Cefazolin in the Treatment of Acute Enteric Fever
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1 ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, JUIY 1976, p Copyright American Society for Microbiology Vol. 10, No. 1 Printed in U.S.A. Cefazolin in the Treatment of Acute Enteric Fever MARWAN UWAYDAH' Departments of Medicine and Bacteriology and Virology, American University Hospital, Beirut, Lebanon Received for publication 11 November 1975 Cefazolin was used in the treatment of nine patients with acute enteric fever proven by positive blood cultures. In seven patients the causative organism was Salmonella typhi and in two it was Salmonella paratyphi B. Minimal inhibitory and minimal bactericidal concentrations of cefazolin against the nine isolates ranged between 1.95 and 3.90,g/ml. Cefazolin was administered either intramuscularly or intravenously in a daily dose of 3 to 6 g for 11 to 16 days. The mean peak serum antibiotic concentration after a 0.5-g intravenous injection was 64.4,mg/ml, and the mean trough concentration, 3 h later, was 12.7,ug/ml. The highest serum inhibitory dilution at peak level was frequently 1/e4, and at trough level it was 1/16 to 1/32. The acute infection was satisfactorily controlled in all patients. Phlebitis, complicating intravenous therapy, in five out of eight patients, was the only side effect observed. Relapse oftyphoid fever, as documented by positive blood culture, occurred in one patient 11 days after treatment course was completed. More extensive clinical studies are required before drawing any conclusions regarding the efficacy of cefazolin in acute enteric fever. Interest in the antimicrobial therapy of acute enteric fever has been revived after the occurrence of outbreaks caused by chloramphenicolresistant Salmonella typhi in Mexico, the United States, and other parts of the world (1, 4, 11). Only two additional antimicrobial agents, ampicillin and cotrimoxazole, are generally considered useful in the treatment of this infection (8, 17). Recently, Pillay et al. claimed amoxycillin to be another alternative therapeutic agent (12). Some of the chloramphenicolresistant S. typhi isolates were also found to be resistant to ampicillin and sulfonamides (1, 11), and it is uncertain whether cotrimoxazole will prove effective in infections caused by organisms highly resistant to sulfonamides. It is a well-recognized, yet poorly understood, fact that not all antimicrobial agents active in vitro against S. typhi or S. paratyphi are necessarily effective in the treatment of the clinical disease (5, 8). This lack of correlation between the results of the in vitro and the in vivo studies may have been related to a number of factors, including the patterns of serum antibacterial activity achieved with the dosage regimens used. The possibility that inadequate serum antibiotic concentration was an important cause of the relatively high incidence of treatment failures reported with oral, but not parenteral, ampicillin therapy has not been alto- ' Address reprint requests to: Dr. Marwan Uwaydah, c/o Dr. Morton Swartz, Chief, Infectious Disease Unit, Massachusetts General Hospital, Boston, MA gether excluded (9, 11, 14). These issues and their practical implications have been discussed previously (16). Cefazolin, when compared with other cephalosporin antibiotics, has been demonstrated to yield significantly higher and better sustained blood levels after either intramuscular (i.m.) or intravenous (i.v.) administration (10). Preliminary in vitro studies conducted in this laboratory have shown that the minimal inhibitory concentrations (MIC) of this antibiotic against eleven locally isolated strains of chloramphenicol and ampicillin-susceptible S. typhi and S. paratyphi B ranged between 0.80 and 3.12,Ag/ ml, suggesting that very high serum antibacterial activity against salmonellae may be expected in patients receiving the recommended antibiotic dosage. The purpose of this study was to evaluate the efficacy of cefazolin in the treatment of acute enteric fever, as monitored by serum antibiotic level and serum inhibitory activity determinations. MATERIALS AND METHODS Only patients with acute enteric fever, proven by positive blood cultures, were selected for this study. Blood for culture was collected in tryptose phosphate broth (BBL), and bottles were incubated at 37 C. Rectal swabs were streaked on salmonella-shigella (BBL) and MacConkey agar (Difco) plates and were inoculated in Selenite cystine broth (BBL). Final identification of Salmonella was based on carbohydrate fermentation patterns and slide agglutination tests, according to standard procedures (6). Suscep- 52
