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Prosthetic valve Endocarditis due to Neisseria skkuensis, novel Neisseria 1
species 2
3
So Yeon Parka, Seung Ji Kangb, Eun-Jeong Jooa, Young Eun Haa, Jin Yong 4
Baekc, Yu Mi Wid, Cheol-In Kanga, Doo Ryeon Chunga, Kyong Ran Pecka, Nam 5
Young Leee, and Jae-Hoon Songa,c 6
7
Division of Infectious Diseases, Samsung Medical Center, Skungyunkwan 8
University School of Medicine, Seoul, Republic of Koreaa 9
Division of Infectious Diseases, Chonnam National University Hospital, 10
Chonnam National University School of Medicine, Gwang-ju, Republic of 11
Koreab 12
Asian-Pacific Foundation for Infectious Diseases (APFID), Seoul, Republic of 13
Koreac 14
Division of Infectious Diseases, Samsung Changwon Hospital, Sungkyunkwan 15
University School of Medicine, Changwon, Republic of Koread 16
Department of Laboratory Medicine, Samsung Medical Center, Sunkyunkwan 17
University School of Medicine, Seoul, Republic of Koreae 18
19
Running head: Endocarditis caused by Neisseria skkunensis 20
Keywords: Neisseria skkunensis; endocarditis 21
Copyright © 2012, American Society for Microbiology. All Rights Reserved.J. Clin. Microbiol. doi:10.1128/JCM.00676-12 JCM Accepts, published online ahead of print on 6 June 2012
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* Corresponding author: Kyong Ran Peck, MD 22
Professor of Medicine 23
Division of Infectious Diseases, Department of Internal Medicine 24
Samsung Medical Center, Sungkyunkwan University School of Medicine, 25
50 Irwon-ro 81, Gangnam-gu, Seoul 135-710, Republic of Korea 26
Phone: +82-2-3410-0322 27
Fax :+ 82-2-3410-0064 28
Email address: [email protected] 29
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Absctract 48 49
We reported the first case of endocarditis due to Neisseria skkuensis. The organism 50
from the blood cultures taken on admission day was identified initially as unidentified 51
gram negative cocci by VITEK2. Finally, it was identified as a Neisseria skkuensis by 16 52
rRNA gene sequence analysis. 53
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CASE REPORT 57
A 41-year old man was admitted to our hospital with a 1-week history of febrile 58
sense, chills, sweating, aggravation on dyspnea, and hypotension during hemodialysis. He 59
had a complicated past history, including liver cirrhosis caused by chronic hepatitis B 60
infection and chronic kidney disease due to glomerulonephritis. He had received entecavir 61
since 2009 and hemodialysis since 2000. In addition to these, he had undergone a mechanical 62
mitral valve replacement due to infective endocarditis caused by methicillin resistant 63
Staphylococcus aureus before one year ago. He denied dental treatment and drug abuse since 64
mitral valve replacement. 65
On arrival at the emergency department, the patient’s vital sign were blood pressure, 66
86/52 mmHg; respiratory rate, 22 breaths per min; and temperature, 37 ℃. Physical 67
examination revealed metallic heart sounds without murmur and no abdominal tenderness 68
with positive shifting dullness. A chest radiography showed cardiomegaly and pulmonary 69
edema. Laboratory investigations revealed a C-reactive protein concentration of 10.0 mg/dl 70
(normal [N], <0.3mg/dl), an erythrocyte sedimentation rate of 37mm/h (N, <22mm/h), a 71
procalcitonin concentration of 152.2 ng/ml. The white blood cell (WBC) count was 72
9850/mm3 with dominant segmented neutrophils (85%), hemoglobin (Hb) 7.5 g/dl, platelet 73
count 57000/ mm3, blood urea nitrogen 49.5mg/dl, creatinine 6.55mg/dl (N, < 1.3mg/dl), and 74
total bilirubin 1.2 mg/dl (N, < 1.5 mg/dl). He was coagulopathic with a prothrobin time of 75
23.1 seconds (N, 12.6 to 14.9), international normalized ratio (INR) of 2.0, activated partial 76
