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MAJOR ARTICLE
Fish Tank Exposure and Cutaneous Infections
Due to Mycobacterium marinum: Tuberculin
Skin Testing, Treatment, and Prevention
Felicia M. T. Lewis, Bryan J. Marsh, and C. Fordham von Reyn
Infectious Disease Section, Department of Medicine, Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire
In the present study, 8 patients with soft tissue infection due to Mycobacterium marinum are described, and
contemporary data on treatment are reviewed. Six patients had positive cultures, all patients had cutaneous
exposure to fish tanks, 7 had sporotrichoid lesions, and 2 had deep infection. All 7 tested patients had tuberculin
skin test reactions ⭓10 mm. Six patients with disease limited to the skin were successfully treated with 2drug combination therapy, including clarithromycin, ethambutol, and rifampin. Optimal treatment should
include 2 drugs for 1–2 months after resolution of lesions, typically 3–4 months in total. Deeper infections
may require more prolonged treatment and surgical debridement. Positive tuberculin reactions may be due
to infection with M. marinum. Persons with open skin lesions or immunosuppression should avoid cutaneous
contact with fish tanks.
Mycobacterium marinum is a slow-growing environmental mycobacterium that was first isolated from dead
fish in a Philadelphia aquarium in 1926 [1] and was
identified as a human pathogen in 1951 after isolation
from granulomatous skin lesions in patients from Sweden. M. marinum is distributed widely in aquatic environments [2], especially in relatively still or stagnant
water, such as in fish tanks and swimming pools, and
in naturally occurring bodies of water [3, 4]. Infection
is acquired by direct inoculation with the bacterium
through broken skin in an aquatic environment. Adequate chlorination has drastically reduced the number
of cases acquired from swimming pools, and recent
reports emphasize acquisition from fish tanks but do
not offer recommendations for prevention [3, 5–10].
Although more potent antimicrobials are now available for the treatment of M. marinum infection, only
limited numbers of cases are available on which to analyze the effects of newer antimicrobials on the outcome
of treatment. Large series typically include reviews of
cases treated by numerous providers, rather than cases
treated by the authors. In addition, although recent
studies have emphasized the influence of asymptomatic
infection with environmental nontuberculous mycobacteria (NTM), such as Mycobacterium avium complex
(MAC), on the tuberculin skin test [11], detailed data
have not been presented on the effect of symptomatic
infections with NTM, such as M. marinum, on the
tuberculin skin test. We present our personal experience
with 8 cases of soft-tissue infection due to M. marinum
and emphasize the mode of acquisition and implications for prevention, the effect on tuberculin skin testing, and responses to combination antibiotic therapy,
including macrolides. We also review other recent studies on treatment to provide recommendations for current management of infections due to M. marinum.
Received 20 December 2002; accepted 14 April 2003; electronically published
18 July 2003.
Reprints or correspondence: Dr. C. F. von Reyn, Infectious Disease Section,
Dartmouth-Hitchcock Medical Center, Lebanon, NH 03756 ([email protected])
METHODS
Clinical Infectious Diseases 2003; 37:390–7
2003 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2003/3703-0011$15.00
Medical records at the Dartmouth-Hitchcock Medical
Center and records of skin test studies from the Infec-
390 • CID 2003:37 (1 August) • Lewis et al.
tious Disease Section were reviewed from May 1990 to 2000
to identify patients with a diagnosis of skin or soft tissue infection due to M. marinum. Data then were abstracted from
patient records and reports of laboratory tests. All case patients
were seen by one of the authors. Case patients were accepted
for inclusion if culture of a cutaneous lesion was positive for
M. marinum or if a patient without a culture performed had
a characteristic chronic cutaneous lesion with sporotrichoid
spread and a plausible aquatic exposure history. The literature
on treatment of M. marinum was reviewed by use of MEDLINE
for the period 1966–2002 using the following keywords: “M.
marinum,” “fish tank granuloma,” “swimming pool granuloma,” and “aquarium granuloma.”
