• 1.

    Dougan G , Baker S , 2014. Salmonella enterica serovar Typhi and the pathogenesis of typhoid fever. Annu Rev Microbiol 68: 317336.

  • 2.

    World Health Organization , 2018. Typhoid. Available at: https://www.who.int/news-room/fact-sheets/detail/typhoid. Accessed September 8, 2021.

  • 3.

    Klemm EJ , Shakoor S , Page AJ , Qamar FN , Judge K , Saeed DK , Wong VK , Dallman TJ , Nair S , Baker S , 2018. Emergence of an extensively drug-resistant Salmonella enterica serovar Typhi clone harboring a promiscuous plasmid encoding resistance to fluoroquinolones and third-generation cephalosporins. mBio 9: e00105e00118.

    • Search Google Scholar
    • Export Citation
  • 4.

    Howard‐Jones A , Kesson AM , Outhred AC , Britton PN , 2019. First reported case of extensively drug‐resistant typhoid in Australia. Med J Aust 211: 286286.e1.

    • Search Google Scholar
    • Export Citation
  • 5.

    Nizamuddin S , Ching C , Kamal R , Zaman MH , Sultan F , 2021. Continued outbreak of ceftriaxone-resistant Salmonella enterica serotype Typhi across Pakistan and assessment of knowledge and practices among healthcare workers. Am J Trop Med 104: 12651270.

    • Search Google Scholar
    • Export Citation
  • 6.

    Ahmad S , Tsagkaris C , Aborode AT , Haque MTU , Khan SI , Khawaja UA , dos Santos Costa AC , Essar MY , Lucero-Prisno DE 3rd , 2021. A skeleton in the closet: the implications of COVID-19 on XDR strain of typhoid in Pakistan. Public Health in Practice 2: 100084.

    • Search Google Scholar
    • Export Citation
  • 7.

    World Health Organization , 2019. Drug resistant Salmonella infections in Pakistan: update. Wkly Epidemiol Monit 12: 34.

  • 8.

    Patra SD , Mohakud NK , Panda RK , Sahu BR , Suar M , 2021. Prevalence and multidrug resistance in Salmonella enterica Typhimurium: an overview in South East Asia. World J Microbiol Biotechnol 37: 17.

    • Search Google Scholar
    • Export Citation
  • 9.

    Hussain A , Satti L , Hanif F , Zehra NM , Nadeem S , Bangash TM , Peter A , 2019. Typhoidal Salmonella strains in Pakistan: an impending threat of extensively drug-resistant Salmonella typhi. Eur J Clin Microbiol Infect Dis 38: 21452149.

    • Search Google Scholar
    • Export Citation
  • 10.

    Shoaib M , Satti L , Hussain A , Khursheed N , Sarwar S , Shah AH , 2021. Disc diffusion testing of azithromycin against clinical isolates of typhoidal Salmonellae: a diagnostic conundrum. Cureus 13: e16777.

    • Search Google Scholar
    • Export Citation
  • 11.

    Lucien MAB , Canarie MF , Kilgore PE , Jean-Denis G , Fénélon N , Pierre M , Cerpa M , Joseph GA , Maki G , Zervos MJ , 2021. Antibiotics and antimicrobial resistance in the COVID-19 era: perspective from resource-limited settings. Int J Infect Dis 104: 250254.

    • Search Google Scholar
    • Export Citation
  • 12.

    Clinical and Laboratory Standards Institute , 2021. Performance Standards for Antimicrobial Susceptibility Testing, 30th edition. CLSI document M100. Wayne, PA: Clinical and Laboratory Standards Institute.

    • Search Google Scholar
    • Export Citation
  • 13.

    Khan S , Kurup P , Vinod V , Biswas R , Pillai GK , Kumar A , 2019. Reconsidering azithromycin disc diffusion interpretive criteria for Salmonellae in view of azithromycin MIC creep among typhoidal and nontyphoidal Salmonella. J Lab Physicians 11: 3944.

    • Search Google Scholar
    • Export Citation
  • 14.

