J Clin Pathol 1986;39:654-660

Biochemical and cultural characteristics of "JK"coryneformsR BAYSTON, J HIGGINS

From the Department ofPaediatric Surgery, Institute of Child Health, London

SUMMARY Antibiotic resistant coryneforms (group JK) have increasingly been reported as causes ofserious sepsis in the immunosuppressed and in patients with implants. Their cultural and biochem-ical characteristics were examined in an attempt to provide a simple scheme for their recognition inthe clinical laboratory. Their susceptibilities to a range of antimicrobials were determined, and anenriched selective medium was developed for their isolation from normally non-sterile sites. The JKcoryneforms fell into a fairly homogeneous group, producing colonial morphology and biochemicalprofiles identical with reference strains, which allowed their recognition and differentiation fromother coryneforms. All strains were resistant to penicillin and susceptible to vancomycin, but therewas considerable variation with respect to other antimicrobials. There is scope for furtherrationalisation of biochemical tests for the recognition of these organisms.

The first major report of infections caused by cory-neforms, other than corynebacterium diphtheriae,was by Johnson and Kaye,' who reviewed fifty twopublished cases. Six years later Hande et al2 reportedfour infections due to "a new species of cory-nebacterium." Three patients with leukaemia hadsepticaemia and one had ventriculoatrial shunt infec-tion. The organisms were resistant to penicillin,aminoglycosides, and, in one case, rifampicin. Pear-son etal3 reported 12 cases in two years in patientsundergoing bone marrow transplantation. Again, allstrains were multiresistant. In the same year RileyetatP collected and examined ninety five strains ofmultiresistant coryneforms and proposed that they bereferred to as "group JK" after Johnson and Kaye.'

Since then, Gronemeyers has reported a case of in-fection of a pacemaker generator and Murray etal6have described 18 cases of prosthetic valve endo-carditis. Gill et al7 reported seven more cases of bacte-raemia on an oncology unit and Finger et al8 reported13 similar cases, including patients on an intensivecare unit. Hoffman9 reported a fatal case of men-ingitis in a patient with lymphoma. Three cases ofperitonitis in patients receiving continuous ambu-latory peritoneal dialysis have also been described(Pierrard et al, 1I Altwegg et al"). More recently, fourpatients with granulocytopaenia'2 and one with apla-stic anaemia13 were reported as having septicaemiadue to JK coryneforms. Many more cases probably

Accepted for publication 30 January 1986

go unreported, or are reported to the CommunicableDisease Surveillance Centre as "diphtheroids". Theorganisms present the routine clinical laboratory withdifficulties in isolation and identification, growingslowly on ordinary media and producing positive bio-chemical results only in the presence of serum or afterseveral days' incubation. A further question is that oftheir natural habitats, as well as their importancewhen isolated from normal sites as part of surveil-lance of patients nursed in protective isolation. Tom-kins,'4 Finger etal,8 and Wichman et'al' conductedsurveys using selective media. Unfortunately, mediacontaining antimicrobials such as cephalosporins oraminoglycosides were used, and these are likely toyield only those strains resistant to these agents, whilenon-selective media will fail to isolate JK cory-neforms due to overgrowth of other commensals.'4We therefore decided to investigate the cultural and

biochemical characteristics of a collection of clinicalisolates with the aim of allowing their rapid recog-nition in the clinical laboratory. We also investigatedvarious selective and enrichment agents with a view todeveloping a medium that could be used in surveil-lance studies.

Material and methods

SOURCES OF ISOLATESMany coryneforms were donated by microbiologistsin the United Kingdom, often after being reported ineither the Communicable Disease Report or the Com-

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"JK"coryneforms

municable Diseases (Scotland) Report. Others were

isolated by us. Three strains had been identified bythe Centers for Disease Control (CDC) Atlanta, as

JK coryneforms. A total of 52 strains were included.

