi.! culture sensi ti vi ty increased with the n umber of b iopsies. Forty-two pa tients had n positive brushing specimen, of which 30 ( 71 '\,) had gastri tis. Gram stain on a brushing specimen had a sensitivity of84.8";, in comparison with the biopsy culture . Of the 2 3 patien ts with positive Warth in-Starry stain , 19 (81'\,) had an histology of gastrnis. T here was a strong correlation between the presence of C fry/on in the stom­ach mucosa and the gastritis. T he incidence of C frylori associated gastri tis is similar in Quebec to other pares of the world . The b iopsy cultu re is a simple and specific test, and at k ast two biopsies arc necessar y for a good sensit ivity. Gram stain on a b rush­ing specimen is an aJequate test for rapid detection nfC f)ylori in the stomach. Can J Gastroe ntc ro l 1988;2( 3):94-98.

Key Word s: Camf1ylo/,acrer, CamfJylolnwer-like organism, Campylobacter pylori, Gwrritis

/)cfiarimcnr of M1cro/)1(1/og~. Ca11rnenrcrolo,l(y ,md Parhology. Ho/nwl de /En/anr-Jcis11s, Qttdicc Cit)', Qttc/,cc

Crme.1/wndencc and rcprntt.1 Dr Mane Gourdeau, I lopital cle /En/anc-Jcsus. Deparremcnr de M1cro/J10/ogrc, J./{_l/, l&mc rnc, Q11chcc C1ty, Q11c/icc G /J IZ-l

Rccett·cd /or pu/,licatwn April /~. /9HS. Accc/ned ) 11ly 21, /91*{

94

R Fl'()RT<; 01 SPIRAi llACTl'RIA IN THE

human s tomach have occurrcJ ~poradically over the l,1s1 century ( 1.21 However, it was only in 1982 that a micro­acroph ilic campylobacter-like organism was isolated by Marshall and Warren ( 'll from gastric antra l b iopsy specimens This mitial publica tion sparked off worlJ

wide enth usiasuc research into this bac terium now named Camfrylobacrer fry/on (4.5). Since th.is time, a numherofscuJ · ies have shown an association between the p resence of C /;ylori in gastric mucosa a nd h istologica lly confi rmed gastri tis

However, there is sri ll some d iscussion whether the organism has a causative role or is simply a secondary invader.

With chis sw dy, it wa~confi rmed that C pylori was correlated with gastritis anJ then differen t methods for C pylori decec· t ion in the huma n srnmc1ch were eval u­ated T he literatu re was also review<.:d. emphasiz ing principal argurn<.:nts in

favour o( th<? causative relationship of the b;icteriu m wi th gnsrritis. Fina lly, some basic nmions for a C trylori de tection pro·

CAN J GASTROENTEROI

tocol in patients undergoing endoscopy are suggested.

PATIENTS AND METHODS Endoscopy: One hu ndred consecutive patients were included wh o were re­ferred for gastroscopy on cl inical grounJs from January co March [987. lnformed consent was obtained from all patients for endoscopy and biopsies. Biopsies were obtained from the duodenal b ulb, antrum, body, fund us and from lesions if there were any. Two biopsies were taken in each a rea. one for culture and the other for h istology, giving eight to JO tis­sue specimens from each patient. A lso. one brushing speci men from the anrrum was spread on a glass slide and air d ried. An endoscopist recorded the cl in ical his­mry, medication and drug use. alcohol consum pt ion, clinical d iagn osis and endoscopic find ings. Microbiology: Samples for culture were immediately immersed in 5 ml of thio­glycolate broth , transported to the labo­ratory within 2 h of collection and mac­erated in 2 ml of the same broth . One drop was then p lated on b lood agar (trypticase soy agar with sheep blood 5'\,) and choce,,are agar (GC agar, bio-X 1% and hemoglobin 1%) a nd incubated microaerophi lically in anaerobic jars for seven days at 37°C. T hegaspak (Campy­Pak, BB L) was replaced every 24 h. C pylori, when isolated. was identified using d irect examination with Gram stain , oxyJase, cata lase, oxydarion ­fcrmenrarion test with pu rple bromocre­sol. nitrate reduction , h ippurace hydroly­sis, urease (C hristensen's u rea medium), indole, and susceptibility to cephalothin and nalidixic acid. The brushing spec­imens were fixed and stained by Gram method. Histology: T he biopsies for h istologi­cal examination were fixed in formalin and routinely processed. Sections were stained with he matoxylin and eosin a nd assessed for gastritis using the same cri­teria as Marsha ll (3 ). that is normal stom­ach, chronic gastritis or active ch ronic gastritis. Chronic gastritis indicates in­flammation with no increase in polymor­phon uclea r le u kocy tes b u t with in­creased or normal number of lym phoid cells and edema, congestion or cell dam­age. Active chronic gastri tis is indicated if polymorpho n uclear leu kocytes arc

