A Literature Review of the Practical Application of Bacteriophage Research
Introduction
Since their discovery, bacteriophages accept been considered to be potential antibacterial therapeutics for the treatment of various infectious diseases in humans. Initially, clinical application of bacteriophages was aimed at the treatment of astute intestinal diseases (Summers, 1999) and pare infections (Bruynoghe and Maisin, 1921). Later, bacteriophages were applied in surgical practice for treatment of purulent wounds and postoperative infectious complications, and this approach was used in the USSR in the thirties and forties of the twentieth century (Tsulukidze, 1940; Kokin, 1941; Krestovnikova, 1947). After the appearance of antibiotics, phage therapy was ceased in nigh countries and considerably decreased in surgical exercise in the USSR. However, the utilise of bacteriophages in the clinical treatment of infected wounds was non stopped in Eastern Europe and the former SU, as antibiotic treatment of such infections sometimes failed, fifty-fifty in cases of antibody-sensitive bacteria. Phage preparations canonical for clinical application take been produced in the Russian Federation, Republic of Georgia, and Poland, and a big number of studies on phage therapy have been reported in these countries (Weber-Dabrowska et al., 2000; Sulakvelidze et al., 2001; Chanishvili, 2009, 2016; Górski et al., 2009; Miedzybrodzki et al., 2012; etc), including investigations published in Russian scientific literature (Zhukov-Verezhnikov et al., 1978; Bogovazova et al., 1991; Perepanova et al., 1995; Brusov et al., 2011; etc.).
The rapid ascent of multi-drug resistant bacteria worldwide has led to a renewed involvement in phage therapy equally a possible culling to antibiotics or, at least, a supplementary approach for the handling of some bacterial infections. Recently, the results of bacteriophage and phage cocktail application for the treatment of various infections accept been reported in a number of clinical cases, case series and clinical trials (Rhoads et al., 2009; Wright et al., 2009; Fish et al., 2016; Jennes et al., 2017). Despite the promising results from phage therapy, still in that location are no usually approved recommendations or therapeutic schemes for phage awarding. Evolution of these schemes is complicated by the diversity of phage preparations used (some of which are not even fully characterized), the variety of routes of administration and courses of phage treatment. Notably, the diverse localizations of bacterial infections require identification of the most preferable routes and therapeutic schemes of phage administration. In this mini-review, we focus on the results of phage therapy applied in the clinical treatment of localized infections in wounds, burns, and trophic ulcers, including diabetic foot ulcers.
Bacteriophage Handling of Wound Infections and Infectious Complications of Surgical Wounds
D'Herelle's enthusiasm concerning the wide possibilities of phage therapy led to all-encompassing attempts to isolate bacteriophages that were active against bacterial agents found in infected wounds and apply them in treatment. As a result, phage therapy was used in the USSR during the Finnish Campaign (1939–1940) and continued during the World War II (Tsulukidze, 1940, 1941; Kokin, 1941, 1946; Pokrovskaya et al., 1941; Krestovnikova, 1947). The majority of this historical data (except the study published by Pokrovskaya et al., 1941) was described in a previously published review (Chanishvili, 2012). It was reported that the mixtures of bacteriophages active against Clostridium perfringens, Staphylococcus spp., and Streptococcus spp. were used for the prevention and treatment of gas gangrene (Kokin, 1941). Several studies demonstrated high effectiveness of phage application in an early phase of infection (Kokin, 1941; Pokrovskaya et al., 1941; Tsulukidze, 1941). To amend the efficacy of phage therapy, "Pyophage" (a poly-specific cocktail of phages) was applied initially, and after detection of the etiologic agents, mono-specific lytic phages were used (Pokrovskaya et al., 1941; Tsulukidze, 1941; Krestovnikova, 1947). The best results were achieved in the treatment of Staphylococcal and Streptococcal infections, and phage application led to the emptying of 69 and fifty% of these bacterial pathogens, respectively (Pokrovskaya et al., 1941). A course of phage treatment included washings of a wound with a phage preparation and subcutaneous injections of phages from one to four times per day. 5 to eight days of therapy were sufficient for clinical comeback in the majority of cases; notwithstanding, if no improvement was accomplished during this period, further phage application was useless (Pokrovskaya et al., 1941; Tabular array 1).
Table 1. Case series and reports of phage therapy of infected wounds in humans.
