Summary
This review focuses on published information on the experimental as well as clinical data on the emergence of quinolone resistant isolates. In the course of clinical use of fluoroquinolones, only a sporadic emergence of quinolone resistance has been noted. The resistant organisms emerged particularly in certain clinical settings where large numbers of organisms frequently causing chronic infections are present and/or in loci where quinolone concentrations may not be optimal. In terms of occurrence in individuals, quinolone resistance has emerged most frequently in hospitalized and nursing-home patients with identifiable risk factors. Epidemiological studies revealed that in nearly all the cases studied one or one predominating quinolone resistant clone was selected that was horizontally transmitted. Thus, the emergence of quinolone resistance is not due to an independent selection of resistant strains in a number of patients, but to the clonal spread of one strain once it has acquired quinolone resistance. Therefore, the rate of quinolone resistance is very likely to be lower than reported.
Zusammenfassung
Die publizierten präklinischen sowie klinischen Daten zur Chinolonresistenz sind synoptisch dargestellt. Im Verlauf der klinischen Anwendung von Fluorochinolonen wurde bislang nur sporadisch das Auftreten Chinolon-resistenter Stämme beobachtet. Diese resistenten Stämme traten vor allem unter solchen klinischen Bedingungen auf, unter denen entweder hohe Bakterienzellzahlen chronische Infektionen verursachen und/oder in solchen Infektlokalisationen, in denen die Chinolonkonzentrationen nicht optimal sein können. Bezogen auf die individuelle Wahrscheinlichkeit des Auftretens Chinolon-resistenter Stämme treten diese vorrangig in hospitalisierten Patienten oder Pflegeheimbewohnern mit identifizierbaren Risikofaktoren auf. Epidemiologische Studien ergaben, daß in nahezu allen untersuchten Fällen ein oder ein vorherrschender Chinolon-resistenter Klon selektiert worden war, der sich anschließend horizontal ausbreitete. Somit ist das Auftreten einer Chinolonresistenz nicht auf eine unabhängige Selektion einer Vielzahl resistenter Stämme in entsprechend vielen Patienten zurück-zuführen, sondern vielmehr auf eine klonale Ausbreitung eines einzigen Stammes sobald dieser eine Chinolonresistenz erworben hat. Folglich ist die Rate der Chinolonresistenz sehr wahrscheinlich geringer als publiziert.
Similar content being viewed by others
References
Kresken, M., Wiedemann, B. Development of resistance to nalidixic acid and the fluoroquinolones after the introduction of norfloxacin and ofloxacin. Antimicrob. Agents Chemother. 32 (1988) 1285–1288.
Wiedemann, B., Zühlsdorf, M. T. Brief report: resistance development to fluoroquinolones in Europe. Am. J. Med. 87 (Suppl. 5A) (1989) 9–11.
Kresken, M., Hafner, D., Mittermayer, H., Verbist, L., Bergogne-Bérézin, E., Giamarellou, N., Esposito, S., Van Klingeren, B., Kayser, F. N., Reeves, D. and Study Group of the Paul Ehrlich Society for Chemotherapy, European Study Group ‘Bacterial Resistance’: Prevalence of antibiotic resistance in Europe, 1990. 6th European Congress of Clinical Microbiology and Infectious Diseases, March 1993, Seville, Abstract No. 308.
Kresken, M., Haftner, D. and Study Group of the Paul Ehrlich Society for Chemotherapy, European Study Group ‘Bacterial Resistance’: Development of resistance to fluoroquinolones between 1983 and 1990 in central Europe. 6th European Congress of Clinical Microbiology and Infectious Diseases, March 1993, Seville, Abstract No. 1046.
Focht, J., Kraus, H., Nosner, K.: Comparativein vitro activity of ofloxacin and other antimicrobial agents used in oral therapy in general practice during the years 1985–1991. 4th International Symposium on New Quinolones, Munich, August 1992, Abstract No. 7.
Grimm, H.: Resistance trend of ofloxacin and ciprofloxacin: monitoring of more than 300,000 strains in the last 5 years. 3rd Int.Symp. New Quinolones, Vancouver, July 1990, Abstract No. 94.
Tillotson, G. S., Culshaw, K. D., O'Keefe, B. J. O.: Longitudinal survey of ciprofloxacin susceptibility in the UK: 5 years' experience. 4th International Symposium on New Quinolones, Munich, August 1992, Abstract No. 10.