CULTURAL CHARACTERISTICSStrains were inoculated on to Columbia blood agar

(Lab M Ltd UK) and incubated aerobically at 37°Cfor 48 hours. Their microscopic and colonial mor-

phologies and catalase reaction were noted. Sub-sequently, all strains were additionally incubatedanaerobically on Columbia blood agar and in thio-glycollate broth supplemented with 1% Tween 80.The plates were incubated in an aerobic jar with 80%nitrogen, 10% hydrogen, and 10% carbon dioxide,and a palladium aluminium catalyst. A plate inocu-lated with Pseudomonas aeruginosa was used as a con-

trol.

ENRICHMENT AGENTSStrains were grown on Columbia blood agar, nutrientagar, brain heart infusion agar, and tryptone soya

agar (Lab M United Kingdom). Each of these was

used plain and supplemented with one of the follow-ing: horse blood 7%, whole, lysed, and heated; tribu-tyrin 1%; and Tweens 20, 40, 60, 80, and 85, all at1%. Further tests were then carried out using brainheart infusion agar to determine the optimum con-

centrations of Tween 80, using 0-05%, 0-1%, 0-5%,1-0%, and 2-0%. Plates were incubated for 48 hoursat 37°C and the number and size of the colonies notedand compared.

SELECTIVE AGENTSBrain heart infusion agar containing 1% Tween 80was supplemented with one of the following: potas-sium tellurite 0-02%, 0-03%, and 0-04%; polymyxinB sulphate; and mupirocin (pseudomonic acid). The

655

optimum concentrations were determined by inocu-lation of the enriched medium containing the selectiveagent with a range of Gram negative and Gram posi-tive organisms (Table 1).

IDENTIFICATION TESTSTo test as many substrates as possible within the con-

straints of the study and to cover the likely range oftests each coryneform was inoculated into both APIStaph and API Strep (API Laboratory Products Ltd).API Staph dilution fluid supplemented with 0-2 mlsterile rabbit serum was used for both to suspend thegrowth from a whole blood agar plate in strains pro-ducing small colonies. Enough of the large colonyproducers was used to give a turbidity equal to No 4on the MacFarland scale. Two drops of API Strepindicator were added to the carbohydrate cupules inthe API Strep strip and the tests were then incubatedfor 48 hours at 37°C before adding reagents and read-ing results.

SUSCEPTIBILITY TO ANTIMICROBIALSStrains were tested for susceptibility to 14 anti-microbials using a modified Stokes method and a ro-

tary inoculator. The medium used was DiagnosticSensitivity Test agar (Oxoid United Kingdom) sup-plemented with lysed horse blood. Susceptibility tomethicillin was tested on Columbia agar plates con-

taining polyvinylpyrrolidone,'6 1% Tween 80, and12-5 mg/l methicillin, and incubated overnight at30°C. Results were converted to a numerical anti-biogram"7 by scoring for resistance (Table 2).

Results

CULTURAL CHARACTERISTICSAfter 48 hours on blood agar strains could be allottedto one of two main groups, depending on colonial

Table I Action ofpotentially selective agents against coryneforms and other organisms

Organism Control Potassium tellurite (%) Polymyxin B Mupirocin SelectiveBHI + T80 (8mg/l) (I mg/i) enriched

0-02 0-03 0-04 medium

JK + - - - + + +Clostridium xerosis + - - - + + +Clostridium pseudodiphtheriticum + - - - + + +Enterococcus + + + - + + +Staphylococcus aureus + + + + +Staphylococcus aureus (methicillin resistant) + + + + +Staphylococcus epidermidis + +Escherichia coli + - - - - +Proteus + + + +Pseudomonas aeruginosa + - - - - +Klebsiella pneunoniae + - - - - +Candida albicans + + + + + + +

BHI + T80 = Brain heart infusion agar with 1% Tween 80.+ = Growth; - = no growth; ± = minimal growth.