Despite the widespread introduction of antibiotics, phage preparations continued to be used in the USSR and, later, in the Russia for the prevention of wound infections and handling of infectious complications of surgical wounds (Tabular array one). Poly-specific (Pyophage, Sekstaphage) and mono-specific therapeutic phage cocktails adult in research institutes and pharmaceutical companies were used in the USSR. In the recent years, phage preparations produced in JSC Microgen (http://world wide web.bacteriofag.ru) have been practical. Bacteriophages were administered locally, past subcutaneous injections, and orally (Tabular array 1). Notably, phage therapy was carried out every bit a mono-therapy (Zhukov-Verezhnikov et al., 1978; Peremitina et al., 1981; Kochetkova et al., 1989; Brusov et al., 2011), or in complex treatments, which included phages and antibiotics administration (Kochetkova et al., 1989; Khairullin et al., 2002). The investigations revealed that complex treatments decreased the healing time by 1.ii–ii.five times compared to an antibiotic treatment (Kochetkova et al., 1989; Khairullin et al., 2002; Table 1). Even application of bacteriophages specific to one of the infectious agents in a wound improved healing and stimulated faster purification (Ponomareva et al., 1985; Khairullin et al., 2002). This positive effect was, probably, due to the partial destruction of biofilms, influence of bacteriophages on the regenerative processes in a wound and on the immune system of a patient (Miedzybrodzki et al., 2009; Górski et al., 2017; Van Belleghem et al., 2017). Importantly, it has been shown that a single application of a bacteriophage could non exist enough to prevent infectious complications of wounds (Brusov et al., 2011; Tabular array 1).
Phage therapy was applied for the handling of infected post-operative wounds in cancer patients (Ponomareva et al., 1985; Kochetkova et al., 1989). Information technology resulted in faster cleaning of wounds from purulent masses, granulation, and healing without deforming scars compared to a group of cancer patients which were treated with antibiotics (Table 1). In one of these studies, the fastest wound healing was observed in patients treated only by bacteriophages (Kochetkova et al., 1989; Tabular array i). Still, information technology would non be correct to conclude that application of bacteriophages without antibiotics is preferable, equally investigators accept used complex treatments in patients with more astringent infections, previously unsuccessfully treated with antibiotics. Based on the obtained information, the authors have suggested that application of phage preparations provided positive upshot in mono-infection, while complex therapy, including bacteriophages and antibiotics, was required in mixed bacterial infection (Kochetkova et al., 1989). One of the reasons for using circuitous treatments may be the disability of quick pick of lytic bacteriophages active confronting all pathogens in a wound.
Another important issue of phage therapy is the question of which is ameliorate to use: one specific bacteriophage or a poly-specific phage cocktail. Awarding of highly specific bacteriophages (adapted by cultivation on a bacterial strain isolated from a patient) was more effective than treatment with poly-specific phage cocktails (Zhukov-Verezhnikov et al., 1978; Tabular array ane). The significantly higher efficiency of this type of personalized phage therapy tin be explained by the improvement of the specificity and virulence of phages to host strains. However, the adapted phage preparations require detailed characterization because they may contain temperate bacteriophages produced by the clinical bacterial strain, which was used for adaptation.
Phage Handling of Infected Burns
Burn surfaces are quickly colonized by bacteria, which are capable of producing biofilms and are oft resistant to multiple antibiotics (Erol et al., 2004; Church building et al., 2006; Asati and Chaudhary, 2017). Additionally, patients with burns frequently suffer from lymphopenia, sepsis, intoxication, and changes in the microbiota (Erol et al., 2004). Phage therapy could potentially be used to care for burns and prevent sepsis. Several instance serial accept been reported (Gomareli et al., 1976; Abul-Hassan et al., 1990; Lazareva et al., 2001; Sivera Marza et al., 2006; Rose et al., 2014), and promising results have been demonstrated in some reports (Tabular array two). Topical application of phages led to the emptying of multiple drug resistant (MDR) P. aeruginosa or successful peel graft accept in 18 of 30 patients with burns, only the method was fourth dimension-consuming, and the authors recommended this therapy only for infections resistant to available antibiotics (Abul-Hassan et al., 1990). In other investigation, it was revealed that bacteriophage awarding in complex therapy (bacteriophages per os and antibiotics) provided better clinical dynamics in patients with infected burns compared to a group of antibiotic-treated patients (Lazareva et al., 2001; Table 2). Notably, the starting time grouping included a higher number (29%) of initially complicated cases (intoxication, sepsis, purulent discharge of wounds), in contrast to 12.vi% of such cases in the antibiotic-treated group (Lazareva et al., 2001).
Table 2. Case series and reports of phage therapy of burns and trophic ulcers in humans.
The dosage of phage preparation is believed to exist very important in phage therapy, and the therapeutic titer should be higher than ten6 pfu/ml. Much more than concentrated phage suspensions are practical in the majority of reported cases (Table 2). However, phage BS24 (Soothill, 1994), which was used at a low titer (ten3 pfu/ml, unmarried application), provided a positive effect (Sivera Marza et al., 2006). In some other investigation (Rose et al., 2014), no positive response was recorded when the phage cocktail BFC-one (Merabishvili et al., 2009) was applied at a loftier titer (10nine pfu/ml, single application). The investigators explained this insufficient result past several possible reasons, such as a delay in phage application, previously initiated systemic and topical antimicrobial treatment, and unsuitable pharmaceutical form of BFC-1 (Rose et al., 2014). It is possible that the result of phage therapy depends on both phage titer and a number of other reasons, including sensitivity and accessibility of bacterial host to the phage, routes of phage administration, duration of phage treatment class, and so on.
