ACCEPTED. Running title: BCG osteomyelitis diagnosed by PCR-Based genomic deletion analysis

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1 JCM Accepts, published online ahead of print on October 00 J. Clin. Microbiol. doi:./jcm Copyright 00, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved Mycobacterium bovis BCG Vertebral Osteomyelitis after Intravesical BCG therapy diagnosed by PCR-Based Genomic Deletion Analysis Takuya Nikaido 1, Kei Ishibashi, Koji Otani 1, Shoji Yabuki 1, Shinichi Konno 1, Shuichi Mori, Kazutaka Ohashi, Takashi Ishida, Michiko Nakano, Osamu Yamaguchi, Tatsuo Suzutani *, Shinichi Kikuchi 1 1 Department of Orthopedics, Department of Microbiology, Department of Urology and Department of Pulmonary Medicine, Fukushima Medical University, Fukushima 0-1, JAPAN Running title: BCG osteomyelitis diagnosed by PCR-Based genomic deletion analysis Abstract words, Text 1 words, Figures. Correspondence to: Tatsuo Suzutani MD, PhD Department of Microbiology, Fukushima Medical University, 1 Hikarigaoka, Fukushima 0-1, JAPAN (phone) (FAX) suzutani@fmu.ac.jp ( ) Downloaded from on May, 01 by guest

2 ABSTRACT We report a case of Mycobacterium bovis BCG vertebral osteomyelitis 1. years after intravesical BCG therapy for bladder cancer. We differentiated BCG from other Mycobacterium tuberculosis complex members by PCR-analysis of deletion regions and started an appropriate chemotherapy regimen resulting in the remission of symptoms within 1 month. Downloaded from on May, 01 by guest

3 Case report An -year-old man was referred to our institution for unrelenting back pain. He first noticed the pain without any particular cause in December 00. He had no fever, chills, cough, or motor or sensory deficits, but his ability to perform daily activities progressively decreased due to his back pain. The patient had a history of hypertension, but denied any history of active tuberculous infection or ever having received BCG vaccine. He also had a history of left ureteral transitional cell carcinoma and bladder cancer diagnosed in 00. As he elected bladder preservation, these tumors were surgically resected by total left nephroureterectomy and transurethral resection followed by cisplatin-based chemotherapy in September 00. As the follow-up cystoscopy and biopsy in December 00 demonstrated a carcinoma in situ, treatment with intravesical BCG (Tokyo strain) immunotherapy was started in January 00. Eight weekly instillations were administered with no significant side effects, and no prophylaxis was given during the BCG treatment. However, follow-up cystoscopy and Downloaded from on May, 01 by guest 1 urine cytology examination again demonstrated the presence of a carcinoma. 1 Subsequently, pelvic radiation therapy (total 0 Gy) was added in April 00 with 1 cisplatin-based chemotherapy on the first day of radiation therapy. Thereafter, the 1 results of follow-up examinations revealed no recurrent carcinoma.

4 Physical examination elicited focal knock pain but motor function was intact Laboratory studies showed a white blood count of 00 /mm, a C-reactive protein level of 1. mg/dl, and an erythrocyte sedimentation rate of mm. Thoracolumbar x-ray and computed tomography showed destructive changes involving the anterior end plate of the T1 and L1 vertebral bodies. A magnetic resonance imaging study confirmed the presence of a destructive lesion involving the T1 and L1 vertebral bodies and intervertebral disc, and also showed an abscessed lesion in the left paraspinal soft tissue of the L1 vertebral body (Figure 1). A needle biopsy of the involved disc space pathologically revealed necrosis and acute inflammation in this region. Ziehl-Neelsen stains were positive for acid-fast bacilli and weeks later yielded a positive culture for mycobacteria. At the Department of Clinical Laboratory which belongs to our hospital, the initial examinations for the differentiation of the acid-fast bacilli used PCR (Amplicor PCR, Roche Diagnostic, Basel, Switzerland) and immunochromatography testing (CapiliaTB, BD, NJ, USA). On the basis of those examinations, the acid-fast Downloaded from on May, 01 by guest 1 bacilli from the biopsy samples were reported to belong to the Mycobacterium 1 tuberculosis complex (MTC). However, using those methods, they could not 1 differentiate between Micobacterium tuberculosis and other acid-fast bacilli including 1 M. bovis, M. bovis BCG, M. africanum and M. microti. To identify the causative bacillus

