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1 JOURNAL OF CLINICAL MICROBIOLOGY, Oct. 1979, p / /05$02.00/0 Vol. 10, No. 4 Rapid Identification of Enterobacteriaceae by Using Noncommercial Micro-Tests in Conjunction with API 20E Profile Data SARAH GEORGE AND G. H. G. DAVIS* Department of Microbiology, University of Queensland, Brisbane, Australia Received for publication 6 February 1979 A total of 371 (97%) of 382 strains of Enterobacteriaceae representing 26 species were identified cheaply, accurately, and rapidly by using a test system based upon standard 96-well microdilution plates and the API 20E profile data. Routine identification of Enterobacteriaceae strains can be rapidly achieved with several commercially available diagnostic systems (1, 2, 14, 20). The API 20E (Analytab Products, Inc.) is convenient and has a proven accuracy against conventional diagnostic methods of ca. 97% (23). It consists of 20 miniaturized tests which yield results in 24 h. A seven-digit code is derived from the test results and interpreted into a species diagnosis by reference to a register of known codes called the API profile register. This is an extension of the diagnostic concepts of Cowan (5) and Fey (10) which confers flexibility to the system and allows an identification to be made despite strain and test variation. The cost of one API 20E strip in Australia is currently ca. $2.00. Although this is an acceptable price for wellendowed laboratories or those that can pass on the cost to the consumer, there are many situations where such costs cannot be met, for example, in less-developed countries or research projects handling large numbers of strains. The possibility also arises that commercial supplies may fail or be unavailable under certain circumstances. For these reasons we have produced a "homemade" miniaturized test system by adapting the API 20E tests to microdilution plates and interpreting the results through the API profile data. MATERIALS AND METHODS Bacterial strains. A total of 349 strains of Enterobacteriaceae freshly isolated from clinical sources at Royal Brisbane Hospital by James Harper and his staff were routinely identified at the hospital by the API 20E system. The names and seven-digit API codes of all strains were filed, and the strains were sent to us labeled with a serial number only in weekly batches. A total of 33 strains representing less commonly encountered species were obtained from Geoff Simmonds, Animal Research Institute, Yeerongpilly, Brisbane, and from Lindsay Sly, Culture Collection, this department. The identity of these 33 strains was confirmed by us, using API 20E. Microdilution system. Standard 96-well (roundbottomed) microdilution plates (Kayline Plastics, Cambden Park, Australia) were sterilized by ultraviolet radiation or propylene oxide, depending upon the numbers needed. Media were dispensed with Pasteur pipettes in a sterile glove box to give ca. 0.2 ml per well. Of the 20 API tests, gelatinase was the only one not readily adapted, and these tests were therefore made in conventional petri dishes by spotting four or more strains per plate of gelatin agar. The remaining 19 tests and one amino acid decarboxylase control (see Table 1) were accommodated in 20 microdilution wells in the order shown in Table 1. By using only well rows A, C, E, and G to avoid overcrowding, four complete test series were accommodated in two plates. Of the tests, 17 were based on semisolid media (Table 1) with agar concentrations ca. 75% of normal gel strength, e.g., 0.9% instead of 1.2% (wt/vol). This allowed these 17 tests to be dispensed, sterility tested by ovemight incubation at 37 C, and stored at 4 C in plastic bags without spillage. The two liquid media tests, tryptophan deaminase (TDA) and Voges-Proskauer/Acetoin (VP/ACE) (Table 1), were aseptically dispensed immediately before inoculation. Microdilution plates were successfully recycled by soaking completed tests in 1 to 2% Medol (William Pearson Ltd., Hull, England) for 24 h, removing spent media, soaking for 18 h in detergent, rinsing in Decon 90 (Decon Laboratories Ltd., Brighton, England), and finally, rinsing in distilled water and resterilizing. Details of test methods. Test methods are summarized in Table 1. The o-nitrophenol-,/-d-galactopyranoside (ONPG) test (18) was with 0.02% (wt/vol) filter-sterilized ONPG in peptone water agar (7). The arginine dihydrolase test (ADH), the lysine decarboxylase test (LDC), and the ornithine decarboxylase test (ODC) were by the method of Moeller (19) as modified by Huhtanen et al. (13), using phenol red as sole indicator. The citratase test (CIT) was by the Simmons (21) method as modified by Edwards and Ewing (9). Hydrogen sulfide (H2S) production was tested with the following simple form of Kligler medium (16): Lab Lemco (L30; Oxoid Ltd., London), 0.3 g; yeast extract (Oxoid L21), 0.03 g; sodium thiosulfate, 0.03 g; ferric citrate, 0.03 g; L-cystine hydrochloride, g; agar, 0.9 g/100 ml. The urease test (URE) was by the Christensen (4) method. The tryptophan deaminase 399

