JOURNAL OF CLINICAL MICROBIOLOGY, Nov. 1982, P. 856-860 0095-1137/82/110856-05$02.00/0 Copyright 1982, Americn Society for Microbiology Vol. 16, No. 5 Pseudomons eruginos Coloniztion in Ptients with Spinl Cord Injuries DONNA S. GILMORE,1 SANDRA K. BRUCE,' ENES M. JIMENEZ,' DONALD G. SCHICK,1 JAMES W. MORROW,23 AND JOHN Z. MONTGOMERIEl 4* Deprtment of Medicine'* nd Deprtment of Surgery,2 Rncho Los Amigos Hospitl, Downey, Cliforni 90242, nd Deprtment of Surgery3 nd Deprtment of Medicine,4 University of Southern Cliforni School of Medicine, Los Angeles, Cliforni 90033 Received 27 My 1982/Accepted 18 August 1982 The prevlence of Pseudomons eruginos coloniztion of ptients with spinl cord injury ws studied nnully from 1976 to 1980. The urethr, perineum, rectum, dringe bg, nd urine of ptients on the spinl cord injury service were cultured. A totl of 224 men nd 32 women were studied. Most ptients were mnged with n externl urinry collection system or pdding, with or without intermittent ctheteriztion. P. eruginos ws cultured from one or more body sites (urethr, perineum, or rectum) in 65% of men nd 18% of women. Dringe bgs on the beds were frequently colonized with P. eruginos (73%). Significnt bcteriuri with P. eruginos ws present in 19% of the men nd 13% of the women. P. eruginos coloniztion of body sites in men ws closely ssocited with the use of n externl urinry collection system. Significntly greter urethrl nd perinel coloniztion ws found in men using n externl urinry collection system. P. eruginos serotype 11 ws the predominnt serotype for the first 3 yers, nd the number of ptients colonized with serotype 11 incresed with length of hospitl sty. The prevlence of serotype 11 significntly decresed in the lst 2 yers. The ntibiotic susceptibility of the strins of P. eruginos isolted from these ptients did not chnge in the 5 yers, except tht there ws incresing susceptibility to crbenicillin in lter yers. This incresing susceptibility to crbenicillin ws reflection of decresed prevlence of serotype 11 in these ptients, since serotype 11 ws more resistnt thn other serotypes to crbenicillin. Pseudomons eruginos hs been frequent cuse of urinry trct infections in ptients with spinl cord injury (SCI). The incidence of P. eruginos bcteriuri hs closely correlted with P. eruginos coloniztion of the urethr, perineum, nd rectum in these ptients. Initil studies in 1976 reveled high incidence (85%) of P. eruginos coloniztion in the urethr, perineum, or rectum in mle ptients on the SCI service (4). Surveillnce of urinry trct infections hs been continued, nd coloniztion of ptients hs been exmined nnully. This pper reports the prevlence of body coloniztion nd bcteriuri with P. eruginos over 5 yers nd exmines the fctors tht my influence this coloniztion. MATERIALS AND METHODS Prevlence studies were crried out nnully from 1976 to 1980. All inptients on the SCI service were included in the study. The ptients were cred for in two wrds, which consisted of six-bed rooms. Most ptients were trnsferred from other hospitls with n indwelling urethrl ctheter which ws removed on dmission, nd intermittent ctheteriztion (IC) ws crried out until spontneous voiding occurred. An externl urinry collection system ws used with mle ptients when spontneous voiding occurred. This system consisted of n externl condom ctheter connected to either leg bg or dringe bg on the bed. Beginning in 1977, the externl urinry collection system ws chnged dily. Before tht time, dringe bgs were chnged weekly. Femle ptients were either dipered or kept on IC. The urethr, perineum, rectum, nd dringe bg of ll ptients were cultured during 72-h period. Sterile cotton swbs (Cheseborough-Ponds) moistened in norml sline were used to culture body sites. Swbs were inserted pproximtely 1 cm into the urethr nd rectum. Perinel cultures were obtined by swbbing the skin surfce. Dringe bg cultures were obtined by collection of urine through the dringe tube into sterile continer. Urine for culture ws obtined by ctheter from ptients on the IC progrm. After IC ws discontinued, urine ws obtined when the residul urine ws mesured. Urinry trct infections (bcteriuri.10,000 colony-forming units per ml in ctheter urine) were treted with ntibiotics, usully minoglycosides, for 5 dys, plus n orl gent for 10 dys. Mny ptients 856