Vol. 2 No. 3. Septemher [988

increased in number, if a few infiltrate one gland neck or pit, or if they a rc scat­tered throughout the superficia l epithe­lium. ln addition, other sections from all b iopsies were stained by the Warth in­Srnrry method (6) and exam ined for presence or absence of small curved bacilli on the surface of the epitheliu m. D ata ana lysis: The resu lts were recorded in each department (gastroentcrology. microbiology and pathology) indepen­den tly. For statistical analysis of the find­ings. the Fisher's exact tesr or rhe xz test was used depending on sam ple size. For the study of the correlation between the presence of C /rylori and gascriu:,, on ly b iopsies from the antrum, bod y and fu n­d us were considered. A patien t was con­sidered positive when there was at least one positive site for C pylori by culture a nd/or h istology.

RESULTS From the [00 patients, 21 were exclu­

ded (two for having taken antibiotics in the week preceding the endoscopy, th ree for upper d igestive neoplasia, one for incomple te clinical data, one for u nin­terpre table cu lture and 14 for peptic ulcers) . T he number of peptic ulcers was too small to study adequately any asso­ciation with C pylori.

C /rylori was isolated from 7 5 biopsie:. o f 3 3 patien ts. T he bacteria were curved or S-shaped Gram-negative rods. ln elec­tronic microscopy, they had three to five sheathed flagella arising from one end of the cell. The biochemical feature was typical of C /Jylori: m icroaerophil ic growth in two to four days at 37°C; pos­itive reaction for oxydasc and catalasc; inert reaction in oxydation-fcrmentation rest; negative reaction fo r hippurate hydrolysis. indole and nitrate reduction; very strong positive reaction for urease ( 5 to [0 mins); susceptibi lity to cephalo­th in and resistance to nalidixic acid .

Among the 79 patients remain ing in the study, 40 had no rmal h istology and 39 had gastri tis (chronic or active ch ro­nic). These two groups were closely matched for sex d istribution, age. medi­cation. excessive alcohol consumption and upper d igestive trac t su rgery.

T he correlation between gastritis and th e presence of C pylori defined by biopsy cultu re was impressive (Table l ). Among the 33 patients with at least one

C p ylori: Association with gastritis

TABLE 1 Correlation between Campylobacter pylori culture and histological exami­nation of gastric mucosa in 79 patients

Histology Culture Positive· Negative

Gastrit is I Active chronic t Chronic

Normal1

23 7 3

4

5 37

•C pylori wos 1so101eo from ct feast one biopsy t P"' 0.0001 (\ ' test/

posi tive biopsy culture, 91 "~ haJ gm,rri­tis (of wh ich 77''(, were active ch ronic) and only 9";, had normal h istology. ·fable 2 shows the number of rosirive ratient~ by cu lture according to d ifferent combi­nations of biopsy sites. The number of positive patients was similar whatever the biopsy si te b u t increased with the num­ber of sites.