2 400 GEORGE AND DAVIS TABLE 1. Summary of microdilution tests, materials and methods Base Positive reaction Added Test" me- Seal' Initial color (37 C, 24 h) reagent Comment dium' needed" ADH 2 0 Yellow Pink/orange No Some strains produce only pale orange LDC positive results ODC CIT 3 None Light green Dark blue No Dark green reactions considered negative H2S 4 0 Colorless Black No Reaction may fade on extended precipitate incubation URE 5 0 Yellow Pink/orange No Some strains of Klebsiella produce only pale orange positive results TDA 6 None Colorless Dark brown Yes IND 1 ST Colorless Dark pink Yes AMY 8 0 Green Yellow No Positive reactions dull yellow VP/ACE 7 MT Colorless Red Yes Inadequate mixing of reagents may produce false-negative results GLU 1 MT Purple Yellow No INO SOR RHA SUC MEL ARA ONPG 9 MT Colorless Yellow No Dull yellow reactions considered negative aglu, Glucose;, mannitol; INO, D-inositol; SOR, D-sorbitol; RHA, D-rhamnose; SUC, sucrose; MEL, D-melibiose; ARA, L-arabinose. See text for other tests. ' Refer to text for modifications made to the original media. Base media were as follows: 1, peptone meat extract agar; 2, Moeller amino acid decarboxylase medium; 3, Simmons citrate agar; 4, Kligler iron agar; 5, Christensen urea medium; 6, 0.5% (wt/vol) tryptophan in saline; 7, glucose phosphate peptone water; 8, Hugh and Leifson oxidation-fermentation medium; 9, peptone water agar. All but the TDA and VP/ACE tests were semisolid media tests; TDA and VP/ACE were liquid media tests. c Sealing devices: MT, sterile Microtiter sealing tape; 0, oil; ST, permeable adhesive tape. test (TDA) was by the method of Singer and Volcani (22), modified to 0.5% (wt/vol) tryptophan in saline and tested with one drop each of 10% (wt/vol) ferric chloride and 1 M hydrochloric acid. The indole test (IND) was with 0.5% (wt/vol) tryptophan in peptone meat extract agar (see below); inoculated indole wells were sealed with white permeable adhesive tape (Leukopor; Biersdorf AG, Hamburg, Germany) ca. 1 cm wide and tested for indole by touching a swab stick wetted with Kovacs reagent (6) onto the tape over each well. VP/ACE, using glucose phosphate peptone water (6), was tested with one drop of each of Barritt's (3) reagents per well; development of a pink or red color within 10 min was considered a positive reaction. J. CLIN. MICROBIOL. Acid production from carbohydrates (except amygdalin, see below) was tested by using filter-sterilized carbohydrate solution to give a 1% (wt/vol) final concentration when added to molten peptone meat extract agar (containing, per liter: peptone, 10 g; Lab Lemco, Oxoid L30, 3 g; sodium chloride, 5 g; and agar, 9 g) at ph 7.4 with 0.006% (wt/vol) bromocresol purple as indicator. Acid from amygdalin (AMY) was tested in the basal medium of Hugh and Leifson (12) without potassium phosphate. The gelatinase test (GEL) was on peptone meat extract agar (without salt) containing 0.12% (wt/vol) glucose and 0.5% (wt/vol) gelatin, tested at 24 h by flooding with saturated ammonium sulfate solution; clear zones around growth represented positives. Inocula and inoculation. Strains were routinely plated and Gram stained to confirm purity. Cell suspensions for inocula were made by subculturing into 10 ml of tryptone soy peptone broth (17) in a 15-ml centrifuge tube. After 24 h of incubation at 37 C, the

3 VOL. 10, 1979 IDENTIFICATION OF ENTEROBACTERIACEAE 401 tryptone soy peptone broth culture was centrifuged (1,200 x g, 15 min), and the pellet was suspended in phosphate-buffered saline (7) containing 0.1% (wt/vol) Oxoid agar no. 1 to a cell density of ca. 109 cells per ml against barium sulfate standard opacity tubes (7). A simpler procedure in which one to two colonies were emulsified in 1 ml of phosphate-buffered saline containing Oxoid agar also proved successful. Inoculations were made with sterile swab sticks or Pasteur pipettes (one drop per well). Seals for microtiter tests. The ADH, LDC, ODC (and control), H2S, AMY, and URE tests were sealed by filling the inoculated wells with sterile liquid paraffin. The IND test was sealed as described above. VP/ACE was sealed with 1-cm-wide clear adhesive