
==== Front
Wellcome Open Res
Wellcome Open Res
Wellcome Open Research
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F1000 Research Limited London, UK

10.12688/wellcomeopenres.22706.1
Case Report
Articles
Case Report: Soft tissue infection with Burkholderia thailandensis capsular variant: case report from the Lao PDR
[version 1; peer review: 2 approved, 1 approved with reservations]

Vannachone Souphaphone Conceptualization Data Curation Formal Analysis Investigation Writing – Original Draft Preparation 1
Luangraj Manophab Investigation Methodology Writing – Review & Editing https://orcid.org/0000-0002-8801-5738
1
Dance David Conceptualization Methodology Writing – Original Draft Preparation Writing – Review & Editing https://orcid.org/0000-0001-9189-7244
123
Chantratita Narisara Data Curation Formal Analysis Investigation Methodology Software Validation Visualization Writing – Review & Editing 45
Saiprom Natnaree Formal Analysis Validation Visualization Writing – Review & Editing 4
Seng Rathanin Formal Analysis Validation Visualization Writing – Review & Editing 4
Tandhavanant Sarunporn Formal Analysis Validation Visualization Writing – Review & Editing https://orcid.org/0000-0003-0261-3233
4
Rattanavong Sayaphet Investigation Methodology Writing – Review & Editing 1
Simpson Andrew Conceptualization Investigation Writing – Original Draft Preparation Writing – Review & Editing https://orcid.org/0000-0003-1239-0782
12
Roberts Tamalee Data Curation Formal Analysis Investigation Methodology Project Administration Resources Supervision Validation Visualization Writing – Original Draft Preparation Writing – Review & Editing https://orcid.org/0000-0001-8599-737X
a12
1 Lao-Oxford-Mahosot Hospital Wellcome Trust Research Unit, Vientiane, Vientiane Capital, 0100, Lao People's Democratic Republic
2 Nuffield Department of Medicine, Centre for Tropical Medicine & Global Health, University of Oxford, Oxford, UK
3 Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK
4 Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
5 Faculty of Tropical Medicine, Mahidol University, Mahidol-Oxford Tropical Medicine Research Unit, Bangkok, Thailand
a tamalee.r@tropmedres.ac
No competing interests were disclosed.

1 8 2024
2024
9 42125 7 2024
Copyright: © 2024 Vannachone S et al.
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background

Burkholderia thailandensis is an environmental bacteria closely related to Burkholderia pseudomallei that rarely causes infection in humans. Some environmental isolates have shown to express a capsular polysaccharide known as B. thailandensis capsular variant (BTCV), but human infection has not previously been reported. Although B. thailandednisis has been identified in environmental samples in Laos before, there have not been any human cases reported.

Case

A 44-year-old man presented to a district hospital in Laos with a short history of fever and pain in his left foot. Physical examination identified a deep soft-tissue abscess in his left foot and an elevated white blood count. A deep pus sample was taken and melioidosis was suspected from preliminary laboratory tests. The patient was initially started on cloxacillin, ceftriaxone and metronidazole, and was then changed to ceftazidime treatment following local melioidosis treatment guidelines.

Laboratory methods

A deep pus sample was sent to Mahosot Hospital microbiology laboratory where a mixed infection was identified including Burkholderia sp. Conventional identification tests and API 20NE were inconclusive, and the B. pseudomallei-specific latex agglutination was positive. The isolate then underwent a Burkholderia species specific PCR which identified the isolate as B. thailandensis. The isolate was sent for sequencing on the Illumina NovaSeq 6000 system and multi-locus sequence typing analysis identified the isolate had the same sequence type (ST696) as B. thailandensis E555, a strain which expresses a B. pseudomallei-like capsular polysaccharide.

Conclusion

This is the first report of human infection with B. thailandensis in Laos, and the first report of any human infection with the B. thailandensis capsular variant. Due to the potential for laboratory tests to incorrectly identify this bacteria, staff in endemic areas for B. thailandensis and B. pseudomallei should be aware and ensure that appropriate confirmatory methods are used to differentiate between the species.

