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Abstract

With the development of matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) and 16S ribosomal RNA (rRNA) gene sequencing, increasing numbers of new microorganisms are being discovered. In this report, Kerstersia gyiorum was isolated for the first time from the sputum of two elderly patients with neurodegenerative disease, and integrated traditional Chinese and Western medicine was used for treatment. The bacteria’s growth characteristics, biochemical reaction characteristics, sensitivity to antibiotics, and the patients’ treatment are described, with a review of previous reports.

Keywords

neurodegenerative disease integrated traditional Chinese and Western medicine case report microbiology gene sequencing antibiotic sensitivity

Introduction

Kerstersia gyiorum is a rare bacterium that belongs to the genus Kerstersia within the family Alcaligenaceae. This family, named¹ in 1986, comprises opportunistic pathogens that are widely distributed in nature; genera include Alcaligenes, Bordetella, and Kerstersia. Unlike the majority of bacterial species, the genus Kerstersia is oxidase-negative and has no special odor.² Currently, the genus Kerstersia comprises K. gyiorum and K. similis. K. gyiorum was first reported by Coenye et al.³ and has been found in house flies, the Yangtze finless porpoise, and brown seaweed.^4–6 K. similis was named by Vandamme et al.⁷ and has similar biological properties to those of K. gyiorum.

Matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) and 16S ribosomal RNA (rRNA) gene sequencing are widely used in clinical microbiology. Based on highly-enriched proteins contained in microorganisms, MALDI-TOF MS detects the protein fingerprints and compares them with a reference database for rapid species identification. This method can also be used to analyze bacterial virulence and drug resistance and detect sterile body fluids to meet the clinical needs of timely infection control.⁸ However, MALDI-TOF MS cannot fully identify anaerobes, fungi, and rare bacteria. Therefore, a combination of detection methods is needed to clarify the etiology of a disease. As a gene detection technology, 16S rRNA gene sequencing is widely used in microbial identification, and taxonomic and phylogenetic research to provide reliable reference for clinical practice.⁹

In this case report, K. gyiorum was identified by MALDI-TOF MS and 16S rRNA gene sequencing at protein and gene levels, respectively, which laid the foundation for drug susceptibility testing and provided comprehensive information for clinical diagnosis and treatment.

Case Report

Case 1

A 92-year-old woman diagnosed with Alzheimer's disease was admitted to our hospital with intermittent disturbance of consciousness. She had hypertension for 40 years, was a non-smoker, and did not drink alcohol. During hospitalization, she developed fever, cough, and expectoration. Inflammatory marker values were as follows: white blood cell count, 12 × 10⁹/L; neutrophil percentage, 90.8%; and procalcitonin, 0.079 ng/mL. Chest computed tomography (CT) revealed multiple inflammatory changes in the lungs, bilaterally.

Gram staining and sputum culture were then performed. Gram-negative bacilli were observed microscopically. The samples were inoculated on Colombian blood agar, MacConkey agar, and chocolate agar, and incubated in a 5% CO₂ incubator at 37°C for 24 hours. Two pure colonies were then isolated and cultured. The first colony was detected using the Vitek2-compact analysis system (bioMerieux, Marcy l’Etoile, France), and the results revealed Aeromonas salmonicida (51%) and Oligella ureolytica (49%), which were unreliable. Subsequently, using the MALDI BioTyper System (Bruker Realtime Classification software, Database 3.0; Microflex LT/SH; Bruker Daltonik GmbH, Bremen, Germany), the organism was identified as K. gyiorum (2.41 points) (Figure 1). This strain was confirmed by 16S rRNA gene sequencing, and the gene sequence results were uploaded to the NCBI GenBank database. Basic local alignment search tool (BLAST) alignment showed that the sequence was most similar to that of K. gyiorum (GenBank accession no. NR_025669.1 ) at approximately 99.73%. The second organism was identified as Pseudomonas aeruginosa. Drug susceptibility testing was performed using the Vitek2-compact analysis system (bioMerieux) and the disc diffusion method in accordance with the Clinical and Laboratory Standards Institute (CLSI) interpretive criteria M100 30th edition¹⁰ (Table 1).

