Culture Based Evaluation of Microbiota in Children with Acute Appendicitis

Juta Kroiča 1 , Aigars Reinis 1 , Mohit Kakar 2 , 4 , Mathilde Delorme 5 , Renārs Broks 1 , Lāsma Asare 6 , Marisa Berezovska 2 , 4 , Vladislavs Jansins 1 , Astra Zviedre 2 , 4 , Arnis Enģelis 2 , 4 , Amulya Saxena 3 ,  and Aigars Pētersons 2 , 4
  • 1 Department of Biology and Microbiology, Rīga Stradiņš University, 1007, Rīga, Latvia
  • 2 Department of Pediatric Surgery, Children’s Clinical University Hospital, 1004, Rīga, Latvia
  • 3 Department of Pediatric Surgery, Chelsea Children’s Hospital, Chelsea and Westminster NHS Fdn Trust, Imperial College London, London
  • 4 Department of Pediatric Surgery, Rīga Stradiņš University, 1004, Rīga, Latvia
  • 5 Faculty of Medicine, Rīga Stradiņš University, 1007, Rīga, Latvia
  • 6 Department of Statistics, Rīga Stradiņš University, 1046, Rīga, Latvia


Treatment strategies for acute uncomplicated appendicitis have evolved and now conservative antibacterial treatment is recommended over surgical treatment, especially for paediatric patients. The aim of this study was to evaluate microbiota in paediatric patients with acute uncomplicated and complicated appendicitis, and antibacterial susceptibility of the causative microorganisms. Bacteriological identification was conducted using the VITEK2 analyser. Antibacterial susceptibility tests were performed and the results were evaluated in accordance with the recommendations of the European Committee on Antimicrobial Susceptibility Testing (EUCAST) “Clinical breakpoints and dosing of antibiotics” (Version 7.0, January 2019). Serodiagnosis of Yersinia enterocolitica was performed using indirect haemagglutination. The results revealed differences in microbiota in cases of acute complicated and acute uncomplicated appendicitis. Pseudomonas aeruginosa was identified more frequently in cases of acute complicated appendicitis. Mixed culture was prevalent in cases of both acute complicated and acute uncomplicated appendicitis. Very few positive extended spectrum beta-lactamase (ESBL) Escherichia coli cultures were identified. Most of strains of Pseudomonas aeruginosa were resistant to amoxicillin with clavulanic acid, ertapenem, ampicillin and cefotaxime. Some of E. coli isolates were resistant to ampicillin and to amoxicillin with clavulanic acid.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Abdussemee, A., Oludolapo, A., Adeyinka, A., Olusegun, F. (2018). Bacterial pattern in acute appendicitis. Ann. Afr. Surg., 15 (1), 8–13.

  • Anonymous (2013). Recommendations for preoperative antimicrobial prophylaxis. Recommendations for the use of antibacterial agents in surgical prophylaxis KS/MET-43-00/2013. Children’s Clinical University Clinic, pp. 9.

  • Anonymous (2019). Clinical breakpoints and dosing of antibiotics. European Committee on Antimicrobial susceptibility testing. (accessed 10 December 2019).

  • Anonymous (2019). National Center for Biotechnology Information. PubChem Database. Avibactam, CID=9835049. (accessed 10 December 2019).

  • Anonymous (2019). National Center for Biotechnology Information. PubChem Database.Amikacin,CID=37768. (accessed 12 December 2019).

  • Anonymous (2019). The Drugbank. Ceftazidime. (accessed 10 December 2019).

  • Baldwin, C. M., Lyseng-Williamson, K. A., Keam, S. J. (2008). Meropenem: A review of its use in the treatment of serious bacterial infections. Drugs, 68 (6), 803–838.

  • Bazzaz, A., Lor, D., Mahdi, N. (2018). Impact of some antibiotics on bacteria isolated from appendices in Kirkuk Province, Iraq. Adv. Biosci. Biotechnol., 9, 1–10.

  • Bhangu, A., Søreide, K., Di Saverio, S., Assarsson, J. H., Drake, F. T. (2015). Acute appendicitis: Modern understanding of pathogenesis, diagnosis, and management. Lancet, 386 (10000), 1278–1287.

  • Chen, C. Y., Chen, Y. C., Pu, H. N., Tsai, C. H., Chen, W. T., Lin, C. H. (2012). Bacteriology of acute appendicitis and its implication for the use of prophylactic antibiotics. Surg. Infect. (Larchmt), 13 (6), 383–390.

  • Drusano, G. L., Neely, M. N., Yamada, W.M., Duncanson, B., Brown, D., Maynard, M., Vicchiarelli, M., Louie, A. (2018). The combination of fosfomycin plus meropenem is synergistic for Pseudomonas aeruginosa PAO1 in a hollow-fiber infection model. Antimicrob. Agents Chemother., 62 (12), e01682-18.