Plain Language Summary

> Burkholderia thailandensis is a bacteria that is found in the environment. Rarely, this bacteria can cause infection in humans. Here we report a B. thailandensis infection in a 44 year old male in Laos. The patient sustained a puncture wound in his left foot and when presenting at a district hospital was prescribed cloxacillin. The wound did not improve and on day three of admission, a pus sample was sent to Mahosot Hospital Microbiology Laboratory for investigation. A preliminary diagnosis of melioidosis, caused by the bacteria Burkholderia pseudomallei, was made and antibiotic treatment was changed. Additional laboratory investigation determined that the isolate was actually B. thailandensis and antibiotic treatment was further changed. Due to the inconclusive results of the initial laboratory tests, the isolate was sent for sequencing and was identified as a strain which expresses a B. pseudomallei-like capsular polysaccharide. This is the first report of infection with B. thailandensis in Laos and the first report of infection with a B. thailandensis capsular variant.

Burkholderia thailandensis
B. thailandensis capsular variant
Lao PDR
Wellcome Trust220211 This work was supported by Wellcome [220211].
==== Body
pmcIntroduction

Burkholderia thailandensis is closely related to Burkholderia pseudomallei, the causative agent of melioidosis, a potentially fatal infectious disease found in Southeast Asia and Northern Australia 1 . B. thailandensis lives in soil and is generally considered non-pathogenic, in comparison to B. pseudomallei 2, 3 . There have, however, been several reports of human infection with B. thailandensis, ranging from localized to life-threatening infection 4, 5 . Some environmental isolates of B. thailandensis, including one from Lao PDR (Laos), have been shown to express a capsular polysaccharide that cross-reacts with that of B. pseudomallei, known as B. thailandensis capsular variants (BTCV), but as yet infection with such a strain has not been reported 6 . In Laos, there have been more than 1000 culture confirmed melioidosis cases in the past two decades since the first report in 1999 7 but there have been no reports of B. thailandensis infection. We report here the first case of soft tissue infection caused by a mixture of bacteria including BTCV that occurred in Vientiane Province, Laos.

Case report

On 9 th January 2019, a 44 year old man was admitted to a local district hospital with a short history of fever and pain in his left foot. The patient was a farmer from Vientiane Province, Laos, and lived approximately 60 kilometers from Vientiane Capital. He was previously considered fit and healthy. Two days prior to presenting to hospital, he suffered a puncture wound to his left foot while cleaning out a fish pond on his property. He started having pain that afternoon and the area started to swell. The next day he went to work in a rice field and self-treated with antibiotics bought from a local pharmacy, however his symptoms did not improve. On admission to hospital, his physical examination identified a deep soft-tissue abscess in his left foot. The patient’s white blood count was elevated at 16.3 × 10 9 cells/L, with a markedly elevated granulocyte count (98.1%) and blood glucose was normal (125 mg/dL). The patient was treated with intravenous (IV) cloxacillin 1 g four times per day. On day three of admission (11 th Jan), the left foot abscess was incised and drained; a deep pus sample was sent to the Microbiology Laboratory at Mahosot Hospital, Vientiane. The same day, the patient developed a high-grade fever and worsening of the abscess on the left ankle with severe pain on the left foot and loss of ability to walk. Ceftriaxone (2 g/day) and metronidazole (500 g 8 hourly) were added and cloxacillin discontinued, along with appropriate wound debridement, dressing and cleaning with normal saline, although without improvement. On day eight, haemoculture, urine and throat swab cultures were collected and sent to the Mahosot Hospital Microbiology Laboratory, as melioidosis was suspected, based on preliminary pus culture results. B. pseudomallei was subsequently not isolated from any sample, but treatment was changed to ceftazidime (2 g three times per day) as per local melioidosis treatment guidelines. On 22 nd January IV treatment was discontinued, the patient was discharged well and with one week of co-trimoxazole oral treatment to complete at home after discharge.

