Efficacy of Using Probiotics with Antagonistic Activity against Pathogens of Wound Infections: An Integrative Review of Literature

Table 3

Eighteen clinical studies and one case study on the antimicrobial effects of probiotics against wound pathogens.

First author, year	Study type noted in paper	Wound type	Patients PR/CO	Wound pathogen	Probiotic/total cfu per day	Antibiotic treatment	Probiotics treatment	Wound infections (%) PR/CO	Outcome
Rayes, 2002 [82]	Prospective, randomized	Abdominal surgery	30/30	Streptococci	L. plantarum 299, (2 × 10^9 cfu) with fibres; heat killed bacteria as placebo	For all patients before surgery. After surgery in cases of expected or proven infection.	Oral (for 4 days after surgery)	0%/3%	Lower incidence of surgical site infections, however not statistically significant. Placebo group received antibiotic therapy significantly longer than group with probiotics and fibres.
Kanazawa, 2005 [83]	Randomized, controlled	Biliary cancer surgery	21/23	S. aureus, E. faecalis, Enterococcus faecium, Enterobacter cloacae	Lactobacillus casei Shirota, Bifidobacterium breve Yakult/(2 × 10^8 cfu)	For all patients before surgery. After surgery in cases of expected or proven infection.	Oral (for 14 days after surgery)	14.3%/26.1%	Significantly lower incidence of overall infections in the synbiotics group. Lower, but not statistically significant, incidence of wound infections. Slightly lower duration of postoperative antibiotic therapy for synbiotics group.
Rayes, 2005 [84]	Randomized, double-blind	Liver transplant surgery	33/33	S. aureus	Pediococcus pentosaceus LMG P-20608, Leuconostoc mesenteroides LMG P-20607, Lactobacillus paracasei subsp. paracasei LMG P-17806; L. plantarum LMG P-20606 (10^10 cfu)	For all patients before surgery. After surgery in case of bacterial infection.	Oral (starting on the day of surgery for two weeks)	0%/3%	Lower incidence of wound infection for probiotics with prebiotics group, significantly lower overall postoperative bacterial infections in the same group. Significantly lower duration of antibiotic therapy in synbiotics group.
Sugawara 2006 [56]	Randomized, controlled	Biliary cancer surgery	40–41^#/0	Not mentioned	L. casei Shirota, B. breve Yakult/(before surgery 5 × 10^10 cfu); (after surgery 2 × 10^8 cfu)	For all patients before surgery. After surgery if needed.	Oral (14 days before and 1^st day after surgery for 14 days) or after surgery for 14 days	4.8%–15%/NR	Lower incidence of wound infection for probiotics with prebiotics perioperative and postoperative treatment, statistically significantly lower overall postoperative infections and duration of antibiotic therapy for the same group.
Rayes, 2007 [85]	Randomized, double-blind	Pancreaticoduodenectomy	40/40	Not mentioned specifically for wound infections	P. pentosaceus LMG P-20608, L. mesenteroides LMG P-20607, L. paracasei subsp. paracasei LMG P-17806; L. plantarum LMG P-20606 (10^10 cfu)	For all patients before surgery. After surgery in case of bacterial infection.	Oral (starting on the day after surgery for 8 days)	10%/15%	Lower incidence of wound infection for probiotics with prebiotics group, statistically significantly lower overall postoperative infections and duration of antibiotic therapy in synbiotics group for same group.
Peral, 2009 [22]	Prospective	Second and third-degree burns	38/42	S. aureus, Pseudomonas aeruginosa, S. epidermidis, E. cloacae, Klebsiella pneumoniae, E. faecalis	L. plantarum ATCC 10241 (10^5 cfu)	Antibiotics are not routinely administered for burn patient due to their cost and of the high degree of antibiotic resistance	Daily topical application for 10 days	NA	Topical probiotic treatment of 2^nd degree burn patients was as effective as silver sulphadiazine in control group in decreasing pathogen load.
Peral, 2010 [86]	Prospective	Chronic infected leg ulcers	34^##/0	S. aureus, P. aeruginosa, S. epidermidis, E. cloacae, K. pneumoniae, E. faecalis	L. plantarum ATCC 10241 (10^5 cfu)	Not administered due to extreme resistance in chronic wounds.	Daily topical application, 10 days	NA	Statistically significant decrease of pathogen load after 10 days () compared to day 1 with topical probiotic treatment. However, non-probiotic group was not applied.
Liu, 2011 [87]	Randomized, double-blind, placebo-controlled	Colorectal cancer surgery	50/50	Not mentioned	L. plantarum CGMCC 1258, L. acidophilus LA-11, Bifidobacterium longum LB-88/(2.6 × 10^14 cfu)	For all patients before surgery. After surgery if needed.	Oral 16 days (6 days preoperatively and 10 days postoperatively)	6%/10%	Low incision site infection rate, however not statistically significant. No statistically significant difference in length of antibiotic therapy.
Usami, 2011 [88]	2-arm, randomized, controlled	Hepatic surgery	32/29	MRSA	L. casei Shirota, B. breve Yakult/(6 × 10^8 cfu)	For all patients before surgery. After surgery if needed.	Oral (14 days before operation and 11 days allowed food intake)	0%/6.9%	No infectious complications after surgery in probiotic group resulting in a statistically significant difference ()