VOL. 16, 1982 P. AERUGINOSA IN SPINAL CORD INJURIES 857 TABLE 1. Clinicl fetures of ptients No. of ptients with Ptient Totl no. of Age in yers No. of sex ptients (men) qudriplegics IC Antibiotics Indwelling urethrl EUCS ctheter Mle Femle 224 32 15-69 (29) 16-62 (30) 122 14 64 15 168 21 21 7 142 EUCS, Externl urinry collection system. were mintined on mcrodntin or trimethoprimsulfmethoxzole s prophylctic gents for 4 to 6 weeks. Swbs were plced in 4 ml of tryptic soy broth (Difco Lbortories) with 0.03% cetrimide (cetrimide broth), incubted for 24 h t 37 C, nd plted onto cetrimide gr (0.03% cetrimide gr; Pseudosel; BBL Microbiology Systems). The identifiction of P. eruginos ws crried out by stndrd techniques. Serotyping ws crried out by using P. eruginos ntiser (Difco) with vible culture. The slide gglutintion technique ws crried out with vible bcteri from isolted colonies mixed directly with ntiser. Antibiotic disk sensitivities were crried out on Mueller-Hinton gr by the Kirby-Buer technique (1). RESULTS A totl of 224 men nd 32 women with SCI were studied over 5 yers. The clinicl fetures of the ptients re shown in Tble 1. Most mle ptients (63%) were using n externl urinry collection system with or without IC t the time of the study. Twenty-eight ptients (21 mle nd 7 femle) hd n indwelling urethrl ctheter t the time of culture. The sites of coloniztion with P. eruginos re shown in Tble 2. P. eruginos ws cultured from one or more body sites (urethr, perineum, or rectum) in 146 of 224 men (65%) nd 5 of 28 women (18%). In men, the perineum ws the body site most frequently colonized. In ptients with dringe bgs (pproximtely hlf the mle ptients), P. eruginos ws cultured from the contents of the bg in 73% of ptients. This coloniztion of the bg ws closely ssocited with coloniztion of one or more body sites. TABLE 2. P. eruginos coloniztion of ptients No. (%) of ptients positive/ Mle Femle Urethr 100/215 (47) 2/22 (9) Perineum 115/223 (52) 3/28 (11) Rectum 91/224 (41) 5/28 (18) Urethr, perineum, or rectum 146/224 (65) 5/28 (18) Dringe bgs 77/105 (73) 2/5 (40) Urine 35/181 (19) 4/31 (13) P. eruginos bcteriuri (greter thn 104 bcteri per ml) ws found in 19% of the men nd 13% of the women. Two of the four women with bcteriuri hd indwelling urethrl ctheters. In men, bcteriuri ws ssocited with coloniztion of one or more body sites in ll but six instnces. Cultures of body sites from women with P. eruginos bcteriuri were ll negtive. Coloniztion with P. eruginos vried from yer to yer in men, with some decrese over the yers (Tble 3). The gretest incidence of P. eruginos bcteriuri ws found in men using n externl urinry collection system or indwelling ctheter (Tble 4). P. eruginos bcteriuri ws uncommon in men mnged solely by IC. Men using n externl urinry collection system hd significntly greter coloniztion with P. eruginos in the urethr (P < 0.001 by chi squre) nd perineum (P < 0.025 by chi squre) thn men who did not use n externl urinry collection system (Tble 5). Antibiotics hd little effect on coloniztion with P. eruginos (Tble 6). The effect of ntibiotics generlly considered ctive ginst P. eruginos (mikcin, tobrmycin, gentmicin, nd crbenicillin) ws exmined seprtely. Less urethrl coloniztion with P. eruginos ws found in men who received ntipseudomonl therpy, but this reduction ws not sttisticlly significnt. Coloniztion ptterns of men chnged with length of hospitl sty (Tble 7). P. eruginos ws found in higher percentge of urethrl cultures obtined from ptients who hd been hospitlized for more thn 3 weeks. Perinel nd rectl coloniztion remined constnt. The predominnt P. eruginos serotype found ws serotype 11, ccounting for 46% of the cultures typed (Tble 8). However, coloniztion with serotype 11 significntly decresed (P < 0.005) in the lst 2 yers. This ws ssocited with significnt increse in serotypes 4 nd 6 (P < 0.005). Severl ptients did hve more thn one serotype cultured from body sites, but only four ptients were found with more thn one type in the sme site. Coloniztion with P. eruginos serotype 11 incresed with length of sty in the hospitl (Tble 9). Significntly greter coloniztion of
