DOI QR코드

DOI QR Code

Diagnosing Balamuthia mandrillaris amebic meningoencephalitis in a 64-year-old woman from the Southwest of China

  • Suhua Yao (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Xiaoting Chen (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Lian Qian (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Shizheng Sun (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Chunjing Zhao (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Zongkai Bai (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Zhaofang Chen (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University) ;
  • Youcong Wu (Department of Medical Microbiology and Immunology, School of Basic Medical Sciences, Dali University)
  • Received : 2023.03.28
  • Accepted : 2023.04.06
  • Published : 2023.05.31

Abstract

Balamuthia mandrillaris amebic encephalitis (BAE) can cause a fatal condition if diagnosis is delayed or effective treatment is lacking. Patients with BAE have been previously reported in 12 provinces of China, with skin lesions being the primary symptom and encephalitis developing after several years. However, a significantly lower number of cases has been reported in Southwest China. Here we report an aggressive BAE case of a 64-year-old woman farmer with a history of skin lesions on her left hand. She was admitted to our hospital due to symptoms of dizziness, headache, cough, vomiting, and gait instability. She was initially diagnosed with syphilitic meningoencephalitis and received a variety of empirical treatment that failed to improve her symptoms. Finally, she was diagnosed with BAE combined with amebic pneumonia using next-generation sequencing (NGS), qRT-PCR, sequence analysis, and imaging studies. She died approximately 3 weeks after the onset. This case highlights that the rapid development of encephalitis can be a prominent clinical manifestation of Balamuthia mandrillaris infection.

Keywords

Acknowledgement

We would like to thank the patient's family for participating in the present research study. We would also like to thank Prof. Di Qu and Yang Wu from Fudan University for their helpful discussions, and Prof. Li Bai and Yuanying Shen from Dali University for the case analysis. This work was supported by the National Natural Science Foundation of China (No. 82060380, 81660346 to WYC), and by Young and the Middle-aged Academic Leader Training Foundation of Yunnan Province (No. 202305AC160038 to WYC). All data generated or analyzed during this study were included in this published article and its Supplementary Fig. S1.

