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Global Status of Tetracycline Resistance Among Clinical Isolates of Vibrio Cholerae: a Systematic Review and Meta‑Analysis Mohammad Hossein Ahmadi*

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Global Status of Tetracycline Resistance Among Clinical Isolates of Vibrio Cholerae: a Systematic Review and Meta‑Analysis Mohammad Hossein Ahmadi* Ahmadi Antimicrob Resist Infect Control (2021) 10:115 https://doi.org/10.1186/s13756-021-00985-w RESEARCH Open Access Global status of tetracycline resistance among clinical isolates of Vibrio cholerae: a systematic review and meta-analysis Mohammad Hossein Ahmadi* Abstract Background: There has been an increasing resistance rate to tetracyclines, the frst line treatment for cholera disease caused by V. cholera strains, worldwide. The aim of the present study was to determine the global status of resistance to this class of antibiotic among V. cholera isolates. Methods: For the study, electronic databases were searched using the appropriate keywords including: ‘Vibrio’, ‘chol- era’, ‘Vibrio cholerae’, ‘V. cholerae’, ‘resistance’, ‘antibiotic resistance’, ‘antibiotic susceptibility’, ‘antimicrobial resistance’, ‘anti- microbial susceptibility’, ‘tetracycline’, and ‘doxycycline’. Finally, after some exclusion, 52 studies from diferent countries were selected and included in the study and meta-analysis was performed on the collected data. Results: The average resistance rate for serogroup O1 to tetracycline and doxycycline was 50% and 28%, respectively (95% CI). A high level of heterogeneity (I2 > 50%, p-value < 0.05) was observed in the studies representing resistance to tetracycline and doxycycline in O1 and non-O1, non-O139 serogroups. The Begg’s tests did not indicate the publica- tion bias (p-value > 0.05). However, the Egger’s tests showed some evidence of publication bias in the studies con- ducted on serogroup O1. Conclusions: The results of the present study show that the overall resistance to tetracyclines is relatively high and prevalent among V. cholerae isolates, throughout the world. This highlights the necessity of performing standard antimicrobial susceptibility testing prior to treatment choice along with monitoring and management of antibiotic resistance patterns of V. cholerae strains in order to reduce the emergence and propagation of antibiotic resistant strains as well as the failure of treatment. Keywords: Vibrio cholerae, Tetracycline, Doxycycline, Resistance Introduction Te causative agent of this life threatening diarrheal Cholera is an ancient infectious disease mainly afecting disease is Vibrio cholerae secreting the cholera toxin. Two developing countries. Te disease is capable to spread major cholera toxin-producing serogroups of this bacte- across many countries leading to vast pandemics and rial pathogen, O1 and O139, have potential to spread and becoming a major public health concern throughout the cause epidemic as well as pandemic disease [2]. Te sero- world [1]. group O1 has two biotypes, classical and El Tor, and each biotype has three serotypes including Ogawa, Inaba, and Hikojima [1, 3]. Te main stay of management of cholera (acute gastro- *Correspondence: [email protected] enteritis) is urgent fuid replacement; however, the use Department of Microbiology, Faculty of Medicine, Shahed University, of an appropriate antibiotic is necessary to eliminate the Tehran, Iran © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecom- mons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ahmadi Antimicrob Resist Infect Control (2021) 10:115 Page 2 of 12 bacteria, lessen the duration of illness, and control the wastewater, water supplies, river, aquaculture water, fsh- disease [4]. ery products, as well as seafood. Tetracyclines (tetracycline and doxycycline) have long Review articles, congress abstracts, studies reported in been the antibiotics of choice for treating severe chol- languages other than English, meta-analyses or system- era efectively worldwide, except for young children atic reviews, duplicate publications of the same study and pregnant women [5]. However, tetracycline resist- and articles available only in abstract form were also ant strains of V. cholerae are being increasingly reported excluded. worldwide. Tese resistant strains have been responsible for major epidemics in some countries and geographical Data extraction areas such as Latin America, Tanzania, Bangladesh, and Te data extracted from each study included