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Afzal A, Sarwar Y, Ali A, Haque A, 2012. Current status of fluoroquinolone and cephalosporin resistance in Salmonella enterica serovar Typhi isolates from Faisalabad, Pakistan. Pak J Med Sci 28: 602–607.
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Deresinski S, 2018. XDR typhoid fever abruptly emerges in Pakistan due to acquisition of a plasmid encoding antimicrobial resistance genes. Clin Infect Dis 66: iii–iv.
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Typhoid Fever in the Eastern Mediterranean Region: A Systematic Review, 1990–2021
Grace D. Appiah
Grace D. Appiah
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Phong Le
Phong Le
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Graeme Prentice-Mott
Graeme Prentice-Mott
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Megan Bias
Megan Bias
Center for Surveillance, Epidemiology, and Laboratory Services, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Caroline Pratt
Caroline Pratt
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Ghassan M. Matar
Ghassan M. Matar
Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon
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Talia Pindyck
Talia Pindyck
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Antoine Abou Fayad
Antoine Abou Fayad
Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon
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Sunkyung Kim
Sunkyung Kim
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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Eric D. Mintz
Eric D. Mintz
Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control and Prevention, Atlanta, Georgia;
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ABSTRACT.
The occurrence and antimicrobial resistance (AMR) of typhoid fever in the WHO Eastern Mediterranean Region (EMR) are poorly characterized. Robust surveillance data are needed to inform strategies for typhoid control and prevention in the region. We conducted a systematic review of typhoid fever occurrence, complications, and AMR patterns in EMR countries. We identified 70 studies published from 1990 to 2021, including a total of 44,541 cases with blood culture confirmed typhoid fever in 12 EMR countries, with 48 (69%) studies and 42,008 cases from Pakistan. Among 56 studies with AMR data, fluroquinolone (68% of 13,013 tested isolates), and multidrug resistance (40% of 15,765 tested isolates) were common. Forty (57%) of the 56 studies were from Pakistan, and all reports of extensively drug resistant Salmonella Typhi (48% of 9,578 tested isolates) were from studies in Pakistan. Our findings support the need for continued efforts to strengthen surveillance and laboratory capacity for blood-culture detection of typhoid fever in the region, including data from an ongoing collaboration among CDC, the American University of Beirut, and the WHO EMR office.
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Author Notes
Financial support: This study was supported by funding from Gavi, the Vaccine Alliance.
Disclosures: The opinions expressed by authors contributing to this manuscript do not necessarily reflect the opinions of the CDC or the institutions with which the authors are affiliated.
Authors’ addresses: Grace D. Appiah, Phong Le, Graeme Prentice-Mott, Caroline Pratt, Talia Pindyck, Sunkyung Kim, and Eric D. Mintz, Division of Foodborne, Waterborne and Environmental Diseases, U.S. Centers for Disease Control, Atlanta, GA, E-mails: ydg3@cdc.gov, pyv8@cdc.gov, qbt1@cdc.gov, yqg5@cdc.gov, nrb1@cdc.gov, wox0@cdc.gov, and ericdmintz@gmail.com. Megan Bias, Center for Surveillance, Epidemiology, and Laboratory Services, U.S. Centers for Disease Control, Atlanta, GA, E-mail: pwj1@cdc.gov. Ghassan M. Matar and Antoine Abou Fayad, Department of Experimental Pathology, Immunology and Microbiology, Faculty of Medicine, American University of Beirut, Beirut, Lebanon, E-mails: gmatar@aub.edu.lb and aa328@aub.edu.lb.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, Döpfer D, Fazil A, Fischer-Walker CL, Hald T, 2015. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med 12: e1001921.
-
2.
Antillón M, Warren JL, Crawford FW, Weinberger DM, Kürüm E, Pak GD, Marks F, Pitzer VE, 2017. The burden of typhoid fever in low-and middle-income countries: a meta-regression approach. PLoS Negl Trop Dis 11: e0005376.
-
3.
Klemm EJ et al., 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: 20.
-
4.
Qamar FN et al., 2018. Outbreak investigation of ceftriaxone-resistant Salmonella enterica serotype Typhi and its risk factors among the general population in Hyderabad, Pakistan: a matched case–control study. Lancet Infect Dis 18: 1368–1376.
-
5.
Buliva E, Elhakim M, Tran Minh NN, Elkholy A, Mala P, Abubakar A, Malik SMMR, 2017. Emerging and reemerging diseases in the World Health Organization (WHO) Eastern Mediterranean Region—progress, challenges, and WHO initiatives. Front Public Health 5: 276.