Figure 1.

Identification and morphological characteristics of Kerstersia gyiorum. a: Mass spectrometry image. b: Gram staining morphology (×1000, oil). Morphological characteristics: c and d (strain in Case 1), f and g (strain in Case 2), on Columbian blood agar after 24 hours and 48 hours, respectively; e (strain in Case 1) and h (strain in Case 2) on MacConkey agar after 48 hours.

Table 1.

The results of drug sensitivity testing of two strains of Kerstersia gyiorum.

Antibiotic	First strain		Second strain
Antibiotic	MIC, µg/mL	Susceptibility	MIC, µg/mL	Susceptibility
Ticarcillin/Clavulanic acid	≤8	S	≤8	S
Piperacillin/Tazobactam	≤4	S	≤4	S
Ceftazidime	2	S	1	S
Cefepime	8	S	≤1	S
Aztreonam	8	S	8	S
Imipenem	≤0.25	S	≤0.25	S
Meropenem	≤0.25	S	≤0.25	S
Tobramycin	≤1	S	≤1	S
Amikacin	≤2	S	≤2	S
Trimethoprim-sulfamethoxazole	≤1/19	S	≤1/19	S
Doxycycline	1	S	≤0.5	S
Ciprofloxacin	≥4	R	≥4	R
Levofloxacin	≥8	R	≥8	R

MIC, minimum inhibitory concentration; S, susceptible; R, resistant; I, intermediate.

The patient was treated with 3.375 g piperacillin/tazobactam every 8 hours (intravenous (IV) drip) and traditional Chinese medicine (TCM) was administered by nasal feeding tube for 14 days (Cortex mori 15 g, Fructus trichosanthis 12 g, Scutellaria baicalensis 12 g, Poria 20 g, Platycodon grandiflorum 10 g, Gardenia jasminoides 10 g, Retinervus citri reticulatae 6 g, Ophiopogon japonicus 10 g, bran-processed rhizoma atractylodis 15 g, Fritillaria thunbergii 16 g, bitter almond 6 g, coix seed 30 g). The patient was also given symptomatic and supportive treatment. After 12 days, the patient’s body temperature and inflammatory marker values returned to normal.

Case 2

A 78-year-old man with Parkinson's disease was admitted to the hospital in a coma. He had a history of unstable hypertension for 20 years and did not smoke or drink alcohol. Ventilator-assisted breathing was initiated after tracheostomy, and at that time, he had a fever and purulent sputum in the airway.

The inflammatory marker values were as follows: white blood cells count, 4.3 × 10⁹/L; neutrophil percentage, 62.1%; and procalcitonin level, 0.196 ng/mL. Bedside chest radiography revealed that lung-marking was increased bilaterally. Using fiberoptic bronchoscopy, a small amount of white viscous sputum was found in the trachea, bronchi, and basal segment of the lower lung lobes, bilaterally; this was collected for Gram staining and culture.

Microscopically, Gram-negative bacilli and Gram-positive cocci were identified. The sputum was cultured, and pure colonies were isolated. The first colony failed to be identified by the Vitek2-compact analysis system (bioMerieux). Then, using the MALDI BioTyper System (Bruker Daltonik GmbH), the colony was identified as K. gyiorum (2.44 points) (Figure 1). This strain was confirmed by 16S rRNA gene sequencing, and the gene sequence results were uploaded to the NCBI GenBank database. BLAST alignment showed that the sequence was most similar to that of K. gyiorum (GenBank accession no. NR_025669.1 ) at approximately 99.59%. Other colonies were identified as Citrobacter koseri and Morganella, and drug susceptibility testing was performed (Table 1).