5 among those of the MTC, cultured sample was send to the Department of Microbiology, and we performed genomic deletion analysis using multiplex PCR targeting RD 1, and (1). Briefly, the sample from the bacterial culture was centrifuged at 00 g for fifteen minutes and the pellet was washed three times with acetone, then resuspended in phosphate buffered saline (PBS). DNA was extracted using a QIAamp DNA Mini Kit (Quiagen, CA) according to manufacturer s protocol. Primer sets and PCR method were described in the literature (1). The PCR deletion analyses revealed 00bp, 0bp and 0bp bands, indicating the absence of RD1, RD, and RD, respectively (Figure ). These results indicated that the isolate was M bovis BCG and not any other mycobacterium. Consequently, the patient was diagnosed with osteomyelitis as a complication of the intravesical M bovis BCG administered 1. years earlier. The patient was immediately placed on a -drug regimen of isoniazid, rifampicin and ethanbutol. Drug susceptibility analysis using bacterial culture (MGIT, BD, NJ) confirmed that the isolate was resistant to pyrazinamide as is characteristic of BCG. To confirm our results, Downloaded from on May, 01 by guest 1 a commercial available system based on DNA hybridization technology and using 1 nitrocellulose strips (GenoType MTBC; Hain Diagnostika, Nehren, Germany) was 1 performed as previously reported (, 1, 1). The band pattern,,,, 1 obtained 1 from the results of the GenoType MTBC based on the gyrase B gene polymorphisms

6 also indicated that the isolates was M bovis BCG. Surgical intervention was not required as the patient s symptoms were improved 1 month after starting the -drug chemotherapy. There was no recurrence of symptoms of osteomyelitis or the bladder cancer for 1 year, but the patient later died of heart disease. Downloaded from on May, 01 by guest

7 Discussion Bacillus Calmette-Guérin (BCG) is a live attenuated strain of M. bovis that was first used for immunization against tuberculosis in 11. After a half of century, Morales, Eidinger and Bruce introduced BCG as an intravesical treatment for superficial bladder cancer (). Since then, BCG has been applied to the treatment of and prophylaxis against Ta and T1 tumors and carcinoma in situ, and recent meta-analysis by the European Organization for Research and Treatment of Cancer has shown that BCG can lower the risk of cancer progression (1). Although it has been considered that complications of BCG instillations for bladder cancer therapy are relatively rare, they are more frequent than in tuberculosis vaccination programs. It is crucial for clinicians to distinguish the causative bacillus from acquired infections from other sources. However, it has been difficult to distinguish M. bovis BCG because of the high degree of sequence conservation and similar biochemical characterizations among the members of the MTC. Downloaded from on May, 01 by guest 1 Intravesical BCG therapy has been regarded as an effective treatment for Ta 1 and T1 tumors and carcinoma in situ. Though the therapy is considered to be safe, many 1 kinds of adverse reactions were noted by Lamm et al., including fever, granulomatous 1 prostatitis, pneumonia, hepatitis, arthrargia, hematuria, rash, ureteral obstruction,