Wolff, M., Buré, A., Pathé, J. P., Pangon, B., Regnier, B., Rouger-Barbier, D., Vachon, F. Evolution des résistances bactériennes à la péfloxacin dans le service de réanimation de l'hôpital Claude-Bernard. In:Pocidalo, J. J., Vachon, F., Regnier, B. (eds): Les nouvelles quinolones. Paris, Editions Arnette 1985, pp. 213–226.
Acar, J. F., Francoual, S. The clinical problems of bacterial resistance to the new quinolones. J. Antimicrob. Chemother. 26 (Suppl. B) (1990) 207–213.
Wadsworth, S. J., Kim, Ki-Ho., Satischandran, V., Axelrod, P., Truant, A. L., Suh, B. Development of new antibiotic resistance in methicillin-resistant but not methicillin-susceptibleStaphylococcus aureus. J. Antimicrob. Chemother. 30 (1992) 821–826.
Schuster, F. X., Holzmann, R. M., Schmidbauer, G. P., Porpaczy, P.: Comparativein vitro activity of ofloxacin and other orally absorbed antimicrobial agents against more than 7,000 urinary tract bacterial pathogens. Eur. Congr. Clin. Microbiol., Nice 1989, Abstract No. 2.
Shalit, I., Haas, H., Berger, S. A. Susceptibility ofPseudomonas aeruginosa to fluoroquinolones following 4 years of use in a tertiary care hospital. J. Antimicrob. Chemother. 30 (1992) 149–152.
Fernandez, P. B., Hanson, C. W., Stamm, J. M., Vojtko, C., Shipkowitz, N. L., Martin, E. St. The frequency ofin vitro resistance development to fluoroquinolones and the use of murine pyelonephritis model to demonstrate selection of resistancein vivo. J. Antimicrob. Chemother. 19 (1987) 449–465.
Michéa-Hamzehpour, M., Auckenthaler, R., Regamey, P., Pechère, J. C. Resistance occurring after fluoroquinolone therapy of experimentalPseudomonas aeruginosa peritonitis. Antimicrob. Agents Chemother. 31 (1987) 1803–1808.
Bayer, A. S., Hirano, L., Yin, J. Development of β-lactam resistance and increased quinolone MICs during therapy of experimentalPseudomonas aeruginosa endocarditis. Antimicrob. Agents Chemother. 32 (1988) 231–235.
Bayer, A. S., Blomquist, J. K., Kim, K. S. Ciprofloxacin in experimental aortic valve endocarditis due toPseudomonas aeruginosa. J. Antimicrob. Chemother. 17 (1986) 641–649.
Chamberland, S., Bayer, A. S., Schollardt, T., Wong, S. A., Bryan, L. E. Characterization of mechanisms of quinolone resistance inPseudomonas aeruginosa strains isolatedin vitro andin vivo during experimental endocarditis. Antimicrob. Agents Chemother. 33 (1989) 624–634.
Gordin, F. M., Hackbarth, C. J., Scott, K. G., Sande, M. A. Activities of pefloxacin and ciprofloxacin in experimentally inducedPseudomonas aeruginosa in neutropenic guinea pigs. Antimicrob. Agents Chemother. 27 (1985) 452–454.
Scribner, R. K., Welche, D. F., Marks, M. J. Low frequency of bacterial resistance to enoxacinin vitro and in experimental pneumonia. J. Antimicrob. Chemother. 16 (1985) 597–603.
Kemmrich, B., Small, G. J., Pennington, J. E. Comparative evaluation of ciprofloxacin, enoxacin and ofloxacin in experimentalPseudomonas aeruginosa pneumonia. Antimicrob. Agents Chemother. 29 (1986) 395–399.
Bamberger, D. M., Peterson, L. R., Gerding, D. N., Fasching, C. E. Ciprofloxacin, azlocillin, ceftizoxime, and amikacin alone and in combination against gram-negative bacilli in an infected chamber model. J. Antimicrob. Chemother. 18 (1986) 51–63.
Norden, C. W., Shinner, E. Ciprofloxacin as therapy for experimental osteomyelitis caused byPseudomonas aeruginosa. J. Infect. Dis. 151 (1985) 291–294.
