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-
1.
Lee HW, Lee PW, Johnson KM, 1978. Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis 137: 298–308.
-
2.
Kim YS, Ahn C, Han JS, Kim S, Lee JS, Lee PW, 1995. Hemorrhagic fever with renal syndrome caused by the Seoul virus. Nephron 71: 419–427.
-
3.
Lee JS, 1991. Clinical features of hemorrhagic fever with renal syndrome in Korea. Kidney Int Suppl 35: S88–S93.
-
4.
Kim WK et al., 2016. Phylogeographic analysis of hemorrhagic fever with renal syndrome patients using multiplex PCR-based next generation sequencing. Sci Rep 6: 26017.
-
5.
Noh JY, Jung J, Song JW, 2019. Hemorrhagic fever with renal syndrome. Infect Chemother 51: 405–413.
-
6.
Mattar S, Guzmán C, Figueiredo LT, 2015. Diagnosis of hantavirus infection in humans. Expert Rev Anti Infect Ther 13: 939–946.
-
7.
Hujakka H, Koistinen V, Kuronen I, Eerikäinen P, Parviainen M, Lundkvist A, Vaheri A, Vapalahti O, Närvänen A, 2003. Diagnostic rapid tests for acute hantavirus infections: specific tests for Hantaan, Dobrava and Puumala viruses versus a hantavirus combination test. J Virol Methods 108: 117–122.
-
8.
Kim WK et al., 2018. Multiplex PCR-based next-generation sequencing and global diversity of Seoul virus in humans and rats. Emerg Infect Dis 24: 249–257.
-
9.
Lagerqvist N, Hagström Å, Lundahl M, Nilsson E, Juremalm M, Larsson I, Alm E, Bucht G, Ahlm C, Klingström J, 2016. Molecular diagnosis of hemorrhagic fever with renal syndrome caused by Puumala virus. J Clin Microbiol 54: 1335–1339.
-
10.
Lednicky JA, 2003. Hantaviruses. a short review. Arch Pathol Lab Med 127: 30–35.
-
11.
Pettersson L, Klingstrom J, Hardestam J, Lundkvist A, Ahlm C, Evander M, 2008. Hantavirus RNA in saliva from patients with hemorrhagic fever with renal syndrome. Emerg Infect Dis 14: 406–411.
-
12.
Jalal S, Jha B, Kim CM, Kim DM, Yun NR, Kim YS, Park JW, Chung JK, 2019. Molecular detection of viruses causing hemorrhagic fevers in rodents in the south-west of Korea. J Neurovirol 25: 239–247.
-
13.
Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Kruger DH, 2006. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12: 838–840.
-
14.
Kim HK, Chung JH, Kim DM, Yun NR, Kim CM, Jalal S, 2019. Hemorrhagic fever with renal syndrome as a cause of acute diarrhea. Am J Trop Med Hyg 100: 1236–1239.
-
15.
Baek LJ et al., 2006. Soochong virus: an antigenically and genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J Med Virol 78: 290–297.
-
16.
Bi Z, Formenty PB, Roth CE, 2008. Hantavirus infection: a review and global update. J Infect Dev Ctries 2: 3–23.
-
17.
Du H, Wang PZ, Li J, Bai L, Li H, Yu HT, Jiang W, Zhang Y, Wang JN, Bai XF, 2014. Clinical characteristics and outcomes in critical patients with hemorrhagic fever with renal syndrome. BMC Infect Dis 14: 191.
-
18.
Manigold T, Vial P, 2014. Human hantavirus infections: epidemiology, clinical features, pathogenesis and immunology. Swiss Med Wkly 144: w13937.
-
19.
Kruger DH, Ulrich RG, Hofmann J, 2013. Hantaviruses as zoonotic pathogens in Germany. Dtsch Arztebl Int 110: 461–467.
-
20.
Zhang X et al., 2011. Comparison of Hantaan and Seoul viral infections among patients with hemorrhagic fever with renal syndrome (HFRS) in Heilongjiang, China. Scand J Infect Dis 43: 632–641.
-
21.
Escadafal C, Avsic-Zupanc T, Vapalahti O, Niklasson B, Teichmann A, Niedrig M, Donoso-Mantke O, 2012. Second external quality assurance study for the serological diagnosis of hantaviruses in Europe. PLoS Negl Trop Dis 6: e1607.
