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Naja Atra) Bites: Determining Bacteriology, Antibiotic Susceptibility, and the Use of Antibiotics-A Cobra BITE Study

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Naja Atra) Bites: Determining Bacteriology, Antibiotic Susceptibility, and the Use of Antibiotics-A Cobra BITE Study toxins Article Wound Infections from Taiwan Cobra (Naja atra) Bites: Determining Bacteriology, Antibiotic Susceptibility, and the Use of Antibiotics-A Cobra BITE Study Heng Yeh 1,2, Shi-Ying Gao 1 and Chih-Chuan Lin 1,2,* 1 Department of Emergency Medicine, Lin-Kou Medical Center, Chang Gung Memorial Hospital, Taoyuan 33305, Taiwan; [email protected] (H.Y.); [email protected] (S.-Y.G.) 2 School of Medicine, College of Medicine, Chang Gung University, Taoyuan 33302, Taiwan * Correspondence: [email protected] Abstract: Wound necrosis and secondary infection are common complications after Naja atra bites. Clinical tools to evaluate the infection risk after Taiwan cobra bites are lacking. In this Cobra BITE study, we investigated the prevalence of wound infection, bacteriology, and corresponding antibiotic usage in patients presenting with Taiwan cobra snakebites. Patients with wound infection lacking tissue necrosis were included in developing Cobra BITE score utilizing univariate and multiple logistic regression, as patients with wound necrosis require antibiotics for infection treatment. 8,295,497 emergency department visits occurred in the span of this study, with 195 of those patients being diagnosed as having cobra bites. Of these patients, 23 had wound necrosis, and 30 had wound infection, resulting in a wound infection rate of 27.2% (53/195). Enterococcus faecalis and Morganella morganii were the main bacteria identified in the culture report regardless of whether patients’ wounds had necrosis. As per our Cobra BITE score, the three factors predicting secondary wound infection after cobra bites are hospital admission, a white blood cell count (in 103/µL) × by neu-trophil-lymphocyte ratio value of ≥114.23, and the use of antivenin medication. The area under the receiver operating characteristic curve for the Cobra BITE score system was 0.88; ideal sensitivity Citation: Yeh, H.; Gao, S.-Y.; Lin, and specificity were 0.89 and 0.76. This scoring system enables the assessment of wound infections C.-C. Wound Infections from Taiwan Cobra (Naja atra) Bites: Determining after N. atra bites, and it could be modified and improved in the future for other Naja spp. bites. Bacteriology, Antibiotic Susceptibility, and the Use of Antibiotics-A Cobra Keywords: wound infections; snakebites; Taiwan cobra; Naja atra BITE Study. Toxins 2021, 13, 183. https://doi.org/10.3390/ Key Contribution: In this study, we investigate the bacteriology and antibiotic susceptibility in toxins13030183 Taiwan cobra snakebite wounds. We further developed a clinical scoring system (Cobra BITE score) to predict wound infection development and hence the necessity of antibiotic initiation. Physicians Received: 26 January 2021 can use the Cobra BITE score to guide appropriate antibiotic use and offer the medical community a Accepted: 25 February 2021 framework for stratifying the risk of developing a wound infection after a cobra bite. Published: 2 March 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- Taiwan, a subtropical island, has many types of snakes; of these, six species of ven- iations. omous snakes are considered clinically important: Naja atra (Taiwan cobra or Chinese cobra), Bungarus multicinctus, Protobothrops mucrosquamatus (Taiwan habu), Trimeresurus stejnegeri (green bamboo viper), Deinagkistrodon acutus (hundred pacer viper), and Daboia siamensis (eastern Russell’s viper). Among these, N. atra are responsible for approxi- Copyright: © 2021 by the authors. mately 20% of venomous snakebites in Taiwan [1]. While other species of cobra cause Licensee MDPI, Basel, Switzerland. neurological complications, Taiwan cobra bites do not; however, they cause wound tissue This article is an open access article damage/necrosis due to the actions of cytotoxins in the venom, and confer a high risk distributed under the terms and of wound infection [2–4]. To our knowledge, there are no clinical parameters that can conditions of the Creative Commons Attribution (CC BY) license (https:// predict or assesses the clinical severity of the cobra bites patients. Although some studies creativecommons.org/licenses/by/ have investigated the bacteriology of cobra bite wounds [5,6], guidelines for differentiating 4.0/). Toxins 2021, 13, 183. https://doi.org/10.3390/toxins13030183 https://www.mdpi.com/journal/toxins Toxins 2021, 13, x FOR PEER REVIEW 2 of 15 Toxins 2021, 13, 183 infection [2–4]. To our knowledge, there are no clinical parameters that can predict or2 of as- 13 sesses the clinical severity of the cobra bites patients. Although some studies have inves- tigated