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�)�*0�*�R2/�T2/; 2/; �	__O_____�)�)O___�*____��������������������������������������������������������������������2/_________�+�:	Bacillus Calmette-Gu�rin (BCG) Vaccine-Induced Disease in Healthy Infants:
Identification of BCG Gene from Formalin-Fixed Paraffin-Embedded Tissue


Takako Yoshioka1, Junichiro Nishi2, Kiyofumi Ohkusu3, Kazuhito Hatanaka1,
Sohsuke Yamada4, Kazuhiko Nakame5, Yoshifumi Kawano2, Tatsuru Kaji5 
and Akihide Tanimoto1*
1Department of Molecular and Cellular Pathology, 2Microbiology and 5Pediatric Surgery, Kagoshima University Graduate School of Medical and Dental Sciences, 3Department of Microbiology, Gifu University Graduate School of Medicine, and 4Department of Pathology and Cell Biology, School of Medicine, University of Occupational and Environmental Health
Running title: BCG granuloma in healthy infants
*Corresponding: Akihide Tanimoto, MD., PhD., Department of Tumor Pathology, Kagoshima University of Graduate School of Medical and Dental Sciences, 8-35-1 Sakuragaoka, Kagoshima 890-8544, Japan
TEL: 81-99-275-5263, FAX: 81-99-264-6348 
E-mail:  HYPERLINK "mailto:akit09@m3.kufm.kagoshima-u.ac.jp" akit09@m3.kufm.kagoshima-u.ac.jp

Abstract
Background: Bacillus Calmette-Gu�rin (BCG) vaccine-induced systemic complication is rare but localized skin lesion develops in the site of inoculation in healthy infants. Methods: In this report, we described three cases of BCG vaccine-induced skin lesions in healthy immunocompetent infants and a method of identification of BCG gene by polymerase chain reaction (PCR) form fresh frozen of formalin-fixed and paraffin-embedded tissue samples. 
Results: These cases had a history of BCG vaccination but no family history of tuberculosis and no contact with patients of tuberculosis. Two cases developed cutaneous granuloma in the axilla of ipsilateral side of BCG inoculation. Another case showed granulomatous osteomyelitis of the left 6th rib. Histological examination demonstrated typical pathologic findings for epithelioid granuloma with caseation necrosis, indicating mycobacterium infection. PCR analysis from fresh frozen or formalin-fixed paraffin-embedded tissue rapidly confirmed the infection of Mycobacterium bovis BCG but not M. tuberculosis. 
Conclusion: BCG infection should be considered even in healthy infants with a history of BCG vaccination and histology of epithelioid granuloma with caseation necrosis. In such cases, BCG gene identification by PCR would be useful even from formalin-fixed and paraffin embedded tissue samples.
Key words: Tuberculosis, BCG, Infant, PCR, Granuloma, Osteomyelitis
List of abbreviations: BCG: Bacillus Calmette-Gu�rin, PCR: polymerase chain reaction, H&E: hematoxylin and eosin, PAS: periodic acid-Schiff, FFPE: formalin-fixed paraffin-embedding 


Intraduction
     Bacillus Calmette-Gu�rin (BCG) vaccination has been widely employed in the world to prevent M. tuberculosis infection. The BCG vaccine contains live attenuated strain of M. bovis and it rarely causes systemic complication but only localized and weak skin irritation at the site of inoculation in healthy infants. In contrast, immunocompromised human immunodeficiency virus-infected infants have a high prevalence of BCG-induced complication [9, 13]. Even in healthy immunocompetent infants, however, BCG diseases such as lymphadenitis and regional abscess formation have been reported [15]. In addition, it has also been reported that BCG diseases may occur as a consequence of immunotherapy for bladder cancer (intravesical installation of BCG) [14]. Herein we report three cases of BCG vaccination-induced osteomyelitis (1 case) and dermal abscess (2 cases) in healthy children more than 6 months after the BCG vaccination.

Materials and Methods
Histological examination
     The resected materials were fixed with phosphate buffered (pH7.4) 20% formalin and routinely processed for preparation of paraffin-embedded tissue. The 5m�M thick sections were stained with hematoxylin and eosin (H&E), Ziehl-Neelsen, Grocott and periodic acid-Schiff (PAS) stains.