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Table 2 Derivation ofnumerical antibiogram

4 Penicillin7 2 Tetracycline

I Chloramphenicol4 Erythromycin

7 2 Cloxacillin1 Trimethoprim4 Clindamycin

7 2 Gentamicin1 Rifampicin4 Amikacin

7 2 NetilmicinI Cefuroxime4 Vancomycin

7 2 SpiramycinI Fusidic acid

Susceptibility scores 0, resistance scores as shown

diameter. The large colony strains were further sub-divided for the purpose of this study into three typesand the small colony strains into two types (Table 3).Reference strains, which had been identified as JKcoryneforms by Centers for Disease Control, fell intocolony type D. Colony type E strains consisted ofthose small colony types that were not type D andwere, therefore, a heterogeneous group. All strainswere non-haemolytic on horse blood, non-motile atroom temperatures and 37°C, and catalase positive.They were all Gram positive rods or cocco-bacilli on

microscopy, though not always displaying the typicalarrangement in pallisades. All strains failed to growanaerobically on blood agar, and when incubated inthioglycollate broth supplemented with 1% Tween 80they grew only in the top 1-2 mm. Two strains were ofcolony type A, one of type B, eight of type C, 38 oftype D, and three of type E.

ENRICHMENT AGENTS

Growth on brain heart infusion agar was superior tothat on Columbia agar, nutrient agar, and tryptonesoya agar, as determined by colony size. The numberof colonies recovered did not differ appreciably. Theaddition of horse blood in any form did not enhancegrowth. Egg yolk did not enhance growth and was

inhibitory to some strains, and tributyrin was also notbeneficial.Although the growth of some coryneforms was en-

hanced by the addition of Tweens 20, 40, and 60 at a

final concentration of 1%, these proved inhibitory tothe small colony types D and E. A 1% concentration

Bayston, Higgins

of Tweens 80 and 85, however, greatly enhancedgrowth, with Tween 80 being superior to Tween 85.Growth enhancement by Tween 80 was still greateron brain heart infusion agar. In view of this the opti-mal concentration of Tween 80 in this medium was

determined and was found to be 1%. The final en-

richment agar consisted of brain heart infusion agar

supplemented with 1% Tween 80.When grown on this medium for 48 hours colonies

of the certified JK coryneforms appeared as yellow-ish, smooth, convex, entire, 2-3 mm in diameter, andsurrounded by a wide halo of hydrolysis products ofTween 80, both in the agar and on its surface. Thishalo became much more pronounced on incubationfor a further 24 hours. All strains of colony type Dclosely resembled the certified JK strains. The en-

riched medium could not, however, be used todifferentiate between colony types as all grew very

well, so that differences in size were no longer appar-

ent, and differentiation was carried out using Col-umbia blood agar (Figure).

SELECTIVE AGENTSTable 1 shows the inhibitory effects of the agentstested against a range of organisms. All concen-

trations of potassium tellurite tested were inhibitoryto coryneforms, though this effect was shown only inthe presence of Tween 80. Polymyxin B sulphate at aconcentration of 8 mg/l permitted the growth of cory-neforms while inhibiting Gram negative rods, withthe exception of Proteus. Similarly, the coryneformswere resistant to mg/l of mupirocin, which was

sufficient to inhibit staphylococci. Faecal streptococciwere not inhibited, but in practice these could be dis-tinguished by colonial appearance and catalase reac-tion. The final selective enriched medium consisted ofbrain heart infusion agar with 1% Tween 80, 8 mg/lpolymyxin B sulphate, and 1 mg/l mupirocin.

IDENTIFICATION TESTS

Table 4 shows the numerical profiles derived from thetest strips: these are grouped according to colonytype. Table 5 shows a short profile derived from a

limited number of substrates.All strains except 7308 (colony type C) gave a posi-

tive Voges Proskauer reaction. All gave a positivereaction for hippurate hydrolase and leucine ary-

Table 3 Colonial types ofcoryneforms on Columbia blood agar (37°C, 48 hours)

Type Diameter (mm) Description

A 2-3 White, rough, dry, matt, crenatedLarge colony types B 2 White/greenish, matt, entire

C 2-5 Greenish, domed, glossySmall colony types D 05-1 Glossy, white or grey, domedE <05-1 Dry, flat, often crenated

