Table of Contents Author Guidelines Submit a Manuscript
Case Reports in Infectious Diseases
Volume 2017 (2017), Article ID 5962463, 5 pages
Case Report

Yokenella regensburgei Septicemia in a Chinese Farmer Immunosuppressed by HIV: A Case Report and Literature Review

Chongqing Public Health Medical Center, Chongqing, China

Correspondence should be addressed to Yaokai Chen; moc.liamtoh@nehciakoay

Received 9 December 2016; Revised 14 March 2017; Accepted 26 April 2017; Published 16 May 2017

Academic Editor: Oguz R. Sipahi

Copyright © 2017 Xiangbo Chi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Yokenella regensburgei is a member in the family Enterobacteriaceae and a few cases have been reported in immunocompromised hosts. Herein, we described a case of septicemia in a human immunodeficiency virus (HIV) infected patient in South West China, which is the first reported case of Y. regensburgei infection in HIV-infected populations. We then reviewed the literature on all the reported cases of Y. regensburgei infection worldwide and presented some common features of them. Our case report and literature review will help increase the knowledge of the bacterium Y. regensburgei and its clinical implications.

1. Introduction

Yokenella regensburgei belongs to the family Enterobacteriaceae and there is no strong evidence to support its clinical importance. There have been no Y. regensburgei infection reports in human immunodeficiency virus (HIV) infected patients, although a few case reports have suggested it is an opportunistic pathogen. Herein, we describe a case of septicemia in South West China caused by Y. regensburgei in a patient with HIV infection and present a review on Y. regensburgei literature.

2. Case Report

A 38-year-old male with a 20-year history of injection drug use was admitted to Chongqing Public Health Medical Center (Chongqing, China) in October 2013 due to a fever in absence of chills and cough. Two months prior to his admission, the patient was admitted to another hospital for epistaxis, dyspnea and odynuria with anemia, leucopenia, thrombocytopenia, and urinary tract infection, which improved with blood transfusions and use of antibiotics (levofloxacin injection, 0.2 grams each time, twice a day, for 14 days). His white blood cell counts ranged from 2.0 × 109 to 2.5 × 109 cells/liter during the period of 1 year prior to this admission.

He was confirmed to be HIV-positive since 2009 and received one year later an antiretroviral regimen containing stavudine, lamivudine, and efavirenz, which was discontinued in March 2013 due to renal impairment. He had been on methadone maintenance treatment for about 1 year.

He worked as a farmer. Family and social history were noncontributory. He smoked 10 cigarettes a day on average but rarely consumed alcohol.

On physical examination, the patient appeared pale and uncomfortable. Temperature was 38.7°C, blood pressure was 127/84 mmHg, heart rate was 104/min, and respiratory rate was 20/min. Oxygen saturation was 100% on 3 liters/minute nasal cannula. Cardiac exam was within normal limits and pulmonary and abdominal exams were benign. His skin was intact and no ulceration was found in his mouth. Chest computed tomography was performed and no abnormalities were found.

Blood examinations revealed anemia with hemoglobin of 42 g/liter (reference range, 130 to 175 grams/liter). Blood tests also revealed thrombocytopenia with a platelet count of 17 × 109 cells/liter (reference rage, 125 × 1012 to 350 × 1012 cells/liter). His white blood cell count was 3.79 × 109 cells/liter (reference rage, 3.5 × 109 to 9.5 × 109 cells/liter), differential with 81% neutrophilic granulocyte (reference rage, 40% to 75%) and 16% lymphocytes (reference rage, 20% to 50%). He was positive for HCV-antibody but HCV RNA was undetectable in his blood. Blood biochemistry showed an increased level of serum creatinine (501.5 μmol/liter; reference rage, 40 to 160 μmol/liter) and urea nitrogen (28.4 mmol/liter; reference rage, 2.2 to 8.3 mmol/liter) and a decreased level of albumin (25.4 grams/liter; reference range, 40 to 55 grams/liter). His CD4 cell count was 111 cells/microliter (reference range, 414 to 1123 cells/microliter) and HIV RNA level was 4.23 × 105 copies/milliliter (reference range, <20 copies/milliliter).

