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RefWorks
Reference Manager
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Zotero
EndNote
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Adesegun O, Adeyemi O, Ehioghae O, Rabor D, Binuyo T, Alafin B, Nnagha O, Idowu A, Osonuga A, 2020. Current trends in the epidemiology and management of enteric fever in Africa: A literature review. Asian Pac J Trop Med 13: 204–213.
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Bebell LM, Muiru AN, 2014. Antibiotic use and emerging resistance: How can resource-limited countries turn the tide? Glob Heart 9: 347–358.
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Elven J, et al., 2020. Non-malarial febrile illness: A systematic review of published aetiological studies and case reports from Africa, 1980–2015. BMC Med 18: 279.
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Tufa TB, et al., 2022. Prevalence and characterization of antimicrobial resistance among gram-negative bacteria isolated from febrile hospitalized patients in central Ethiopia. Antimicrob Resist Infect Control 11: 8.
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Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K, 2004. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol 42: 5636–5643.
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14.
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF, 2004. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 42: 3164–3168.
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Malorny B, Paccassoni E, Fach P, Bunge C, Martin A, Helmuth R, 2004. Diagnostic real-time PCR for detection of Salmonella in food. Appl Environ Microbiol 70: 7046–7052.
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Grywna K, Kupfer B, Panning M, Drexler JF, Emmerich P, Drosten C, Kümmerer BM, 2010. Detection of all species of the genus Alphavirus by reverse transcription-PCR with diagnostic sensitivity. J Clin Microbiol 48: 3386–3387.
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Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, de Lamballerie X, 2007. A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 7: 467–477.
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Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Krüger DH, 2006. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12: 838–840.
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Ethiopian Ministry of Health, 2017. Ethiopian Primary Health Care Clinical Guidelines: Care of Children 5-14 years and Adults 15 years of older in Health Centers. Available at: https://www.researchgate.net/publication/343609968_Ethiopian_Primary_Health_Care_Clinical_Guidelines. Accessed January 6, 2023.
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Kotepui M, Kotepui KU, De Jesus Milanez G, Masangkay FR, 2020. Summary of discordant results between rapid diagnosis tests, microscopy, and polymerase chain reaction for detecting Plasmodium mixed infection: A systematic review and meta-analysis. Sci Rep 10: 12765.
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Detection of Bacterial Infections and Malaria among Blood Culture-Negative Samples of Hospitalized Febrile Patients from a Tertiary Hospital in Ethiopia
Tafese Beyene Tufa
tafeseb.tufa@yahoo.com
Tafese Beyene Tufa
Hirsch Institute of Tropical Medicine, Asella, Ethiopia;
College of Health Sciences, Arsi University, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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College of Health Sciences, Arsi University, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Ignacio Postigo-Hidalgo
Ignacio Postigo-Hidalgo
Institute of Virology, Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany;
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André Fuchs
André Fuchs
Internal Medicine III–Gastroenterology and Infectious Diseases, University Hospital of Augsburg, Augsburg, Germany;
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Hans Martin Orth
Hans Martin Orth
Hirsch Institute of Tropical Medicine, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Dieter Häussinger
Dieter Häussinger
Hirsch Institute of Tropical Medicine, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Tom Luedde
Tom Luedde
Hirsch Institute of Tropical Medicine, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Marco Kaiser
Marco Kaiser
TIB Molbiol Syntheselabor GmbH, Berlin, Germany
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Pranav Patel
Pranav Patel
TIB Molbiol Syntheselabor GmbH, Berlin, Germany
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Olfert Landt
Olfert Landt
TIB Molbiol Syntheselabor GmbH, Berlin, Germany
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Jan Felix Drexler
Jan Felix Drexler
Institute of Virology, Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany;
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Torsten Feldt
Torsten Feldt
Hirsch Institute of Tropical Medicine, Asella, Ethiopia;
Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany;
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ABSTRACT.