Recently, a phase I/II clinical trial was defended to the study of safety, effectiveness, and pharmacodynamics of two phage cocktails to care for E. coli, and P. aeruginosa burn wound infections (http://www.phagoburn.eu). The results of this study, which was conducted for iii years in France, Switzerland, and Belgium, may help the evolution of dose and treatment scheme recommendations for phage therapy of infected burns.
Phage Therapy of Patients With Infected Ulcers
Chronic trophic ulcers occur as a complication of some disorders, such as chronic insufficiency of blood circulation (atherosclerosis, varicosity), diabetes, peripheral polyneuropathy of the limbs, and so on. It is believed that the rate of healing of ulcers depends on the concurrent infection; meanwhile, the spectrum of aerobic and anaerobic microorganisms inhabiting chronic wounds is very diverse (Rhoads et al., 2012; Wolcott et al., 2016). Microbiomes of chronic ulcers and, particularly, of diabetic foot ulcers (DFU) are associated with clinical factors: superficial ulcers and those with a shorter duration are commonly infected with Staphylococcus spp., mainly Due south. aureus, in a relatively high titer; deep ulcers and those with a longer duration are colonized with the diverse microbiota that contains Proteobacteria and anaerobes, including Anaerococcus, Peptonihilus, Bacteroides, and Clostridium genera (Gardner et al., 2013; Spichler et al., 2015). According to 16S rDNA pyrosequence analyses of microbiomes from ~iii,000 ulcers, simply i infectious agent was found in 7% of infected ulcers (Wolcott et al., 2016). S. aureus and P. aeruginosa were establish to be predominant and the about pathogenic species commonly persisting in chronic wounds (Wolcott et al., 2016), and their elimination would lead to improvement and wound healing in the majority of cases. Yet, antibacterial treatment of ulcers infected with diverse microbial agents is normally complicated, primarily by microbial biofilm formation and high level of antibiotic resistance (Malik et al., 2013; Rahim et al., 2016; Di Domenico et al, 2017). Long-term administration of antibiotics is sometimes ineffective; peculiarly in diabetes mellitus patients, long-term administration of antibiotics is oft unsafe, considering they may suffer from diabetic nephropathy and hepatic insufficiency.
Phage therapy could be an culling to antibiotics or, at least, a supplementary approach to the treatment of infected ulcers. Currently, several studies (Table ii) have reported the efficiency and safety of phage treatment of infected trophic ulcers in humans (Markoishvili et al., 2002; Rhoads et al., 2009; Fish et al., 2016, 2018; Vlassov et al., 2016; Morozova et al., 2018). A big case series (96 patients) demonstrated a positive upshot of PhagoBioDerm (a biodegradable wound dressing impregnated with the phage cocktail Pyophage) on the healing of venous leg ulcers (Markoishvili et al., 2002; Table 2). These biodegradable polymers contain different antimicrobial substances and are of particular involvement because of their power to degrade slowly and release active antimicrobials, including phage particles, for a long time. The utilize of PhagoBioDerm reduced the number of treatments and hence, injuring of wounds; therefore, this type of material is promising for both therapy and prevention of microbial infections in wounds (Markoishvili et al., 2002; Jikia et al., 2005).
After, a stage I safety trial of a cocktail of bacteriophages WPP-201 was performed (Rhoads et al., 2009). WPP-201 was applied topically to venous leg ulcers, and its condom was confirmed as it did not lead to an increase in the number of side effects compared to the standard therapy. Meanwhile, the charge per unit of wound healing was the same in both the experimental and command groups (Rhoads et al., 2009). Since the aim of the trial was to demonstrate the safety of the phage cocktail rather than its effectiveness, the study did not provide data on the limerick and number of infectious microorganisms, which might not be sensitive to phages from the WPP-201 cocktail.
The utilise of bacteriophages that were specific to infectious agents demonstrated clear positive results (Table 2). Staphylococcus phage Sb-one (Kvachadze et al., 2011) was successfully used in the handling of patients with DFU infected with methicillin-resistant and methicillin-sensitive S. aureus strains, as it has been described in a case serial report (Fish et al., 2016). Phage therapy without antibiotics resulted in subsequent wound healing in all treated patients (Fish et al., 2016, 2018; Tabular array 2). Another investigation reported phage treatment of patients with diverse infections of DFU, in whom previous antibiotic treatment was non successful (Vlassov et al., 2016; Morozova et al., 2018; Table 2). Chiefly, commercially available phage cocktails were selected in each example individually according to their specificity to particular infectious agents in an ulcer. When no specific phage cocktail was plant, a custom-fabricated phage training was prepared. Phage treatment was virtually effective in ulcers with one bacterial agent (100%), simply a personalized approach led to the elimination of pathogens, fifty-fifty in several cases with mixed infections. The main difficulty in treating of wounds infected with several pathogenic leaner was the inability to rapidly select phages against all identified bacterial agents (Vlassov et al., 2016; Morozova et al., 2018; Tabular array 2).