Under the impression that he had severe septicemia, we initiated early goal-directed therapy and 4 separate blood specimens were sampled at 1-hour intervals consecutively for bacterial culture before empirical antibiotics were given. The patient was treated with 1 g cefoxitin every 6 hours and 10 mg dexamethasone every 12 hours intravenously, combined with blood transfusions and erythropoietin injections. The patient’s condition stabilized the next day and his body temperature returned to normal 3 days later. The cefoxitin treatment was given for another 7 days and was discontinued when his white blood cell count returned to 2.51 × 109 cells/liter (reference rage, 3.5 × 109 to 9.5 × 109 cells/liter) and two posttreatment blood cultures yielded negative results. Three weeks after this admission, his blood creatinine and urea nitrogen levels normalized, his anemia and thrombocytopenia improved, and he was discharged in a stable condition. No recurrence was reported on a follow-up 1 year after discharge.

All four blood cultures grew Gram-negative rods. In our laboratory, we used the MicroScan Walkaway (Siemens, Memphis, TN) for the identification of the organism and the results of a series of biochemical assays revealed it to be Y. regensburgei with 97.8% probability. It was positive for glucose, sorbitol, rhamnose, L-arabinose, melibiose, lysine, ornithine, citrate, galactoside, and cellobiose tests and negative for sucrose, raffinose, inositol, adonitol, urea, hydrogen sulfide, indole, arginine, tryptophan deaminase, aesculin, acetoin, malonate, tartrate, acetamide, cetrimide, and Voges-Proskauer tests. Susceptibility testing was performed using the MicroScan Walkaway and the Enterobacteriaceae criteria of CLSI were used by our laboratory [1]. The MIC results as shown in Table 1.

Table 1: Susceptibility of the isolated Y. regensburgei stain.

3. Systematic Review

We searched PubMed ( with the keyword of Yokenella regensburgei on March 31, 2017, and found 10 articles. And then we used Koserella trabulsii as the keyword to search on PubMed on the same day and found another 6 articles. We reviewed all the 16 articles and found seven cases of Y. regensburgei infection as well as useful information about Y. regensburgei.

Y. regensburgei is one of a number of infrequent members of the family Enterobacteriaceae that have only rarely been isolated in humans. It was originally identified by Kosako et al. [2] through DNA hybridization in 1984 and later recognized by Hickman-Brenner et al. [3], working independently, in 1985, under the name of Koserella trabulsii. Subsequently, it was found that Y. regensburgei and K. trabulsii referred to the same Enterobacteriaceae and therefore the use of K. trabulsii has been dropped since 1991 [4].

Y. regensburgei closely resembles Hafnia alvei biochemically and has been misidentified as Hafnia alvei by automated systems [4]. It, therefore, has been hypothesized that infections due to Y. regensburgei have been underestimated due to misidentification of the bacterium. By studying susceptibility patterns and biochemical properties, Stock et al. [5] found that hydroxyproline amidase, maltosidase, tripeptidase, proline deaminase, catalase reaction, Voges-Proskauer test, and fermentation of glycerol, melibiose, and myo-inositol were suitable parameters to separate Y. regensburgei from H. alvei. Y. regensburgei is noted to possess amp C genes and express highly inducible, potent beta-lactamases and is intrinsically resistant to azithromycin and some beta-lactam antibiotics. However, it is weakly catalase positive and unable to produce hydroxyproline amidase, tripeptidase, or proline deaminase. Jachymek et al. [6] discovered novel trisaccharide repeating units of bacterial O antigens that are characteristic and unique to the Y. regensburgei species. Niedziela et al. [7] described the structures of the core oligosaccharides representing novel core types of bacterial LPS that are characteristic for Y. regensburgei.