Febrile illnesses contribute significantly to morbidity and mortality in sub-Saharan Africa, but the lack of diagnostic facilities and the broad spectrum of pathogens can lead to inadequate clinical management. The timely and reliable identification of the causative pathogens in febrile patients is the basis for the administration of optimal treatment. We aimed to evaluate the performance of a multiplex polymerase chain reaction (PCR) among blood culture-negative patients presenting with febrile diseases in Central Ethiopia. From April 2016 to June 2018, we collected blood samples from adults and children ≥1 year of age admitted with febrile diseases to the Asella Referral and Teaching Hospital, which is located at an altitude of 2,400 m. Total nucleic acids were extracted from frozen plasma samples using a MagNA Pure 96 instrument (Roche, Mannheim, Germany). The multiplex PCR assays were used in combination with LightCycler multiplex DNA master mix (Roche) on a LightCycler 480 instrument (Roche). We used the pathogen-specific assays targeted to Plasmodium spp., Borrelia spp., Rickettsia spp., Leptospira spp., Salmonella spp., and arboviruses. We tested plasma samples of 511 patients and found positive results for Plasmodium spp. (13, 2.5%), Borrelia spp. (12, 2.3%), and Rickettsia species (7, 1.3%); in total, pathogens were detected in 32 of the samples (6.3%). No pathogen was detected by multiplex PCR in 94% of blood culture-negative samples. Even if the pathogens identified by PCR were not necessarily causes of fever, molecular testing using a multiplex PCR can contribute to pathogen diagnosis in a proportion of febrile patients in the highland part of Ethiopia and help to improve the clinical management.
Author Notes
Financial support: There was no direct financial support for this study. However, Hirsch Institute of Tropical Medicine in Asella, Ethiopia, supported the sample and data collection and the Institute of Virology, Charité–Universitätsmedizin Berlin, Germany, performed the laboratory testing. We thank the Bayer Foundation’s “Talents for Africa” scholarship program and the Heinz Ansmann Foundation for AIDS Research for supporting T. B. Tufa’s scholarship.
Disclosure: Our study protocol received ethical approval from the ethical review boards of Arsi University (reference number A/U/H/S/C/120/6443/2017), Oromia Regional Health Bureau (reference number BEFO/AHBTFH/1-8/2017), National Ethical Review Board of the Ministry of Science and Technology, Ethiopia (reference number 310/204/2017), and the University Hospital of Düsseldorf, Germany (reference number 5729).
Current contact information: Tafese Beyene Tufa, Hirsch Institute of Tropical Medicine, Asella, Ethiopia, College of Health Sciences, Arsi University, Asella, Ethiopia, and Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany, E-mail: tafeseb.tufa@yahoo.com. Ignacio Postigo-Hidalgo and Jan Felix Drexler, Institute of Virology, Charité–Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany, E-mails: ignacio.postigo@charite.de and felix.drexler@charite.de. André Fuchs, Internal Medicine III–Gastroenterology and Infectious Diseases, University Hospital of Augsburg, Augsburg, Germany, E-mail: fuchs.andre@googlemail.com. Hans Martin Orth, Dieter Häussinger, Tom Luedde, and Torsten Feldt, Hirsch Institute of Tropical Medicine, Asella, Ethiopia, and Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany, E-mails: hansmartin.orth@med.uni-duesseldorf.de, haeussin@uni-duesseldorf.de, tom.luedde@med.uni-duesseldorf.de, and torsten.feldt@med.uni-duesseldorf.de. Marco Kaiser, Pranav Patel, and Olfert Landt, TIB Molbiol Syntheselabor GmbH, Berlin, Germany, E-mails: mkaiser@tib-molbiol.de, pranav412_ahd@yahoo.com, and olandt@landtberlin.de.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
GBD 2016 Causes of Death Collaborators, 2017. Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 390: 1151–1210.
-
2.
Boutayeb A, 2010. The impact of infectious diseases on the development of Africa. Preedy VR & Watson RR Handbook of Disease Burdens and Quality of Life Measures. Springer Nature, 1171–1188.
-
3.
Ogoina D, 2011. Fever, fever patterns and diseases called ‘fever’—A review. J Infect Public Health 4: 108–124.
-
4.
Birkhold M, Coulibaly Y, Coulibaly O, Dembele P, Kim DS, Sow S, Neuzil KM, 2020. Morbidity and mortality of typhoid intestinal perforation among children in sub-Saharan Africa 1995–2019: A scoping review. World J Surg 44: 2892–2902.
-
5.