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( _IFigure (a) Large colony coryneform; (b) large colony coryneform; (c) small colony coryneform,colony type D (JK); (d) small colony coryneform, colony type E. All were grown on Columbia bloodagarfor 48 hours.

lamidase and, with the exception of one strain of co-lony type D, for alkaline phosphatase. Typical JKcoryneforms, exemplified by the Centers for DiseaseControl certified strains, were found to be of colonytype D and to give positive reactions for Voges Pros-kauer, leucine arylamidase, hippurate hydrolase, andalkaline phosphatase, and negative reactions for ni-trate reduction and pyrrolidonylarylamidase; theyfailed to acidify maltose or fructose. Some stainsacidified glucose and a few hydrolysed urea. Theshort profile was based on reactions for the abovetests. The typical JK coryneforms profiles were: APIStaph 200 4100; API Strep 306 2000, short profile7420, colony type D.

SUSCEPTIBILITY TO ANTIMICROBIALSThe results were converted into numerical anti-biograms (Table 2), and these profiles are shown in

Table 4. The colony type D strains may be seen toshow resistance to more antimicrobials than other co-lony types, with a few exceptions among colony typesA and C. Eight large colony strains were found to besusceptible to penicillin. Most strains were resistant tomethicillin. Only seven colony type D strains weresusceptible to cefuroxime. Twenty eighS of the thirtyeight colony type D strains were susceptible to rifam-picin, and all were susceptible to vancomycin.

Discussion

Organisms considered to be JK coryneforms gener-ally grew poorly and slowly on ordinary non-inhibitory media. The very small grey-white coloniesusually appeared only after at least forty eight hours'incubation. Various supplemented media have beenused, such as that described by Finger etal,8 which

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658 Bayston, HigginsTable 4 Results ofcolony typing, biochemical profiles, and antibiograms for large colony types

No Colony type APIstaph API strep Antibiogram "Short profile"

710459447580/4B73087576/27580/la/b7580/4c7580/27580/3729472957579/25937593674277573/573537394/1664966487573/4593872096651613666526542665365436960654166506540721070717065706365396536727570197579/573097576/47573/17577357576/370167271727273077276

AABC

C

C

C

C

C

C

C

DDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDDEEE

6306100000610067041006004000631015063101506704100000010000040020006102000610220041002004100200410020041002004100200410000041020000102200410020041002004100200410000041002004100200410000041022004100000400020041000004100200410020041000004100000410020041002004100200410020041002004100200410020041002000100200410020041002004100200410020041002004100420610161060106314110

3062003306200030620032062000316201331620133062003116000030600003160000316000030620003062000306200030620003062000306000020600033040000306000030620003062002306200030620003062000306200030600003062000306000030620003062000306000030620003060000306000030620003060000306200030620103060000306200030601003060020306201030620003060000306200030620003062010206040030600002062013

170005566203000010000300003000030007746257412010000100077402774137741377672577737777353010577727767357773774137767277773776737767377772776727767377403732707767357672777737741347402776725767277677277673776737300043000776737777357773430007770243000200003000035402

7561750074617021766176617461560074007710771074207420742074207420742074106410742074207420742074007420742074107420740074207410742074207400740074207420742074207420742074207420742074207420742074207420744175217461

Table 5 Derivation of "short profile"

PAL HIPP LEUC NIT PYR VP UREA GLU MAL FRU1 2 4 1 2 4 1 2 4

7 7 7 1

Results are scored 0 when negative, and as shown when positive.PAL = Alkaline phosphatase; HIPP = Hippurate hydrolase; LEUC = Leucine arylamidase; NIT = Nitrate reduction; PYR =Pyrrolidonylarylamidase; VP = Voges-Proskauer; UREA = Urease production; GLU = Acidification of glucose; MAL = Acidification ofmaltose; FRU = Acidification of fructose.