Dworkin, R., Modin, G., Kunz, S., Rich, R., Zak, O., Sande, M. Comparative efficacies of ciprofloxacin, pefloxacin and vancomycin in combination with rifampicin in a rat model of methicillin-resistantStaphylococcus aureus chronic osteomyelitis. Antimicrob. Agents Chemother. 34 (1990) 1014–1016.
Henry, N. K., Rouse, M. S., Whitesell, A. L., McConnell, M. E., Wilson, W. Treatment of methicillin-resistantStaphylococcus aureus experimental osteomyelitis with ciprofloxacin or vancomycin alone or in combination with rifampin. Am. J. Med. 82 (Suppl. 4A) (1987) 73–75.
Lucain, C., Regamy, C., Bellido, F., Pechère, J. C. Resistance emerging after pefloxacin therapy of experimentalEnterobacter cloacae peritonitis. Antimicrob. Agents Chemother. 33 (1989) 937–943.
Roosendaal, R., Bakker-Woudenberg, I. A. J. M., van den Berghevan Raffe, M., van den Berg, J. C. V., Michel, M. F. Comparative studies of ciprofloxacin und ceftazidime againstKlebsiella pneumoniae in vitro and in experimental pneumonia in leukopenic rats. Antimicrob. Agents Chemother. 31 (Suppl. 11) (1987) 1809–1815.
Thauvin, C. L., Lecomte, F., Le Boete, I., Grise, G., Lemeland, J. F. Efficacy of ciprofloxacin alone and in combination with azlocillin in experimental endocarditis due toPseudomonas aeruginosa. Infection 17 (Suppl. 1) (1989) 31–34.
Kaatz, G. W., Barriere, S. L., Schaberg, D. R., Fekety, R. The emergence of resistance to ciprofloxacin during treatment of experimentalStaphylococcus endocarditis. J. Antimicrob. Chemother. 20 (1987) 753–758.
Kaatz, G. W., Seo, S. M., Ruble, C. A. Mechanisms of fluoroquinolone resistance inStaphylococcus aureus. J. Infect. Dis. 163 (1991) 1080–1086.
Kaatz, G. W., Barriere, S. L., Schaberg, D. R., Fekety, R. Ciprofloxacin versus vancomycin in the therapy of experimental methicillin-resistantStaphylococcus aureus endocarditis. Antimicrob. Agents Chemother. 31 (1987) 527–530.
Fernandez-Guerrero, M., Rouse, M., Henry, N., Wilson, W. Ciprofloxacin therapy of experimental endocarditis caused by methicillin-susceptible or methicillin-resistantStaphylococcus aureus. Antimicrob. Agents Chemother. 32 (1988) 747–751.
Kaatz, G. W., Seo, S. M., Barriere, S. L., Albrecht, L. M., Rybak, M. J. Development of resistance to fleroxacin during therapy of experimental methicillin-susceptibleStaphylococcus aureus endocarditis. Antimicrob. Agents Chemother. 35 (1991) 1547–1550.
Thauvin, C., Lemeland, J. F., Humbert, G., Fillastre, J. P. Efficacy of pefloxacin-fosfomycin in experimental endocarditis caused by methicillin-resistantStaphylococcus aureus. Antimicrob. Agents. Chemother. 32 (1988) 919–921.
Davey, P., Barza, M., Stuart, M. Tolerance ofPseudomonas aeruginosa to killing by ciprofloxacin, gentamicin and imipenemin vitro andin vivo. J. Antimicrob. Chemother. 21 (1988) 395–404.
Kaatz, G. W., Seo, S. M., Ruble, C. A. Mechanisms of fluoroquinolone resistance inStaphylococcus aureus. J. Infect. Dis. 163 (1991) 1080–1086.
Schacht, P., Arcieri, G., Branolte, J., Bruck, H., Chysky, V., Griffith, E., Gruenwaldt, G., Hullmann, R., Konopka, C. A., O'Brien, B., Rahm, V., Ryoki, T., Westwood, A., Weuta, H. Worldwide clinical data on efficacy and safety of ciprofloxacin. Infection 16 (Suppl. 1) (1988) 29.
Ball, P. Emergent resistance to ciprofloxacin amongstPseudomonas aeruginosa andStaphylococcus aureus: clinical significance and therapeutic approaches. J. Antimicrob. Chemother. 26 (Suppl F.) (1990) 165–179.
