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Review Phages and Their Application Against Drug- Resistant Bacteria Journal of Chemical Technology and Biotechnology J Chem Technol Biotechnol 76:689±699 2001) DOI: 10.1002/jctb.438 Review Phages and their application against drug- resistant bacteria N Chanishvili,1* T Chanishvili,1 M Tediashvili1 and PA Barrow2 1George Eliava Institute of Bacteriophage, Microbiology and Virology, Georgian Academy of Sciences, Tbilisi, Georgia 2Institute for Animal Health, Compton, Newbury, Berkshire R620 7NN, UK Abstract: At the beginning of the 20th century the phenomenon of spontaneous bacterial lysis was discovered independently by Twort and d'Herelle. Despite the suggestion at that time by d'Herelle that these agents might be applied to the control of bacterial diseases in the west this idea was explored in a desultory fashion only and was eventually discarded largely due to the advent of extensive antibiotic usage. However,interest was maintained in countries of the former Soviet Union where bacteriophage therapy has been applied extensively since that time. Central to this work was the Eliava Institute of Bacteriophage,Microbiology and Virology in Tbilisi,Georgia,which was founded in 1923 through the joint efforts of d'Herelle and the Georgian George Eliava. Ironically,given his contributions to public health in the Soviet Union,Eliava was branded as an enemy of the people in 1937 and executed. d'Herelle never again returned to Georgia. In spite of these tragic events this institute remained the focus for phage therapy in the world and despite being continuously active in this ®eld for 75 years,now struggles for its ®nancial life. In the Eliava Institute,phages were sought for bacterial pathogens implicated in disease outbreaks in different parts of the Soviet Union and were dispatched for use in hospitals throughout the country. Although infections caused by a wide variety of bacterial pathogens have been treated,much of this has been published in Russian and is not readily available in the west. Work has also been carried out in Poland over many years and this has only recently been published in English. By contrast,interest in the west has been limited to a small number of enthusiasts and academics and until very recently little interest has been shown. The main reason that the medical and scienti®c communities are now beginning to take notice,is the continuing world-wide rise in the incidence of multiply-antibiotic-resistant bacterial pathogens and the absence of effective means for their control. Recent publicity over the work of the Eliava Institute has concentrated the minds of the western world on the potential for infectious disease control that bacteriophage offer,a procedure that is biologically more acceptable than antibiotic use and which has been in use for several decades already. # 2001 Society of Chemical Industry Keywords: bacteriophage therapy; disease control; phage±vaccine therapy; prophylaxis 1 THE PRINCIPAL ACTIVITIES OF injects its nucleic acid into the cell where it either BACTERIOPHAGES RELEVANT TO THEIR replicates itself or, as in the case with some phages, APPLICATION IN THERAPY integrates into the bacterial chromosome. Replication Bacteriophages are viruses for which bacteria are the results in formation of mature particles around the natural hosts. Most of the Eubacteria, amongst which newly synthesised phage nucleic acid followed by lysis human and animal pathogens occur, are hosts to of the cell and release of the new daughter phages Fig speci®c phages. There are exceptions, eg phages have 2). Integration of the nucleic acid into the host not yet been isolated for Neisseria meningitidis or N chromosome results in suppression of free replication gonorrhoeae. The initial stage of infection is adsorption and prevents further infection by the same type of of an individual phage particle to a susceptible phage. The phage nucleic acid becomes an integral bacterium. This occurs usually through the interaction part of the chromosome and does not excise, except between the phage tail and a speci®c attachment under certain conditions when it reverts to a replicative molecule on the bacterial surface Fig 1). There is cycle. Phages for clinical use therefore must be great speci®city in this attachment and a phage will not selected from virulent, non-lysogenic phages. generally attach to unrelated bacteria. The phage The relevance of this is related to the speci®city of * Correspondence to: N Chanishvili, George Eliava Institute of Bacteriophage, Microbiology and Virology, Georgian Academy of Sciences, Tbilisi, Georgia E-mail: [email protected] Contract/grant sponsor: INTAS; contract/grant number: GE-97 N1341 (Received 12 March 2001; accepted 13 March 2001) # 2001 Society of Chemical Industry. J Chem Technol Biotechnol 0268±2575/2001/$30.00 689 N Chanishvili et al Figure 1. Phage Sb-1 attaching to Staphylococcus aureus. phages in that they may be speci®c not just for 2 CLINICAL EFFICACY OF BACTERIOPHAGES IN bacterial species but for clones/strains possessing the THERAPY