2 VOL. 10, 1976 tibility of isolates to cefazolin, ampicillin, and chloramphenicol was determined by the Kirby-Bauer disk agar diffusion technique (3) and by the serial twofold dilution technique in Mueller-Hinton broth (BBL) (7), using as an inoculum a 10-4 dilution of overnight broth culture (final concentration, approximately 105 organisms/ml). After overnight incubation, the lowest antibiotic concentration inhibiting visible growth was recorded as the MIC value. All clear tubes were subcultured on Mac- Conkey agar plates using a 0.01-ml calibrated loop. The lowest concentration from which no more than one colony grew was considered as the minimal bactericidal concentration. Cefazolin (Kefzol, Eli Lilly & Co.) was administered either i.v. or i.m. in a daily dose of 3 to 6 g. Treatment was continued for 11 to 16 days, and patients were examined daily for evaluation of their clinical response. Blood cultures were obtained from all patients 6 and 24 h after initiating antibiotic therapy and whenever indicated thereafter. Blood samples were obtained from every patient on two or three different occasions during treatment for determining serum cefazolin concentrations and serum antibacterial activity against the infecting organism. On every occasion, two blood samples were collected to detect peak levels (10 to 15 min after the i.v. dose and 60 min after the i.m. dose) and trough levels (just before the next dose). Assay of cefazolin concentrations was performed by the two-layer cylinder-plate method using antibiotic medium 5 (Difco) after adjusting its ph to 6.0. A Bacillus 8ubtili8 spore suspension (Difco) served as the test organism. Serum antibacterial activity was determined by the twofold dilution technique (2). For comparative purposes, both pooled normal human serum and Mueller-Hinton broth (BBL) were used as diluents. The inoculum was a 1O-4 dilution of an overnight broth culture (final concentration, approximately 105 organisms/ml). After overnight incubation, the highest serum dilution inhibiting visible growth was recorded. Clear tubes were subcultured on MacConkey agar plates using a 0.01-ml calibrated loop. The highest dilution from which no more than one colony grew was regarded as the highest bactericidal dilution. Other laboratory tests done on every patient before, during, and after the treatment course included urinalysis, complete blood count, blood urea nitrogen, and serum creatinine. In addition, serum electrolyte and liver function tests were done whenever indicated. RESULTS Patients. Nine patients, five females and four males, ranging in age between 15 and 32 years, were selected for this trial. All presented with the classic clinical picture of acute enteric fever. The duration of the febrile illness prior to initiating antibiotic therapy varied between 4 and 12 days, and the peak temperatures ranged between 39.7 and 41.0 C. Pretreatment blood cultures from seven patients grew S. typhi, and from the other two S. paratyphi B grew. Serum CEFAZOLIN FOR TREATING ACUTE ENTERIC FEVER 53 creatinine values were normal in all subjects. Leukocyte counts were either normal or low, consistent with the diagnosis of acute enteric fever. None of the patients showed evidence of intestinal hemorrhage or perforation. In vitro susceptibility tests. All Salmonella isolates recovered from the nine patients proved to be susceptible to cefazolin, ampicillin, and chloramphenicol. The results of inhibition zone sizes, together with MIC and minimal bactericidal concentration values of the three antibiotics against the nine isolates, are given in Table 1. It is clear that the inhibitory concentrations are readily achievable in sera of patients receiving the regularly recommended