Guibert, J. M., Distree, D. M., Acar, J. F. Ciprofloxacin (Bay 0 9867): clinical evaluation in urinary tract infections due toPseudomonas aeruginosa. Chemioterapia 6 (Suppl 2) (1987) 524–525.
Scully, B. E., Neu, H. C., Parry, M. F., Mandell, W. Oral ciprofloxacin therapy of infections due toPseudomonas aeruginosa. Lancet i (1986) 819–822.
Van Poppel, H., Wegge, M., Dammekens, H., Chysky, V. Oral treatment ofPseudomonas induced urinary tract infections with ciprofloxacin. Chemotherapy 32 (1986) 83–87.
Brown, E. M., Morris, R., Stephenson, T. P. The efficacy and safety of ciprofloxacin in the treatment of chronicPseudomonas aeruginosa urinary tract infection. J. Antimicrob. Chemother. 18 (Suppl D) (1986) 123–127.
Leigh, D. A., Emmanuel, F. X. S., Petch, K. J. Ciprofloxacin therapy in complicated urinary tract infections caused byPseudomonas aeruginosa and other resistant bacteria. J. Antimicrob. Chemother. 18 (Suppl D) (1986) 117–121.
Dalhoff, A. Clinical perspectives of quinolone resistance inPseudomonas aeruginosa. Antibiotic Chemother. Basel 44 (1991) 221–239.
Lesse, A. J., Freer, C., Salate, P. A., Francis, J.-B., Scheld, W. M. Oral ciprofloxacin therapy for gram-negative bacillary osteomyelitis. Am. J. Med. 82 (Suppl 4A) (1987) 247–253.
Gilbert, D. N., Tice, A. D., Marsh, P. K., Craven, P. C., Preheim, L. C. Oral ciprofloxacin therapy for chronic contiguous osteomyelitis caused by aerobic gram-negative bacilli. Am. J. Med. 82 (Suppl 1) (1987) 254–258.
Slama, T. G., Misinski, J., Sklar, S. Oral ciprofloxacin for osteomyelitis caused by aerobic gram-negative bacilli. Am. J. Med. 82 (Suppl 4A) (1987) 259–261.
Trexler-Hessen, M., Ingerman, M. J., Kaufman, D. H., Weiner, P., Santoro, J., Korzeniowski, O. M., Boscia, J., Topiel, M., Bush, L. M., Kaye, D., Levison, M. E. Clinical efficacy of ciprofloxacin therapy for gram-negative bacillary osteomyelitis. Am. J. Med. 82 (Suppl 4A) (1987) 262–265.
Daikos, G. L., Lolans, V. T., Jackson, G. G. Alterations in outer membrane proteins ofPseudomonas aeruginosa associated with selective resistance to quinolones. Antimicrob. Agents Chemother. 32 (1988) 785–787.
Piddock, L. J. V., Wijnands, W. J. A., Wise, R. Quinolone/ureidopenicillin cross-resistance. Lancet i (1987) 907.
Piddock, L. J. V., Hall, M. C., Bellido, F., Bains, M., Hancock, R. E. W. A pleiotropic, posttherapy, enoxacin-resistant mutant ofPseudomonas aeruginosa. Antimicrob. Agents Chemother. 36 (1992) 1057–1061.
Cherubin, C. E. Activity of amoxycillin clavulanic acid againstEscherichia coli in vivo. J. Antimicrob. Chemother. 30 (1992) 229–242.
Chin, N. Y., Clynes, N., Neu, H. C. Resistance to ciprofloxacin appearing during chemotherapy. Am. J. Med. 87 (Suppl 5A) (1989) 285–315.
Diver, J. M., Scholaardt, T., Rabin, H. R., Thorson, C., Bryan, L. E. Persistence mechanisms inPseudomonas aeruginosa from cystic fibrosis patients undergoing ciprofloxacin therapy. Antimicrob. Agents Chemother. 35 (1991) 1538–1546.
Masecar, B. L., Celesk, R. A., Robillard, N. J. Analysis of acquired ciprofloxacin resistance in a clinical strain ofPseudomonas aeruginosa. Antimicrob. Agents Chemother. 34 (1990) 281–286.