8 epididymitis, contracted bladder, renal abscess, sepsis and cytopenia (). While adverse effects such as hematuria, cystitis and fever are considered to be relatively common, extravesical complications are rare. BCG osteomyelitis is a rare complication of BCG vaccination for the prophylaxis of tuberculosis. The incidence of osteitis following BCG vaccination was calculated to be 0 to. cases per 0,000 (1). Several factors, such as age at vaccination and BCG strain, may contribute to the frequency of osteites after BCG vaccination (). However, BCG osteomyelitis following intravesical BCG therapy is an extremely rare complication with only cases reported in English-language literature (1). Among those reports, cases were diagnosed with M. bovis BCG infection using high-performance liquid chromatography (HPLC) (,,, ). The MTC includes Micobacterium tuberculosis, M. bovis, M. bovis BCG, M. africanum and M. microti. In our case, though the isolate was revealed to be MTC by conventional bacterial examinations, identification of the causative bacillus was not Downloaded from on May, 01 by guest 1 possible due to the fact that commercial DNA probes and amplification assays based on 1 1S rrna gene sequences, which show a high degree of sequence conservation, 1 identify all MTC members. Although it is remotely possible that, in the patient we 1 describe, the M. bovis or M. africanum were acquired from another source,

9 differentiation of the members of the MTC is necessary both for treatment and for epidemiological purposes. Although HPLC has been reported to be a reliable method for the identification of mycobacterium (), it is cumbersome and expensive and is used in only a very few laboratories. Recently, on the basis of data from comparative genomic studies of mycobacterium that found that some regions are deleted among the members of the MTC (), rapid and simple assays for precise identification of the MTC have been reported (1). Using molecular amplification methods that showed that RD1, and were all region-absent for the isolate, the patient was diagnosed with osteomyelitis as a complication of the intravesical M. bovis BCG administered 1. years earlier. In addition to the PCR deletion analysis, the GenoType MTBC identified M. bovis BCG based on gyrase B gene polymorphisms. Our case indicates that these methods of genotypic identification would be clinically useful. Although all strains of M. bovis are intrinsically resistant to pyrazinamide, M. bovis BCG is generally susceptible to antituberculosis drugs, such as isoniazid, Downloaded from on May, 01 by guest 1 rifampicin, paraaminosalicylic acid, ethanbutol and streptomycin. In our case, 1 successful treatment was obtained using a -drug regimen of isoniazid, rifampicin and 1 ethanbutol following the rapid diagnosis. 1 In conclusion, intravesical BCG therapy may disseminate the bacilli to the

10 bone. The PCR amplification methods targeting RD1, and are rapid, simple and precise compared with conventional examinations and allow the immediate introduction of appropriate treatment. Downloaded from on May, 01 by guest

11 Acknowledgments We thank HAIN Lifescience GmbH (Nehren, Germany) for the kind identification of the clinical isolate by GenoType MTBC. This work was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (No.0) and by a Grant-in-Aid for Research Project from Fukushima Medical University. Downloaded from on May, 01 by guest

12 References Abu-Nader, R., and C. L. Terrell. 00. Mycobacterium bovis vertebral osteomyelitis as a complication of intravesical BCG use. Mayo Clin Proc :-.. Aljada, I. S., J. K. Crane, N. Corriere, D. G. Wagle, and D. Amsterdam. 1. Mycobacterium bovis BCG causing vertebral osteomyelitis (Pott's disease) following intravesical BCG therapy. J Clin Microbiol :-.. Behr, M. A., M. A. Wilson, W. P. Gill, H. Salamon, G. K. Schoolnik, S. Rane, and P. M. Small. 1. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science :-.. Civen, R., G. Berlin, and C. Panosian. 1. Vertebral osteomyelitis after intravesical administration of bacille Calmette-Guerin. Clin Infect Dis 1:1-.. Fishman, J. R., D. T. Walton, N. M. Flynn, D. R. Benson, and R. W. devere Downloaded from on May, 01 by guest 1 White. 1. Tuberculous spondylitis as a complication of intravesical bacillus 1 Calmette-Guerin therapy. J Urol 1:-. 1. Floyd, M. M., V. A. Silcox, W. D. Jones, Jr., W. R. Butler, and J. O. Kilburn Separation of Mycobacterium bovis BCG from Mycobacterium