thromboplastin time (APTT) of 72.7 seconds (N, 29.1 to 41.9), and D-dimer of 3.42 ug/ml (N, 77
0 to 0.5). Ascites analysis showed WBC count of 310/mm3, with 39% neutrophils, an albumin 78
level of 1.3 g/dl, and a negative gram stain. Fluid was cultured and none grew any organism. 79
The transthoracic echocardiography showed well functioning prosthetic mitral valve and 80
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moderate tricuspid valve regurgitation. There was no dilatation of the left ventricle and no 81
vegetation was visualized. The transesophageal echocardiography showed oscillating mass 82
lesions on prosthetic mitral valve (Fig. 1). 83
Blood cultures were conducted on admission day prior to antibiotic treatment. The 84
aerobic bottles from each of three separately taken sets of blood cultures were incubated in a 85
BacT/ALERT 3D (bioMérieux, Durham, NC., USA) and grew gram negative cocci in all 86
three bottles. The Vitek 2 GNI card system (bioMérieux, Durham, NC., USA) didn’t identify 87
them. For molecular identification, we performed 16S rRNA gene sequence analysis and it 88
was formally identified at the Asian-Pacific Foundation for Infectious Diseases (APFID) as 89
Nesseria skkuensis based on the sequence of the 16S rRNA gene. The 16S rRNA gene was 90
amplified using primer sets 16S-F2 (5′-AGAGTTTGATCMTGGCTCAG-3′) and 16S-R2 (5′-91
GGTTACCTTGTTACGACTT-3′). A 1406 bp sequence of the 16S rRNA gene was obtained 92
from our strain. The 16S rRNA gene sequence was compared with those in the EzTaxone 93
public database (http://www.eztaxon.org) (Table 1) and the GenBank database 94
(http;//www.ncbi.nlm.nih.gov/blast) using BLAST searches (1). When the sequence was 95
compared to the 16S rRNA sequence of strain SMC-A9199T of Nesseria skkuensis (AC N 96
FJ763637, GenBank AC N FJ763637.1), it was 100% identical to SMC-A9199T. 97
Antibiotic susceptibility tests were performed and the MICs determined by the 98
broth microdilution method in accordance with the guidelines established by the Clinical and 99
Laboratory Standards Institute (CLSI) (2). The MICs were as follows: penicillin, 1 mg/liter; 100
ceftriaxone, 0.12 mg/liter; piperacillin/tazobactam 0.25 mg/liter; rifampicin 1 mg/liter; and 101
ciprofloxacin, <0.06 mg/liter. It was susceptible to ceftriaxone, piperacillin/tazobactram, 102
rifampicin, and ciprofloxacin, but was showed intermediate resistance against penicillin. 103
Interpretive criteria for susceptibility were those for Nesseria gonorrhoeae because no 104
breakpoints were provided by CLSI (2). 105
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The patient was treated for prosthetic valve endocarditis with intravenous vancomycin 1g 106
every three days, piperacillin/tazobactam 2.25g four times daily, gentamicin 100mg daily, and 107
oral rifampicin 900mg daily. On hospital day 4, the patient was received mitral valve 108
replacement and tricuspid anuuloplasty. Gram staining and culture of mitral valve specimen 109
removed at operation were performed. No microorganism were recovered from culture of the 110
replaced mitral valve after surgery. We applied 16S rRNA gene sequencing to identify 111
bacterial species in mitral valve tissue, too. However, the result was negative. We performed 112
acid-fast stain and mycobacterial culture on specimen of mitral valve tissue taken during the 113
operation. The results of acid-fast stain and mycobacterial culture were negative. The next 114
day after surgery, rifampicin was stopped. On hospital day 28, a result of 16S rRNA gene 115
sequence was identified as Nesseria skkuensis and we changed the antibiotics regimen. We 116
stopped intravenous administration of vancomycin and piperacillin/tazobactam. Therapy was 117