AND PROPHYLAXIS: EXPERIENCE FROM attachment antigen. They have no effect on inert THE ELIAVA INSTITUTE FOR BACTERIOPHAGE, bacteria that may also be present, ie they do not affect MICROBIOLOGY AND VIROLOGY (IBMV) the normal ¯ora. Since the discovery of spontaneous bacterial lysis by The whole idea involves the exploitation and Twort and by d'Herelle phage therapy has been used application of a biological system that is already in extensively with miscellaneous bacterial infections in operation naturally and for which there is good the areas of oto-laryngology,3 stomatology,4 ophthal- evidence for its ability to determine the outcome of mology,5,6 dermatology,7±11 paediatrics,12 gynaecol- natural and experimental infections. Thus it is likely ogy,13±15 surgery especially against wound that conditions exist under which the system operates infections),16,17 urology,18 and pulmonology.19±21 optimally and all attempts must be made to reproduce Reviewing the old Soviet literature it becomes these conditions to achieve optimal activity. obvious that mass application of bacteriophages was Figure 2. Intracellular propagation of Sb-1 in Staphylococcus aureus. 690 J Chem Technol Biotechnol 76:689±699 2001) Use of phages against drug-resistant bacteria ®rst facilitated in relation to the Finnish campaign operated cases of osteomyelitis and wounds on the 1938±1939) and then during the Second World War stumps of limbs. 1941±1945). The period between 1930 and 1940 Phages were administered topically and applied coincides with the peak of a number of scienti®c through tampons and bathing. These methods of publications on phage therapy, this is why it is application are simple and less traumatic for patients, sometimes dif®cult to ®nd access to the old data. This in comparison with subcutaneous or intra-muscular in part explains why most of the results of the clinical injections. The bandages, soaked with mixtures of experiments are not properly designed and registered, anaerobic and aerobic phages, were changed every 2±3 the data for the control groups are often missing days. Observation of 15 patients indicated a complete Migration of patients from one hospital to another did cure after 2±3 weeks of treatment in 13 cases and an not allow proper monitoring of the clinical effect of improvement was observed in the other two cases. It is phage therapy. remarkable that in three cases of osteomyelitis, to The previous experiences of patients with chronic avoid disturbance of newly operated wounds, it was infections, including non-effective treatment with decided to mix the phages with 0.7% agar and use this antibiotics etc, are usually presented as alternative jelly mass as a ®lling of the wound. This method data to conventional control group information. enabled the long-term circulation of phages in the Unfortunately, this erroneous approach to experimen- wounds. Phages remained in the wounds for 7±8 days tal methodology and data presentation continued in and post-operational recovery was smooth and pain- the Soviet Union in post-war publications. less. Although the study was performed on a limited Kokin 1947 cited in Ref 22) describes application of number of patients the results have been assessed as the mixtures of anaerobic phage and Staphylococcus and highly promising. Streptococcus phage produced by the IBMV, Tbilisi, Others24,25 have thoroughly studied the dynamic Georgia) for treatment of gas gangrene in soldiers. The cytological and morphological changes occurring mixture was applied to 767 cases and resulted in a death during healing of the wounds treated with phages rate of 18.8% compared with 42.2% in the control and demonstrated positive effects of the therapy group of soldiers treated by other methods. Other performed with the dry phage mixture specially authors have observed death rates of 19.2% in the designed for treatment of wounds. The authors group of soldiers treated with the same mixture of underline the positive effect of phage therapy in phages against 54.2% treated with other medications activation of phagocytosis and increase in number of Lvov and Pasternak, 1947 ± cited in Ref 22). neutrophils, etc. In addition to therapy, this phage mixture has been Tsulukidze18 describes the application of phage used by the mobile health brigades as an emergency therapy in urology, in particular in cases of acute 13 aid for treatment of wounds prophylactics for gas cases) and chronic cystitis 15), pyelocystitis 5) and gangrene).22 This paper summarises the observations purulent paranephritis 4). Duration of chronic cystitis of the three mobile, brigades. Observation was carried varied from 1 month to several years. The majority of out within 2±6 weeks during the course of patients these cases were caused by E coli infection 78.4%), evacuation to the front-line hospitals. In the ®rst group the rest by Staphylococcus aureus and Staphylococcus of 2500 soldiers treated with phages, only 35 1.4%) epidermidis. Treatment was performed with the speci®c showed the symptoms of gas gangrene.
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