Polymerase chain reaction and sequencing of BCG gene
     DNAs from fresh frozen tissue (Case 1) or formalin-fixed paraffin-embedding (FFPE) tissue sections (Cases 2 and 3) were extracted with proteinase K buffer for PCR amplification of BCG gene. A primer set targeting the M. bovis BCG-specific region of difference 1 (RD1) was designed according to the genomic DNA sequence as 5�-CAAGCACTGGCGGTCAACCT-3� and 5�-CGACGGGCAGCTATGCCAGA-3  (GenBank accession number AM408590.1) [16]. The PCR was performed in a volume of 50m�L with the template DNA. The thermal profile was 48 cycles at 95�C (30sec), 66.5�C (30sec) and 74�C (30sec). The PCR products (167bp) were then electrophoresed on a 3% agarose gel and the sequence was confirmed. No PCR product was amplified with a primer set (ET2 and ET3 [16]) for detection of M. tuberculosis (data not shown).

Results
Case 1
     A 15-month-old male was admitted to the hospital with a swelling of the left anterior chest wall. Under a diagnosis of bone tumor of the left 6th rib, a biopsy was undertaken and histological examination showed findings of osteomyelitis by epithelioid granuloma with caseation necrosis. His family had no history of tuberculosis and he and his family had no contact with patients of tuberculosis. He was vaccinated with BCG (Tokyo strain) by an inoculation in the left upper arm at his 4 months of age. Computed tomography (CT) showed a soft tissue density mass around the left 6th rib (Fig. 1A). The tuberculosis-specific interferon-g� (Quantiferon, Cellestis Limited, Australia) was not detected. After chemotherapy, the lesion including the rib was surgically removed. No immunological abnormality was demonstrated by clinical tests.
Macroscopic and microscopic examination of the resected lesion demonstrated osteomyelitis featured by osteolytic bone tissue with epithelioid granulomas and caseation necrosis (Fig. 1B, 1C and 1D). The adjacent connective tissue and skeletal muscles were involved by the granuloma. PCR analysis using DNA extracted from the fresh frozen tissue to amplify the M. bovis BCG-specific region of difference 1 (RD1) confirmed the diagnosis of BCG-induced granuloma (Fig. 3).
Case 2
     A 3-year and 7-month-old male was admitted to the hospital due to a subcutaneous mass in the left axilla. Lymphangioma was suspected and the lesion was surgically resected. Chest CT showed no abnormal findings. His family had no history of tuberculosis and he and his family had no contact with the patients of tuberculosis. He was vaccinated with BCG (Tokyo strain) by an inoculation in the left upper arm at his 8 months of age. No immunological abnormality was demonstrated by clinical tests.
Macroscopic and microscopic examination of the cutaneous mass demonstrated epithelioid granulomas with caseation necrosis and calcification (Fig. 2A and 2B). PCR analysis using DNA extracted from the FFPE tissue section to amplify the M. bovis BCG-specific RD1 region confirmed the diagnosis of BCG-induced granuloma (Fig. 3).
Case 3
     A 23-month-old male was hospitalized by a subcutaneous mass at the left axilla (Fig. 2C), which was suspected to be lymphangioma and the lesion was surgically resected. Chest CT disclosed no significant findings. His family had no history of tuberculosis and he and his family had no contact with the patients of tuberculosis. He was vaccinated with BCG (Tokyo strain) by an inoculation in the left upper arm at his 4 months of age. No immunological abnormality was demonstrated by clinical tests.
     Microscopic examination of the cutaneous mass demonstrated epithelioid granulomas with caseation necrosis and calcification (Fig. 2D). PCR analysis using the FFPE tissue section did not detect the genes of M. tuberculosis but BCG-specific RD1 region of M. bovis was confirmed (Fig. 3).