frst author’s Zaire [6]. name, year of publication, geographical area of study To date, numerous studies have reported the difer- (country), clinical sample (specimen type), serogroup, ent antibiotic resistance patterns for V. cholerae isolates biotype, and serotype of the isolates, number of investi- throughout the world. Nevertheless, the overall status gated isolates (sample size), method of susceptibility test- of the resistance to teracyclines among the strains is not ing, and number of isolates resistant to each antibiotic. intensively studied. Te present study was conducted to determine the Statistical analysis global status of resistance to the antibiotics of tetra- Te data were analyzed using Comprehensive Meta- cycline family, including tetracycline and doxycycline, Analysis Software Version 2.0 (Biostat, Englewood, NJ, among diferent V. cholerae isolates using a systematic USA). Te resistance rate was reported by 95% conf- review and meta-analysis according to the Preferred dence intervals (CIs). Reporting Items for Systematic Reviews and Meta-Analy- Cochrane Q-statistic test and I2 test were performed ses (PRISMA) statement [7]. to estimate heterogeneity between studies, and in all cal- culations of which I2 was above 50%, the random efect Methods model was chosen to estimate the average rate because of Search strategies its conservative summary estimate; otherwise, the fxed Te electronic databases, including OVID databases, efect model was applied. To assess possible publication PubMed, Web of Science, Scopus, MEDLINE, EMBASE, bias, a funnel plot, Begg’s rank correlation and Egger’s Cochrane Library, as well as Google Scholar, were weighted regression methods were used. Two-tailed searched for papers reporting the resistance rate for dif- p < 0.05 was considered indicative of a signifcant publi- ferent Vibrio cholerae isolates to the antibiotics of tet- cation bias. Te relative weight for each study was also racyclines family from December 1980 to April 2020. calculated. Te search was restricted to original research articles throughout the world, published in English using the Results following keywords with the help of Boolean opera- A total of 138 articles were collected for assessment. tors (AND, OR): ‘Vibrio’, ‘ cholera’, ‘ Vibrio cholerae’, ‘ V. Trough the frst screening, 15 articles were excluded cholerae’, ‘resistance’, ‘antibiotic resistance’, ‘antibiotic on the basis of the title evaluation, as nine of them susceptibility’, ‘antimicrobial resistance’, ‘antimicrobial were duplicate publications of the same study, and six susceptibility’, ‘tetracycline’, and ‘doxycycline’. Refer- have titles irrelevant to the present study. By the second ences from reviewed articles were also searched for more assessment, nine papers were discarded because they information. had represented the study of Vibrio species other than V. cholerae, or were review articles. Finally, after full- Inclusion and exclusion criteria text evaluation, 62 studies were ruled out because they Included studies were all original research articles as well had reported resistance to antibiotics other than tetra- as some letter to editors presenting the resistance rates cyclines, used environmental isolates of the bacterium for Vibrio cholerae isolates to the tetracyclines including instead of clinical ones, and/or had no sufcient data. tetracycline and doxycycline. Terefore, 52 articles published between 1980–2020 were Excluded articles were those that: (1) had no suf- selected and included in the fnal analysis (Fig. 1 and cient data to be analyzed; (2) reported antibiotic resist- Table 1). ance of Vibrio species other than V. cholerae; (3) studied Te included studies were carried out in 20 difer- resistance to antibiotics other than tetracyclines; and (4) ent countries, majority of which (38 studies) located in tested environmental isolates of the bacterium instead Asia, 12 in Europe, one in Caribbean, and one in Oceania of clinical ones; for example, the strains isolated from (Table 1). Ahmadi Antimicrob Resist Infect Control (2021) 10:115 Page 3 of 12 Fig. 1 Flow chart of the literature search, systematic review and study selection. *Articles representing study of Vibrio species other than V. cholerae; **Articles reported resistance to antibiotics other than tetracyclines; ***Studies using environmental instead of clinical isolates of V. cholerae Ahmadi Antimicrob Resist Infect Control (2021) 10:115 Page 4 of 12 Table 1 Studies
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