    Kobayashi T , Hayakawa K , Mawatari M , Mezaki K , Takeshita N , Kutsuna S , Fujiya Y , Kanagawa S , Ohmagari N , Kato Y , 2014. Case report: failure under azithromycin treatment in a case of bacteremia due to Salmonella enterica Paratyphi A. BMC Infect Dis 14: 14.

    • Search Google Scholar
    • Export Citation
  • 15.

    Manesh A , Balaji V , Kumar DRN , Rupali P , 2017. A case of clinical and microbiological failure of azithromycin therapy in Salmonella enterica serotype Typhi despite low azithromycin MIC. Int J Infect Dis 54: 6263.

    • Search Google Scholar
    • Export Citation
  • 16.

    Qureshi S , Naveed AB , Yousafzai MT , Ahmad K , Ansari S , Lohana H , Mukhtar A , Qamar FN , 2020. Response of extensively drug resistant Salmonella typhi to treatment with meropenem and azithromycin, in Pakistan. PLoS Negl Trop Dis 14: e0008682.

    • Search Google Scholar
    • Export Citation
  • 17.

    Iqbal J , Dehraj IF , Carey ME , Dyson ZA , Garrett D , Seidman JC , Kabir F , Saha S , Baker S , Qamar FN , 2020. A race against time: reduced azithromycin susceptibility in Salmonella enterica serovar Typhi in Pakistan. mSphere 5: e00215e00220.

    • Search Google Scholar
    • Export Citation
  • 18.

    Fida S , Mansoor H , Saif S , Iqbal J , Khan AQ , 2021. Clinical perspectives of multiple and extensively drug-resistant typhoid: result from a tertiary care hospital from Pakistan. J Infect Dev Ctries 15: 530537.

    • Search Google Scholar
    • Export Citation
  • 19.

    Goldblatt J , Ward A , Day M , Godbole G , Morris-Jones S , 2020. In-house azithromycin MIC estimation by gradient strip in Salmonella enterica var Typhi and Paratyphi: do you believe it? Access Microbiol 2: 214.

    • Search Google Scholar
    • Export Citation
  • 20.

    Goldblatt J , Ward A , Yusuf M , Day M , Godbole G , Morris-Jones S , 2020. Azithromycin susceptibility testing for Salmonella enterica isolates: discordances in results using MIC gradient strips. J Antimicrob Chemother 75: 18201823.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 299 299 69
Full Text Views 1789 1789 82
PDF Downloads 188 188 61
 
 
 
 
 
 
 
 
 
 
 

Reporting of Azithromycin Activity against Clinical Isolates of Extensively Drug-Resistant Salmonella enterica Serovar Typhi

Kokab JabeenUniversity of Health Sciences, Lahore, Pakistan;

Search for other papers by Kokab Jabeen in
Current site
Google Scholar
PubMed
Close
,
Sidrah SaleemUniversity of Health Sciences, Lahore, Pakistan;

Search for other papers by Sidrah Saleem in
Current site
Google Scholar
PubMed
Close
,
Summiya NizamuddinShaukat Khanum Memorial Cancer Hospital, Lahore, Pakistan;

Search for other papers by Summiya Nizamuddin in
Current site
Google Scholar
PubMed
Close
,
Faiqa ArshadUniversity of Health Sciences, Lahore, Pakistan;

Search for other papers by Faiqa Arshad in
Current site
Google Scholar
PubMed
Close
,
Shah JahanUniversity of Health Sciences, Lahore, Pakistan;

Search for other papers by Shah Jahan in
Current site
Google Scholar
PubMed
Close
,
Faisal HasnainSheikh Zayed Hospital, Rahim Yar Khan, Pakistan;

Search for other papers by Faisal Hasnain in
Current site
Google Scholar
PubMed
Close
,
Waleed TariqLahore General Hospital, Lahore, Pakistan;

Search for other papers by Waleed Tariq in
Current site
Google Scholar
PubMed
Close
,
Muhammad Junaid TahirPakistan Kidney and Liver Institute and Research Center (PKLI & RC), Lahore, Pakistan;

Search for other papers by Muhammad Junaid Tahir in
Current site
Google Scholar
PubMed
Close
,
Zohaib YousafTower Health, Reading, Pennsylvania;

Search for other papers by Zohaib Yousaf in
Current site
Google Scholar
PubMed
Close
, and
Muhammad Sohaib AsgharDow University of Health Sciences, Karachi, Pakistan

Search for other papers by Muhammad Sohaib Asghar in
Current site
Google Scholar
PubMed
Close
View More View Less
Restricted access

ABSTRACT.