continued with 2g intravenous ceftriaxone daily for 6 weeks. All blood cultures performed 118
after the beginning of antibiotics remained negative. The patient recovered fully. 119
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The genus Neisseria includes a group of closely related gram negative bacteria that 122
are primarily commensal inhabitants of the mucus membrane of mammals. Within the 15 123
species are of human origin, only Neisseria gonorrhoeae and Neisseria meningitides are 124
considered important pathogens, whereas the others are opportunistic pathogen sporadically 125
involved in infections (4). However, several Neisseria species other than N. gonnhoeae and N. 126
meningitides cause human infections. Neisseria elongata and Neisseria sicca have been 127
isolated from endocarditis (3, 5). Neisseria bacilliformis, also causes endocarditis and various 128
human infections (4, 8, 9). 129
A novel Neisseria species, ‘Neisseria skkuensis’ was first described in 2010 (7). N. 130
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skkuensis isolated from blood and wound pus of a diabetic patient with a foot ulcer. The 131
bacteria was identified as Neisseria spp by conventianl methods, but comparative 16S rRNA 132
gene sequence analysis along with phenotypic analysis showed that the isolate is a novel 133
species of Neisseria (7). Lee et al performed phenotypic analysis and N. skkuensis showed 134
oxidase and catalase positive, consistent with most Neisseria species (6, 7). In addition, N. 135
skkuensis could produce acid from ribose, glucose, fructose, mannitol, sucrose and gluconate, 136
but not the remaining carbohydrates (7). Based on the 16S rRNA gene sequence, that isolate 137
was most closely related with Nesseria animalis same as our case. 138
We examined the genetic relationship of the two N. skkuensis isolates (one reported in 139
reference 7 and one in this study) by pulsed-field gel electrophoresis (PFGE). PFGE DNA 140
preparation followed standard procedure and PFGE analyses were performed following the 141
interpretative procedures described previously (10-12). The PFGE patterns were analyzed 142
using GelCompar II software (Applied Maths, Belgium). Isolates that produced patterns that 143
were < 85% similar were considered different. The PFGE patterns showed the two isolates 144
were different strain from each other (Fig2). 145
To our knowledge, there have been no prior case reports of endocarditis due to N. 146
skuuensis. In present case, the patient had prosthetic mitral valve, predisposing factor for 147
infective endocarditis, and had received hemodialysis since 2000. The previous reported 148
patient was admitted to our hospital in 2009 and the N. skkuensis was identified at the Asian-149
Pacific Foundation for Infectious Diseases (APFID) (7). In our case, N. skkuensis was 150
identified as Neisseria spp. by 16S rRNA sequence analysis in a clinical microbiology lab, 151
but correct identification at the species level could not be obtained. It was identified at APFID 152
as Nesseria skkuensis based on the sequence of the 16S rRNA gene. 153
In conclusion, we describe the first reported case of endocarditis due to N. 154
skkuensis, identified by 16S rRNA sequence analysis. Although most Nesseria spp. are 155
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opportunistic pathogens, physicians should be aware of the possibility of endocarditis due to 156
Neiserria species. More Neisseria species may cause human disease. 157
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References 181
1. Chun, J., J. H. Lee, Y. Jung, M. Kim, S. Kim, B. K. Kim, and Y. W. Lim. 2007. 182
EzTaxon: a web-based tool for the identification of prokaryotes based on 16S 183
ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259-61. 184