The foot abscess pus was cultured on blood agar (Oxoid, incubated in 5–10% CO 2 for 48 h) and Ashdown agar (made in-house, incubated in air and read daily for 4 days). Direct Gram staining demonstrated Gram-positive cocci in chains and Gram-negative coccobacilli. No acid-fast bacilli were seen in the Ziehl Neelsen stain. Culture yielded a mixed growth of five organisms which were identified using standard biochemical and API tests (bioMerieux, Marcy L’Etoile, France). Comprehensive antimicrobial susceptibility testing (AST) profiles were determined using disk diffusion on Mueller-Hinton agar (Oxoid) following US Clinical and Laboratory Standards Institute (CLSI) guidelines (M100, 28 th edition, January 2018). The organisms identified were as follows: Proteus vulgaris, susceptible to co-amoxiclav, ciprofloxacin, gentamicin, ceftriaxone and co-trimoxazole but resistant to ampicillin; Aeromonas sobria, susceptible to chloramphenicol, ciprofloxacin, gentamicin, ceftriaxone, co-trimoxazole and intermediate to co-amoxiclav; ESBL-positive Escherichia coli, susceptible to amikacin, chloramphenicol, ciprofloxacin, gentamicin, meropenem, intermediate to co-amoxiclav and resistant to ampicillin, ceftriaxone, co-trimoxazole and tetracycline and confirmed as an ESBL producer using the double-disk method (cefotaxime +/- clavulanate and ceftazidime +/- clavulanate [BD]); Edwardsiella tarda, susceptible to ampicillin, co-amoxiclav, ciprofloxacin, gentamicin, ceftriaxone and co-trimoxazole; and a probable Burkholderia species, susceptible to co-amoxiclav, ceftazidime, meropenem and co-trimoxazole was also identified. The Burkholderia sp. isolate grew on Ashdown’s agar, was oxidase positive and B. pseudomallei-specific latex agglutination positive (Faculty of Tropical Medicine Mahidol University, Thailand), however the API 20NE gave a low result of 50.7% for B. pseudomallei (profile 1157577). Due to this low percentage identification, the isolate had molecular confirmation testing by PCR with a Burkholderia species panel which included B. pseudomallei, B. thailandensis and B. cepacia targeting a Tat domain protein, 70-kDa protein and a conserved 12-kDa protein respectively using an adapted previously published method 8 and was identified as B. thailandensis. The isolate was then referred to the Mahidol Oxford Research Unit (MORU) in Bangkok where the latex agglutination test was confirmed as positive and the isolate was then identified by MALDI-TOF (Bruker Daltonik GmbH) as B. thailandensis using a recently constructed library 9 . The latex agglutination test (latex beads coated with 4B11 monoclonal antibody specific for the 200kDa exo-polysaccharide of B. pseudomallei) is used to rapidly identify suspect B. pseudomallei colonies in the Mahosot Hospital Microbiology Laboratory.

DNA was extracted from the isolate using QIAamp DNA Mini Kit (Catalogue number 56304, Qiagen, Germany), then processed for the 150-base-read library preparation and sequenced by Illumina NovaSeq 6000 system with paired-end runs at the Center for Medical Genomics, Faculty of Medicine, Ramathibodi Hospital, Bangkok, Thailand. FastQC v.0.11.9 ( https://github.com/s-andrews/FastQC) was used to pre-process sequenced reads. Raw reads were de novo assembled using SPAdes v3.13.1 ( https://github.com/ablab/spades). The species was identified using fIDBAC 10 and confirmed using FastANI v.1.31 11 against B. pseudomallei K96243, B. thailandensis E264, B. thailandensis FDAARGOS_238 and B. thailandensis E555.

Seven candidate housekeeping genes ( lepA, gmhD, nhd, lipA, nark, gltB, ace, nhd) were selected using the sequences of B. pseudomallei K96243. The sequences of each gene were retrieved from the clinical isolate using Basic Local Alignment Search Tool (BLAST). Multi-locus sequence typing (MLST) was identified using B. pseudomallei MLST website ( https://pubmlst.org/bpseudomallei/).