This study aimed to evaluate the minimum inhibitory concentration (MIC) of azithromycin (AZM) in clinical isolates of extensively drug-resistant (XDR) Salmonella Typhi (i.e., resistant to chloramphenicol, ampicillin, trimethoprim-sulfamethoxazole, fluoroquinolones, and third-generation cephalosporin) using the E-test versus the broth microdilution method (BMD). From January to June 2021, a retrospective cross-sectional study was carried out in Lahore, Pakistan. Antimicrobial susceptibility was performed initially by the Kirby-Bauer disk diffusion method for 150 XDR Salmonella enterica serovar Typhi isolates, and MICs of all the recommended antibiotics were determined by the VITEK 2 (BioMérieux) fully automated system using Clinical Laboratory Standard Institute (CLSI) 2021 guidelines. The E-test method was used to determine AZM MICs. These MICs were compared with the BMD, which is the method recommended by the CLSI but not adopted in routine laboratory reporting. Of 150 isolates, 10 (6.6%) were resistant by disk diffusion. Eight (5.3%) of these had high MICs against AZM by the E-test. Only three isolates (2%) were resistant by E-test, having an MIC of 32 μg/mL. All eight isolates had a high MIC by BMD with different MIC distributions, but only one was resistant, having an MIC of 32 μg/mL by BMD. The sensitivity, specificity, negative predictive value, positive predictive value, and diagnostic accuracy of the E-test method versus BMD were 98.65%,100%, 99.3%, 33.3%, and 98.6%, respectively. Similarly, the concordance rate was 98.6%, negative percent agreement was 100%, and positive percent agreement was 33%. The BMD is the most reliable approach for reporting AZM sensitivity in XDR S. Typhi compared with the E-test and disk diffusion methods. Potentially, AZM resistance in XDR S. Typhi is around the corner. Sensitivity patterns should be reported with MIC values, and if possible, higher values should be screened for the presence of any potential resistance genes. Antibiotic stewardship should be strictly implemented.

Author Notes

Address correspondence to Muhammad Sohaib Asghar, Dow University of Health Sciences, B328 Block 6 Gulshan E Iqbal, Karachi, Sindh 75300, Pakistan. E-mail: sohaib_asghar123@yahoo.com

The datasets used and/or analyzed during the current study are not publicly available because the study was completely anonymous. This study was conducted using the bacterial strains that were isolated for diagnostic and treatment purposes. However, they are available from the corresponding author upon reasonable request.

Authors’ addresses: Kokab Jabeen, Sidrah Saleem, Faiqa Arshad, and Shah Jahan, University of Health Sciences, Lahore, Pakistan, E-mails: kaukab_jabeen@yahoo.com, sidrah.78@gmail.com, drfaiqaimran@gmail.com, and shahjahan@uhs.edu.pk. Summiya Nizamuddin, Shaukat Khanum Memorial Cancer Hospital, Lahore, Pakistan, E-mail: summiyan@skm.org.pk. Faisal Hasnain, Sheikh Zayed Hospital, Rahim Yar Khan, Pakistan, E-mail: riofaisy@gmail.com. Waleed Tariq, Lahore General Hospital, Lahore, Pakistan, E-mail: tariqwaleed635@gmail.com. Muhammad Junaid Tahir, Pakistan Kidney and Liver Institute and Research Center (PKLI & RC), Lahore, Pakistan, E-mail: junaid262626@gmail.com. Zohaib Yousaf, Tower Health, Reading, PA, E-mail: zohaib.yousaf@gmail.com. Muhammad Sohaib Asghar, Dow University of Health Sciences, Karachi, Pakistan, E-mail: sohaib_asghar123@yahoo.com.

Save