Moyo SJ, et al., 2020. Bacteraemia, malaria, and case fatality among children hospitalized with fever in Dar es Salaam, Tanzania. Front Microbiol 11: 2118.
-
6.
Adesegun O, Adeyemi O, Ehioghae O, Rabor D, Binuyo T, Alafin B, Nnagha O, Idowu A, Osonuga A, 2020. Current trends in the epidemiology and management of enteric fever in Africa: A literature review. Asian Pac J Trop Med 13: 204–213.
-
7.
Tawiah T, et al., 2016. Economic costs of fever to households in the middle belt of Ghana. Malar J 15: 68.
-
8.
Hopkins H, et al., 2017. Impact of introduction of rapid diagnostic tests for malaria on antibiotic prescribing: Analysis of observational and randomised studies in public and private healthcare settings. BMJ 356: j1054.
-
9.
Bebell LM, Muiru AN, 2014. Antibiotic use and emerging resistance: How can resource-limited countries turn the tide? Glob Heart 9: 347–358.
-
10.
Elven J, et al., 2020. Non-malarial febrile illness: A systematic review of published aetiological studies and case reports from Africa, 1980–2015. BMC Med 18: 279.
-
11.
Mulders-Manders C, Simon A, Bleeker-Rovers C, 2015. Fever of unknown origin. Clin Med (Lond) 15: 280–284.
-
12.
Tufa TB, et al., 2022. Prevalence and characterization of antimicrobial resistance among gram-negative bacteria isolated from febrile hospitalized patients in central Ethiopia. Antimicrob Resist Infect Control 11: 8.
-
13.
Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K, 2004. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol 42: 5636–5643.
-
14.
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF, 2004. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 42: 3164–3168.
-
15.
Liu J, et al., 2016. Development of a TaqMan Array Card for Acute-Febrile-Illness Outbreak Investigation and Surveillance of Emerging Pathogens, Including Ebola Virus. J Clin Microbiol 54: 49–58.
-
16.
Ahmed A, van der Linden H, Hartskeerl RA, 2014. Development of a recombinase polymerase amplification assay for the detection of pathogenic Leptospira. Int J Environ Res Public Health 11: 4953–4964.
-
17.
Malorny B, Paccassoni E, Fach P, Bunge C, Martin A, Helmuth R, 2004. Diagnostic real-time PCR for detection of Salmonella in food. Appl Environ Microbiol 70: 7046–7052.
-
18.
Grywna K, Kupfer B, Panning M, Drexler JF, Emmerich P, Drosten C, Kümmerer BM, 2010. Detection of all species of the genus Alphavirus by reverse transcription-PCR with diagnostic sensitivity. J Clin Microbiol 48: 3386–3387.
-
19.
Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, de Lamballerie X, 2007. A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 7: 467–477.
-
20.
Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Krüger DH, 2006. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12: 838–840.
-
21.
Yimer M, Abera B, Mulu W, Bezabih B, Mohammed J, 2014. Prevalence and risk factors of louse-borne relapsing fever in high risk populations in Bahir Dar city Northwest, Ethiopia. BMC Res Notes 7: 615.
-
22.
Ethiopian Ministry of Health, 2017. Ethiopian Primary Health Care Clinical Guidelines: Care of Children 5-14 years and Adults 15 years of older in Health Centers. Available at: https://www.researchgate.net/publication/343609968_Ethiopian_Primary_Health_Care_Clinical_Guidelines. Accessed January 6, 2023.
-
23.
Kotepui M, Kotepui KU, De Jesus Milanez G, Masangkay FR, 2020. Summary of discordant results between rapid diagnosis tests, microscopy, and polymerase chain reaction for detecting Plasmodium mixed infection: A systematic review and meta-analysis. Sci Rep 10: 12765.
-
24.
Röttgerding F, et al., 2022. Novel approaches for the serodiagnosis of louse-borne relapsing fever. Front Cell Infect Microbiol 12: 983770.
-
25.
Kularatne SA, Gawarammana IB, 2009. Validity of the Weil-Felix test in the diagnosis of acute rickettsial infections in Sri Lanka. Trans R Soc Trop Med Hyg 103: 423–424.
-
26.