Hirai, K. I., Suzue, S., Irikua, S., Iyobe, S., Mitsuhashi, S. Mutations producing resistance to norfloxacin inPseudomonas aeruginosa. Antimicrob. Agents Chemother. 31 (1987) 582–586.
Jakics, E. V., Iyobe, S., Hirai, K., Fukuda, H., Hashimoto, H. Occurrence of the nfxB type mutation in clinical isolates ofPseudomonas aeruginosa. Antimicrob. Agents Chemother. 36 (1992) 2562–2565.
Chamberland, S., Malouin, F., Rabin, W. R., Schollardt, T., Parr, T. R., Bryan, L. E. Persistence ofPseudomonas aeruginosa during ciprofloxacin therapy of a cystic fibrosis patient: transient resistance to quinolones and protein F deficiency. J. Antimicrob. Chemother. 25 (1990) 995–1010.
Gotoh, N., Wakebe, H., Yoshihara, E., Nakae, T., Nishino, T. Role of protein F in maintaining structural integrity ofPseudomonas aeruginosa outer menbrane. J. Bacteriol. 171 (1989) 983–990.
Neu, H. C. Bacterial resistance to fluoroquinolones. Rev. Infect. Dis. 10 (Suppl. 1) (1989) 57–63.
LeBel, M. Fluoroquinolones in the treatment of cystic fibrosis: a critical appraisal. Eur. J. Clin. Microbiol. Infect. Dis. 10 (1991) 316–324.
Ogle, J. W., Reller, L. B., Vasil, M. L. Development of resistance inPseudomonas aeruginosa to imipenem, norfloxacin and ciprofloxacin during therapy: proof provided by typing with a DNA probe. J. Infect. Dis. 157 (1988) 743–748.
Döring, G., Hörz, M., Ortelt, J., Rössle, R., Wolz, C. Molecular epidemiology ofPseudomonas aeruginosa in an intensive therapy unit. Epidemiol. Infect. 110 (1993) 427–436.
Worlitzsch, D., Wolz, C., Botzenhart, K., Hansis, M., Burgdorfer, H., Ogle, J. W., Döring, G. Molecular epidemiology ofPseudomonas aeruginosa — urinary tract infections in paraplegic patients. Zbl. Hyg. 189 (1989) 175–184.
Naber, K. G., Witte, W., Bauernfeind, A., Wiedemann, B., Grimm, H. Resistenzentwicklung gegenüber Fluorochinolonen. Chemotherapie J. 2 (1993) 106–111.
Brumfitt, W., Hamilton-Miller, J. Methicillin-resistantStaphylococcus aureus. N. Engl. J. Med. 320 (1989) 1188–1196.
Aboukasm, A. G., Buu-Hoi, A. Y., el Solh, N., Morvan, A., Acar, J. F. Epidemiological study ofStaphylococcus aureus resistance to new quinolones in a university hospital. J. Hosp. Infect. 17 (1990) 25–33.
Humphreys, H., Mulvihill, E. Ciprofloxacin-resistantStaphylococcus aureus. Lancet 17 (1985) 383.
Milne, L. M., Faiers, M. C. Ciprofloxacin resistance in epidemic methicillin-resistantStaphylococcocus aureus. Lancet 8 (1988) 843.
Mulligan, M. E., Ruane, L., Johnston, L., Wong, P., Wheelock, J. P., MacDonald, K., Reinhardt, J.-F., Johnson, C. C., Statner, B., Blomquist, I., McCarthy, J., O'Brien, W., Gardner, S., Hammer, L., Citron, D. Ciprofloxacin for eradication of methicillin resistantStaphylococcus aureus colonization. Am. J. Med. 82 (1987) 215–219.
Valtonen, V., Karppinen, L., Kariniecni, A. L. A comparative study of ciprofloxacin and conventional therapy in the treatment of patients with chronic lower leg ulcers infected withPseudomonas aeruginosa and other gram-negative rods. Scand. J. Infect. Dis. (Suppl. 60) (1989) 79–83.
Weightman, N. C., Brass, A. S. Ciprofloxacin-resistant methicillin sensitiveStaphylococcus aureus. Antimicrob. Agents Chemother. 31 (1993) 179–180.