dosages of any of the three antibiotics. In contrast to the bacteriostatic effect of chloramphenicol, the bactericidal effects of cefazolin and ampicillin were demonstrated by MIC and minimal bactericidal concentration values that were essentially identical. Treatment regimens. In eight patients, cefazolin was administered initially by the i.v. route. In four patients this was continued until treatment was completed, but in the rest the occurrence of severe pain necessitated a change to the i.m. route 8 to 14 days after starting therapy. One patient received the antibiotic i.m. throughout the entire treatment course. Probenicid was given to one patient (number 8) in a dose of 0.5 g every 6 h, starting on day 6 of cefazolin therapy. The details of the antibiotic regimens are summarized in Table 2. Serum cefazolin concentrations and serum antibacterial activity. Serum peak and trough cefazolin concentrations and highest serum bacteriostatic and bactericidal dilutions are outlined in Table 2. The mean peak serum cefazolin concentration after a 0.5-g i.v. injection was 64.4,ug/ml and the mean trough concentration, 3 h later, was 12.7 ug/ml. Thus, serum antibiotic concentration was continuously maintained well above the MIC value against the infecting organism. This was also confirmed by the results of serum inhibitory activity determinations. The serum inhibitory dilution (static effect) at peak level was frequently 1/64, and at trough level it was either 1/16 or 1/ 32. Serum antibacterial activity was more pronounced when the samples were diluted in pooled normal serum rather than in broth. This may be attributed to the nonspecific inhibitory factors present in normal serum, which itself produced bacteriostatic and bactericidal effects in a dilution of 1/4 (in broth). The mean serum cefazolin concentration after a 1.0-g i.v. dose was about twice that obtained with a 0.5-g dose. The only exception was encountered in the first
3 54 UWAYDAH ANTIMICROB. AGENTS CHZMOTHZR. TABLz 1. Susceptibility of seven S. typhi and two S. paratyphi B isolates to cefazolin, ampicillin, and chloramphenicol as determined by disk agar and broth dilution techniques Cefazolin AmpicillUn Chloramphenicol Pa- Zone Zone Zone tient Organism size MIC MBCa size MIC MBC size MIC MBCb tient(mm; (,ug/ (Agl (mm; (Ag/ (/g/ (mm; (^gg (ILgg 30-,ug ml) ml) 1O-;sg ml) ml) 30-;Lg ml) ml) disk) disk) disk) 1 S. typhi S. typhi S. typhi S. paratyphi B S. typhi S. typhi S. typhi S. paratyphi B S. typhi a MBC, Minimal bactericidal concentration. b Values may represent concentrations required to carry over enough chloramphenicol in the inoculum to the plate to inhibit growth thereon, and thus they do not necessarily indicate true "bactericidal" activity. TABLz: 2. Dosage regimen, peak and trough serum antibiotic concentrations, and serum antibacterial activity determinations in nine enteric fever patients treated with cefazolin Serum antibacterial activity (reciprocal) Cefazolin se- Pa- Treat- rum concn (jlg/ Diluent-broth Diluent-normal serum en ~~~~ Peak Trough Peak Trough tient Dosage regimen ment ml) ~~~~~day Peak Trough Static Cidal Static Cidal Static Cidal Static Cidal g i.v. every 3 h for days; then 0.5 g i.m every 6 h for 2 days g i.v. every 3 h for days; then 0.5 g i.m every 6 h for 1 day g i.v. every 3 h for days; then 0.5 g i.m every 6 h for 4 days g i.v. every 3 h for days; then 1.0 g i.v. ev ery 4 h for 4 days g i.v. every 4 h for days g i.v. every 4 h for days; then 1.0 g i.m every 6 h for 4 days g i.v. every 4 h for days g i.v. every 4 h for days 7a lla g i.m. every 4 h for days a Patient was receiving 0.5 g of probenicid by mouth every 6 h. sample from patient 7. Trough antibiotic con- biotic concentration and inhibitory activity (pacentrations 4 h after injection varied widely, tient 8, samples 2 and 3). but adequate inhibitory activity was main- Response to therapy and post-treatment tained. Administration of probenicid resulted follow-up. The acute infection was satisfactoin substantially increased trough serum anti- rily controlled in all nine patients. Details per-