The isolate was identified using assembled genome sequence data. When submitting the genome sequences to the database through fIDBAC 10 , the whole genome Average Nucleotide Identity (ANI) of the isolate was 98.97% compared to B. thailandensis E264. The species was then confirmed by incorporating B. pseudomallei K96243, B. thailandensis FDAARGOS_238 and B. thailandensis E555. The isolate shared only 92.95% compared to B. pseudomallei K96243, while the ANI was 99.72% and 99.78% when compared to B. thailandensis FDAARGOS_238 and B. thailandensis E555, respectively. B. thailandensis E555 is a strain which expresses a B. pseudomallei-like capsular polysaccharide (BTCV). The MLST analysis revealed that the patient strain (LPD1900722) shared the same sequence type (ST696) as B. thailandensis strains E555, but was different from E264 (ST80). While the capsule gene cluster was absent in B. thailandensis E264, it was present in LPD1900722, similar to the configuration found in B. pseudomallei K96243 and B. thailandensis E555 ( Figure 1A). A maximum-likelihood phylogeny tree was constructed based on complete 16S ribosomal RNA (BTH_RS17800 of B. thailandensis E264) which showed the clinical isolate grouping within the B. thailandensis clade ( Figure 1B).

Figure 1. ( A) Read coverage of LPD1900722 mapped to capsular polysaccharide gene cluster of B. thailandensis E264 (top), B. pseudomallei K96243 (middle) and B. thailandensis E555 (bottom). ( B) Phylogenetic tree analysis of full-length of 16s ribosomal rna of Burkholderia spp. and clinical isolate (LPD1900722) using a maximum-likelihood with 100 bootstraps. Number on the branches indicate branch length (black) and bootstrap values (red).

Discussion

B. thailandensis is a Gram negative bacterium that is closely related to B. pseudomallei, the causative agent of melioidosis. B. thailandensis is widely present in Southeast Asia and Northern Australia but has also been detected in North America and West Africa 3, 12 . B. thailandensis is usually considered non-pathogenic and is commonly found in the environment (surface water and soil) in tropical or subtropical climates 13 . B. thailandensis was first discovered in Thailand in 1996 and is differentiated from B. pseudomallei phenotypically by its ability to assimilate arabinose and it was classified as a new species in 1998 14, 15 . BTCV produce a capsular polysaccharide that cross-reacts with that of B. pseudomallei, giving rise to the potential for confusion in the laboratory 6 . Occasional cases of infection with B. thailandensis have been reported in the United States, China, Thailand and Malaysia 4, 5, 16– 19 .

As B. thailandensis is found in the environment, and the patient pus sample yielded a very mixed culture result, it is difficult to comment on the clinical significance of the BTCV isolate. However, this is the first documented isolation of B. thailandensis from a clinical specimen in Laos, and the first report of the isolation of BTCV from a clinical sample of which we are aware. The potential for confusion with B. pseudomallei is significant and is something of which laboratory staff should be aware to avoid incorrectly labelling a patient as having melioidosis. There have been no further B. thailandensis isolates identified from the Mahosot Hospital Microbiology laboratory since this isolate (up to May 2024). The isolate was initially mis-identified by latex agglutination, but subsequently confirmed to be B. thailandensis by PCR and MALDI-TOF having failed to identify as B. pseudomallei by API 20NE. Although the pathogenicity of the BTCV within this mixed infection was questionable, this undoubtedly had the potential to lead to misdiagnosis meaning that the patient could have ended up being treated unnecessarily for melioidosis, involving antibiotic treatment for more than 3 months.

Conclusion

This is the first case of B. thailandensis reported in Laos and the first report of infection with BTCV of which we are aware. Laboratory staff in melioidosis-endemic areas should be aware of the possibility of B. thailandensis and should ensure that appropriate confirmatory methods are used to differentiate between B. pseudomallei and B. thailandensis rather than relying on latex agglutination or other serological methods alone.

Public and patient involvement

There was no formal patient or public involvement in the design or conduct of this work.

Ethics and consent

Written informed consent for publication of their clinical details was obtained.

Data availability

All data underlying the results are available as part of the article and no additional source data are required.