-
22.
Schilling S, Emmerich P, Klempa B, Auste B, Schnaith E, Schmitz H, Krüger DH, Günther S, Meisel H, 2007. Hantavirus disease outbreak in Germany: limitations of routine serological diagnostics and clustering of virus sequences of human and rodent origin. J Clin Microbiol 45: 3008–3014.
-
23.
Engler O et al., 2013. Seroprevalence of hantavirus infections in Switzerland in 2009: difficulties in determining prevalence in a country with low endemicity. Euro Surveill 18: 20660.
-
24.
Prince HE, Lieberman JM , 2013. Impact of the Yosemite hantavirus outbreak on hantavirus antibody testing at a national reference laboratory. Clin Vaccine Immunol 20: 1213–1216.
-
25.
Hofmann J, Grunert HP, Donoso-Mantke O, Zeichhardt H, Kruger DH, 2015. Does proficiency testing improve the quality of hantavirus serodiagnostics? Experiences with INSTAND EQA schemes. Int J Med Microbiol 305: 607–611.
-
26.
Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412–441.
-
27.
Amada T, Yoshimatsu K, Yasuda SP, Shimizu K, Koma T, Hayashimoto N, Gamage CD, Nishio S, Takakura A, Arikawa J, 2013. Rapid, whole blood diagnostic test for detecting anti-hantavirus antibody in rats. J Virol Methods 193: 42–49.
-
28.
Noh JY, Cheong HJ, Song JY, Kim WJ, Song KJ, Klein TA, Lee SH, Yanagihara R, Song JW, 2013. Clinical and molecular epidemiological features of hemorrhagic fever with renal syndrome in Korea over a 10-year period. J Clin Virol 58: 11–17.
-
29.
Dzagurova TK, Klempa B, Tkachenko EA, Slyusareva GP, Morozov VG, Auste B, Kruger DH, 2009. Molecular diagnostics of hemorrhagic fever with renal syndrome during a Dobrava virus infection outbreak in the European part of Russia. J Clin Microbiol 47: 4029–4036.
-
30.
Brorstad A, Oscarsson KB, Ahlm C, 2010. Early diagnosis of hantavirus infection by family doctors can reduce inappropriate antibiotic use and hospitalization. Scand J Prim Health Care 28: 179–184.
-
31.
Nunez JJ et al., 2014. Hantavirus infections among overnight visitors to Yosemite National Park, California, USA, 2012. Emerg Infect Dis 20: 386–393.
-
32.
Roehr B, 2012. US officials warn 39 countries about risk of hantavirus among travellers to Yosemite. BMJ 345: e6054.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 842 | 193 | 16 |
| Full Text Views | 85 | 27 | 1 |
| PDF Downloads | 88 | 27 | 0 |
Utility of Nested Reverse-Transcriptase Polymerase Chain Reaction of Clinical Specimens for Early Diagnosis of Hemorrhagic Fever with Renal Syndrome
Jun-Won Seo
Jun-Won Seo
Department of Internal Medicine, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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Da Young Kim
Da Young Kim
Department of Internal Medicine, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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Choon-Mee Kim
Choon-Mee Kim
Department of Premedical Science, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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Na-Ra Yun
Na-Ra Yun
Department of Internal Medicine, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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Yu-Mi Lee
Yu-Mi Lee
Biomedical Sciences, Graduate School of Chosun University, Gwangju, Republic of Korea
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Merlin Jayalal Lawrence Panchali
Merlin Jayalal Lawrence Panchali
Department of Premedical Science, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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Dong-Min Kim
Dong-Min Kim
Department of Internal Medicine, College of Medicine, Chosun University, Gwangju, Republic of Korea;
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ABSTRACT.