  • Du, S.-J., Kuo, Cheng, C. H., Fei, A., Wei, H.-W., Chang, S.-K. (2010). Molecular mechanisms of ceftazidime resistance in Pseudomonas aeruginosa isolates from canine and human infections. Original Paper Veterin. Med. 55, 172–182.

  • Essenmacher, A. C., Nash, E., Walker, S. K., Pitcher, G. J., Buresh, C. T., Sato, T. S. (2018). Stump appendicitis. Clin. Pract. Cases Emerg. Med., 2 (3), 211–214.

  • Feng, Y., Bakker, R. T., van Hest, R. M., Hodiamont, C. J., Brul, S., Schultsz, C., ter Kuile, B. H. (2017). Optimization of therapy against Pseudomonas aeruginosa with ceftazidime and meropenem using chemostats as model for infections, FEMS Microbiol. Lett., 364 (14), fnx142.

  • Fisher, J. F., Mobashery, S. (2014). The sentinel role of peptidoglycan recycling in the β-lactam resistance of the Gram-negative Enterobacteriaceae and Pseudomonas aeruginosa. Bioorg. Chem., 56, 41–48.

  • Gebbers, J. O., Laissue, J. A. (2004). Bacterial translocation in the normal human appendix parallels the development of the local immune system. Ann. NY Acad. Sci., 1029, 337–343.

  • Gracia, J., Gruenberg, K., Nguyen, L., MacDougall, C. (2018). Multidrug-resistant Pseudomonas aeruginosa Iinfections: Hard to treat, but hope on the horizon? Contagion Live – Infectious Diseases Today, received from ContagionLive, Database on the World Wide Web. (accessed 10 December 2019).

  • Guillet-Caruba, C., Cheikhelard, A., Guillet, M., Bille, E., Descamps, P., Yin, L., Khen-Dunlop, N., Zahar, J. R., Sarnacki, S., Revillon, Y., Berche, P., Ferroni, A. (2011). Bacteriologic epidemiology and empirical treatment of pediatric complicated appendicitis. Diagn. Microbiol. Infect. Dis., 69 (4), 376–381.

  • Guinane, C. M., Tadrous, A., Fouhy, F., Ryan, C. A., Dempsey, E. M., Murphy, B., Andrews, E., Cotter, P. D., Stanton, C., Ross, R. P. (2013). Microbial composition of human appendices from patients following appendectomy. MBio., 4 (1), e00366-12.

  • Jackson, H. T., Mongodin, E. F (2014). Culture-independent evaluation of appendix and rectum microbiomes in children with and without appendicitis. PLOS One, 9 (4), 1–9.

  • Kakars, M., Rekevica, A., Engelis, A., Petersons, A. (2017). An update of a single center review in the management of acute appendicitis in children. In: International Scientific Conference, 6–7 April 2017, Rīga, Latvia. Rīga Stradiņš University, Rīga, p. 59.

  • Kos V. N., McLaughlin R. E., Gardner H. A. (2016). Elucidation of mechanisms of ceftazidime resistance among clinical isolates of Pseudomonas aeruginosa by using genomic data. Antimicrobial agents and chemotherapy, 60 (6), 3856–3861.

  • Lamps, L. W. (2010). Infectious causes of appendicitis. Inf. Dis. Clin. North Amer., 24 (4), 995-1018-ix-x.

  • Loho, T., Sukartini, N., Astrawinata, D. A. W, Immanuel, S., Aulia, D., Priatni, I. (2018). In vitro antibacterial interaction of Doripenem and Amikacin against multidrug-resistant Acinetobacter baumannii, Pseudo-monas aeruginosa, and Klebsiella pneumoniae isolates. Can. J. Infect. Dis. Med. Microbiol. Article ID 1047670, 6 pages.

  • Mazuski, J. E., Gasink, L. B., Armstrong, J., Broadhurst, H., Stone, G. G., Rank, D., Llorens, L., Newell, P., Pachl, J. (2016). Efficacy and safety of ceftazidime-avibactam plus metronidazole versus meropenem in the treatment of complicated intra-abdominal infection: Results from a randomized, controlled, double-blind, phase 3 program. Clin. Infect. Dis., 62 (11), 1380–1389.

  • Naher, H. S., Ktab, F. K. (2013). Bacterial profile associated with appendicitis. Int. Res. J. Medical Sci., Vol. 1 (2), 1–4.

  • Noha, A. H., Amany, H. I. M., Sahar,M. A. E., Hazem, A. W. A. R. (2015). High prevalence of multidrug resistant Pseudomonas aeruginosa recovered from infected burn wounds in children. Arch. Clin. Microbiol., 4 (4), 1–7.