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"JK"coryneformscontained tryptose agar, histidine, egg yolk, Tween 80(3%), sodium thiosulphate, and glycerol, along withbroad spectrum antibiotics. Jadeja etaal8 used brainheart infusion agar supplemented with 5% rabbit se-rum, but they dealt only with laboratory stockstrains. Our strains showed a distinct tendency to be-come less demanding on storage and subculture,though the difference in growth on blood agar andbrain heart infusion agar containing Tween 80 wasstill considerable. The inclusion of broad spectrumantibiotics such as aminoglycosides and cepha-losporins is likely to lead to failure to isolate certainstrains. Twelve of the thirty eight typical JK cory-neforms in our series were susceptible to gentamicinon disc testing. Tomkins etaal4 found that failure toinclude a cephalosporin in their selective medium per-mitted overgrowth of any JK coryneforms by coagu-lase negative staphylococci, but seven of our JKstrains proved to be susceptible to cefuroxime.

This problem was one reason why therapeuticallyapplicable antimicrobials were avoided in the selec-tive medium reported here. All coryneforms tested sofar in this laboratory seem to be intrinsically resistantto polymyxin B and mupirocin, and the use of thesetwo agents in an ecological survey, or for specimensfrom "normal flora" sites, would be expected to leadto isolation of both susceptible and multiresistantstrains. The use of brain heart infusion agar with 1%Tween 80 is recommended for routine isolation of JKcoryneforms on solid media from normally sterilesites, or from catheters. Polymyxin B and mupirocinshould be added for sites not normally sterile, such asskin and mucous membranes. Nalidixic acid could beadded if Proteus is likely to be troublesome. It mayalso be helpful to supplement blood culture mediawith Tween 80 for use in the immunosuppressedpatient or those otherwise considered to be at riskfrom JK coryneform infections.

Corynebacteria are usually described as being"aerobic, facultative."'9 Some authors do not statethe oxygen requirement of their isolates, but thosewho do find that they are strict aerobes.2 38 13 20 21Only two authors, however, have paid much attentionto this. Hande et a!2 went on to attempt to grow theirstrains in supplemented thioglycollate broth andfound only surface growth, as is reported here.Downie et al' 3 were able to grow their isolate only inthe aerobic bottles of blood cultures and commentedthat this caused a delay of recognition of its clinicalimportance. All our strains of coryneforms werefound to be strict aerobes.The use of API Strep for identification of JK cory-

neforms was suggested by Kelly etal.22 When exam-ining large numbers of biochemical characteristics ona large group of organisms with the usual time con-straints, systems such as API Staph and API Strep are

659

invaluable. It is inevitable, however, that not all thetests will be of value. The small colony type cory-neforms are relatively biochemically inactive, andmost carbohydrates were not attacked, the only use-ful ones being glucose, fructose, and maltose. The"short profiles" were compiled from those tests thatwere considered to be helpful, and if the use of this, ora similar group of tests, becomes accepted then manu-facturers might be persuaded to consider the prod-uction of a more relevant test strip. Alternatively, arange of laboratory made substrates in microtitretrays could be considered. Generally, the profiles re-ported here correspond to those already published,but with some exceptions. Comparing the results withthose of Riley et al,4 shows that the biggest discrep-ancy lies in the Voges-Proskauer test. All our strainswere Voges Proskauer positive, whereas all of Riley'swere negative. This is most probably explained by thedifferent test substrates. The Voges Proskauer test de-termines the ability to produce acetoin from glucose,but in the API system the substrate is pyruvate, whichrepresents a starting point further into the pathway.In addition, eight of the JK coryneforms listed inTable 2 failed to acidify glucose, whereas all of Riley'sstrains were positive in this test. Similarly, none of thecolony type ofD JK strains acidified maltose or fruc-tose, whereas 44% and 35%, respectively, of Riley'sstrains were positive: this probably reflects differencesbetween test conditions, which in turn can affect therates of reactions to change results read in a definedtime scale.The JK coryneforms have been described several