Hemorrhagic fever with renal syndrome (HFRS) is confirmed by the isolation of hantavirus from serum, detection of virus-specific IgM, or a four-fold change in IgG titers during the acute and convalescent periods measured using an immunofluorescence assay (IFA). However, these tests are inefficient for early diagnosis. Therefore, this study investigated the usefulness of reverse-transcriptase nested polymerase chain reaction (RT-nPCR) for early diagnosis of HFRS using clinical samples such as urine and serum. Electronic medical records of eight patients with confirmed HFRS using IFA and RT-nPCR between May 2016 and May 2020 at Chosun University Hospital were reviewed. The virus was detected in all patients using RT-nPCR targeting the large (L) segment of hantavirus during the early phase in urine and serum. Importantly, the virus was identified in urine at a time when it was not identified in serum. Additionally, the virus was detected in urine and serum for up to 1 month after initial presentation with illness, but not in saliva, using RT-nPCR. We report eight HFRS cases diagnosed using urine and serum, but not using saliva, with RT-nPCR targeting the L-segment. Hantavirus RNA detection by RT-nPCR in urine and serum may aid the rapid diagnosis of HFRS during the early phase of the disease. In particular, HFRS should not be ruled out based on negative RT-PCR results in serum, and RT-PCR should be performed using urine as well as serum during the early phase of symptoms.
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Author Notes
Disclosure: Individual participant data collected during the study will be available after de-identification and immediately after publication, with no end date. Data will be available to researchers providing a methodologically sound proposal. Proposals should be directed to the corresponding author.
Authors’ addresses: Jun-Won Seo, Da Young Kim, Na-Ra Yun, and Dong-Min Kim, Chosun University College of Medicine, Internal Medicine, Gwangju, Gwangju, Republic of Korea, E-mails: kaist-105@daum.net, dayz02@hanmail.net, shine@chosun.ac.kr, and drongkim@chosun.ac.kr. Choon-Mee Kim, Yu-Mi Lee, and Merlin Jayalal Lawrence Panchali, College of Medicine, Premedical Science, Dong-Gu, Gwangju, Republic of Korea, E-mails: choonmee@chosun.ac.kr, moksha1001@hanmail.net, and lpmjlal@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Lee HW, Lee PW, Johnson KM, 1978. Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis 137: 298–308.
-
2.
Kim YS, Ahn C, Han JS, Kim S, Lee JS, Lee PW, 1995. Hemorrhagic fever with renal syndrome caused by the Seoul virus. Nephron 71: 419–427.
-
3.
Lee JS, 1991. Clinical features of hemorrhagic fever with renal syndrome in Korea. Kidney Int Suppl 35: S88–S93.
-
4.
Kim WK et al., 2016. Phylogeographic analysis of hemorrhagic fever with renal syndrome patients using multiplex PCR-based next generation sequencing. Sci Rep 6: 26017.
-
5.
Noh JY, Jung J, Song JW, 2019. Hemorrhagic fever with renal syndrome. Infect Chemother 51: 405–413.
-
6.
Mattar S, Guzmán C, Figueiredo LT, 2015. Diagnosis of hantavirus infection in humans. Expert Rev Anti Infect Ther 13: 939–946.
-
7.
Hujakka H, Koistinen V, Kuronen I, Eerikäinen P, Parviainen M, Lundkvist A, Vaheri A, Vapalahti O, Närvänen A, 2003. Diagnostic rapid tests for acute hantavirus infections: specific tests for Hantaan, Dobrava and Puumala viruses versus a hantavirus combination test. J Virol Methods 108: 117–122.
-
8.
Kim WK et al., 2018. Multiplex PCR-based next-generation sequencing and global diversity of Seoul virus in humans and rats. Emerg Infect Dis 24: 249–257.
-
9.
Lagerqvist N, Hagström Å, Lundahl M, Nilsson E, Juremalm M, Larsson I, Alm E, Bucht G, Ahlm C, Klingström J, 2016. Molecular diagnosis of hemorrhagic fever with renal syndrome caused by Puumala virus. J Clin Microbiol 54: 1335–1339.
-
10.
Lednicky JA, 2003. Hantaviruses. a short review. Arch Pathol Lab Med 127: 30–35.
-
11.
Pettersson L, Klingstrom J, Hardestam J, Lundkvist A, Ahlm C, Evander M, 2008. Hantavirus RNA in saliva from patients with hemorrhagic fever with renal syndrome. Emerg Infect Dis 14: 406–411.
-
12.
Jalal S, Jha B, Kim CM, Kim DM, Yun NR, Kim YS, Park JW, Chung JK, 2019. Molecular detection of viruses causing hemorrhagic fevers in rodents in the south-west of Korea. J Neurovirol 25: 239–247.
-
13.
Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Kruger DH, 2006. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12: 838–840.
-
14.