-
6.
Raslan R, El Sayegh S, Chams S, Chams N, Leone A, Hajj Hussein I, 2017. Re-emerging vaccine-preventable diseases in war-affected peoples of the eastern Mediterranean region—an update. Front Public Health 5: 283.
-
7.
Marmot M, Al-Mandhari A, Ghaffar A, El-Adawy M, Hajjeh R, Khan W, Allen J, 2021. Build back fairer: achieving health equity in the Eastern Mediterranean region of WHO. Lancet 397: 1527–1528.
-
8.
Chenoweth J, Hadjinicolaou P, Bruggeman A, Lelieveld J, Levin Z, Lange MA, Xoplaki E, Hadjikakou M, 2011. Impact of climate change on the water resources of the eastern Mediterranean and Middle East region: modeled 21st century changes and implications. Water Resour Res 47: W06506.
-
9.
World Health Organization , 2021. Progress on Household Drinking Water, Sanitation and Hygiene 2000–2020: Five Years into the SDGs. Geneva, Switzerland: WHO.
-
10.
Kim J-H, Mogasale V, Im J, Ramani E, Marks F, 2017. Updated estimates of typhoid fever burden in sub-Saharan Africa. Lancet Glob Health 5: e969.
-
11.
Carey ME, MacWright WR, Im J, Meiring JE, Gibani MM, Park SE, Longley A, Jeon HJ, Hemlock C, Yu AT, 2020. The surveillance for enteric fever in Asia project (SEAP), severe typhoid fever surveillance in Africa (SETA), surveillance of enteric fever in India (SEFI), and strategic typhoid alliance across Africa and Asia (STRATAA) population-based enteric fever studies: a review of methodological similarities and differences. Clin Infect Dis 71: S102–S110.
-
12.
Stanaway JD et al., 2019. The global burden of typhoid and paratyphoid fevers: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19: 369–381.
-
13.
Tajbakhsh M, Hendriksen RS, Nochi Z, Zali MR, Aarestrup FM, Garcia-Migura L, 2012. Antimicrobial resistance in Salmonella spp. recovered from patients admitted to six different hospitals in Tehran, Iran from 2007 to 2008. Folia Microbiol (Praha) 57: 91–97.
-
14.
Ghenghesh KS, Franka E, Tawil K, Wasfy MO, Ahmed SF, Rubino S, Klena JD, 2009. Enteric fever in Mediterranean north Africa. J Infect Dev Ctries 3: 753–761.
-
15.
Rotimi VO, Jamal W, Pal T, Sonnevend A, Dimitrov TS, Albert MJ, 2008. Emergence of multidrug-resistant Salmonella spp. and isolates with reduced susceptibility to ciprofloxacin in Kuwait and the United Arab Emirates. Diagn Microbiol Infect Dis 60: 71–77.
-
16.
Bukhari N et al., 2016. Frequency of typhoid fever and its association with seasonal variations in Taxila, Pakistan. Asian Pac J Trop Dis 6: 608–610.
-
17.
Kalsoom, Fazal A, Muhammad Y, Umber T, Muhammad S, Ali SS, Shahid A, Anila R, 2014. Prevalence of typhoid fever in five Southern districts of Khyber Pakhtunkhwa, Pakistan: a preliminary study. Int J Biosci 4: 325–330.
-
18.
Al-Ameri G, Saif N, 2014. A prevalence study of typhoid fever in Taiz and Al-Hodiedahcities in Yemen. Br Microbiol Res J 4: 214–223.
-
19.
Essayagh M, Rhaffouli AE, Essayagh S, Essayagh T, 2020. Epidemiology profile of fever typhoid in Meknes (Morocco) 2013–2016 [in French]. Rev Epidemiol Sante Publique 68: 45–49.
-
20.
Jamro B, Shaikh NA, Sohu KM, Soomro AA, Lal S, Jamro S, 2012. Treatment outcome of enteric fever in children at tertiary care hospital Sukkur Pakistan. Medical Forum Monthly 23: 8–11.
-
21.
Muhammad Abbas B, Tassawer e M, Musharraf AB, Fatima T, Amjad H, Mudassar Abbas B, 2018. Assessment of prevalence, diagnostic tests and prescription trends of typhoid fever in children below 12 years in Sialkot, Pakistan. Pharmacologyonline 1: 1–8.
-
22.
