In vitro porphyrin-based photodynamic therapy against mono and polyculture of multidrug-resistant bacteria isolated from integumentary infections in animals

Integumentary lesions, such as otitis and pyodermas, are highly prevalent in companion animals, causing itchiness, discomfort, and pain. Bacterial infection is frequently associated with such lesions as a primary or secondary agent; in both cases, the infection impairs the healing of the lesion [1], [2], [3], [4], [5]. In addition, dermatological conditions and infected wounds are commonly associated with microbial infection in large animals [6], [7], [8], [9]. Multidrug-resistant (MDR) organisms have been frequently isolated from these lesions, and their elimination is a significant issue for small and large animals [7,8,10].

Integumentary infections in animals are usually associated with more than one pathogen, making the choose of the appropriate antimicrobial therapy challenging. In addition, the increased isolation of MDR bacteria from these lesions further hinders therapeutical interventions; this is because there are only a handful of commercially available drug alternatives or even no effective drugs for use in animal species due to restrictions imposed by some countries [1].

The World Health Organization published a list of pathogens be considered a priority for searching for new antibacterial drugs, including Staphylococcus sp. methicillin and vancomycin resistant, Pseudomonas aeruginosa carbapenem resistant, and members of the Enterobacteriacea family carbapenem and/or third-generation cephalosporin resistant [11]. Thus, new therapies are urgently needed to deal with the resistance problem that all health domains face now. In fact, numerous therapies such as ozone, laser, and antimicrobial photodynamic therapy (aPDT) have emerged as new alternatives to face this concerning scenario [12], [13], [14]. aPDT involves light energy, a photosensitizer (PS), and molecular oxygen, and it has been employed to eliminate human tumor cells and integumentary infections, including labial herpes, oral candidiasis, osteomyelitis treatment, and others [15], [16], [17], [18]. For this, the PS is added to the target site, and the area is irradiated with a visible light, which excites the PS to its singlet excited state, generating reactive oxygen species (ROS). The ROS act in the cell, producing chemical changes in more than one target, such as oxidation of DNA, membrane lipids, cholesterol, and amino acids, in addition to causing cross-linking of proteins [13]. Some PS present antimicrobial effects, including indocyanine green, methylene blue, rose bengal, and tetrapyrrole derivatives [19], [20], [21]. In vivo experiments with aPDT using indocyanine green and methylene blue have been conducted and shown promising results, including inactivating Pseudomonas aeruginosa in a dog with chronic otitis and craniomandibular osteopathy [20,21], in a sheep with a cutaneous streptococcal abscess [22], against bovine digital dermatitis [23], caseous lymphadenitis in sheep [24], bovine subclinical mastitis [25], infectious stomatitis in snakes [26] and footpad dermatitis in penguins [27].

Porphyrins have been efficiently used to inactivate microorganisms in vitro, as demonstrated against bacteria isolated from dog otitis and rapidly growing mycobacteria [28,29], enveloped and non-enveloped bovine virus [30], and fungus [31]. There are many kinds of porphyrins, such as cationic, neutral, and anionic porphyrins [13], with or without metal ion coordination in the macrocycle core. Additionally, some researchers have investigated its antimicrobial effects, although how it works against MDR mono and polyculture is still unclear. Given the above, this paper addressed the action of aPDT using two isomeric water-soluble tetra-cationic porphyrins against MDR bacteria isolated from integumentary lesions (otitis, pyoderma, and wound infection) in dogs, cats, and horses in mono and polyculture and analyzed how aPDT affects bacterial morphology, and adhesive force properties.

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