858 GILMORE ET AL. J. CLIN. MICROBIOL. TABLE 3. P. eruginos coloniztion of ptients in different body sites in different yers Ptient No. (%) of cultures positive/ sex 1976 1977 1978 1979 1980 Urethr Mle 22/38 (58) 17/33 (52) 23/43 (53) 21/51 (41) 17/50 (34) Femle 0/0 0/4 0/8 1/3 1/7 Perineum Mle 27/39 (67) 17/40 (42) 30/43 (70) 20/51 (39) 21/50 (42) Femle 0/5 0/5 0/8 1/3 2/7 Rectum Mle 21/39 (54) 15/41 (37) 24/43 (53) 18/51 (35) 13/50 (26) Femle 0/5 0/5 2/8 1/3 2/7 Any body site Mle 34/39 (85) 25/41 (63) 33/43 (77) 26/51 (51) 28/50 (56) Urine Mle 14/43 (37) 15/40 (38) 5/43 (12) 1/31 (3) 0/24 (0) the perineum (P = 0.015 by Fisher exct) ws found in men hospitlized longer thn 8 weeks compred with men hospitlized less thn 3 weeks. Urethrl nd rectl crrige with this serotype lso incresed with time. The ntibiotic susceptibility of the strins of P. eruginos isolted from ptients is shown in Tble 10. There ws no significnt chnge in the susceptibility of these strins to the ntibiotics tested, except tht there ws n incresing susceptibility to crbenicillin with time. When the susceptibility of the min serotypes of P. eruginos ws exmined, serotype 11 ws found to be more resistnt thn the other strins to crbenicillin (Tble 11). Therefore, the incresing susceptibility of the strins s group over the yers depended on the reduced numbers of serotype 11 isolted. Tobrmycin nd gentmicin resistnce ws greter in serotype 4 thn in serotypes 6 nd 11. DISCUSSION These studies confirm our previous results, which showed high incidence of P. eruginos coloniztion in ptients with SCI (4, 5). This coloniztion ws gin shown to be significntly influenced by the use of n externl urinry collection system, nd men were much more TABLE 4. P. eruginos bcteriuri ssocited with urinry mngement in men Mngement No. (%) of men positive/ techniqueb EUCS only... 16/78 (21) EUCS with IC... 6/30 (20) IC only... 1/32 (3) Indwelling ctheter... 10/17 (59) No device... 2/24 (8) >104 colony-forming units per ml in ctheter specimen. b EUCS, Externl urinry collection system. frequently colonized thn women. The perineum proved to be the most frequent site of P. eruginos coloniztion, nd P. eruginos frequently colonized dringe bgs on the beds. A predominnce of P. eruginos serotype 11 ws seen the first 3 yers. This prticulr strin ws lso cultured more frequently from ptients hospitlized longer thn 3 weeks. Cultures, including environmentl smpling to exmine n endemic sitution in this group of ptients, identified no reservoirs for this strin of P. eruginos other thn the ptients themselves (4). Serotypes 4 nd 6 emerged in the lst 2 yers of the study. The reson for the chnge in serotypes is not cler. Serotype 4 ws more resistnt to gentmicin nd tobrmycin, which re frequently used in these ptients. However, coloniztion TABLE 5. P. eruginos coloniztion ssocited with urinry mngement in men nd technique No. (%) of men positive/ Urethr EUCS only... 69/108 (64) EUCS nd IC... 14/31 (45) IC only... 5/32 (16) Indwelling ctheter... 4/15 (27) No device... 8/29 (28) Perineum EUCS only... 63/110 (57) EUCS nd IC... 17/32 (52) IC only... 7/32 (22) Indwelling ctheter... 15/20 (75) No device... 13/29 (45) Rectum EUCS only... 46/110 (42) EUCS nd IC... 15/32 (47) IC only... 10/32 (31) Indwelling ctheter... 7/21 (33) No device... 13/29 (45) EUCS, Externl urinry collection system.