Thomson, 2012 [55]	Case study	Deep-dermal and full-thickness burn patient	1	XDR P. aeruginosa	L. casei Shirota (6.5 × 10^9 cfu)	Patient received 10 different antibiotics during her hospital stay.	Oral (for 2 weeks after infection which occurred 5 months after burn)	NA	Pathogen from wound changed from multidrug resistant to multidrug sensitive strain, thus implying effective intervention
Zhang, 2012 [89]	Randomized, double-blind, placebo-controlled	Colorectal cancer surgery	30/30	Not mentioned	B. longum, Lactobacillus acidophilus, Enterococcus faecalis (3 × 10^8 cfu)	For all patients before surgery and after surgery for 3 to 5 days. If infection occurred an additional regimen was given.	Oral (3 to 5 days before surgery)	3.3%/13.3%	Lower surgical site infection rate for probiotics group, however not statistically significant
Zhang, 2013 [90]	Prospective, randomized	Liver transplant surgery	34/33	Enterococci spp, Enterobacter spp, Escherichia coli	L. acidophilus LA-14, L. plantarum LP-115, Bifidobacterium lactis BBL-04, L. casei LC-11, Lactobacillus rhamnosus LR-32, Lactobacillus brevis LBr-35/(2.75 × 10^10 cfu)	Antibiotic therapy post operation, if necessary.	Oral (at least 7 days after oral fluid tolerance after operation)	5.9%/15.2%	Incidence of postoperative infections was lower for probiotic with fibre group compared to fibre only. Significantly shorter duration of antibiotic therapy in group with probiotics and fibre.
Sadahiro, 2014 [57]	Prospective, randomized, double-blinded, controlled	Colorectal cancer surgery	99/95	E. coli, S. aureus, P. aeruginosa, S. epidermidis, E. faecalis, Bacteroides fragilis, Serratia marcescens	Bifidobacterium bifidum (3.3 × 10^9 cfu)	For all patients before surgery. After surgery only for antibiotic group.	Oral (7 days before and 5 to 10 days after operation)	6.1%/17.9%	The probiotics group had a slightly higher rate of surgical site infections vs. control group. The probiotics group had a statistically significant higher rate of surgical site infections than the antibiotic group.
Aisu, 2015 [91]	Clinical trial	Colorectal cancer surgery	75/81	Not mentioned	E. faecalis T110, Clostridium butyricum TO-A, Bacillus mesentericus TO-A (no information on concentration)	For all patients before surgery and after surgery for two days.	Oral (15 days prior surgery, restarted the same day the patient started drinking water after surgery	6.7%/19.8%	Significant lower surgical superficial incisional site infection ()
Kotzampassi, 2015 [58]	Randomized, double-blinded, placebo-controlled	Colorectal cancer surgery	84/80	Acinetobacter baumannii, P. aeruginosa, MRSA	L. acidophilus LA-5, L. plantarum, B. lactis BB-12, Saccharomyces boulardii/(5.5 × 10^9 cfu)	Not mentioned	Oral (1 day prior to operation and 14 days after surgery)	7.1%/20.0%	Statistically significant decrease in surgical site infections ()
Mayes, 2015 [92]	Randomized, blinded	Burn injury	10/10	Not specified	L. rhamnosus GG (1.5 × 10^10 cfu)	Days of receiving antibiotic medications recorded	Oral (start within 10 days after burn and until 95% wound closure)	NA	Trend of less requirement for antifungal agents () in probiotic group. No significant difference in number of days of antibiotic therapy
El-Ghazely, 2016 [93]	Randomized, double-blinded, controlled	Burn	20/20	Not specified	Lactobacillus fermentum and Lactobacillus delbrueckii/(2.0 × 10^9 cfu)	Not mentioned	Oral – during hospital stay	35%/60%	Trend towards decrease in infection incidence ().
Kotmatsu, 2016 [94]	Single-centre, randomized controlled	Colorectal resection	168/194	Not specified	L. casei Shirota, B. breve Yakult/(4.0 × 10^10 cfu)	For all patients before surgery.	Oral (7–11 days before surgery and reintroduced at 2–7 postoperative days)	17.3%/22.7%	Trend towards lower surgical site infection rate for synbiotic group, however not statistically significant (). Study was not blinded and no placebo product was used.
Yang, 2016 [95]	Randomized, double-blinded	Colorectal cancer surgery	30/30	Not specified	B. longum, L. acidophilus, E. faecalis/(3.0 × 10^7 cfu)	For all patients before surgery. After surgery if needed.	Oral 12 days (5 before, 7 after surgery)	3.3%/3.3%	No statistically significant differences in wound infection rates. Slightly lower postoperative duration of antibiotic therapy for probiotics group.

PR/CO, probiotic vs. control group; NR, not reported specifically for wound infection; NA, not applicable; strain not specified; additional antibiotic group in study (100 patients), ^#40 patients received postoperative synbiotics treatment and 41 patients received both preoperative and postoperative synbiotic treatment, probiotic used together with prebiotic or fibre, ^##14 diabetic patients and 20 nondiabetic patients; MRSA: methicillin-resistant S. aureus, XDR: multidrug resistant.