10.21956/wellcomeopenres.25008.r92510
Reviewer response for version 1
Burnard Delaney 12Referee
1 University of the Sunshine Coast (Ringgold ID: 5333), Sippy Downs, Queensland, Australia
2 Queensland Cyber Infrastructure Foundation, Saint Lucia, Queensland, Australia
5 9 2024 Copyright: © 2024 Burnard D
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove-with-reservations
Report is detailed and sound in all the above categories, with the outcome and importance of accurate laboratory diagnosis clearly conveyed.

There are a few sentences that need to be revised to improve reading. Please see text below to be revised:

The patient was initially started on cloxacillin, ceftriaxone and metronidazole, and was then changed to ceftazidime treatment following local melioidosis treatment guidelines.  Can you include the identification of  Burkholderia thailandensis somewhere in  here, as this has been skipped completely in the abstract.

Some environmental isolates of  B. thailandensis, including one from Lao PDR (Laos), have been shown to express a capsular polysaccharide that cross-reacts with that of  B. pseudomallei, known as  B. thailandensis capsular variants (BTCV), but as yet infection  with such a strain has not been reported 6 .

  do you mean "but as of yet"?

The MLST analysis revealed that the patient strain (LPD1900722) shared the same sequence type (ST696) as  B. thailandensis strains E555, but was different from E264 (ST80).  "differing from strain E264 (ST80)"

The potential for confusion with  B. pseudomallei is significant and is something of which laboratory staff should be aware to avoid incorrectly labelling a patient as having melioidosis. "should be aware of"

I would also like to ask the authors why they chose to provide a 16S phylogeny over a whole genome, cgMLST or MLST phylogeny. Given the authors performed typing on the isolate and further describe relatedness of strains using MLST, I expected to see a  B. thailandensis MLST phylogeny. I think the paper would be more robust, provide greater insight into the relatedness of strains and align with the manuscript text better with a MLST phylogeny in Figure 1.

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Yes

Is the case presented with sufficient detail to be useful for other practitioners?

Yes

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Yes

Is the background of the case’s history and progression described in sufficient detail?

Yes

Reviewer Expertise:

Bacteria, Antimicrobial Resistance, Genomics, MLST, Phylogenetics, Microbiology, Clinical Microbiology.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

10.21956/wellcomeopenres.25008.r92503
Reviewer response for version 1
Raih Mohd Firdaus 1Referee https://orcid.org/0000-0003-4275-4663

1 Universiti Kebangsaan Malaysia, Bangi, Malaysia
5 9 2024 Copyright: © 2024 Raih MF
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove
Increasing reports of B. thailandensis infections is an important contribution to the field in order to highlight the threat also posed by B. thailandensis which was previously thought to be less or even non-infectious.

The manuscript is clearly written and all the elements required of a case report is presented.

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Yes

Is the case presented with sufficient detail to be useful for other practitioners?

Yes

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Yes

Is the background of the case’s history and progression described in sufficient detail?

Yes

Reviewer Expertise:

Bacterial pathogenesis, bacterial genomics

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

10.21956/wellcomeopenres.25008.r92509
Reviewer response for version 1
Zueter Abdel Rahman 1Referee https://orcid.org/0000-0001-9960-4290

1 The Hashemite University, Zarqa, Jordan
31 8 2024 Copyright: © 2024 Zueter AR
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove
The case description is concise and to the point. It provides essential clinical details, including the patient's symptoms, physical examination findings, and initial treatment. The progression from preliminary suspicion of melioidosis to the adjustment of treatment according to local guidelines is logical and well-explained.

Since the case is very rare, it is good to add a table to review all similar cases 

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Yes

Is the case presented with sufficient detail to be useful for other practitioners?

Yes

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Yes

Is the background of the case’s history and progression described in sufficient detail?

Yes

Reviewer Expertise:

Interested in Laboratory Medicine and Infectious Diseases. Did and joined several helminthology and bacteriology projects and case reports. Current area of expertise include Clinical epidemiology, MLST-based molecular epidemiology; tropical infections, and laboratory diagnostics.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.
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