Discussion
      In general, the complications following BCG vaccination are estimated to be 0.01% to 3.6% in frequency and most BCG complication diseases are local or regional diseases manifested by such as local skin ulceration at the site of inoculation and ipsilateral lymphadenitis, respectively [8, 9, 15]. However, distant or disseminated BCG-related disease occurs even in immunocompetent infants and children [1, 4, 5, 15]. Recent classification of BCG disease includes five categories: (1) local disease, (2) regional disease, (3) distant disease, (4) disseminated disease, and (5) other BCG syndromes [9]. The local disease is manifested by abscess or ulcer formation at the site of vaccination. The regional disease includes lymph node involvement beyond the vaccination site such as ipsilateral axillary, supraclavicular and cervical lymph nodes. These two conditions accounted for 88% of the total BCG-related diseases. The distant disease involves at least one distant site beyond local or regional ipsilateral process. This includes any of following: osteomyelitis, distant skin lesions, and pulmonary, gastric or urinary tract lesions. The disseminated disease is shown to have more than one lesion as described under the distant disease. Thirty two % of cases presented with distant or disseminated disease; 20 % of cases had both local and distant or disseminated disease. According to this classification, the cutaneous granuloma observed in the Case 2 and Case 3 may be classified into regional disease. In contrast, the granulomatous osteomyelitis of the Case 1 would be categorized into distant disease group.
A high prevalence of BCG complications, containing local to more critical disseminated diseases, has been known in immunocompromised children [2, 6, 9, 13]. The BCG-induced diseases, however, have also been reported in immunocompetent children. These include local or regional diseases and even distant osteomyelitis [7, 10-12] and disseminated military granulomas [1, 4, 5], indicating a presence of unknown or very subtle form of immunodeficiency [15]. In the present cases, at least, no major immunodeficiency diseases such as HIV infection and severe combined immunodeficiency disease, was detected.
     The pathological findings in the present cases revealed granulomatous lesions consisted of epithelioid cells and Langerhans giant cells with central caseous necrosis, which are essentially identical to those described in the case of M. tuberculosis and other mycobacterial infection. Since we could not find acid-fast bacilli in the histological sections, the PCR detection of M. bovis BCG-specific gene was quite useful for the final diagnosis of BCG-related diseases. By the appropriate design of primer set for PCR to target the RD1 region, we could show the specific 167bp PCR products using DNA extracted even from the FFPE tissue in 2 cases. Since the genomic RD1 region includes specifically deleted sequence in the M. bovis [3, 16], we could differentiate M. bovis from M. tuberculosis. The conventional bacterial culture takes long time before mycobacterial growth to extract the bacterial DNA and is unable to distinguish BCG and other mycobacterial strains. Thus, FFPE tissue-based PCR would be still very beneficial as a diagnostic tool for early detection of M.bovis BCG, even though the sensitivity of PCR detection from FFPE tissue would be lower than that from fresh tissue or cultured colonies. In the previously reported cases, the PCR recognition of M. bovis BCG strain was achieved using the DNA extracted from colony isolates [7, 10, 12]. In contrast, one autopsy case of disseminated disease has been reported that M. tuberculosis complex genome but not specific for BCG strain was detected from FFPE tissue section [5]. To our knowledge, however, demonstration of M. bovis BCG-specific genome from FFPE tissue has rarely been reported.
The diagnosis of BCG diseases must be considered even in healthy infants who manifest the histology of granulomas with caseous necrosis and history of BCG vaccination. In addition to microscopic examination, molecular identification of M. bovis BCG genome by PCR using DNA extracted from FFPE sections would be available for rapid and confirmative diagnosis, especially when the diagnosis of tuberculosis is not suspected and all the specimens are fixed with formalin for routine histological examination.

Conclusion
BCG infection should be considered even in healthy infants with a history of BCG vaccination and histology of epithelioid granuloma with caseation necrosis. In such cases, BCG gene identification by PCR would be useful even from formalin-fixed and paraffin embedded tissue samples.

Acknowledgements
     This work was supported in part by the Kodama Memorial fund Medical Research.




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Figure 2  Pathological presentation of Cases 2 and 3
A) Gross appearance of the resected lesion of left axillary subcutaneous mass of Case 2 B) Epithelioid granuloma with caseation necrosis and calcification is noted in the histological section of Case 2 (H&E stain). C) Gross feature of the left axillary skin of Case 3 D) Microscopic appearance of the resected lesion. Epithelioid granuloma with giant cells and caseation necrosis is observed in Case 3(H&E stain).

Figure 3  PCR detection of BCG-specific genome. A 167bp band is amplified from the fresh frozen tissue (Case 1) or FFPE tissue (Cases 2 and 3) in each case. M, molecular size marker; N, negative control; P, positive control of BCG Tokyo strain DNA








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