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BMC Infectious Diseases

, 19:598 | Cite as

A lung abscess caused by secondary syphilis – the utility of polymerase chain reaction techniques in transbronchial biopsy: a case report

  • Shinji Futami
  • Takayuki TakimotoEmail author
  • Futoshi Nakagami
  • Shingo Satoh
  • Masanari Hamaguchi
  • Muneyoshi Kuroyama
  • Kotaro Miyake
  • Shohei Koyama
  • Kota Iwahori
  • Haruhiko Hirata
  • Izumi Nagatomo
  • Yoshito Takeda
  • Hiroshi Kida
  • Atsushi Kumanogoh
Open Access
Case report
  • 230 Downloads
Part of the following topical collections:
  1. Sexually transmitted diseases

Abstract

Background

In Japan and other countries, the number of patients with syphilis is increasing year by year. Recently, the cases of the pulmonary involvement in patients with secondary syphilis have been reported. However, it is still undetermined how to obtain a desirable specimen for a diagnosis of the pulmonary involvement, and how to treat it if not cured.

Case presentation

A 34-year-old man presented with cough and swelling of the right inguinal nodes. A physical examination revealed erythematous papular rash over the palms, soles and abdomen. A 4 cm mass in the right lower lobe of the lung was detected on computed tomography. He was diagnosed as having secondary syphilis, because he was tested positive for the rapid plasma reagin and Treponema pallidum hemagglutination assay. Amoxycillin and probenecid were orally administered for 2 weeks. Subsequently, rash and serological markers were improved, however, the lung mass remained unchanged in size. Transbronchial biopsy (TBB) confirmed the pulmonary involvement of syphilis using polymerase chain reaction techniques (tpp47- and polA-PCR). Furthermore, following surgical resection revealed the lung mass to be an abscess.

Conclusions

To our knowledge, this is the first surgically treated case of a lung abscess caused by syphilis, which was diagnosed by PCR techniques in TBB. This report could propose a useful diagnostic method for the pulmonary involvement of syphilis.

Keywords

Secondary syphilis Lung abscess Polymerase chain reaction Transbronchial biopsy Surgical treatment Case report 

Abbreviations

BAL

Bronchoalveolar lavage

CTNA

Computed tomography-guided percutaneous needle aspiration

PCR

Polymerase chain reaction

RPR

Rapid plasma reagin test

TBB

Transbronchial biopsy

TPHA

Treponema pallidum hemagglutination test

Background

Syphilis is a sexually transmitted disease caused by infection with Treponema pallidum, which is classified into four stages (primary, secondary, latent and tertiary). If the patients with primary syphilis do not receive treatment, the bacterium will spread through their bloodstream, and set the stage for secondary syphilis. Syphilis can cause a wide range of systemic manifestations, such as papular rash, malaise, weight loss, muscle aches, generalized lymphadenopathy and meningitis [1]. In Japan and other countries, the number of patients with syphilis is increasing year by year [2, 3, 4]. Recently, several dozen reports showed the pulmonary involvement in patients with secondary syphilis [5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16]; however, it is still undetermined how to obtain a desirable specimen for a diagnosis of the pulmonary involvement, and how to treat it if not cured.

Here, we report a rare case of a lung abscess caused by secondary syphilis, that was definitely diagnosed by polymerase chain reaction (PCR) tests from the transbronchial biopsy (TBB) specimen and followed by surgery.

Case presentation

A 34-year-old Japanese heterosexual man presented to our hospital with a 4 cm heterogeneous mass in the right lower lobe (Fig. 2). He had had a symptom of productive coughing, sore throat and nasal discharge for 5 days, but he had no fever and no dyspnea, and his general condition was good. He had a medical history of minimal lesion nephrotic syndrome and had received corticosteroid therapy until 4 months prior to his first visit to our institution. He was a current smoker (15 pack-years). He had had sexual intercourse with a woman other than his wife 4 months prior to his first visit. Physical examination revealed right inguinal nontender enlarged lymph nodes, and erythematous papular rash over the palms, soles and abdomen (Fig. 1). However, cervical and supraclavicular lymph nodes were not palpable, and he did not have abnormal neurologic findings.
Fig. 1

Erythematous popular rash. a: Erythematous popular rash over the solesm, b: Erythematous popular rash over the abdomen

C-reactive protein level was elevated at 1.02 mg/dL as shown in the laboratory tests (Table 1). The rapid plasma reagin (RPR) and Treponema pallidum hemagglutination test (TPHA) revealed titers 1:64 and 1:5,120, respectively, although Human immunodeficiency virus testing was negative. Chest X-ray (Fig. 2a) and computed tomography (Fig. 2b) revealed a single mass lesion (4 cm in size) in the right lower lobe, and enlarged lymph nodes (4.5 cm in size) in the right inguinal region.
Table 1