Naeem Khan M, Shafee M, Hussain K, Samad A, Arif Awan M, Manan A, Wadood A, 2013. Typhoid fever in paediatric patients in Quetta, Balochistan, Pakistan. Pak J Med Sci 29: 929–932.
-
23.
Tohme A, Zein E, Nasnas R, 2004. Typhoid fever. Clinical and therapeutic study in 70 patients [French]. J Med Liban 52: 71–77.
-
24.
Elshayeb AA, Ahmed AA, El Siddig MA, El Hussien AA, 2017. Prevalence of current patterns and predictive trends of multidrug-resistant Salmonella typhi in Sudan. Ann Clin Microbiol Antimicrob 16: 73.
-
25.
Hassan Alredaisy SMA, 2009. Typhoid fever in Sudan: some geographic and time considerations from 2000 through 2008. Arab World Geogr 12: 173–187.
-
26.
Afzal A, Sarwar Y, Ali A, Haque A, 2012. Current status of fluoroquinolone and cephalosporin resistance in Salmonella enterica serovar Typhi isolates from Faisalabad, Pakistan. Pak J Med Sci 28: 602–607.
-
27.
Rasul F, Sughra K, Mushtaq A, Zeeshan N, Mehmood S, Rashid U, 2017. Surveillance report on typhoid fever epidemiology and risk factor assessment in district Gujrat, Punjab, Pakistan. Biomed Res (India) 28: 6921–6926.
-
28.
Bhutta ZA, 1998. Epidemiology of typhoidal salmonellosis in childhood: the Pakistan country report. Med J Indones 7: 9.
-
29.
Dimitrov T, Dashti AA, Albaksami O, Jadaon MM, 2010. Detection of mutations in the gyrA gene in fluoroquinolone resistance Salmonella enterica serotypes typhi and paratyphi A isolated from the Infectious Diseases Hospital, Kuwait. J Clin Pathol 63: 83–87.
-
30.
Deresinski S, 2018. XDR typhoid fever abruptly emerges in Pakistan due to acquisition of a plasmid encoding antimicrobial resistance genes. Clin Infect Dis 66: iii–iv.
-
31.
Bobin AN, Parkhomenko Iu G, 2009. [Complications of typhoid fever and its causes in an epidemic focus]. Arkh Patol 71: 46–50.
-
32.
Abro AH, Siddiqui FG, Sarfraz A, 2012. Demographic and surgical evaluation of typhoid ileal perforation. J Ayub Med Coll 24: 87–89.
-
33.
Farid Z, 1992. Multiresistant Salmonella typhi infection in Cairo. Trans R Soc Trop Med Hyg 86: 224.
-
34.
Munir T, Lodhi M, Ansari JK, Andleeb S, Ahmed M, 2016. Extended spectrum beta lactamase producing cephalosporin resistant Salmonella typhi, reported from Rawalpindi, Pakistan. J Pak Med Assoc 66: 1035–1036.
-
35.
Petrin CE, Steele RW, Margolis EA, Rabon JM, Martin H, Wright A, 2019. Drug-resistant Salmonella typhi in Pakistan. Clin Pediatr 59: 31–33.
-
36.
el-Sherbini A, 1992. An outbreak of typhoid fever resistant to chloramphenicol and other drugs in Gharbeya Governorate in Egypt. J Trop Pediatr 38: 331–334.
-
37.
Saida NB, Mhalla S, Bouzouïa N, Boukadida J, 2007. Genotypic analysis of Salmonella enterica serovar Typhi collected during two successive autumnal typhoid outbreaks in southeast Tunisia. Pathol Biol (Paris) 55: 336–339.
-
38.
Srikantiah P, Girgis FY, Luby SP, Jennings G, Wasfy MO, Crump JA, Hoekstra RM, Anwer M, Mahoney FJ, 2006. Population-based surveillance of typhoid fever in Egypt. Am J Trop Med Hyg 74: 114–119.
-
39.
Ali Shah SA, Nadeem M, Syed SA, Fatima Abidi ST, Khan N, Bano N, 2020. Antimicrobial sensitivity pattern of Salmonella typhi: emergence of resistant strains. Cureus 12: e11778.
-
40.
Fatima M et al., 2021. Morbidity and mortality associated with typhoid fever among hospitalized patients in Hyderabad District, Pakistan, 2017–2018: retrospective record review. JMIR Public Health Surveill 7: e27268.
-
41.
Qamar FN et al., 2020. Antimicrobial resistance in typhoidal Salmonella: surveillance for Enteric Fever in Asia Project, 2016–2019. Clin Infect Dis 71: S276–S284.
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