Kotilainen, P., Nikoskelainen, J., Huovinen, P. Emergence of ciprofloxacin-resistant coagulase-negative staphylococcal skin flora in immunocompromised patients receiving ciprofloxacin. J. Infect. Dis. 161 (1990) 41–44.
Oppenheim, B. A., Hartley, J. W., Lee, W., Burnie, J. P. Outbreak of coagulase-negativeStaphylococcus highly resistant to ciprofloxacin in a leukaemia unit. Br. Med. J. 299 (1989) 294–297.
Piercy, E. A., Barbaro, D., Luby, J. P., Mackowiak, P. A. Ciprofloxacin for methicillin-resistantStaphylococcus aureus infections. Antimicrob. Agents Chemother. 33 (1989) 128–130.
Smith, S. M., Eng, R. H. K., Bais, P., Fan-Havard, P., Teeson-Tumang, F. Epidemiology of ciprofloxacin resistance among patients with methicillin-resistantStaphylococcus aureus. J. Antimicrob. Chemother. 26 (1990) 567–572.
Schaefler, S. Methicillin-resistant strains ofStaphylococcus aureus resistant to quinolones. J. Clin. Microbiol. 27 (1989) 335–336.
Budnick, L. D., Schaefler, S. Ciprofloxacin-resistant methicillin-resistantStaphylococcus aureus in New York health care facilities, 1988. Am. J. Pub. Health 80 (1990) 810–813.
Peterson, L. R., Quick, J. N., Jensen, B., Homan, S. Johnson, S., Tenquist, J., Shanholtzer, C. Petzel, R. A., Sinn, L., Gerding, D. N. Emergence of ciprofloxacin resistance in nosocomial methicillin resistantStaphylococcus aureus isolates. Arch. Intern. Med. 150 (1990) 2151–2155.
Shalit, I., Berger, S. A., Gorea, A., Frimerman, H. Widespread quinolone resistance among methicillin-resistantStaphylococcus aureus isolates in a general hospital. Antimicrob. Agents Chemother. 33 (1989) 593–594.
Hadorn, K., Lenz, W., Kayser, F. H., Shalit, I., Krasemann, C. Use of a ribosomal RNA gene probe for the epidemiological study of methicillin and ciprofloxacin resistantStaphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 9 (1990) 649–653.
Blumberg, H. M., Rimland, D., Carroll, D. J., Terry, P., Wachsmuth, I. K. Rapid development of ciprofloxacin resistance in methicillin-susceptible and -resistantStaphylococcus aureus. J. Infect. Dis. 163 (1991) 1279–1285.
Blumberg, H. M., Rimland, D., Kiehlbauch, J. A., Terry, P. M., Wachsmuth, I. K. Epidemiologic typing ofStaphylococcus aureus by DNA restriction fragment length polymorphisms of rRNA genes, elucidation of the clonal nature of a group of bacteriophage-nontypeable, ciprofloxacin-resistant, methicillin-susceptibleS. aureus isolates. J. Clin. Microbiol. 30 (1992) 362–369.
Etienne, J., Brun, Y., Billard, M., Fleurette, J. Hospital dispersion ofStaphylococcus epidermidis isolates resistant to a fluoroquinolone, pefloxacin. Epidemiol. Infect. 103 (1989) 459–464.
Harnett, N., Brown, S., Krishnan, C. Emergence of quinolone resistance among clinical isolates of methicillin-resistantStaphylococcus aureus in Ontario, Canada. Antimicrob. Agents Chemother. 35 (1991) 1911–1913.
Daum, T. E., Schaberg, D. R., Terpenning, M. S., Sottile, W. S., Kauffman, C. A. Increasing resistance ofStaphylococcus aureus to ciprofloxacin. Antimicrob. Agents Chemother. 34 (1990) 1862–1863.
Goetz, M. B., Mulligan, M. E., Kwok, R., O'Brien, H., Caballes, C., Garcia, J. P. Management and epidemiologic analysis of an outbreak due to methicillin-resistantStaphylococcus aureus. Am. J. Med. 92 (1992) 607–614.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Dalhoff, A. Quinolone resistance inPseudomonas aeruginosa andStaphylococcus aureus. Development during therapy and clinical significance. Infection 22 (Suppl 2), S111–S121 (1994). https://doi.org/10.1007/BF01793575
Issue Date:
DOI: https://doi.org/10.1007/BF01793575