Wi th the Gram stain on the brushing specimen , a good correlation between gastritis and presence of C pylori was obtained n:.1ble 3 l In comparison with the culture, the Gram sensitivity was 84.8"1, since 28 of the 33 positive patients by culture were also Gram-positive.

Sections stained with the Warthi n­Starry method were not all easy to inter­pret. When there was a doubt. o ften cau~ed by artefacts. the specimen was considered negative. However, a corre­lat ion between gastritis and C /rylori was established by ch is method (Table > ). Only 23 ca~es were posi tive but 8n, had gastritis and on ly l7"o had a normal histology.

Fina ll y, the endo~copic findings were compared with the histological diagno­sis. There were 20 cases with endosco­pical diagnosis of gastritis. One-half of these patients had gawiti~ by h istology

TABLE 2 Number of positive patients by c ulture a ccording to differe nt c ombinations of biopsy site s

Biopsy sites Patients with positive cutture(s)"

Antrum 22 Body 22 Fundus 23

Antrum a nd body 27 Antrum a nd fundus 28 Body and fundus 28

Antrum. body and fundus 33

•C pylon wos 1sofoted from cf feast one biopsy

95

PARAl11S el al

TABLE 3 Correlation between Gram and Warthin-Starry results fo r C pylori and histological examination of gastric mucosa in 77 patients

Histo logy Grom Worth in-Starry Positive Negative Posltlve t Negative

Gastritis · Normal

30 12

9 26

19 4

19 35

Grom onct Worth1n-S1orry were lock,ng ,n two po11en1s. 1 Boclefla cterectect ,n al reos t one biopsy • Acr,ve chrornc or chronic goslfll1s. P < 00005(.\',, fest}gosfr,t,s versus normal

and the remaining were no rmal. ln the group with endoscopical diagnosis o(

normal gastric mucos;i . 30 h;id normal b iopsies and 29 had gastritis confirmed by hisrology.

DISCUSSION Findings about the identification of the

C pylori were similar to those of ocher authors ( l.7). The very strong urease activity i~ thl' striking feature, indeed C /rylori is the sole Campylobact.er species with a positive urease test (8 ) and this test could su ffice in itself to presump­tive ide ntification .

A high correlation was found between the presence of C [lylori and gastritis in the biopsies. Thirty of 33 (91 %) of the patie nts who tested positi ve for C pylroi also had~ gastritis. It was confirmed that the incidence of C [lylori associated gas­tritis in Quebec was similar to that found in other parts of the world . Mar:,hall (7)

in Australia discovered 100% ( 52 of 52) of the patie nts who tested positive to C /rylori also had gastritis while Jones (9) in the Un ited S tates had a 96''{, ( 26 o f 27)

correlation and ·faylor ( 10) in Alberta. C anada obtained a 95ci;, correlat io n .

O ther authors had similar data ( 11 - 14 ). Despite its strong association with gas­

tritis, the pathogenic role of C [lylori is still controversia l. ls it simply a colonizer

of a mucosa altered by gastritis or the prim;iry dise::isc etiology I Severn I obser­vatio ns suppo rt the latter hypothesis.

First, C /rylori in the smmach seems lO

provoke a local ( 12,1 3, 15, 16) and systemic immune response (9, ll ,17-ZO). Second,

C /1ylori is present in primary gasrrin~ and not in secondary g;istritis. ic. with known predisposing cause ( 14.21-23). T h ird , C pylori :-ippears particularly

adapted to gastric epithelia l cells in which ir is associated with well described spe­ci fic lesions ( 7, 15, 16,24-26). Further, few

treatment studies h;ive been done but the available data up to now are very

96

much in favour of a pathogenic role of C pylori. Bismurh compo unds o r amoxy­ci ll in clc:-ir the organism and the associ­ated gastritis (27-29). Finally, o ne of the most convincing argumen rs for t h e pathogenic action of C [lylori comes fro m the demonstration of third and fourth Koch's postulates. Two volunteers with normal stomach developed symptomatic