tape. CIT and TDA were not sealed. The plate containing the remaining 10 tests was sealed with microtiter sterile adhesive plate sealer (Cooke Engineering Co., Alexandria, Va.). All plates were lidded and incubated at 37 C for 24 h in plastic bags. Interpretation of results. The 20 characters for each strain were recorded and translated into a numerical code for genus and species identification by using the API coder and profile index (1). Statistical tests. Chi-square and t tests were used to determine whether significant differences occurred between microdilution and API results (11). RESULTS Of the 382 strains tested, the microdilution system correctly identified 98% to genus level and 97% to species level (Table 2). No identification was obtained for eight strains and identities different from those produced by the API system were obtained for three strains. The aberrant reactions of these 11 strains (2.8% of 382) are shown in Table 3. The distribution of false microdilution reactions in 19 tests is shown TABLE 2. Identification of IEnterobacteriaceae to species level by the micirodilution system Strains cor- No. of rectly identistrains fied' Bacteria tested Escherichia coli Klebsiella pneumoniae Proteus mirabilis Enterobacter cloacae Proteus vulgaris Citrobacter freundii Providencia stuartii Serratia marcescens Proteus morganii Enterobacter aerogenes Salmonella spp... Edwardsiella tarda Proteus rettgeri... Providencia alcalifaciens Yersinia pseudotuberculosis Salmonella arizonae Shigella sonnei Yersinia enterocolitica Klebsiella ozaenae Enterobacter hafniae Enterobacter agglomerans Shigella dysenteriae Salmonella biogroup 1 Shigella boydii Salmonella typhi... Salmonella paratyphi A Total a Eleven strains were (Table 3) imperfectly identified TABLE 3. API codes and aberrant reactions of 11 strains wrongly or not readily identified by the microdilution results Strain no. 4 API result ; Salmonella spp. Microdilution result b Aberrant reaction(s) with': VP/ACE ; E. cloacae b URE,, AMY ; K. pneumoniae ; K. pneumoniae ; K. pneumoniae ; E. coli ; K. pneumoniae ; K. pneumoniae ; P. morganii ; P. vulgaris? ; K. pneumoniae "See footnote a to Table 1. 'Not readily identified b b b b b " ; P. mirabilis ; P. rettgeri ; E. aerogenes URE, CIT, VP, AMY ODC, CIT, RHA, MEL, AMY VP/ACE,, SOR, SUC, ARA H2S IND,, H2S ODC

4 402 GEORGE AND DAVIS in Table 4. A total of 184 microdilution reactions (2.5% of 7,258) were different from those obtained with the API system. The highest rates of error (6%) occurred in the CIT, ADH, and AMY tests. Statistical analyses supported the null hypothesis, i.e., no significant difference between microdilution and API results or in the ability of the two systems to identify Enterobacteriaceae. DISCUSSION The microdilution system described here reproduced the API 20E species diagnosis in 97% of the strains tested. When retested, four strains (59, 101, 168, and 340) gave positive mannitol reactions and were readily identified as Klebsiella pneumoniae. Although several tests showed 5% or more differences in the results of the two systems (Table 4), the diagnosis was not necessarily different. For example, 24 of the 25 falsepositive ADH reactions (Table 4) were given by E. coli strains. The microdilution ADH test appeared more sensitive than the API test. Similarly, the microdilution CIT test was more sensitive than the API counterpart. Differences in the melibiose tests probably arose because we used the D-isomer, whereas the API method uses the L-isomer (2); this was not known to us when the work began. The amount of acid produced from glucose after the primary hydrolysis of TABLE 4. Distribution of correct and false test reactions in 19 microdilution tests for 382 strains Microdilution results Correct No. false Test" False False Total posi- negative tive ONPG ADH LDC ODC CIT H2S URE TDA IND VP/ACE GLU INO SOR RHA SUC MEL AMY ARA "See footnote a to Table 1. J. CLIN. MICROBIOL. TABLE 5. API code biotypes among 154 strains of E. coli identified by the microdilution and API systems and the frequency in which they occurred Frequency of occurrence Biotype Microdilution API amygdalin is small, and even with the special procedure we used there were 21 false-negative reactions. Preliminary work showed that a suitable redox potential was produced in microdilution H2S tests by incorporating % (wt/ vol) L-cystine hydrochloride in the medium. The white tape used to seal the IND tests limited the loss and cross diffusion of indole and also provided a good material upon which to detect indole. The omission of sodium chloride from the GEL medium successfully limited swarming