  • Ny, S., Kozlov, R., Dumpis, U., Edquist, P., Gröndahl-Yli-Hannuksela, K., Kling, A. N., Lis, D. O., Lübbert, C., Pomorska-Wesołowska, M., Palagin, I., Vilde, A., Vuopio, J., Walter, J., Wisell, K.T., Tegmark, K., NoDARS ESBL-carrier working group. (2018). Large variation in ESBL-producing Escherichia coli carriers in six European countries including Russia. Eur. J. Clin. Microbiol. Infect. Dis., 37, 2347–2354.

  • Parthiban, N., Harish, M. (2017). A study on microbiology culture of acute appendicectomy specimen and its correlation with wound infection. Int. Surg. J., 4, 2212–2215.

  • Qin, X., Tran, B. G., Kim, M. J., Wang, L., Nguyen, D. A., Chen, Q., Song J., Laud, P. J., Stone, G. G. Chow, J. W. (2017). A randomised, double-blind, phase 3 study comparing the efficacy and safety of ceftazidime/avibactam plus metronidazole versus meropenem for complicated intra-abdominal infections in hospitalised adults in Asia. Int. J. Antimicrob. Agents, 49 (5), 579–588.

  • Rhee, K. J., Jasper, P. J., Sethupathi, P., Shanmugam, M., Lanning, D., Knight, K. L. (2005). Positive selection of the peripheral B cell repertoire in gut-associated lymphoid tissues. J. Exp. Med., 201 (1), 55–62.

  • Rickard, J. (2018). Antibiotic use and antimicrobial resistance of surgical patients with peritonitis at a tertiary referral hospital in Rwanda. Surg. Infect., 19 (4), 382–387.

  • Roberts, J. P. (1988). Quantitative bacterial flora of acute appendicitis. Arch. Dis. Childhood, 63 (5), 536.

  • Rogers, M. B., Brower-Sinning, R., Firek, B., Zhong, D., Morowitz, M. J. (2016). Acute appendicitis in children is associated with a local expansion of fusobacteria. Clin. Infect. Dis., 63 (1), 71–78.

  • Salö, M., Marungruang, N., Roth, B., Sundberg, T., Stenström, P., Arnbjörnsson, E., Fåk, F., Ohlsson, B. (2017). Evaluation of the microbiome in children’s appendicitis. Int. J. Colorectal Dis., 32 (1), 19–28.

  • Schulin, S., Schlichting, N., Blod, C., Opitz, S., Suttkus, A., Stingu, C. S., Barry, K., Lacher, M., Bühligen, U., Mayer, S. (2017). The intra- and extraluminal appendiceal microbiome in pediatric patients. Medicine, 96, 52(e9518).

  • Snyder, M. J., Guthrie, M., Cagle, S. (2018). Acute appendicitis: Efficient diagnosis and management. Amer. Fam. Physician, 98 (1), 25–33.

  • Solomkin, J., Hershberger, E., Miller, B., Popejoy, M.., Friedland, I., Steenbergen, J., Yoon, M., Collins, S., Yuan,G., Barie, P. S., Eckmann, C. (2015). Ceftolozane/tazobactam plus metronidazole for complicated intra-abdominal infections in an era of multidrug resistance: results from a randomized, double-blind, phase 3 trial (ASPECT-cIAI). Clin. Infect. Dis., 60 (10), 1462–1471.

  • Terentjeva, M., Streikiša, M., Avsejenko, J., Trofimova, J., Kovaļenko, K., Elferts, D., Bērziņš, A. (2019). Prevalence and antimicrobial resistance of Escherichia coli, Enterococcus spp. and the major foodborne pathogens in calves in Latvia. Foodborne Pathog. Dis., 16 (1), 35–41.

  • Turel, O. Mirapoglu, S. Y., Yuksel, M., Ceylan, A., Gultepe, B. S. (2018). Perforated appendicitis in children: Antimicrobial susceptibility and antimicrobial stewardship. J. Global Antimicrob. Resist., 16, 159–161.

  • Wagenlehner, F. M., Umeh, O., Steenbergen, J., Yuan, G., Darouiche, R. O. (2015). Ceftolozane-tazobactam compared with levofloxacin in the treatment of complicated urinary tract infections, including pyelonephritis: A randomised, double-blind, phase 3 trial (ASPECT-cUTI). The Lancet, 385 (9981), 1949–1956.

  • Xipell, M., Bodro, M., Marco, F., Losno, R. A., Cardozo, C., Soriano, A. (2017). Clinical experience with ceftazidime/avibactam in patients with severe infections, including meningitis and lung abscesses, caused by extensively drug-resistant Pseudomonas aeruginosa. Int. J. Antimicrob. Agents, 49 (2), 266–268.

  • Zhong, D., Brower-Sinning, R., Firek,B., Morowitz, M. J. (2014). Acute appendicitis in children is associated with an abundance of bacteria from the phylum Fusobacteria. J. Pediatr. Surg., 49 (3), 441–446.


Journal + Issues