Y. regensburgei appears to primarily belong to the bacterial flora of insects and has been recovered from the intestinal tracts of insects. Also, it has been isolated from the general environment such as in well water. Isolation of Y. regensburgei from a human specimen is rare and only seven cases of Y. regensburgei infection have been reported worldwide based on the literature we reviewed. Abbott and Janda [8] described two isolations of Y. regensburgei associated with extra-intestinal sites in humans immunocompromised due to alcohol abuse. The first isolate was from a left-knee wound of a 74-year-old male with a provisional diagnosis of a septic knee and a history of alcohol abuse. He was treated with amikacin, and no further data were available regarding the patient’s clinical course. In the second case, a 35-year-old woman who abused alcohol suffered from an upper gastrointestinal bleeding. A blood culture grew Y. regensburgei during her hospital course, although she had no overt signs of sepsis such as fever or chills. The patent was subsequently treated with ciprofloxacin and released. Lo et al. [9] described a patient with membranous glomerulonephritis on immunosuppressive therapy with high-dose steroids (prednisolone total of 30 mg per day) and cyclophosphamide. The patient subsequently developed a soft tissue infection after abrasions to his leg, which had been contaminated with soil. He experienced fevers with chills, and his blood cultures grew Y. regensburgei. After receiving treatment with ceftriaxone for 3 weeks, he was discharged from hospital in stable conditions. Bhowmick and Weinstein [10] reported a 48-year-old male with multiple myeloma who had undergone an autologous stem cell transplant and had been on corticosteroids for liver disease. Later, the patient had a bulla on his right leg but had no fevers and chills. The bulla aspirate and 2 blood cultures grew Y. regensburgei. Fajardo Olivares et al. [11] described an 82-year-old male with chronic renal failure, venous thrombosis, and perimalleolar ulcer. Y. regensburgei was isolated from his ulcerous wound and he was cured with ciprofloxacin. Penagos et al. [12] presented a case of postsurgical secondary osteomyelitis due to Y. regensburgei in an immunocompetent woman who had undergone a craniotomy. The patient was successfully treated with ciprofloxacin for 42 days and there was no recurrence of infection at the end of 1-year follow-up. Jain et al. [13] reported a 5-year-old male child with continuous high-grade fever and chills for 7 days. Two blood cultures yielded positive results and the identification of both isolates was confirmed as Y. regensburgei. The child was treated with ciprofloxacin for 7 days and he responded clinically to the treatment. No recurrence was reported on a follow-up 3 months later.

4. Discussion

The patient in our present report, a confirmed HIV-infected individual with pancytopenia, was viremic in absence of ART when he was admitted due to a fever. The fact that Y. regensburgei was isolated from all 4 separate blood samples and the patient was successfully cured with cefoxitin demonstrated that the organism was definitely the cause of septicemia. Noticeably, the patient’s white blood cell count was higher compared with his baseline values and the number decreased to its pretreatment levels after 10 days of antibiotic treatment, suggesting that Y. regensburgei infection could result in elevated white blood cell counts. We did not observe any evidence for the association between the patient’s septicemia and his farming practice, although the organism could have been from the general environment like the soil. This is the first case of infection caused by Y. regensburgei in an HIV-infected patient to the best of our knowledge and our case supports the hypothesis that Y. regensburgei is an opportunistic pathogen in humans. However, we were not able to confirm the bacterial identification with sequencing, which is the limitation of this article. All the eight reported cases are summarized in Table 2.

Table 2: Summary of Y. regensburgei infection cases reported worldwide.

Some common features can be observed from the seven reported cases and our case. Firstly, almost all cases have underlying diseases or immunocompromising conditions. Secondly, the majority of those cases have no systematic symptoms like fever and chills. Thirdly, the outcome of Y. regensburgei infection appears to be not too severe; only one death occurred among the eight cases, while five cases were cured. And lastly but interestingly, almost all the cases are from regions known for hot and humid weather.

In summary, we report a case of Y. regensburgei septicemia in a patient with HIV infection and pancytopenia. There are some similarities among the eight cases with regard to underlying conditions, clinical presentations, outcome, and geographical regions. From all the eight cases worldwide, it is reasonable to assume that Y. regensburgei is an opportunistic pathogen with a predilection to infect hosts severely immunocompromised by underlying diseases or conditions.

Ethical Approval

The Chongqing Public Health Medical Center Ethics Committee reviewed and approved this case report.


Informed consent was obtained from the patient described in the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


The authors thank Professor Jean-Pierre Routy of Centre Universitaire de Santé McGill for his suggestions about language improvement and case discussion. This work was funded by Chongqing Municipal Health and Family Planning Committee (2016HBRC008).