References

  1. Baquero RA, Reyes-Batlle M, Nicola GG, Martin-Navarro CM, Lopez-Arencibia A, et al. Presence of potentially pathogenic free-living amoebae strains from well water samples in Guinea-Bissau. Pathog Glob Health 2014;108(4):206-211. https://doi.org/10.1179/2047773214Y.0000000143
  2. Dunnebacke TH, Schuster FL, Yagi S, Booton GC. Balamuthia mandrillaris from soil samples. Microbiology (Reading) 2004;150(Pt 9):2837-2842. https://doi.org/10.1099/mic.0.27218-0
  3. Niyyati M, Karamati SA, Lorenzo Morales J, Lasjerdi Z. Isolation of Balamuthia mandrillaris from soil samples in NorthWestern Iran. Parasitol Res 2016;115(2):541-545. https://doi.org/10.1007/s00436-015-4770-y
  4. Schuster FL, Dunnebacke TH, Booton GC, Yagi S, Kohlmeier CK, et al. Environmental isolation of Balamuthia mandrillaris associated with a case of amebic encephalitis. J Clin Microbiol 2003;41(7):3175-3180. https://doi.org/10.1128/JCM.41.7.3175-3180.2003
  5. Retana-Moreira L, Abrahams-Sandi E, Cabello-Vilchez AM, Reyes-Batlle M, Valladares B, et al. Isolation and molecular characterization of Acanthamoeba and Balamuthia mandrillaris from combination shower units in Costa Rica. Parasitol Res 2014;113(11):4117-4122. https://doi.org/10.1007/s00436-014-4083-6
  6. Visvesvara GS, Martinez AJ, Schuster FL, Leitch GJ, Wallace SV, et al. Leptomyxid ameba, a new agent of amebic meningoencephalitis in humans and animals. J Clin Microbiol 1990;28(12):2750-2756. https://doi.org/10.1128/jcm.28.12.2750-2756.1990
  7. Finnin PJ, Visvesvara GS, Campbell BE, Fry DR, Gasser RB. Multifocal Balamuthia mandrillaris infection in a dog in Australia. Parasitol Res 2007;100(2):423-426. https://doi.org/10.1007/s00436-006-0302-0
  8. Kinde H, Visvesvara GS, Barr BC, Nordhausen RW, Chiu PH. Amebic meningoencephalitis caused by Balamuthia mandrillaris (leptomyxid ameba) in a horse. J Vet Diagn Invest 1998;10(4):378-381. https://doi.org/10.1177/104063879801000416
  9. Cope JR, Landa J, Nethercut H, Collier SA, Glaser C, et al. The Epidemiology and clinical features of Balamuthia mandrillaris disease in the United States, 1974-2016. Clin infect Dis 2019;68(11):1815-1822. https://doi.org/10.1093/cid/ciy813
  10. Farnon EC, Kokko KE, Budge PJ, Mbaeyi C, Lutterloh EC, et al. Transmission of Balamuthia mandrillaris by organ transplantation. Clini Infect Dis 2016;63(7):878-888. https://doi.org/10.1093/cid/ciw422
  11. Yamanouchi K, Arima H, Sakamoto Y, Kanto K, Kasai K, et al. First report of the isolation of Balamuthia mandrillaris in the northern region of Japan. Parasitol Res 2018;117(9):2895-2900. https://doi.org/10.1007/s00436-018-5980-x
  12. Kum SJ, Lee HW, Jung HR, Choe M, Kim SP. Amoebic Encephalitis Caused by Balamuthia mandrillaris. J Patho Transl Med 2019;53(5):327-331. https://doi.org/10.4132/jptm.2019.05.14
  13. Lee JY, Yu IK, Kim SM, Kim JH, Kim HY. Fulminant disseminating fatal granulomatous amebic encephalitis: the first case report in an immunocompetent patient in South Korea. Yonsei Med J 2021;62(6):563-567. https://doi.org/10.3349/ymj.2021.62.6.563
  14. Hara T, Yagita K, Sugita Y. Pathogenic free-living amoebic encephalitis in Japan. Neuropathology 2019;39(4):251-258. https://doi.org/10.1111/neup.12582
  15. Intalapaporn P, Suankratay C, Shuangshoti S, Phantumchinda K, Keelawat S, et al. Balamuthia mandrillaris meningoencephalitis: the first case in southeast Asia. Am J Trop Med Hyg 2004;70(6):666-669. https://doi.org/10.4269/ajtmh.2004.70.666
  16. Krasaelap A, Prechawit S, Chansaenroj J, Punyahotra P, Puthanakit T, et al. Fatal Balamuthia amebic encephalitis in a healthy child: a case report with review of survival cases. Korean J Parasitol 2013;51(3):335-341. https://doi.org/10.3347/kjp.2013.51.3.335
  17. Sangruchi T, Martinez AJ, Visvesvara GS. Spontaneous granulomatous amebic encephalitis: report of four cases from Thailand. Southeast Asian J Trop Med Public Health 1994;25(2):309-313.
  18. Khurana S, Hallur V, Goyal MK, Sehgal R, Radotra BD. Emergence of Balamuthia mandrillaris meningoencephalitis in India. Indian J Med Microbiol 2015;33(2):298-300. https://doi.org/10.4103/0255-0857.154887
  19. Safavi M, Mehrtash V, Habibi Z, Mohammadpour M, Haghi Ashtiani MT, et al. Case report: encephalitis caused by Balamuthia mandrillaris in a 3-year-old iranian girl. Am J Trop Med Hyg 2021;104(5):1836-1840. https://doi.org/10.4269/ajtmh.20-1257
  20. Wang L, Cheng W, Li B, Jian Z, Qi X, et al. Balamuthia mandrillaris infection in China: a retrospective report of 28 cases. Emerg Microbes Infect 2020;9(1):2348-2357. https://doi.org/10.1080/22221751.2020.1835447
  21. Shehab KW, Aboul-Nasr K, Elliott SP. Balamuthia mandrillaris granulomatous amebic encephalitis with renal dissemination in a previously healthy child: case report and review of the pediatric literature. J Pediatric Infect Dis Soc 2018;7(3):e163-e168. https://doi.org/10.1093/jpids/pix089
  22. Wu X, Yan G, Han S,Ye Y, Cheng X, et al. Diagnosing Balamuthia mandrillaris encephalitis via next-generation sequencing in a 13-year-old girl. Emerg Microbes Infect 2020;9(1):1379-1387. https://doi.org/10.1080/22221751.2020.1775130
  23. Yang Y, Hu X, Min L, Dong X, Guan Y. Balamuthia mandrillaris-related primary amoebic encephalitis in China diagnosed by next generation sequencing and a review of the literature. Lab Med 2020;51(2):e20-e26. https://doi.org/10.1093/labmed/lmz079
  24. Booton GC, Carmichael JR, Visvesvara GS, Byers TJ, Fuerst PA. Identification of Balamuthia mandrillaris by PCR assay using the mitochondrial 16S rRNA gene as a target. J Clin Microbiol 2003;41(1):453-455. https://doi.org/10.1128/JCM.41.1.453-455.2003.
  25. Kiderlen AF, Radam E, Lewin A. Detection of Balamuthia mandrillaris DNA by real-time PCR targeting the RNase P gene. BMC Microbiol 2008;8:210. https://doi.org/10.1186/1471-2180-8-210
  26. Mittal SO, Alsinaidi O. Teaching neuro Images: Balamuthia mandrillaris amebic encephalitis: clinical-radiologic-pathologic correlation. Neurology 2017;88(18):e183. https://doi.org/10.1212/WNL.0000000000003891
  27. Booton GC, Schuster FL, Carmichael JR, Paul AF, Thomas JB. Balamuthia mandrillaris: identification of clinical and environmental isolates using genus-specific PCR. J Eukaryot Microbiol 2003;50(suppl):508-509. https://doi.org/10.1111/j.1550-7408.2003.tb00611.x
  28. Yohannan B, Feldman M. Fatal Balamuthia mandrillaris encephalitis. Case Rep Infect Dis 2019;2019:9315756. https://doi.org/10.1155/2019/9315756
  29. Siddiqui R, Matin A, Warhurst D, Stins M, Khan NA. Effect of antimicrobial compounds on Balamuthia mandrillaris encystment and human brain microvascular endothelial cell cytopathogenicity. Antimicrob Agents Chemother 2007;51(12):4471-4473. https://doi.org/10.1128/AAC.00373-07
  30. Laurie MT, White CV, Retallack H, Wu W, Moser MS, et al. Functional assessment of 2,177 U.S. and international drugs identifies the quinoline nitroxoline as a potent amoebicidal agent against the pathogen Balamuthia mandrillaris. mBio 2018;9(5):e02051-18. https://doi.org/10.1128/mBio.02051-18