Intradermal skin tests were approved by the Dartmouth
Committee for the Protection of Human Subjects and were
performed with 0.1 mL M. avium sensitin (MAS; 10/2; State
Serum Institute) and 0.1 mL (5 TU) Mycobacterium tuberculosis
PPD (Connaught Laboratories). Skin tests were performed at
the time that patients were seen by one of the authors. Tests
were administered intradermally by use of the Mantoux technique and were read by trained personnel 48–72 h after placement, as described elsewhere [11]. Cultures for M. marinum
were performed by use of both solid medium (Middlebrook
7H11; Lowenstein-Jensen) and broth medium (Middlebrook
7H9; MB/BacT) at both 30C and 35C when a sufficient sample
was available.
RESULTS
Clinical features. Clinical features of the 8 patients are summarized in table 1. Four cases occurred in men and 4 in women
(age range, 25–59 years; mean age, 45 years). All patients reported cutaneous contact with fish tanks at home or work
before the onset of infection. In 1 instructive case (patient 2),
a nurse working on a medical ward cleaned a fish tank on
several occasions while she had an open lesion on her finger
from a recent wart removal. Cultures were positive for M.
marinum for all 6 patients who had cultures performed. One
patient (patient 7) was diagnosed on the basis of a positive
acid-fast bacillus (AFB) stain and typical clinical features. One
patient (patient 8) was diagnosed on the basis of a typical
cutaneous lesion with sporotrichoid spread and fish tank exposure. Overall, AFB stains were positive in 3 patients, and
biopsy specimens showed granuloma formation in 6 patients.
Infections began on the finger or hand in all 8 patients, and,
in 6 patients, remained confined to the skin. Deep tissue infection developed in 2 patients. Patient 5 had sporotrichoid
spread (figure 1) and extensive deep infection, including osteomyelitis. Patient 7 developed tenosynovitis of the right index
finger. Six patients (75%) demonstrated sporotrichoid spread
with secondary nodules along proximal lymphatic channels.
Three patients had significant underlying medical conditions, including both patients with deep infection extending
to a site beyond the skin. Patient 5 who had extensive deep
disease had psoriasis and was receiving treatment with prednisone. Patient 6 who had cutaneous disease had rheumatoid
arthritis and was receiving treatment with plaquenil and nonsteroidal anti-inflammatory agents. Patient 7 who had tenosynovitis had type II diabetes mellitus. Chest radiograph findings were negative for all 4 patients who had x-rays performed
in this study (patients 1 and 5–7). Human immunodeficiency
virus (HIV) risk factors were not noted in any patient, and
HIV testing was not performed.
Skin test results. Seven patients had skin testing with PPD
and MAS antigens. Of these 7 patients, all 7 (100%) had PPD
reactions ⭓10 mm in diameter, and 2 (29%) had reactions ⭓15
mm in diameter. Three (50%) of 6 tested patients had MAS
reactions ⭓10 mm in diameter. Three patients had PPD and
MAS reactions differing by !5 mm (nondominant), 2 had larger
MAS reactions by ⭓5 mm in size, and 1 had a PPD reaction
that was greater by ⭓5 mm. None of the patients were foreign
born, and there was no known history of bacille CalmetteGuérin (BCG) immunization. Four patients had a history of a
previous negative tuberculin skin test result, and 1 patient had
a history of a previous positive tuberculin skin test result (patient 6).
Treatment results. Treatment regimens and outcomes are
summarized in table 1. All 6 patients with cutaneous disease
alone responded completely to antibiotic therapy with or without excisional biopsy. Four of these patients received therapy
with clarithromycin and ethambutol for 3–6 months. Two received therapy with rifampin and ethambutol, one for 2 months
and another for 14 months before resolution. Of the 2 patients
who had extension of disease, patient 7 responded to 2 months
treatment with of clarithromycin and ethambutol, and patient
5 with metastatic melanoma had not resolved after ∼2 years of
multiple excisions and a drug regimen that included clarithromycin, ethambutol, and rifabutin. For most patients, duration of therapy was typically 1–2 months after resolution of
lesions.