Conclusion
Extensive empirical experience of phage therapy of localized infections has been accumulated over 100 years of bacteriophage application in treatment of infectious diseases (Weber-Dabrowska et al., 2000; Sulakvelidze et al., 2001; Miedzybrodzki et al., 2012; Chanishvili, 2016; Górski et al., 2017), and the rubber of bacteriophages for use in humans has been repeatedly demonstrated (Bruttin and Brüssow, 2005; Rhoads et al., 2009; Wright et al., 2009; Rose et al., 2014). Different schemes and routes of phage assistants take been applied, varying from single oral or intravenous applications to multiple topical treatments per solar day for 12–15 weeks (Arsentieva, 1941; Meladze et al., 1982; Weber-Dabrowska et al., 2000; Brusov et al., 2011; Miedzybrodzki et al., 2012; Fish et al., 2016; Jennes et al., 2017; Chan et al., 2018; etc). Analysis of reported results of phage therapy of localized infections allowed u.s. to depict several conclusions.
Phage application was more than effective in an early stage of acute wound infection and 5–10 days of phage therapy provided positive clinical results in the majority of cases (Kokin, 1941; Pokrovskaya et al., 1941; Tsulukidze, 1941). The results of phage treatment depended on the pathogen species, and the best results were achieved in the treatment of infections acquired by Staphylococcus spp. and Streptococcus spp. (Kokin, 1941; Pokrovskaya et al., 1941; Miedzybrodzki et al., 2012).
In the treatment of infected chronic ulcers, mostly long-term application of phage preparations (up to several weeks) provided positive clinical effect (Weber-Dabrowska et al., 2000; Markoishvili et al., 2002; Miedzybrodzki et al., 2012; Fish et al., 2016). Importantly, multiple changes of dominant pathogens may occur in infected chronic ulcers during phage treatment (Morozova et al., 2018). This situation requires timely replacement of ineffective bacteriophages. Therefore, big collections of therapeutic phage preparations would be useful, because diverse bacterial communities take been recorded in most chronic wounds and ulcers. Even when simply office of the infectious agents are susceptible to therapeutic phages, phage therapy might exist a reasonable supplementary approach providing the elimination of dominant pathogens. Moreover, different bacteria in the ulcer's microbiota may be resistant to various antibiotics, leading to the inability to choose one advisable antibody for therapy. And then, circuitous treatments, including antibiotics and bacteriophages, may exist the optimal solution in this instance.
It is possible that phage therapy should be personalized, which means private selection and custom-made phage preparation, and in some cases, an adaptation of bacteriophage to infectious agent isolated from a patient (Zhukov-Verezhnikov et al., 1978; Pirnay et al., 2011, 2018; Schooley et al., 2017; Rohde et al., 2018). Poly-specific cocktails of bacteriophages might be applied preventively or at the starting time of treatment before identification of etiologic agents.
Phages were applied topically in the bulk of studies (Tables 1, ii); though the early Soviet investigations reported subcutaneous, intramuscular, and intravenous administration of phages in successful treatment of wound infection (Arsentieva, 1941; Kokin, 1941; Krestovnikova, 1947, etc). Information technology should be noted, that Staphylococcus phage adult by the Eliava Institute of Bacteriophage (Tbilisi, Democracy of Georgia) was successfully applied intravenously for treatment of infections in children and adults in the belatedly soviet times (Meladze et al., 1982; Samsygina and Boni, 1984). A range of doses of phage preparations provided positive results, presumably reflecting their ability to replicate where the target pathogen is nowadays. Further accumulation of data in the field of phage therapy of localized infections should help to develop optimal dosage and routes of administration of phage preparation.
Writer Contributions
All co-authors accept fabricated equal contribution to the writing and editing of the commodity. All authors read and approved the final version of the manuscript.
Funding
This report was supported by the Programme of Primal Scientific Research of Russian Academy of Sciences Projection ST No 0309-2018-0011, and Russian Federal Agency for Science and Innovation projection VI.55.ane.1, No 0309-201 6-0002.
Disharmonize of Interest Statement
The authors declare that the research was conducted in the absence of whatsoever commercial or financial relationships that could be construed every bit a potential disharmonize of interest.
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Source: https://www.frontiersin.org/articles/10.3389/fmicb.2018.01696/full
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