  1. CLSI, Performance Standards for Antimicrobial Susceptibility Testing, CLSI Supplement M100, Clinical and Laboratory Standtards Institutes, Wayne, Pa, USA, 27th edition, 2017.
  2. Y. Kosako, R. Sakazaki, and E. Yoshizaki, “Yokenella regensburgei gen. nov., sp. nov.: a new genus and species in the family Enterobacteriaceae,” Japanese Journal of Medical Science and Biology, vol. 37, no. 3, pp. 117–124, 1984. View at Publisher · View at Google Scholar · View at Scopus
  3. F. W. Hickman-Brenner, G. P. Huntley-Carter, G. R. Fanning, D. J. Brenner, and J. J. Farmer III, “Koserella trabulsii, a new genus and species of Enterobacteriaceae formerly known as Enteric Group 45,” Journal of Clinical Microbiology, vol. 21, no. 1, pp. 39–42, 1985. View at Google Scholar
  4. A. C. McWhorter, R. L. Haddock, F. A. Nocon et al., “Trabulsiella guamensis, a new genus and species of the family Enterobacteriaceae that resembles Salmonella subgroups 4 and 5,” Journal of Clinical Microbiology, vol. 29, no. 7, pp. 1480–1485, 1991. View at Google Scholar · View at Scopus
  5. I. Stock, K. J. Sherwood, and B. Wiedemann, “Antimicrobial susceptibility patterns, β-lactamases, and biochemical identification of Yokenella regensburgei strains,” Diagnostic Microbiology and Infectious Disease, vol. 48, no. 1, pp. 5–15, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. W. Jachymek, T. Niedziela, C. Petersson, C. Lugowski, J. Czaja, and L. Kenne, “Structures of the O-specific polysaccharides from Yokenella regensburgei (Koserella trabulsii) strains PCM 2476, 2477, 2478, and 2494: high-resolution magic-angle spinning NMR investigation of the O-specific polysaccharides in native lipopolysaccharides and directly on the surface of living bacteria,” Biochemistry, vol. 38, no. 36, pp. 11788–11795, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Niedziela, W. Jachymek, J. Lukasiewicz et al., “Structures of two novel, serologically nonrelated core oligosaccharides of Yokenella regensburgei lipopolysaccharides differing only by a single hexose substitution,” Glycobiology, vol. 20, no. 2, pp. 207–214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. L. Abbott and J. M. Janda, “Isolation of Yokenella regensburgei (‘Koserella trabulsii’) from a patient with transient bacteremia and from a patient with a septic knee,” Journal of Clinical Microbiology, vol. 32, no. 11, pp. 2854-2855, 1994. View at Google Scholar · View at Scopus
  9. Y.-C. Lo, Y.-W. Chuang, and Y.-H. Lin, “Yokenella regensburgei in an immunocompromised host: a case report and review of the literature,” Infection, vol. 39, no. 5, pp. 485–488, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Bhowmick and M. P. Weinstein, “A deceptive case of cellulitis caused by a Gram-negative pathogen,” Journal of Clinical Microbiology, vol. 51, no. 4, pp. 1320–1323, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Fajardo Olivares, J. Blanco Palenciano, I. Márquez Laffón, and J. M. Ruiz León, “Yokenella regensburgei infection in a perimalleolar ulcer,” Medicina Clinica, vol. 125, no. 9, pp. 358-359, 2005 (Spanish). View at Publisher · View at Google Scholar
  12. S. C. Penagos, S. Gómez, P. Villa, S. Estrada, and C. A. Agudelo, “Osteomyelitis due to Yokenella regensburgei following craniotomy in an immunocompetent patient,” Biomedica, vol. 35, no. 4, pp. 471–474, 2015 (Spanish). View at Publisher · View at Google Scholar · View at Scopus
  13. S. Jain, R. Gaind, K. B. Gupta et al., “Yokenella regensburgei infection in India mimicking enteric fever,” Journal of Medical Microbiology, vol. 62, no. 6, pp. 935–939, 2013. View at Publisher · View at Google Scholar · View at Scopus