Laboratory findings on the first visit to our institution

< Blood cell count >

 White blood cell

7,150 /μL

 Red blood cell

520 × 104 /μL

 Hemoglobin

14.8 g/dL

 Platelet

27.8 × 104 /μL

< Serum chemistry>

 Total protein

8.1 g/dL

 Albumin

4.6 g/dL

 Total-bilirubin

0.5 mg/dL

 Alkaline phosphatase

252 IU/L

 Aspartate transaminase

15 IU/L

 Alanine transaminase

23 IU/L

 γ-Glutamyl transpeptidase

30 IU/L

 Lactate dehydrogenase

158 IU/L

 Blood urea nitrogen

11 mg/dL

 Creatinine

0.84 mg/dL

 C-reactive protein

1.02 mg/dL

 Sodium

141 mmol/L

 Potassium

4.4 mmol/L

 Chlorine

103 mmol/L

< Coagulation>

 Prothrombin time (International normalized ratio)

1.09

 Activated partial thromboplastin time

50 s

< Infection >

 Rapid plasma reagin test

Positive (titers 1:64)

Treponema pallidum hemagglutination test

Positive (titers 1:5,120)

 Hepatitis B surface antigen

Negative

 Hepatitis C antibody

Negative

 Human immunodeficiency virus antibody

Negative

 Aspergillus antigen

Negative

 Cryptococcus antigen

Negative

< Tumor marker >

 Carcinoembryonic antigen

<  1 ng/mL

 Soluble cytokeratin fragment

0.5 ng/mL

 Pro-gastrin releasing peptide

27.0 pg/mL

<Autoantibody>

 Proteinase3-antineutrophil cytoplasmic antibody

<  1 U/mL

 Myeroperoxidase-antineutrophil cytoplasmic antibody

<  1 U/mL

Fig. 2

Images of the lung mass. a Chest X-ray on the first visit to our hospital. A mass lesion was shown in the right lower field (arrow), b Chest computed tomography on the first visit to our hospital. A single mass lesion (4 cm in size) was shown in the right lower lobe of the lung (arrow), c Fluorodeoxyglucose-positron emission tomography (FDG-PET) before the surgery, 4 months after the first visit. A single mass lesion was still remained in spite of the antibiotic treatment. It had abnormal uptake with a maximal standardized uptake value (SUV max) of 2.51 (arrow)

Diagnosed as secondary syphilis, amoxycillin 1500 mg per day and probenecid 1000 mg per day were orally administered for 2 weeks. Subsequently, rash, inguinal lymph nodes and serological markers were improved (Fig. 3), however, the lung mass remained unchanged in size (Fig. 2c). TBB confirmed the pulmonary involvement of syphilis by PCR techniques (tpp47-, and polA-PCR) (Fig. 4), whereas malignancy and other possible infections such as bacteria and fungi were negative (Table 2). Five months after the first visit, right basal segmentectomy was performed to exclude other comorbid diseases, especially malignancy. The remained lung mass was an abscess and histological analysis showed the granuloma formation by epithelioid histiocytes and Langhans giant cells with necrosis (Fig. 5). The comprehensive PCR tests for multi-microbes were performed in the resected lung specimens, and no microbes were significantly positive (Table 2). Subsequently, penicillin G 2.4 million units per day was intravenously administered for 2 weeks, and the pulmonary involvement has resolved without relapse after 8 months follow-up.
Fig. 3

Clinical course of the treatment. The induction of the oral antibiotics caused fever, headache and exacerbation of erythematous papular rash on the next day, which was considered as Jarisch-Herxheimer reaction. Treatment for 2 weeks improved the rash and serological data. However, the lung mass had not changed in size. Surgical resection was followed, and then, additional intravenous antibiotics for 2 weeks was administered. Abbreviation; rapid plasma reagin test: RPR; Treponema pallidum hemagglutination test: TPHA

Fig. 4

Electrophoresis of the amplified products from the lung mass with polymerase chain reaction (PCR) techniques. BAL was performed with 20 mL saline. The two types of gene fragments of Treponema pallidum (tpp47 and polA) acquired from bronchoalveolar lavage (BAL) and transbronchial biopsy (TBB) was amplified by PCR techniques. Both gene fragments were positive in samples from TBB, but not BAL

Table 2

Microbiological analysis in specimens obtained by bronchofiberscopy and surgery

1. Bronchofiberscopy

PCR tests for Treponema pallidum

 Bronchoalveolar lavage

Undetected

 TBB

Detected (tpp47-PCR and polA-PCR)