VOL. 16, 1982 TABLE 6. P. eruginos coloniztion ssocited with recent ntibiotic use in men No. (%) of Antibiotic use men positive/ Urethr Yes 72/162 (44) No 25/53 (53) Antipseudomonl ntibiotic 9/33 (27) Perineum Yes 82/168 (49) No 33/55 (60) Antipseudomonl ntibiotic 13/36 (36) Rectum Yes 67/169 (40) No 24/55 (44) Antipseudomonl ntibiotic 13/35 (37) Ptients receiving ntibiotics or urinry ntiseptics t time of culture or within 2 weeks before culture. TABLE 7. P. eruginos coloniztion in reltion to durtion of hospitl sty No. (%) of ptients positive/ c3 weeks 4 to 8 weeks >8 weeks Urethr 17/52 (33) 31/66 (47) 52/96 (54) Perineum 25/55 (45) 37/69 (54) 53/99 (54) Rectum 24/55 (44) 29/70 (41) 38/99 (38) with P. eruginos of ny serotype did not seem to be influenced by ntibiotic use. The decresing prevlence of serotype 11 in the lst 2 yers ws ssocited with decrese in the prevlence of significnt bcteriuri with P. eruginos nd rised the possibility tht sero- P. AERUGINOSA IN SPINAL CORD INJURIES 859 TABLE 9. P. eruginos serotype 11 coloniztion of ptients in reltion to durtion of hospitl sty No. (%) of serotype 11 isoltes/ no. of P. eruginos isoltes c3 weeks 4 to 8 weeks >8 weeks Urethr 2/11 (18) 12/24 (50) 20/36 (55) Perineum 4/17 (24) 18/36 (50) 24/38 (63) Rectum 5/18 (28) 9/28 (32) 16/30 (53) type 11 my be more virulent. The incidence of serotype 11 in body sites (112 of 282 [40%]) ws compred with the incidence of serotype 11 isolted from the urine of ptients with significnt bcteriuri (13 of 23 [61%]). This difference did not rech significnt level (P = 0.07), but mny urine cultures were not vilble for serotyping. The body coloniztion of these ptients with P. eruginos ws only prtilly influenced by the durtion of hospitl sty. Mny ptients dmitted to Rncho Los Amigos Hospitl, Downey, Clif., were lredy colonized with P. eruginos (5). Mny of these ptients hd lredy spent time t cute hospitls in intensive cre units nd hd cquired P. eruginos t those hospitls. There ws no increse in the coloniztion of these ptients in reltion to length of hospitl sty, except tht urethrl coloniztion incresed fter 4 weeks. This ws ssocited with incresed use of n externl urinry collection system, since reflex voiding usully occurs fter 4 weeks. In ddition, however, there ws chnge in serotype with durtion of hospitl sty. Serotype 11 ws endemic t TABLE 8. P. eruginos serotypes No. of isoltes of serotype: Yr 1 2 3 4 5 6 8 9 10 11 12 15 Mlil Multiple NT Urethr 1976 1 1 1 1 6 2 1977 1 1 1 9 3 1 1978 1 1 1 1 3 12 2 1 1979 1 4 3 7 3 3 1980 1 1 3 1 1 2 1 4 Perineum 1976 1 1 1 1 1 14 2 3 1977 1 2 11 1 2 1978 1 2 1 1 1 2 16 1 1 4 1979 1 1 4 3 5 4 2 1980 2 3 3 1 5 1 1 1 2 1 Rectum 1976 1 1 1 1 8 2 5 1977 2 1 9 1 2 1 1978 2 3 1 1 1 2 9 1 2 1 1979 1 3 3 1 4 2 4 1980 2 1 2 2 1 1 1 No isoltes of serotypes 7, 13, or 14 were found. b NT, Not typble.