4 VOL. 10, 1976 taining to clinical illness and response to therapy are outlined in Table 3. Definite subjective improvement was consistently observed within 2 to 3 days of antibiotic treatment. All blood cultures taken 6 and 24 h after beginning therapy remained sterile. The first drop in rectal temperature to 37.9 C or less occurred within 2 to 8 days, with a mean interval of 4.3 days. Three patients who did not develop frank evidence of phlebitis at the i.v. injection site and ofie patient who received the antibiotic by the i.m. route alone remained completely afebrile after 3 to 11 days of treatment, with a mean interval of 6.5 days. The other patients continued to have irregular spikes of fever which persisted until phlebitis subsided, indicating that this was probably the cause, particularly since all systemic symptoms related to the typhoidal illness were absent and repeated blood cultures were negative. No other side effects of cefazolin were noted. After discontinuation of treatment, all patients were followed-up for a period of 5 to 8 weeks. Relapse of typhoid fever, as documented by positive blood culture, occurred in one patient (number 1) 11 days after the treatment course was completed. The relapse was successfully controlled with cotrimoxazole. There was no change in the in vitro susceptibility pattern of the S. typhi isolated during the relapse as compared to that recovered previously. The other patients remained afebrile and asymptomatic. Rectal swabs for stool cultures were obtained on single occasions from seven patients 2 to 3 weeks after treatment was completed, and all were negative for salmonellae. DISCUSSION Of the several cephalosporin antibiotics available for clinical use, none had been shown CEFAZOLIN FOR TREATING ACUTE ENTERIC FEVER to be of therapeutic value in enteric fever. The results of this preliminary study indicate that cefazolin is effective in controlling the infection, since all nine patients studied responded satisfactorily to this antibiotic. Only one patient showed a relapse within the follow-up period of 5 to 8 weeks. Phlebitis complicating i.v. therapy in five out of eight patients was the only untoward effect observed. This precluded the use of the temperature curve as a reliable index for evaluating treatment response. The reasons for the superior efficacy of chloramphenicol over other antimicrobial agents in the treatment of enteric fever have not been elucidated. A noticeable characteristic of this antibiotic is its prolonged serum half-life, so that dosage administration every 6 to 8 h results in its accumulation (15). This might suggest that well-sustained serum antibacterial activity is advantageous for satisfactory control of the typhoidal infection. Studies conducted in this laboratory on typhoid patients receiving chloramphenicol in a dose of 750 mg by mouth every 6 h revealed that the peak inhibitory serum dilution was 1/16 to 1/32 and the trough inhibitory dilution was 1/8 to 1/16. These results are similar to the data obtained with cefazolin reported in this study, although the peak inhibitory activity produced by cefazolin was frequently higher. The relative efficacy of cefazolin in acute enteric fever and specific recommendations regarding its optimal dosage regimen should await more extensive studies that would consider, among other parameters, the incidence of the chronic carrier state after acute infection. In this respect, cefazolin offers the advantage of reaching bile in very high concentrations (13). Possibly, the high frequency and severity of troublesome phlebitis complicating treatment vv TABLE 3. Clinical and bacteriological responses in nine enteric fever patients treated with cefazolin D Duration of Duration of Duration of Duration treatment treatment treatment Blood cultures ob- Pa- Age Sex of illness before sub- before first before com- tained after start- Phlebitis tient (yr) treatment jective im- tal temp to plete defer- ing treatment (all C o escence negative) trm(den) provement val (ays) noted (days) 37.9 Cor less v(days) (dys) 1 32 M h, days Present 2 17 M h, days Absent 3 15 F h, day 2 Absent 4 20 F h, days Present 5 15 F h, day 2 Present 6 17 M h, days Present 7 20 M h, day 2 Absent 8 29 F h, days Present 9 15 F h, days (Cefazolin admin- I I istered i.m.)