The patient's body temperature returned to normal after 1 day. TCM was prescribed by nasal feeding tube for 14 days (Ginger-Pinellia 10 g, fried Scutellaria 10 g, Coptis chinensis 5 g, Prince ginseng 20 g, jujube 12 g, Amomum villosum lour 6 g, tangerine peel 10 g, Fructus aurantii 10 g, magnolia 12 g, Poria 15 g, bran-processed Rhizoma atractylodis 15 g, bitter almond 10 g, Glehnia littoralis 15 g, fried coix seeds 30 g, Bupleurum 12 g, licorice 6 g, Pueraria 15 g, bran-processed Paeonia lactiflora 12 g). Following treatment, the inflammatory marker values returned to normal.

Informed consent for publication and treatment was obtained from both patients. The reporting of this study conforms to the CARE guidelines.¹¹ Ethics Committee approval was not required for a case report in our institution.

Discussion

Both strains of K. gyiorum in this study were isolated for the first time from the sputum of patients with neurodegenerative disease. The strains were identified as Gram-negative Pumilus spp., with single or paired distributions. After culture for 24 hours, the strains grew as a flat, uneven surface, with small point-like gray-white moist colonies and irregular edges. After 48 hours, the colonies increased in size with fan-shaped growth, and the edges appeared as a zigzag pattern. The colonies were nonadhesive and easy to scrape. However, compared with the strain in Case 1, the strain in Case 2 grew slowly, and the colony was white, slightly convex, and difficult to emulsify (Figure 1).

K. gyiorum is easily mistaken as Proteus because of its protracted growth on Colombian blood agar; however, K. gyiorum also has protracted growth on MacConkey agar.¹²

In the biochemical tests, no carbohydrate breakdown products were observed. The strain in Case 2 was positive for tyrosine arylamidase, L-lactate assimilation, L-lactate alkalinization, succinate alkalinization, and L-malate and citrate assimilation, whereas the strain in Case 1 was negative, which may explain why the strains grew differently. These findings were inconsistent with previously reported results.^2,12

Both strains were resistant to the fluroquinolones, ciprofloxacin, and levofloxacin, which may be related to the frequent use and even abuse of various antibiotics. As a rare bacterium, K. gyiorum gradually became resistant to some antibiotics, such as piperacillin/tazobactam, cefepime, ceftazidime, trimethoprim-sulfamethoxazole, gentamicin, aztreonam, fosfomycin, and colistin.^12–14 Fluoroquinolones penetrate bacterial cells through outer membrane porin and phospholipid, and induce changes in the configuration of enzymes, inhibit enzyme activity, and eventually lead to bacterial DNA degradation and cell death.¹⁵ Under the action of fluoroquinolones, bacteria develop drug resistance through chromosomal gene mutation or a plasmid-mediated mechanism, including target site change, decreased membrane permeability, and drug inactivation.¹⁶ The mechanism of drug resistance in K. gyiorum may involve a gene-encoding efflux pump;¹⁷ however, this requires further study.

Both cases in this report were elderly patients admitted to the intensive care unit. The first patient’s body temperature fluctuated between 37.1°C and 38.1°C. Additionally, the inflammatory marker values were elevated, and the lungs showed inflammation. Sputum culture identified a mixed infection; therefore, the patient was treated with antibiotics and TCM. In accordance with the Guidelines for Clinical Use of Antibacterials,¹⁸ piperacillin/tazobactam was selected as empirical treatment, for which drug susceptibility testing confirmed susceptibility. The fever in the second patient was transient, and there were no significant elevations in inflammatory marker values. K. gyiorum was detected in both the primary and second examinations. On the basis of the clinical manifestations and auxiliary examination results, the patient was considered to have a mild infection and was treated with TCM. Among the Chinese medicine prescriptions for the patients, Scutellaria baicalensis and Coptis chinensis have antibacterial effects. Ginger-Pinellia, tangerine peel, bran-processed Rhizoma atractylodis, bitter almond, and Glehnia littoralis have lung-clearing function. Platycodon grandiflorum, Retinervus citri reticulatae, and Fritillaria thunbergii have expectorant effects.¹⁹ Most previous reports used cephalosporins or fluoroquinolones for the treatment of K. gyiorum infections, such as ceftriaxone and ciprofloxacin.^13,20,21 The antibiotics used for treatment of some patients with severe mixed infection varied in previous reports and comprised piperacillin/tazobactam,^22,23 ampicillin/sulbactam,² imipenem,²⁴ or meropenem¹⁴ (Table 2). Among the previously reported cases with mixed infections, multiple species were identified, including Enterobacteriaceae, non-fermenting Gram-negative bacilli, Staphylococcus aureus, and diphtheroids.^13,20,24,25 Therefore, as an opportunistic pathogen, K. gyiorum may easily develop in concomitant infections. The patient in Case 1 had a mixed bacterial infection. To our knowledge, ours is the first report of integrated treatment for K. gyiorum infection using with TCM and Western medicine. The addition of TCM to Western medicine can improve inflammation, prolong survival time, and reduce mortality.²⁶ Unfortunately, TCM emphasizes dialectical treatment; therefore, it is difficult to unify standards and quickly popularize a treatment protocol. Therefore, considerable research is needed to explore the feasibility of a treatment.