860 GILMORE ET AL. J. CLIN. MICROBIOL. TABLE 10. P. eruginos strins susceptible to ntibotics No. (%) of susceptible strins/ Antibiotic 1976 1977 1978 1979 1980 Crbenicillin 2/5 (40) 23/33 (55) 19/33 (58) 20/31 (65) 24/31 (77) Gentmicin 4/5 (80) 18/22 (82) 21/33 (64) 24/31 (77) 24/31 (77) Tobrmycin 4/5 (80) 19/22 (86) 31/33 (94) 28/31 (90) 26/31 (84) Amikcin 4/5 (80) 19/22 (86) 32/33 (97) 28/31 (90) 31/31 (100) Rncho Los Amigos Hospitl nd becme the predominnt serotype with incresing hospitl sty. We cn only speculte s to why the use of n externl urinry collection system influences coloniztion. Others hve shown tht grmnegtive bcilli my persist more redily nd show mrked increse in number in continuously moist, occluded res on the skin (3). Such n re of skin on the penis is creted by continuous use of n externl urinry collection system. We hve shown tht coloniztion of the perinel skin is ssocited with n increse in ph on the skin (D. S. Gilmore, D. G. Schick, nd J. Z. Montgomerie, Abstr. Annu. Meet. Am. Soc. Microbiol. 1982, B3, p.18). The mount of P. eruginos coloniztion nd the serotypes were episodic, with some decrese in the incidence of P. eruginos urinry trct infections nd coloniztion over the 5 yers. In 1977, the dringe system on the bed ws chnged dily, which my hve ccounted for some reduction in P. eruginos urinry trct infections, lthough it did not significntly chnge the prevlence of body coloniztion. Over these yers, there ws lso incresing infection surveillnce, improved inservice trining for nursing nd medicl personnel, nd improved techniques, which my lso hve influenced the incidence of urinry trct infection. During the 5 yers, some ttempts were mde to influence the coloniztion of these ptients with P. eruginos. A study ws crried out to TABLE 11. Antibiotic susceptibility of dominnt serotypes Antibiotic No. (%) of susceptible strins/ Serotype 11 Serotype 6 Serotype 4 Crbenicillin 19/39 (49) 10/13 (77) 5/12 (42) Gentmicin 31/39 (79) 11/13 (85) 5/12 (42) Tobrmycin 37/39 (95) 13/13 (100) 6/12 (50) Amikcin 36/39 (92) 12/13 (92) 11/12 (92) determine whether coloniztion of ptients with P. eruginos could be reduced by discontinuing the use of externl urinry collection systems t night. Removl of externl urinry collection systems t night significntly reduced the rtes of urethrl coloniztion with P. eruginos, but did not lter the rtes of perinel or rectl coloniztion (unpublished observtions). In tht study, ptient prticiption ws difficult to mintin becuse of number of wet beds. Urine spills from urinls were frequent becuse of body spsms. In lter study, we exmined the effect of bthing on P. eruginos coloniztion. Meticulous bthing with regulr bth sops did not lter long-term coloniztion of the perineum (2). Further studies will be necessry to understnd nd lter the pttern of P. eruginos coloniztion nd urinry trct infection in SCI ptients. ACKNOWLEDGMENTS We cknowledge the technicl ssistnce of Glori Aeilts, Brbr Alldis, Mry Ashley, Jenette Rockenmcher, Anitr Wirtz, nd Mny N. Young. We lso cknowledge Jen Lloyd for her ssistnce nd secretril help in the preprtion of the mnuscript. Support ws supplied for these studies by the Ntionl Institute for Hndicpped Reserch Foundtion (no. 13-P- 59174) nd the Weingrt Foundtion. LITERATURE CITED 1. Buer, A. W., W. M. Kirby, J. C. Sherris, nd M. Turck. 1966. Antibiotic susceptibility testing by stndrdized single disk method. Am. J. Clin. Pthol. 45:493-4%. 2. Gilmore, D. S., E. M. Jimenez, G. D. Aelits, B. A. AIldis, S. K. Bruce, D. G. Schick, J. W. Morrow, nd J. Z. Montgomerie. 1982. Effects of bthing on coloniztion of spinl cord injury ptients with Pseudomons nd Klebsiell. J. Clin. Microbiol. 14:404-407. 3. Mrples, R. R. 1965. The effect of hydrtion on the bcteril flor of the skin, p. 33-41. In H. I. Mibch nd G. Hicdick-Smith (ed.), Skin bcteri nd their role in infection. McGrw-Hill Book Co., New York. 4. Montgomerie, J. Z., nd J. W. Morrow. 1978. Pseudomons coloniztion in ptients with spinl cord injury. Am. J. Epidemiol. 108:326-336. 5. Montgomerie, J. Z., nd J. W. Morrow. 1980. Long-term Pseudomons coloniztion in spinl cord injury. Am. J. Epidemiol. 112:508-517.