5 56 UWAYDAH may be reduced by using different methods of parenteral administration. The value of probenicid in maintaining high trough serum antibacterial activity should be weighed against the possible side effects of this drug. Determinations of serum antibiotic concentration and serum antibacterial activity should reveal useful information for monitoring therapy. The procedure for determining serum inhibitory activity requires better standardization in respect to technical details and interpretation of static and cidal end points (2). If this could be established, the test may serve to lay down general guidelines for predicting whether an antimicrobial agent is likely to be effective in enteric fever and in what dosage regimen it should be used, as indicated by the MIC value against the infecting organism and the pharmacokinetic characteristics of the drug in question. ACKNOWLEDGMENTS I thank Shak6 Albarian for exellent technical assistance. Cefazolin (Kefzol) used in this study was supplied by Eli Lilly & Co., Beirut, Lebanon. LITERATURE CITED 1. Anderson, E. S., and H. R. Smith Chloramphenicol resistance in the typhoid bacillus. Br. Med. J. 3: Barry, A. L., and L D. Sabath Special tests: bactericidal activity and activity of antimicrobics in combination, p In E. H. Lennette, E. H. Spaulding, and J. P. Truant (ed.), Manual of clinical microbiology, 2nd ed. American Society for Microbiology, Washington, D.C. 3. Bauer, A. W., W. M. M. Kirby, J. L. Sherris, and M. Turek Antibiotic susceptibility testing by a standaized single disk method. Am. J. Clin. Pathol. 45: Butler, T., N. N. Linh, K. Arnold, and M. Pollack Chloramphenicol-resistant typhoid fever in ANTIMICROB. AGENTS CHEMOTHER. Vietnam associated with R factor. Lancet 2: Dawkins, A. T., Jr., and R. B. Honick Evaluation of antibiotics in a typhiod model, p Antimicrob. Agents Chemother Edwards, P. R., and W. H. Ewing Identification of Enterobacteriaceae, 3rd ed. Burgess Publishing Co., Minneapolis. 7. Ericson, H. M., and J. C. Sherris Antibiotic sensitivity testing. Report of an international collaborative study. Acta Pathol. Microbiol. Scand. Suppl. 217: Garrod, L. P., H. P. Lambert, and F. O'Grady Antibiotic and chemotherapy, 4th ed. Churchill Livingstone, Edinburgh. 9. Kaye, D., H. Rocha, L. Eyckmans, A. Prata, and E. W. Hook Comparison of parenteral ampicillin and parenteral chloramphenicol in the treatment of typhoid fever. Ann. N.Y. Acad. Sci. 145: Kirby, W. M. M., and C. Reganey. Pharmacokinetics ofcefazolin compared with four other cephalosporins. J. Infect. Dis. 128(Suppl.):S341-S Overturf, G., K. I. Marton, and A. W. Mathies, Jr Antibiotic resistance in typhoid fever. chloramphenicol resistance among clinical isolates of SalmoneUa typhowa in Los Angeles, Epidemiologic and bacteriologic characteristics. N. Engl. J. Med. 289: Pillay, N., E. B. Aams, and D. North-Coombes Comparative trial of amoxycillin and chloramphenicol in treatment of typhoid fever in adults. Lancet 2: Ram, M. D., and S. Watanatittan Levels of cefazolin in human bile. J. Infect. Dis. 123(Suppl.):S361- S Robertson, R. P., M. F. Abdel-Wahab, and F. 0. Raach Evaluation of chloramphenicol and ampicillin in salmonella enteric fever. N. Engl. J. Med. 278: Snyder, M. J., and T. E. Woodward The clinical use of chloramphenicol. Med. Clin. North Am. 54: Uwaydah, M Choice of antimicrobial agents in enteric fever. J. Antimicrob. Chemother. 1: Uwaydah, M., R. Matosian, and M. Balabanian Cotrimoxazole compared to chloramphenicol in the treatment of enteric fever. Scand. J. Infect. Dis. 7:
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