Table 2.

Previous case reports of infections with Kerstersia gyiorum.

Year	Sex/Age (years)	Infection type	Diagnosis	Specimen type	Resistant antibiotics	Antibiotic treatment regimen	Country
2003³	/	/	/	lower extremity secretion	/	/	Belgium
2012²	M/16	single	otitis media	ear secretion	/	#A/S, *CRO, CIP, A/C	Argentina
2013²⁹	M/55	single	ear infection	ear secretion	CIP	#CIP ear drops, *added SXT	USA
2013²⁹	F/54	single	leg wound	lower-extremity secretion	CIP	CIP	USA
2014¹⁸	M/53	mixed	otitis media	ear secretion	/	CIP ear drops	Tanzania
2014¹⁸	M/33	mixed	otitis media	ear secretion	/	CIP ear drops	Tanzania
2014²⁰	F/63	mixed	respiratory failure	bronchoalveolar lavage	CIP (I)	#PIP/TAZ, DOR*PIP/TAZ, DOR, CAZ, CIP, COL	USA
2015¹²	F/69	single	lower-extremity ulcer	blood	FEP, PIP/TAZ	#CIP, CLI, VAN, *CIP, CLI	USA
2015²⁸	M/57	single	leg ulcer	lower-extremity secretion	/	/	USA
2015²²	M/25	mixed	otitis media	ear secretion	ATM, CIP, SXT; LEV (I)	IPM	Turkey
2015²⁵	M/82	mixed	bladder cancer	urine	/	LEV	Japan
2017¹⁹	M/47	mixed	Buerger’s disease	foot secretion	COL	#A/S, CIP, Mupirocin*Added CAZ, Metronidazole	Turkey
2017²¹	M/47	mixed	osteomyelitis	lower-extremity secretion	/	PIP/TAZ	China
2018²³	F/51	mixed	otitis media	ear secretion	CIP	#Cefpodoxime, *Cefcapene	Korea
2018¹³	F/21	single	otitis media	ear secretion	CAZ, CIP, GM	CIP ear drops, CRO	Turkey
	M/21	single		ear secretion	GM, SXT	CIP ear drops, CRO
	M/27	mixed		ear secretion	CIP, GM, SXT	CIP ear drops, CRO, MXF
2019²⁴	F/70	/	respiratory infection	sputum	/	/	China
2020¹⁷	F/85	mixed	venous insufficiency	lower-extremity secretion	CIP	/	Brazil
2021¹⁴	M/48	mixed	congestive dermatitis	leg secretion	ATM, CIP, FOS, LEV	#LEV, TDT*MEM, A/C, AMC	Japan

M, male; F, female; /, data not available; I, intermediate; #, treatment before drug susceptibility testing; *, treatment after drug susceptibility testing; A/C, amoxicillin/clavulanate; AMC, amoxicillin; A/S, ampicillin/sulbactam; ATM, aztreonam; CAZ, ceftazidime; CRO, ceftriaxone; CIP, ciprofloxacin; CLI, clindamycin; COL, colistin; DOR, doripenem; FEP, cefepime; FOS, fosfomycin; GM, gentamicin; IPM, imipenem; LEV, levofloxacin; MEM, meropenem; MXF, moxifloxacin; PIP/TAZ, piperacillin/tazobactam; SXT, trimethoprim-sulfamethoxazole; TDT, terbinafine; VAN, vancomycin.