the bacteriology of cobra bite wounds [5,6], guidelines for differentiating patients basedpatients on basedwhether on they whether have they wound have infections wound infections are lacking. are Wound lacking. necrosis Wound is necrosis a common is a complicationcommon complication associated associated with cobra with bites cobra [2], bites and [2affected], and affected patients patients may be may treated be treated with antibiotics.with antibiotics. Knowledge Knowledge on whether on whether nonnecrotic nonnecrotic cobra cobra wounds wounds are infected are infected is important. is impor- Furthermore,tant. Furthermore, to provide to provide appropriate appropriate antibiotics antibiotics to patients to patients with wound with woundinfections, infections, wound bacteriologywound bacteriology must be must investigated. be investigated. This stu Thisdy investigated study investigated the wound the wound bacteriology bacteriology of ne- crosisof necrosis wounds wounds and infected and infected wounds wounds without without necrosis necrosis to develop to develop a clinically a clinically useful wound useful infectionwound infection prediction prediction rule (Cobra rule (Cobra Bites/Bacteriology Bites/Bacteriology of Infections of Infections in Taiwanese in Taiwanese snake snake En- venomationEnvenomation (Cobra (Cobra BITE) BITE) study study)) to gui to guidede antibiotic antibiotic use use (Figure (Figure 1).1 ). January 2001–May 2017 patients attending ERs (n= 8,295,497). Patients with snakebites: 1128 (0.01%) Patients with Taiwan cobra bites n =195 Wound tissue Nonnecrosis group Wound tissue Necrosis group n = 172 (88.21%) n = 23 (11.79%) Wound infection, if 1) Positive wound/pus cultures, 2) Admission diagnoses of cellulitis, abscess, necrotizing fasciitis Necrotic tissue wound 3) Underwent surgical wound Bacteriology No wound Wound infection Nonnecrosis tissue wound infection group group Bacteriology n = 142 (82.55%) n = 30 (17.44%) Development of a wound infection prediction rule (Cobra BITE score) Clinical application of antibiotic administration for Taiwan cobra bites Figure 1. Study flow diagram for Cobra BITE score. The enrolled cobra bites patients were divided Figure 1. Study flow diagram for Cobra BITE score. The enrolled cobra bites patients were divided into wound tissue necrosis and nonnecrosis group. Patients were defined as having wound necrosis into wound tissue necrosis and nonnecrosis group. Patients were defined as having wound necro- if they met the criteria of positive wound/pus culture or admission diagnoses of cellulitis, abscess, sis if they met the criteria of positive wound/pus culture or admission diagnoses of cellulitis, ab- scess,and necrotizing and necrotizing fasciitis. fasciitis. The nonnecrosis The nonnecrosis wound wound infection infection group group was compared was compared with the with no woundthe no woundinfection infection group to group develop to develop the Cobra the BITE Cobra score. BITE The score. bacteriology The bacteriology of necrosis of wound necrosis and wound nonnecrosis and nonnecrosiswound infection wound groups infection was employed groups was to provideemployed the to clinical provide application the clinical of antibioticapplication administration of antibiotic administrationfor Taiwan cobra for bites. Taiwan cobra bites. 2. Results 2.1. Patient Characteristics In total, data on 195 patients with cobra bites were retrieved from data on 8,295,497 emergency department (ED) visits from January 2001 to May 2017. The Chang Gung Toxins 2021, 13, 183 3 of 13 Research Database (CGRD) contains data on 1128 patients with snakebites (0.01% of total ED visits); men accounted for the majority of this study population (n = 144, 73.8%; mean age: 49.97 ± 17.42 years). Generally, two vials (median) of freeze-dried neurotoxic antivenin (interquartile range: 1–4) were administered to each patient, suggesting that these patients were mostly mildly to moderately envenomed. A total of 74 patients (37.9%) required hospital admission. Of these 195 patients, 53 (27.2%) developed wound infections. Among them, 23 and 30 patients had wound tissue necrosis and nonnecrosis but wound infections. These 53 patients with wound infections received larger antivenin doses (median (interquartile range) = 2 (1–3) vs 2 (1–4), p = 0.002), had more admissions (n = 47 vs 27, p < 0.0001), and had longer hospital stays (3.07 ± 2.67 vs 16.09 ± 13.99, p < 0.0001) than patients without infected wounds, implying that their clinical conditions were severe. Patients with Taiwan cobra bites lacked neurological complications but had the most severely infected wounds, and they underwent the most serious envenomation and surgical procedures, such as debridement, fasciotomy, and graft. Of the 195 patients with cobra bites, 23, 16, and 15 patients received debridement, fasciotomy, and graft. 2.2.
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