DISCUSSION
The present study demonstrates that cutaneous exposure to
fish tanks is the principal contemporary source of M. marinum
infections in our inland area of the United States and is consistent with other recently published reports [6, 12]. Fish and
shellfish injuries are responsible for a small proportion of cases
in other studies, but acquisition from swimming pools is now
unusual [6, 12, 13]. As demonstrated by patients 2 and 5 (who
had psoriasis), fish tank–related infections may be related to
immersion of an open cutaneous lesion. Despite the known
Fish Tanks, Tuberculin Tests, and M. marinum • CID 2003:37 (1 August) • 391
40/M
57/M
55/M
36/F
50/F
59/F
3
4
5
6
7
8
Fish tank None
Fish tank Diabetes mellitus
Fish tank Rheumatoid arthritis,
hydroxychloroquine therapy
Fish tank Psoriasis, melanoma,
prednisone
therapy
Fish tank None
Fish tank None
Fish tank None
Fish tank None
13
14
13
11
20
11
20
ND
ND
0
18
9
0
13
20
ND
ND
+/ND
Granuloma
Cutaneous, sporotrichoid ND
Tendonitis, sporotrichoid Granuloma
Cutaneous
Osteomyelitis,
sporotrichoid
⫺/+
+/+
Cutaneous, sporotrichoid Early histiocytic
infiltrate
⫺/+
Granuloma
Cutaneous, sporotrichoid Granuloma
⫺/+
Resolved
Outcome
Resolved
Clarithromycin and ethambutol Resolved
(6 months)
Clarithromycin and ethambutol Resolved
(2 months);
tenosynovectomy
Ethambutol and rifampin (14
months)
Ciprofloxacin, rifampin, etham- Resolving (lost to
butol, clarithromycin, rifabufollow-up)
tin, and amikacin; excision
of nodules
Clarithromycin and ethambutol Resolved
(6 months)
Clarithromycin and ethambutol Resolved
(3 months)
Clarithromycin and ethambutol Resolved
(4 months)
Cutaneous, sporotrichoid Granuloma
Treatment regimen (duration)
⫺/+
Pathologic findings
Cutaneous, sporotrichoid Mild acute inflammation Rifampin and ethambutol (2
months); excisional biopsy
Infection type
+/+
AFB
stain/
PPD MAS culture
AFB, acid-fast bacillus; MAS, Mycobacterium avium sensitin; ND, not done; +, positive; ⫺, negative.
38/F
2
NOTE.
25/M
1
Underlying
disease or
condition
Skin test
reaction
diameter,
mm
Characteristics of 8 patients with Mycobacterium marinum infection.
Age in
Type of
Patient years/sex exposure
Table 1.
Figure 1. Mycobacterium marinum nodules and inflammation of proximal interphalangeal joints (top) and wrist and forearm (bottom) in a patient
with underlying psoriasis (patient 5).
association of fish tanks with M. marinum infections our informal review of national aquarium supply stores indicates that
instructions for home fish tanks do not typically recommend
avoidance of water contact or the use of waterproof gloves for
persons with open skin lesions.
M. marinum should be suspected when a characteristic skin
lesion occurs 8–30 days (median, 21 days; ⭓30 days in 35%
of cases) after fish tank exposure [6]. Primary lesions typically
present as a bluish-red papule, nodule, or plaque with a ver-
rucous surface, most often at the site of a small abrasion or
cut on the dominant hand [14, 15]. As in the present study,
most patients have a sportotrichoid presentation on the upper
extremity [15]. Lesions may have purulent drainage, and satellite lesions may appear and coalesce. Lesions are painful in
fewer than one-half of cases [16], lymphadenopathy is rare and
typically mild [3, 17], and systemic symptoms are distinctly
unusual [18]. Infection is usually confined to the skin, because
of preferential growth of M. marinum at temperatures !37C
Fish Tanks, Tuberculin Tests, and M. marinum • CID 2003:37 (1 August) • 393
[19]. However, as demonstrated here, deeper extension of infection may lead to tenosynovitis, arthritis, bursitis, and osteomyelitis [20–24]. Disseminated infection is rare and almost
always occurs in immunosuppressed individuals [18, 25, 26].
Our experience demonstrates that infection with these organisms also is associated with sufficient tuberculin skin test
reactivity to trigger consideration of treatment for latent tuberculosis. This issue has not been emphasized in recent studies.