gastritis after ingestion of C pylon sus­pension ( I 'i, 16 ). A II these observations su pport a cy topmhogcnic activity by C /!ylon and militate against the hypothe­

sis that the organism is associated with gastritis merely by colon izing the mucosa

after inflammation has occurred. C pylori associated gastritis is d iagnoscd

by hisrological and/or micro bio logical

examination of gastric biopsy specimen. T he culture of biopsy specimen is the most specific test. The typical idcntifi­c;ition profile o f the bacteriu m provides

very li ttle risk of false-posi tive culture. The tech nique is simple and may be per­

formed in a rou tine laboratory. Numer­ous causes of false-negative result arc pos­s ible, such as recent antibiotic therapy,

bur can be avo ided witho ut difficulty (7 ). As demonstrated in Table 2, the culture sensitivity increases with the number of

biopsies. However, although the num­ber of positive patie n ts is similar what­

ever the observed site, it cannot be con­cluded that rhc choice of b iopsy site docs not influence the sensitivity of the cul­tu re. As the biopsy forceps were not ster­

ilized between each area and as the order of biopsies was always the same, a cross­

contamination of cu ltu re from preced­ing samples was theoretically possible. particu larly from the antrum. wh ich is positive in most positive patients. Haze ll

et al ( 30), in a study of C pylori distribu­tion with in the sto mach, (in which they cleaned and rinsed b iopsy forceps be­tween each site) suggested taking biop­

sies fro m both the a n trum and body because the bacterium may be limited

to one of these areas. Unfortunately, their method was not perfect since the endo­scope lumen was not ste rili zed between

each biopsy. The principal d isadvan tage with the

culture is the delay of several d;iys before

obtaining results. A Gram-stained brush­ing srecimcn is useful because results may be available with in I h , ie , when the patient is still in the gastroscopy clinic. Presen t results demonstrated a good sen­sitivity of84.8% in comparison with cul­ture but a decreased specificity since 10 patients with negative cultu re and nor­mal histology were positive o n Gram­sta in. Unfortunately, it is impossible to establish if these positive Gram stains are true posi tive since there was no culture from the brushing specimens. Also . pres­ent resu lts cannot be compared wi th others since most s tudies used Gram­staining on b iopsy specimens instead of brushing specimens and none evaluated the test specifica ll y.

Other rapid detection tests have been previously investigated. Urcase tests per­formed directly o n b iopsy speci mens obmined diffe rent results depending on technique. lts sensitivity varied from 50% to 100°/o( 14,25,3 1-35) bu ttherc is a com­mercially available urease test (CLO Test) with h igh specifici ty and sensit iv ity ( 36,3 7). Fu rchc rmorc, ;i recen t study

Jcmonstrntcd a correlatio n between the urease reactio n time and the grades of inflammatio n a nd number of bacteria seen in biopsi es ( 32). T h e 11C - ure a breath test also exploits the strong ure­ase activity of C Jrylori and its initial results arc encouraging (38). Detection of the bacterium by phase contrast m icroscopy ( 39) or immunofluoresccnce (40) is pos­sible but, like the 11C-u rea breath test, is no t available in many hospitals.

As wi th most previous stud ies, the

Warth in-Sta rry stain was used for h isto­logical detection o f C [lylori. Data wi th this sta in we re less interesting than wi th cultu re and Gram stain. The test was time consu ming and difficu lt to interpret because the re were ;i lot o f utefacts. Some p;ichologists suggest, as an alter­native, the Gie msa, hemacoxylin and eosin or fluorescent acrid ine o range tests ( 10,41.42). In a recent study, the bacte­rium was detected with the hematoxy­lin and eosin stain in 95% of positive cu l­ture biopsies (29).