Kim HK, Chung JH, Kim DM, Yun NR, Kim CM, Jalal S, 2019. Hemorrhagic fever with renal syndrome as a cause of acute diarrhea. Am J Trop Med Hyg 100: 1236–1239.
-
15.
Baek LJ et al., 2006. Soochong virus: an antigenically and genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J Med Virol 78: 290–297.
-
16.
Bi Z, Formenty PB, Roth CE, 2008. Hantavirus infection: a review and global update. J Infect Dev Ctries 2: 3–23.
-
17.
Du H, Wang PZ, Li J, Bai L, Li H, Yu HT, Jiang W, Zhang Y, Wang JN, Bai XF, 2014. Clinical characteristics and outcomes in critical patients with hemorrhagic fever with renal syndrome. BMC Infect Dis 14: 191.
-
18.
Manigold T, Vial P, 2014. Human hantavirus infections: epidemiology, clinical features, pathogenesis and immunology. Swiss Med Wkly 144: w13937.
-
19.
Kruger DH, Ulrich RG, Hofmann J, 2013. Hantaviruses as zoonotic pathogens in Germany. Dtsch Arztebl Int 110: 461–467.
-
20.
Zhang X et al., 2011. Comparison of Hantaan and Seoul viral infections among patients with hemorrhagic fever with renal syndrome (HFRS) in Heilongjiang, China. Scand J Infect Dis 43: 632–641.
-
21.
Escadafal C, Avsic-Zupanc T, Vapalahti O, Niklasson B, Teichmann A, Niedrig M, Donoso-Mantke O, 2012. Second external quality assurance study for the serological diagnosis of hantaviruses in Europe. PLoS Negl Trop Dis 6: e1607.
-
22.
Schilling S, Emmerich P, Klempa B, Auste B, Schnaith E, Schmitz H, Krüger DH, Günther S, Meisel H, 2007. Hantavirus disease outbreak in Germany: limitations of routine serological diagnostics and clustering of virus sequences of human and rodent origin. J Clin Microbiol 45: 3008–3014.
-
23.
Engler O et al., 2013. Seroprevalence of hantavirus infections in Switzerland in 2009: difficulties in determining prevalence in a country with low endemicity. Euro Surveill 18: 20660.
-
24.
Prince HE, Lieberman JM , 2013. Impact of the Yosemite hantavirus outbreak on hantavirus antibody testing at a national reference laboratory. Clin Vaccine Immunol 20: 1213–1216.
-
25.
Hofmann J, Grunert HP, Donoso-Mantke O, Zeichhardt H, Kruger DH, 2015. Does proficiency testing improve the quality of hantavirus serodiagnostics? Experiences with INSTAND EQA schemes. Int J Med Microbiol 305: 607–611.
-
26.
Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412–441.
-
27.
Amada T, Yoshimatsu K, Yasuda SP, Shimizu K, Koma T, Hayashimoto N, Gamage CD, Nishio S, Takakura A, Arikawa J, 2013. Rapid, whole blood diagnostic test for detecting anti-hantavirus antibody in rats. J Virol Methods 193: 42–49.
-
28.
Noh JY, Cheong HJ, Song JY, Kim WJ, Song KJ, Klein TA, Lee SH, Yanagihara R, Song JW, 2013. Clinical and molecular epidemiological features of hemorrhagic fever with renal syndrome in Korea over a 10-year period. J Clin Virol 58: 11–17.
-
29.
Dzagurova TK, Klempa B, Tkachenko EA, Slyusareva GP, Morozov VG, Auste B, Kruger DH, 2009. Molecular diagnostics of hemorrhagic fever with renal syndrome during a Dobrava virus infection outbreak in the European part of Russia. J Clin Microbiol 47: 4029–4036.
-
30.
Brorstad A, Oscarsson KB, Ahlm C, 2010. Early diagnosis of hantavirus infection by family doctors can reduce inappropriate antibiotic use and hospitalization. Scand J Prim Health Care 28: 179–184.
-
31.
Nunez JJ et al., 2014. Hantavirus infections among overnight visitors to Yosemite National Park, California, USA, 2012. Emerg Infect Dis 20: 386–393.
-
32.
Roehr B, 2012. US officials warn 39 countries about risk of hantavirus among travellers to Yosemite. BMJ 345: e6054.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 842 | 193 | 16 |
| Full Text Views | 85 | 27 | 1 |
| PDF Downloads | 88 | 27 | 0 |