2. CLSI. 2011. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-185
First Informational Supplement, M100-S21, Wayne, PA. Clinical and Laboratory 186
Standards Institute. 187
3. Evans, M., F. Yazdani, H. Malnick, J. J. Shah, and D. P. Turner. 2007. Prosthetic 188
valve endocarditis due to Neisseria elongata subsp. elongata in a patient with 189
Klinefelter's syndrome. J Med Microbiol 56:860-2. 190
4. Han, X. Y., T. Hong, and E. Falsen. 2006. Neisseria bacilliformis sp. nov. isolated 191
from human infections. J Clin Microbiol 44:474-9. 192
5. Heiddal, S., J. T. Sverrisson, F. E. Yngvason, N. Cariglia, and K. G. Kristinsson. 193
1993. Native-valve endocarditis due to Neisseria sicca: case report and review. Clin 194
Infect Dis 16:667-70. 195
6. Lawson, P. A., H. Malnick, M. D. Collins, J. J. Shah, M. A. Chattaway, R. 196
Bendall, and J. W. Hartley. 2005. Description of Kingella potus sp. nov., an 197
organism isolated from a wound caused by an animal bite. J Clin Microbiol 43:3526-9. 198
7. Lee, M. Y., E. G. Park, J. Y. Choi, H. S. Cheong, D. R. Chung, K. R. Peck, J. H. 199
Song, and K. S. Ko. 2010. 'Neisseria skkuensis' sp. nov., isolated from the blood of a 200
diabetic patient with a foot ulcer. J Med Microbiol 59:856-9. 201
8. Masliah-Planchon, J., G. Breton, V. Jarlier, A. Simon, O. Benveniste, S. Herson, 202
and L. Drieux. 2009. Endocarditis due to Neisseria bacilliformis in a patient with a 203
bicuspid aortic valve. J Clin Microbiol 47:1973-5. 204
9. Michaux-Charachon, S., J. P. Lavigne, A. Le Fleche, N. Bouziges, A. Sotto, and P. 205
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A. Grimont. 2005. Endocarditis due to a new rod-shaped Neisseria sp. J Clin 206
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10. Starnino, S., and P. Stefanelli. 2009. Azithromycin-resistant Neisseria gonorrhoeae 208
strains recently isolated in Italy. J Antimicrob Chemother 63:1200-4. 209
11. Su, X., and I. Lind. 2001. Molecular basis of high-level ciprofloxacin resistance in 210
Neisseria gonorrhoeae strains isolated in Denmark from 1995 to 1998. Antimicrob 211
Agents Chemother 45:117-23. 212
12. Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. 213
Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction 214
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Finacial: Nothing to disclose 228
Conflict of Interest: Nothing to disclose 229
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Table 1. Results of 16S rRNA Gene Sequence (1,406) Alignment (EzTaxon Server) 230 231 Rank Name/Title Authors Strain Accession Pairwise
Similarity
Different
nucleotides/
Total
nucleotides
1 Neisseria
skkuensis
Lee et al. 2010 SMC-
A9199(T)
FJ763637 100 0/1406
2 Neisseria
animalis
Berger 1960 NCTC
10212(T)
AJ239388 97.491 34/1355
3 Neisseria
cinerea
(Von Lingelsheim
1906) Murray
1939
ATCC
14685(T)
ACDY020
00019
97.021 42/1410
4 Neisseria
subflava
(Flugge 1886)
Trevisan 1889
U37(T) AJ239291 96.753 44/1355
5 Neisseria
meningitidis
(Albrecht and
Ghon 1901)
Murray 1929
MC58 AE002098 96.738 46/1410
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Figure legends. 233
FIG 1 Transesophageal echocardiogram showing (0.84cm x 0.61 cm and 0.42 x 0.3cm) 234
mobile vegetations (arrow) on the prosthetic mitral valve strut. 235
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FIG 2 PFGE analysis of genomic DNA from N. skkuensis strains digested with NheI and 237
SpeI. A and B show N. skkuensis strains digested with NheI and SpeI respectively. Two 238
isolates showed <85% similarity. The isolates were considered unrelated to each other. N. 239
skkuensis 1 is SMC-A9199 (reference 7). N. skkuensis 2 is the isolate from this case patient. 240
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