CAN J GASTROENTl:ROI

CONCLUSION Despite several major reasons to con­

sider C pylori as a pathogen, some con­tinue ro refute this idea because the bac­terium is found in apparently healthy subjects. However. as with othe r bacte­ria, such as group A streptococcus in the pharynx, a carrier state is possible. Although fu rther clinical trials o n C pylori infection treatment are required to confirm its parhogenicity, an investi­gation of different gastroduodcnal dis­eases, particularly gastritis, should in­clude an attempt to detect C pylori within the stomach in addition to the usual his­tological colouration. At least two biop­sies are necessary, one from the antrum. A rapid detection of the bacterium by Gram stained brushing specimen is very simple bur not specific enough. The rapid ureasc test deserves much consid­eration, however, it should be evaluated in the clinical setti ng before being used routinely. Any ki nd of rapid test should be confirmed by culture . Special stain­ing of biopsies to find the bacterium is not indispensable if rapid rest and cul­ture are done.

ACKNOWLEDGEMENTS: The authors acknowledge Myriam Noel ( technologist), Jac­queline Larochelle (nurse). Louise Rochette (,tacistician) and Lucie P. Jobin (mcJical sec­retary) for their indispensable contribution.

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Vol. 2 No. 3, September 1988

C pylori: Association with gostritis

La detection du Campylobacter pyloridis clans la muqueuse gastrique: son association avec la gastrite RESUME: A fin d 'c tudier !'association existan t cntre le Campylobacter Jryloridis et la gastrite, dcux biopsies Ont e tc prelevees au niveau du bulbe duodena], d e l'antre, d u corps, Ct du fond (et lcs lesions, le cas echcant) chez 100 patien ts COnSCCUtifs refcrcs a la cliniquc gastroscopique. Pour chaque sire, unc biopsic ctait dcstince ii l'histologic ct ii la detection du C pyloridis, et la seconde ii la culture . De plus, pou r chaque patient, un brossagc gastrique subissait une coloration de Gram. Vin t-ct-un patients ont ere exclus de cetrc ctudc. Parmi lcs au tres. 3 3 patients avaicnt unc biopsic posi­tive pou r le C pylondis et parmi ceux-ci, 30 (91 %) souffraient d'une gastrite (dont 23, d'unc gasrrice chronique en evolution). On releve unc augmentation de la sensibilitc de la culture avec le nombrc de biopsies. Quarante-deux patients ont cu unc piece de brossage positive, ct parmi eux, 30 (71 %) etaient atteints de gastri te. La coloration de Gram applliquee sur les pieces de brossage avait une sensibilitc de 84.8% comparee aux cu ltures de biopsies. Des 23 patients avec une coloration de Warthin-Starry positive, 19 (83%) avaient une histologie de gastrite. 11 exisrc u ne forte correlation entre la presence du C pyloridis dans la muqueusc stomacale e t la gastrite. L'incidence du C pyloridis associc ii la gastrite est similai re au Quebec, Canada ct dans lcs autrcs regions du mondc. La culture des biopsies est un test simple ct specifique, qui rcquier t deux biopsies au moins pour une bonne sensibilite. La coloration de Gram sur une piece de brossage consti tue un test adequat pou r detecter rapidcment la presence d u C Jryloridis dans l'estomac.

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urea hydrolysis by gastric Campylo­baccers. Lancer 198S;i: lll. (Letter)

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10. Taylor DE. Hargreaves JA, Lai-King NG, Sherbaniuk RW, Jewcll LO. Isolation and characterization of Campylobaccer pyloridis from gastric biopsies. AmJ Clin Parhol 1987;87:49-54.

I I. Booth L, Holdstuck G, MacBride H, et al. Clinical importance of Campylobaccer pyloridis and associated serum lgG and lgA antibody responses in patients undergoing upper gastrointestinal endoscopy.) Clin Pacho! 1986;39:215-9.

12. Rathbone BJ, Wyatt JI. Worsley BW, et al. Systemic and local antibody responses to gastric Campylobaccer Jryloridis in non-ulcer dyspepsia. Gut 1986;27:642-7.

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