13 tuberculosis and Mycobacterium bovis by using high-performance liquid chromatography of mycolic acids. J Clin Microbiol 0:1-0.. Gomez, M. P., L. Herrera-Leon, M. S. Jimenez, and J. G. Rodriguez. 00. Comparison of GenoType MTBC with RFLP-PCR and multiplex PCR to identify Mycobacterium tuberculosis complex species. Eur J Clin Microbiol Infect Dis :-.. Lamm, D. L., P. M. van der Meijden, A. Morales, S. A. Brosman, W. J. Catalona, H. W. Herr, M. S. Soloway, A. Steg, and F. M. Debruyne. 1. Incidence and treatment of complications of bacillus Calmette-Guerin intravesical therapy in superficial bladder cancer. J Urol 1:-00.. Lotte, A., O. Wasz-Hockert, N. Poisson, N. Dumitrescu, M. Verron, and E. Couvet. 1. BCG complications. Estimates of the risks among vaccinated subjects and statistical analysis of their main characteristics. Adv Tuberc Res 1:-. Downloaded from on May, 01 by guest 1. Morales, A., D. Eidinger, and A. W. Bruce. 00. Intracavitary Bacillus 1 Calmette-Guerin in the treatment of superficial bladder tumors. 1. J Urol 1 1:1-; discussion Morgan, M. B., and M. D. Iseman. 1. Mycobacterium bovis vertebral

14 osteomyelitis as a complication of intravesical administration of Bacille Calmette-Guerin. Am J Med 0:-. 1. Parsons, L. M., R. Brosch, S. T. Cole, A. Somoskovi, A. Loder, G. Bretzel, D. Van Soolingen, Y. M. Hale, and M. Salfinger. 00. Rapid and simple approach for identification of Mycobacterium tuberculosis complex isolates by PCR-based genomic deletion analysis. J Clin Microbiol 0:-. 1. Richter, E., M. Weizenegger, A. M. Fahr, and S. Rusch-Gerdes. 00. Usefulness of the GenoType MTBC assay for differentiating species of the Mycobacterium tuberculosis complex in cultures obtained from clinical specimens. J Clin Microbiol : Richter, E., M. Weizenegger, S. Rusch-Gerdes, and S. Niemann. 00. Evaluation of genotype MTBC assay for differentiation of clinical Mycobacterium tuberculosis complex isolates. J Clin Microbiol 1:-. 1. Sylvester, R. J., M. A. van der, and D. L. Lamm. 00. Intravesical bacillus Downloaded from on May, 01 by guest 1 Calmette-Guerin reduces the risk of progression in patients with superficial 1 bladder cancer: a meta-analysis of the published results of randomized clinical 1 trials. J Urol 1: Ulstrup, J. C., S. Jeansson, H. G. Wiker, and M. Harboe. 1. Relationship

15 of secretion pattern and MPB0 homology with osteoblast-specific factor to osteitis following Mycobacterium bovis BCG vaccination. Infect Immun :-. Downloaded from on May, 01 by guest

16 1 Figure legends Figure 1 Magnetic resonance imaging scans of the lumbar spine. A: T1-weighted image demonstrates a destructive lesion of the Th1 and L1 vertebrae and intervening disk. B: Axial image of the L1 destructive lesion. C: T1-weighted image obtained with gadolinium contrast reveals an abscess with contrasted border (white arrow). Figure Results of PCR for RD1,, and. T; M. tuberculosis HRv strain, B; M. bovis BCG Tokyo strain, S; clinical isolate sample from the vertebral osteomyelitis patient. Downloaded from on May, 01 by guest

17 Figure 1 A B C Downloaded from on May, 01 by guest

18 Fig. (bp) T B S T B S T B S R D 1 R D R D Downloaded from on May, 01 by guest

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