5 VOL. 10, 1979 by Proteus sp., and the tests were readable in 24 h (cf. ref. 15). Davies (8) used the API 20E code system to biotype Escherichia coli strains. Table 5 shows our analysis of 154 E. coli strains by microdilution and API. Both systems recognized four common biotypes at approximately similar frequencies, but microdilution recognized an additional 30 biotypes, compared with 20 recognized by API. Analysis of the two systems used here for time and material cost showed that it took ca. 40 min to prepare, inoculate, and read four strains by the microdilution method (using sterile plates, premelted media, and the simple inoculum preparation procedure described under Materials and Methods), compared with ca. 20 min to handle four strains by the API method, ignoring incubation times. The materials cost ca. $1.50 and $8.00, respectively. ACKNOWLEDGMENT We thank Jenny MacIvor for technical help. ADDENDUM The editor has drawn our attention to the fact that if the current API profile index (April 1978) is used, the results in Table 3 may be interpreted differently (see also our comments in the Discussion section). LITERATURE CITED 1. Analytab Products Inc A.P.I. analytical profile index, 2nd ed. Analytab Products Inc., Plainview, N. Y. 2. Aldridge, K. E., B. B. Gardner, S. J. Clark, and J. M. Matsen Comparison of Micro-ID, API20E, and conventional media systems in identification of Enterobacteriaceae. J. Clin. Microbiol. 7: Baritt, M. M The intensification of the Voges- Proskauer reaction by the addition of a-naphthol. J. Pathol. Bacteriol. 42: Christensen, W. B Urea decomposition as a means of differentiating Proteus and Paracolon cultures from each other and from Salmonella and Shigella types. J. Bacteriol. 52: Cowan, S. T Principles and practice of bacterial taxonomy-a forward look. J. Gen. Microbiol. 39: Cowan, S. T., and K. J. Steel Cowan and Steel's manual for the identification of medical bacteria, 2nd ed. Cambridge University Press, Cambridge, England. 7. Cruickshank, R., J. P. Duguid, B. P. Marmion, and IDENTIFICATION OF ENTEROBACTERIACEAE 403 R. H. A. Swain Medical microbiology, 12th ed. Churchill Livingstone, Edinburgh, Scotland. 8. Davies, B. I Biochemical typing of urinary Escherichia coli strains by means of the API20E Enterobacteriaceae system. J. Med. Microbiol. 10: Edwards, P. R., and W. H. Ewing Identification of Enterobacteriaceae, 3rd ed. Burgess Publishing Co., Minneapolis. 10. Fey, H Differenzierungsschema fur gramnegative aerobe Stabchen. Schweiz. Z. Pathol. Bakteriol. 22: Hamburg, M Statistical analysis for decision making, international ed., p , Harcourt, Brace and World, New York. 12. Hugh, R., and E. Leifson The taxonomic significance of fermentative versus oxidative metabolism of carbohydrates by various gram-negative bacteria. J. Bacteriol. 66: Huhtanen, C. N., J. Naghski, and E. S. Dellamonica Microfermentation series for identification of single colonies of Enterobacteriaceae. Appl. Microbiol. 24: Isenberg, H. D., and B. G. Painter Comparison of conventional methods, the R/B system, and modified R/B system as guides to the major divisions of Enterobacteriaceae. Appl. Microbiol. 22: Jayne-Williams, D. J The application of miniaturized methods for the characterization of various organisms isolated from the animal gut. J. Appl. Bacteriol. 40: Kligler, I. J A simple medium for the differentiation of members of the typhoid-paratyphoid group. Am. J. Public Health 7: Lennette, E. H., E. H. Spaulding, and J. P. Truant (ed.) Manual of clinical microbiology, 2nd ed. American Society for Microbiology, Washington, D.C. 18. Lowe, G. H The rapid detection of lactose fermentation in paracolon organisms by the demonstration of,8-galactosidase. J. Med. Lab. Technol. 19: Moeller, V Simplified tests for some amino acid decarboxylase and for the arginine dihydrolase system. Acta Pathol. Microbiol. 36: Nord, C. E., A. A. Lindberg, and A. Dahlback Evaluation of five test-kits-a.p.i., Auxotab, Enterotube, Pathotec and R/B-for identification of Enterobacteriaceae. Med. Microbiol. Immunol. (Berlin) 159: Simmons, J. S A culture medium for differentiating organisms of typhoid-colon aerogenes groups and for isolation of certain fungi. J. Infect. Dis. 39: Singer, J., and B. E. Volcani An improved ferric chloride test for differentiating Proteus-Providence group from other Enterobacteriaceae. J. Bacteriol. 69: Smith, P. B., K. M. Tomfohrde, D. L. Rhoden, and A. Balows API system: a multitube micromethod for identification of Enterobacteriaceae. Appl. Microbiol. 24:

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