Since K. gyiorum was named, it has been reported in various diseases, such as chronic ear infection,² chronic lower limb infection,¹² hemorrhagic dermatitis,¹⁴ chronic venous insufficiency,¹⁷ respiratory tract infection,²⁷ urinary tract infection,²⁸ thromboangiitis obliterans,²¹ and chronic osteomyelitis²³ (Table 2). K. gyiorum mainly causes chronic ear and leg infections, the pathogenic mechanism of which remains unclear. To our knowledge, this is the first report of K. gyiorum in neurodegenerative disease. Owing to poor immunity, long-term coma, or tracheal intubation, our patients were susceptible to opportunistic infection, which may be a complication. Like K. gyiorum, Alcaligenes faecalis also belongs to the family Alcaligenaceae. Most patients with cystitis owing to A. faecalis had neurological comorbidities.²⁹ It is possible that K. gyiorum is closely related to neurodegenerative disease. Studies have shown that the occurrence and development of neurodegenerative disease was affected by persistent inflammation in the systemic immune system.³⁰ As a common inflammatory risk factor, bacterial infection can activate the peripheral immune system followed by an immune response in the nervous system, which may affect neurological function.³⁰ Additionally, some Gram-negative bacteria secrete lipopolysaccharide and participate in the immune response.³⁰ In both of our cases, the persistent inflammation caused by infection with K. gyiorum and other pathogens may have affected the nervous system and promoted disease progression.

Genome sequencing of K. gyiorum has been reported previously,^27,31 which laid the foundation for further research. In previous reports, smoking, drinking alcohol, obesity, and unhealthy residential environments were considered risk factors for infection.^2,21,32 The following are also risk factors: advanced age; invasive or traumatic operations, such as the use of a ventilator, or surgery; diseases such as hypertension, diabetes, and cancer; and treatment with glucocorticoids, immunosuppressants, or broad-spectrum antibiotics.^22,25,28 In this study, the source of the samples differed in each patient; therefore, the relationship between K. gyiorum and the isolation site deserves further study.

In conclusion, K. gyiorum was isolated from the sputum of two patients with neurodegenerative disease, and the infections were cured using integrated TCM and Western medicine. With the use of MALDI-TOF MS and 16S rRNA gene sequencing, K. gyiorum has been identified in various diseases. However, the pathogenic mechanism, inflammatory response, and effective prevention and treatment require further study.

Research Data

Research Data for Kerstersia gyiorum isolated for the first time from two patients with neurodegenerative disease: report of two unusual cases and a review of the literature

Research Data for Kerstersia gyiorum isolated for the first time from two patients with neurodegenerative disease: report of two unusual cases and a review of the literature by Yanwen Sun, Danqing Liu, Xuejing Yang, Wenjie Li and Shaohua Lin in Journal of International Medical Research

Footnotes

Acknowledgements

We are grateful to the patients who provided information selflessly, and we thank our colleagues for their help.

Author contributions

Yanwen Sun performed the data analysis and wrote the manuscript. Danqing Liu and Xuejing Yang participated in the data analysis and manuscript revision. Wenjie Li participated in the laboratory examinations. Shaohua Lin oversaw the study design and manuscript revision. All authors read and approved the final manuscript.

Data availability

The raw data used in this article are available from the corresponding author on reasonable request.

Declaration of conflicting interest

The authors declare that there is no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

ORCID iDs

Yanwen Sun

Shaohua Lin

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