times as a new species of corynebacteriwn, but re-cently reports of their similarity to biovars I to VI ofC genitalium and biovar C6 of C pseudogenitaliumhave appeared.23 These organisms are found in theurethra, and in the case of C genitalium, are consid-ered by some to be a cause of non-specific urethritis.24They are obligate aerobes and produce colonies onblood agar, which are morphologically identical withJK coryneforms. Their biochemical reactions are alsosimilar. Biovars II and IV of C genitalium oxidise glu-cose, and biovar VI hydrolyses urea. Biovar C6 of Cpseudogenitalium oxidises fructose but not glucose.The strains reported in studies were multiresistant toantimicrobials and their growth was enhanced byTween 80. These biovars of C genitalium and Cpseudogenitalium might be synonymous with JKcoryneforms. More chemotaxonomic investigations,however, are needed. We believe that coryneformsconsidered to be of clinical importance should be sentto reference experts for further study, but there is aconsiderable amount that the clinical laboratory cando to identify provisionally such strains. We hopethat the observations reported here will help in theisolation and recognition of these strains.

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We are grateful to those microbiologists who kindlysent strains for study. JH was supported by a grantfrom Essex ASBAH.

References

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2Hande KR, Witebsky FG, Brown MS, etal. Sepsis with a new

species of corynebacterium. Ann Intern Med 1976;85:423-6.3Pearson TA, Braine HG, Rathburn HK. Corynebacterium species

in oncology patients. JAMA 1977;238:1737-40.Riley PS, Hollis DG, Utter GB, Weaver RE, Baker CN. Character-

isation and identification of 95 diphtheroid (group JK) culturesisolated from clinical specimens. J Clin Microbiol1979;9:418-24.

'Gronemeyer PS, Weissfeld AS, Sonnenwirth AC. Corynebacteriumgroup JK bacterial infection of an epicardial pacemaker. Am JClin Pathol 1980;74:838-42.

6Murray B, Karchmer W, Moellering R. Diphtheroid prostheticvalve endocarditis; a study of clinical features and infecting or-ganisms. Am J Med 1980;69:838-48.

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Finger H, von Koenig C-HW, Wichman S, Becker-Boost E,Drechsler HJ. Clinical significance of resistant corynebacteriagroup JK. Lancet 1983;i:538.

9 Hoffman S, Ersgaard H, Justesen T, Friis H. Fatal meningitis withgroup JK corynebacterium in a leucopenic patient. Eur J ClinMicrobiol 1983;2:213-5.

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Altwegg M, Zaruba K, von Graevenitz A. Corynebacterium groupJK. Peritonitis in patients on continuous ambulatory peritonealdialysis. Klin Wochenschr 1984;62:793-4.

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16Bayston R. Use of polyvinylpyrrolidone in the testing of staphylo-cocci for sensitivity to methicillin and cephradine. J Clin Pathol1979;31:434-6.

Bayston R. Bacteriological examination of removed cerebrospinalfluid shunts. J Clin Pathol 1983;36:987-90.

18Jadeja L, Feinstein V, le Blanc B, Bodey GP. Comparative in vitroactivities of teichomycin and other antibiotics against JK diph-theroids. Antimicrob Agents Chemother 1983;24:145-6.

'9Bergey's manual of determinative bacteriology. Eighth ed. Bucha-nan RE, Gibbons NE, ed. Baltimore: Williams and Williams,1974.

20 Smith RF. Characterisation of human cutaneous lipophilic diph-theroids. J Gen Microbiol 1969;55:433-43.

21von Koenig C-HW, Wichman S, Finger H. Infections caused bycorynebacterium Group JK. Zbl Bakt Hyg I Abt Orig A1982:370-6.

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24Fumess G, Evangelista AT. Infection of a non-specific urethritispatient and his consort with pathogenic species of non-specificurethritis corynebacteria, Corynebacterium genitalium n sp. In-vest Urol 1976;14:202-5.

Requests for reprints to: Dr R Bayston, Department of Pae-diatric Surgery, Institute of Child Health, 30 GuilfordStreet, London WC1N IEH, England.

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