Jolly and Seabury [27] reported tuberculin reactions ⭓10 mm
in diameter in 14 (67%) M. marinum–infected patients tested
with PPD-S, and Mollohan and Romer [7] reported positive
reactions to the relatively nonspecific Vollmer patch test in 55
(77%) of 71 patients. In our study, all tested patients had tuberculin reactions ⭓10 mm in diameter (some would be candidates for treatment of latent tuberculosis if they were in defined risk groups), and 2 had reactions ⭓15 mm in diameter
(both would be candidates for treatment of latent tuberculosis)
[28]. Although one-half our patients did not have preinfection
skin tests to prove unequivocally that their reactions were due
to M. marinum, most healthy adults living in the United States
have negative reactions to tuberculin [11], and infection with
various NTMs often results in tuberculin reactivity [29]. Evaluation for tuberculosis always should be performed in those
with positive tuberculin skin test results, and treatment should
be provided on the basis of current guidelines [28]. However,
positive tuberculin reactions in patients with M. marinum infection can be attributed to this infection and should not always
be considered an indication for treatment of latent tuberculosis.
The cross -reactions that we observed to tuberculin in patients
with M. marinum infection were larger than tuberculin crossreactions that we have observed in patients with MAC disease.
This is consistent with genetic studies showing that M. marinum
is closely related to M. tuberculosis [30].
Reactions ⭓10 mm to the MAS skin test were observed in
3 (60%) of 5 patients. This is higher than the 30%–40% rate
of MAS reactions expected in a general US population [11],
but lower than the rate of positive PPD reactions in patients
with M. marinum infection. This is consistent with the greater
genetic difference between MAC and M. marinum. In the study
by Jolly and Seabury [27], which used a different M. avium
antigen, 14 (67%) of 21 patients had reactions ⭓10 mm in
diameter. In their study and the present study, most dual skin
test reactions with these 2 antigens were nondominant (i.e.,
neither the PPD nor the MAS antigen produced a consistently
larger reaction than the other). Distinction between infection
with M. tuberculosis and M. marinum with a single tuberculin
skin test, dual skin tests with tuberculin and an NTM antigen,
or newer in vitro assays of IFN-g production may not be possible [31].
There have been no controlled trials that compare treatment
regimens for M. marinum infection, only case reports and case
394 • CID 2003:37 (1 August) • Lewis et al.
series. Recent treatment reports that include 110 patients are
summarized in table 2. Combination therapy, typically with 2
drugs, as reported in several small series, appears to have a low
failure rate in superficial infection and is generally recommended [2, 6, 32–37]. A review of 44 cases concluded that
combination therapy with ethambutol and rifampin might be
highly effective, on the basis of successful outcomes for 8 of 9
patients treated with this regimen [38]. Combination therapy,
most commonly with clarithromycin plus rifampin, was used
for 40 of 63 patients from France who were treated for an
average of 3.5 months during 1996–1998 [12]. Surgical debridement or excision was required for 30 (48%) patients. Deep
infection was present in 18 (29%) patients and was found to
be the principal determinant of outcome. Infection resolved in
42 (93%) of 45 patients with localized infection versus 13 (72%)
of 18 with deep structure infection. Monotherapy failed more
often in deep than in cutaneous infections. Failure of clarithromycin-containing regimens was reported in only 2 (10%) of
20 patients with infection limited to the skin [12]. Success with
azithromycin in combination with ethambutol and minocycline
has been reported for the treatment of skin and soft tissue
infection in 1 lung transplant recipient [39].
We believe that clarithromycin is the optimal first agent in
combination treatment of M. marinum. Experience in the treatment of other NTMs suggests that azithromycin might be a
reasonable alternative. Published series and our experience support ethambutol as a reasonable second agent, whereas in vitro
studies and published clinical series suggest that rifampin also
would be appropriate. There is not enough clinical experience
from the treatment of infection with either M. marinum or
other NTMs with any of the other agents that have demonstrated activity in vitro to judge their potential efficacy as second
agents. Even if the organism is deemed susceptible to an antibiotic, we believe that monotherapy should be avoided because of the unreliability of susceptibility testing for this organism and the possibility of emerging resistance.