Di Tanna GL, et al., 2019. Effect of Xpert MTB/RIF on clinical outcomes in routine care settings: Individual patient data meta-analysis. Lancet Glob Health 7: e191–e199.
-
27.
Dailey PJ, Osborn J, 2019. Blood Culture: Landscape of Simplified and Integrated Systems for Pathogen Identification and Antimicrobial Susceptibility Testing. Geneva, Switzerland: FIND.
-
28.
Ramos JM, et al., 2019. Arthropod-borne bacteria cause nonmalarial fever in rural Ethiopia: A cross-sectional study in 394 patients. Vector Borne Zoonotic Dis 19: 815–820.
-
29.
Aarsland SJ, Castellanos-Gonzalez A, Lockamy KP, Mulu-Droppers R, Mulu M, White AC, Cabada MM, 2012. Treatable bacterial infections are underrecognized causes of fever in Ethiopian children. Am J Trop Med Hyg 87: 128–133.
-
30.
Zerfu B, Medhin G, Mamo G, Getahun G, Tschopp R, Legesse M, 2018. Community-based prevalence of typhoid fever, typhus, brucellosis and malaria among symptomatic individuals in Afar Region, Ethiopia. PLoS Negl Trop Dis 12: e0006749.
-
31.
Reta A, Bitew Kifilie A, Mengist A, 2019. Bacterial infections and their antibiotic resistance pattern in Ethiopia: A systematic review. Adv Prev Med 2019: 4380309.
-
32.
Mohammed MA, Hong T, 2021. Role of vector control in fighting against malaria: Evidence from Ethiopian health-related indicators. J Infect Public Health 14: 527–532.
-
33.
Tegegne Y, Worede A, Derso A, Ambachew S, 2021. The prevalence of malaria among children in Ethiopia: A systematic review and meta-analysis. J Parasitol Res 2021: 6697294.
-
34.
Kendie FA, Hailegebriel WKT, Nibret Semegn E, Ferede MW, 2021. Prevalence of malaria among adults in Ethiopia: A systematic review and meta-analysis. J Trop Med 2021: 8863002.
-
35.
Girum T, Shumbej T, Shewangizaw M, 2019. Burden of malaria in Ethiopia, 2000–2016: Findings from the Global Health Estimates 2016. Trop Dis Travel Med Vaccines 5: 11.
-
36.
Ketema T, Getahun K, Bacha K, 2011. Therapeutic efficacy of chloroquine for treatment of Plasmodium vivax malaria cases in Halaba district, South Ethiopia. Parasit Vectors 4: 46.
-
37.
Ramos JM, Malmierca E, Reyes F, Tesfamariam A, 2008. Results of a 10-year survey of louse-borne relapsing fever in southern Ethiopia: A decline in endemicity. Ann Trop Med Parasitol 102: 467–469.
-
38.
Cutler SJ, Abdissa A, Trape JF, 2009. New concepts for the old challenge of African relapsing fever borreliosis. Clin Microbiol Infect 15: 400–406.
-
39.
Badiaga S, Brouqui P, 2012. Human louse-transmitted infectious diseases. Clin Microbiol Infect 18: 332–337.
-
40.
Nordmann T, Feldt T, Bosselmann M, Tufa TB, Lemma G, Holtfreter M, Haussinger D, 2018. Outbreak of louse-borne relapsing fever among urban dwellers in Arsi Zone, Central Ethiopia, from July to November 2016. Am J Trop Med Hyg 98: 1599–1602.
-
41.
Yimer M, Mulu W, Ayalew W, Abera B, 2014. Louse-borne relapsing fever profile at Felegehiwot referral hospital, Bahir Dar city, Ethiopia: A retrospective study. BMC Res Notes 7: 250.
-
42.
Teshale S, Kumsa B, Menandro ML, Cassini R, Martini M, 2016. Anaplasma, Ehrlichia and rickettsial pathogens in ixodid ticks infesting cattle and sheep in western Oromia, Ethiopia. Exp Appl Acarol 70: 231–237.
-
43.
Kumsa B, Parola P, Raoult D, Socolovschi C, 2014. Molecular detection of Rickettsia felis and Bartonella henselae in dog and cat fleas in Central Oromia, Ethiopia. Am J Trop Med Hyg 90: 457–462.
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