 Culture tests for bacteria and mycobacteria

 Bronchoalveolar lavage

Undetected

 Lavage of forceps in TBB

Undetected

2. Surgery

 Real-time PCR tests for Treponema pallidum

Undetected

 Culture test for bacteria in pus inside the abscess

Undetected

 Real-time PCR tests for multi-microbes [17]

Number

Bacteria name

Quantity

1

Staphylococcus aureus

Undetected

2

Bacillus anthracis

Undetected

3

Listeria monocytogenes

Undetected

4

Streptococcus pyogenes

Undetected

5

Streptococcus agalactiae

Undetected

6

Streptococcus mutans

Undetected

7

Streptococcus sobrinus

Undetected

8

Streptococcus sanguinis

Undetected

9

Streptococcus oralis

Undetected

10

Streptococcus salivaris

Undetected

11

Streptococcus pneumoniae

Undetected

12

Enterococcus faecalis

Undetected

13

Enterococcus faecium

Undetected

14

Clostridium tetani

Undetected

15

Clostridium difficile

Undetected

16

Peptostreptococcus anaerobius

Undetected

17

Actinomyces

Undetected

18

Corynebacterium diphtheriae

Undetected

19

Mycobacterium tuberculosis

Undetected

20

Mycobacterium laprae

Undetected

21

Mycobacterium chelonae

Undetected

22

Mycobacterium kansasii

Undetected

23

Mycobacterium avium complex

Undetected

24

Nocardia asteroids

Undetected

25

Bacteroides fragills

Undetected

26

Elizabethkingia meningosepticum

Undetected

27

Campylobacter jejuni

Undetected

28

Helicobacter cinaedi

Undetected

29

Helicobacter pylori

Undetected

30

Rickettsia prowazekii

Undetected

31

Rickettsia japonica

Undetected

32

Orientia tsutsugamushi

Undetected

33

Bartonella henselae

Undetected

34

Brucella

Undetected

35

Bordetella pertussis

Undetected

36

Burkhoderia mallei

Undetected

37

Burkhoderia cepacian

Undetected

38

Neisseria gonorrhoeae

Undetected

39

Neisseria meningitidis

Undetected

40

Francisella tularensis

Undetected

41

Legionella pneumophilia

Undetected

42

Moraxella catarrhalis

Undetected

43

Pseudomonas aeruginosa

Undetected

44

Acinetobacter baumannii

Undetected

45

Aeromonas hydrophia

Undetected

46

Vibrio cholerae

Undetected

47

Vibrio parahaemolyticus

Undetected

48

Vibrio vulnificus

Undetected

49

Haemophilus influenzae

Undetected

50

Escherichia coli

Undetected

51

Salmonella enterica

Undetected

52

Shigella

Undetected

53

Klebsiella pneumonia

Undetected

54

Yersinia psttis

Undetected

55

Yersinia enterocolitica

Undetected

56

Citrobacter freundii

Undetected

57

Proteus mirabilis

Undetected

58

Morganella morganii

Undetected

59

Providencia

Undetected

60

Mycoplasma pneumoniae

Undetected

61

Fusobacterium nucleatum

Undetected

62

Leptospira interrogans

Undetected

63

Chlamydia psittaci

Undetected

64

Chlamydia trachomatis

Undetected

65

Chlamydia pneumoniae

Undetected

66

Aspergillus fumigatus

Undetected

67

Aspergillus nigar

Undetected

68

Aspergillus flavus

Undetected

69

Cryptococcus

Undetected

70

Histoplasma

Undetected

71

Trichosporon

Undetected

72

Mucor

Undetected

73

Coccidioides

Undetected

74

Propionibacterium acnes

Detected (not significant)

75

Stenotrophomonas maltophilia

Detected (not significant)

76

Candida albicans

Detected (not significant)

Abbreviations: TBB Transbronchial biopsy, PCR Polymerase chain reaction

Fig. 5

Gross and microscopic pathology of lung specimens obtained by surgery a Gross pathology showed pus inside the lung abscess (arrow), b Microscopic pathology showed granuloma formation by epithelioid histiocytes and Langhans giant cells (arrow), in addition to necrosis (arrow-head). Original Magnification X100. Hematoxylin and eosin (HE) staining

Discussion and conclusions

This is a rare case of a lung abscess caused by secondary syphilis, that was diagnosed by PCR techniques in TBB. The abscess was not improved by antibiotics and required surgery.