Published studies and our experience suggest that optimal
combination therapy would therefore be clarithromycin and
either rifampin or ethambutol. In a patient who cannot tolerate
clarithromycin, the combination of rifampin and ethambutol
may be considered, although our experience with patient 6
demonstrates that response to this regimen may sometimes be
delayed. The optimal duration of therapy is not known, and
results of published studies have been highly variable. The drugs
recommended for treatment do not have prominent doserelated or time-dependent side effects. Thus, a reasonable approach is to treat with 2 agents for 1–2 months after the resolution of all lesions (typically 3–4 months in total) [35, 36].
Susceptibility testing is not routinely recommended and should
be reserved for cases of treatment failure.
As evidenced by patient 5, treatment of deep or extensive
38 (NA)
31 (0)
12 (6)
[37]
[35]
[41]
Specific therapy,
no. of patients (% cured)
NA
6–7 Mean, 8 months
19 Mean, 4 months
22 Mean, 15 weeks
20
Doxycyline, 4–5 (100); TMP-SMZ, 2
(100); rifampin, 1 (100)
Minocycline, 14 (71); doxycycline, 3
(67); tetracycline, 1 (100); TMPSMZ, 1 (100)
TMP-SMZ, 19 (93); minocycline, 3
(100)
Minocycline 12 (NA); rifampin, 4 (NA)
23 Median, 3.5 months Minocycline, 19 (NA); clarithromycin,
4 (NA)
Duration
Specific therapy,
no. of patients (% cured)
Mean, 5 months
Mean, 15 weeks
NA
Rifampin + ethambutol, 3–4(100);
rifampin, ethambutol, and ciprofloxacin, 1 (100)
Ethambutol + rifampin, 5 (100);
other, 3 (100)
TMP-SMZ + minocycline, 5 (100)
Clarithromycin + ethambutol, 7 (NA)
Median, 3.5 months Clarithromycin + rifampin, 20 (NA);
cycline + clarithromycin, 11 (NA)
Duration
5–6 Mean, 8 months
8
12
7
40
n
Combination therapy
12 (100)
1 (NA)
1 (100)
NA
30 (NA)
Surgery
performed,
no. of patients
(% cured)
Surgical series: resolution in
all patients with long-term
antibiotic therapy and
debridement
Relapse in 2 patients after 4
months of minocycline;
recommend treatment for
2 months after resolution
for minimum of 6 months
Of patients with adequate
follow up, none worsened
after treatment; only 2
failed to improve
Resolution within 2–4
months of treatment in
most patients
Resolution in 55 (87%) of 66
overall but only 13 (72%)
of 18 with deep infection
Comments
Includes studies with minimum of 10 patients published since 1966, not including case series from literature surveys. NA, not available; TMP-SMZ, trimethoprim-sulfamethoxazole.
39 (NA)
[13]
NOTE.
66 (18)
[12]
n
Monotherapy
Published studies on treatment of Mycobacterium marinum soft tissue infection.
No.
of patients
(no. with deep
Reference
infection)
Table 2.
disease, especially in an immunocompromised patient, can be
challenging. Rifampin may be a preferred second or third agent
in bone or joint infection, where this drug has been shown to
improve outcome with infections due to other susceptible organisms [40]. It is possible that patients with disseminated
infection or extensive deep infection, and the potential for a
large burden of organisms, may benefit from treatment with 3
active agents, at least until clinical and microbiological response
has been documented. Treatment of deep infection, especially
in the immunocompromised host, typically requires surgical
debridement. Multicenter controlled trials are needed to define
the optimal regimen and duration of treatment for both superficial and deep infection.
In summary, fish-tank exposure is the source of most cases
of cutaneous M. marinum infections and may be preventable
through the use of waterproof gloves for persons with acute or
chronic open skin lesions. Tuberculin skin test reactivity is common after infection with M. marinum and should not generally
be attributed to tuberculosis. Treatment with a 2-drug regimen
that includes a macrolide should be successful in most patients
with disease limited to the skin.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
Acknowledgments
We wish to thank Kaare Haslov (State Serum Institute, Copenhagen), for donation of M. avium sensitin skin tests, and
Richard Waddell and Sue Tvaroha, for assistance with the study.
23.
24.
25.
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