Coleman showed the criteria for the clinical diagnosis of secondary syphilis with pulmonary involvement in 1983 [5], and several dozen cases have been reported [6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16]. In some of them, PCR was used for the diagnosis of pulmonary involvement (Table 3) [13, 14, 15, 16]. PCR is useful for the diagnosis of the infection of Treponema pallidum [18, 19], because it is difficult to directly visualize Treponema pallidum. In those reports, PCR was used in samples from TBB, bronchoalveolar lavage (BAL), bronchial aspirate, or computed tomography-guided percutaneous needle aspiration (CTNA) [13, 14, 15, 16]. Thus far, only one case has been reported on lung abscess caused by secondary syphilis, that was diagnosed by PCR in CTNA [15]. In our case, the results of PCR in samples from TBB, but not BAL, was positive. For the detection of some infectious diseases, TBB or the combination of BAL and TBB was reported to be useful [20, 21]. Thus, it could be important to perform TBB to detect the pulmonary involvement by Treponema pallidum.
Table 3

Reported cases of secondary syphilis with pulmonary involvement which was diagnosed by PCR techniques

Case no.

Age

Gender

Respiratory symptoms

Extrapulmonary symptoms

Chest imaging

Sample collection method

Reporting year

Reference

1

34

Male

Chest pain

Progressive weakening, anorexia, weight loss, and night sweats

Several bilateral, round, excavated opacities and subtracheal adenopathy

BAL

2006

[13]

2

49

Female

Dry cough

Disabling cervical pain, fever, and night sweats

Lung lobe parenchymal lesion

BAL and bronchial aspirate

2015

[14]

3

30

Male

Hemoptysis, chest pain, dyspnea

Fever and rash

a 3 cm, irregularly-shaped, well-defined consolidation and a 1 cm hilar node

CTNA

2018

[15]

4

62

Male

No respiratory symptoms

epigastric pain

Multiple nodular bibasilar subpleural nodules

TBB

2018

[16]

Abbreviation: PCR Polymerase chain reaction, BAL Bronchoalveolar lavage, CTNA Computed tomography-guided percutaneous needle aspiration, TBB Transbronchial biopsy

The lung abscess was not improved by 2 weeks of oral antibiotics. It may be because penetration of antibiotics into the abscess was impaired. We treated the present case with amoxicillin and probenecid, because there is no insurance coverage for intramuscular penicillin for syphilis in Japan. Administration of intravenous penicillin G was considered as a more potent antibiotic treatment. However, as in this case, it is necessary to consider surgical resection as the treatment for uncontrolled infection and in order to exclude other diseases, including malignancy, when the lung involvement is poorly improved by antibiotics.

Lung lesions associated with syphilis are still rare, but the reported cases have been increasing as the number of patients with syphilis increases [5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16]. Thus, we should consider chest X-ray in the cases of the patients with syphilis who have pulmonary symptoms.

In conclusion, to our knowledge, this is the first surgically treated case of a lung abscess caused by syphilis, which was diagnosed by PCR techniques in TBB. This report could propose a useful diagnostic method for the pulmonary involvement of syphilis.

Notes

Acknowledgments

The authors thank Shu-Ichi Nakayama, Makoto Ohnishi (Department of Bacteriology I), and Harutaka Katano (Department of Pathology, National Institute of Infectious Diseases, Tokyo, Japan), for their assistance with the PCR techniques. The authors obtained patient permission to publish this information.

Authors’ contributions

SF and TT drafted the manuscript. SF, TT and FN were responsible for the clinical care of the patient. SS, MH, MK and KM contributed to the acquisition of the TBB specimen. SK, KI, HH and IN analyzed and interpreted the patient’s data, including the microbiology data. YT, HK and AK critically revised the manuscript. All authors read and approved the final manuscript.

Funding

Not applicable.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Written informed consent was obtained from the patient for publication of this case report.

Competing interests

The authors declare that they have no competing interests.

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© The Author(s). 2019

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  • Shinji Futami
    • 1
  • Takayuki Takimoto
    • 1
    • 3
    Email author
  • Futoshi Nakagami
    • 2
  • Shingo Satoh
    • 1
  • Masanari Hamaguchi
    • 1
  • Muneyoshi Kuroyama
    • 1
  • Kotaro Miyake
    • 1
  • Shohei Koyama
    • 1
  • Kota Iwahori
    • 1
  • Haruhiko Hirata
    • 1
  • Izumi Nagatomo
    • 1
  • Yoshito Takeda
    • 1
  • Hiroshi Kida
    • 1
  • Atsushi Kumanogoh
    • 1
  1. 1.Department of Respiratory Medicine and Clinical ImmunologyOsaka University Graduate School of MedicineOsakaJapan
  2. 2.Department of General Internal MedicineOsaka University HospitalOsakaJapan
  3. 3.Department of Internal Medicine, National Hospital OrganizationKinki-Chuo Chest Medical CenterOsakaJapan

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