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Viral Disease Transmitted by Laser-Generated Plume (Aerosol)
Jerome M. Garden, MD;
M. Kerry O'Banion, MD, PhD;
Abnoeal D. Bakus, PhD;
Carl Olson, DVM, PhD
Arch Dermatol. 2002;138:1303-1307.
ABSTRACT
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Objective To evaluate the possibility of disease transmission through liberated
plume from virally infected tissue that is exposed to the carbon dioxide laser.
Design Bovine papillomavirus–induced cutaneous fibropapillomas were exposed
to the carbon dioxide laser. Laser settings were within the range of clinically
used settings. The laser plume (aerosol) was suctioned and collected and then
reinoculated onto the skin of calves.
Setting University laboratory research center.
Main Outcome Measures Laser plume viral content and postinoculation tumor growth were analyzed
and documented.
Results Collected laser plume contained papillomavirus DNA in all tested laser
settings. The viral DNA was most likely encapsulated. Tumors developed at
laser plume–inoculated sites for all laser parameter settings. Histological
and biochemical analyses revealed that these tumors were infected with the
same virus type as present in the laser plume.
Conclusions Laser plume has been shown, for the first time to our knowledge, to
actually transmit disease. Strict care must be maintained by the laser practitioner
to minimize potential health risks, especially when treating viral-induced
lesions or patients with viral disease.
INTRODUCTION
THERE HAS been an increasing awareness of the potential health risk
of laser-generated plume (aerosol). Many laser systems, on impact with targeted
tissue, produce a plume of smoke containing debris and vapor, which is released
into the surrounding area. Concerns involving aerosolized carbonized material,
viable tumor cell dispersion, and infection transmission have been evaluated.
The carbon dioxide (CO2) laser is used by various medical
specialties to vaporize, ablate, or cut tissue. This instrument emits light
energy in the lower infrared range (10 600 nm), which is effectively absorbed
by water. Because of the relatively high water content of tissue, the laser
energy is readily converted to heat. Copious amounts of plume are generated,
which necessitates constant suction away from the procedural area through
a filter system.
Early studies that evaluated the laser plume for aerosolized infectious
material were prematurely reassuring. Besides occasional bacterial spores
recovered from experimentally inoculated tissue, there was no other discovered
aerosolized infectious material.1-4 In
1988, intact bovine papillomavirus (BPV) and human papillomavirus (HPV) DNA
specimens were recovered from the plume of CO2 laser–treated
human and bovine lesions.5 Several subsequent
investigations6-8 have
confirmed these results with the papillomavirus, while viable bacteriophages
have been found in the CO2 laser plume using an agar model.9 Although a simian immunodeficiency virus model failed
to recover any virus from the laser plume,10 positive
results were obtained with an in vitro study11 of
the human immunodeficiency virus. Also, clinical surveys of laser users have
revealed increased user infections with HPV; however, direct lesional contact
may be the source of infectivity.12-14
Intact papillomavirus DNA is a potential infectious agent.15-17 Although
in vitro methods have detected liberated infective virus in the collected
plume, in the papillomavirus6 and the human
immunodeficiency virus11 models using the CO2 laser, and in an in vitro study18 of
erbium (ER):YAG laser–generated aerosol, the induction of actual infection
by the laser plume, to our knowledge, has not been documented. Reproducing
the infection, with identification of the causative agent, would confirm the
potential of laser aerosol in transmitting disease.
To determine whether laser-generated plume from infected tissue can
reproduce disease, the bovine fibropapilloma, a BPV-induced lesion, was used.
Various CO2 laser settings were evaluated, and laser plume at each
laser setting was collected and inoculated into animals. Typical BPV lesions
containing BPV developed for all laser settings. These viral tumors confirm
the ability of the laser plume to produce infection.
MATERIALS AND METHODS
Bovine cutaneous fibropapillomas, produced from the inoculation of BPV-1,
were surgically excised from the cattle and promptly frozen and stored at
-65°C. All study of animal subjects received prior institutional
review board approval. Fibropapillomas positive for BPV by the peroxidase-antiperoxidase
technique19-21 were
exposed to various CO2 laser exposures in triplicate. All of the
fibropapillomas were at room temperature during the laser exposures. Laser
settings included the following: (1) 12 W and a 2-mm circular spot size delivered
in a continuous fashion (power density, 380 W/cm2; and spatially
averaged energy fluence, 400 J/cm2); (2) 4 W, a 2-mm spot size,
and continuous exposure (power density, 130 W/cm2; and spatially
averaged energy fluence, 130 J/cm2); and (3) 8 W, a 0.2-mm spot
size, and a pulse duration of 0.1 second (power density, 25 400 W/cm2; and spatially averaged energy fluence, 2540 J/cm2).
A bubble chamber containing phosphate-buffered saline solution (pH,
7.4) was placed within a vacuum suction line (500 mm Hg) used to collect the
laser-generated plume. The suction tip was placed approximately 2 cm from
the tumor. Extreme care was taken not to have the suction tip directly contact
the papilloma.22 The collected material was
initially evaluated for BPV content and later inoculated in duplicate on the
scarified skin of 3 calves. Control BPV inoculates were also placed on the
skin of these animals. Growth at inoculation sites was excised after 106 days
and analyzed histologically and biochemically for viral content and typing.
DNA extraction from the collected plume material in phosphate-buffered
saline and from each tumor was performed. Deoxyribonuclease sensitivity experiments
used pooled vapor material mixed with purified pGEM5 plasmid DNA (Promega
Corp, Madison, Wis). The sample was then divided into 3 equal volumes and
digested with 1.0 µg, 0.1 µg, or no deoxyribonuclease (Worthington
Biochemical Corp, Lakewood, NJ). Purified DNA samples were subjected to gel
electrophoresis, transferred to membranes23 (Duralon;
Stratagene, La Jolla, Calif), and UV cross-linked (Stratagene). A purified
BPV-2 virion DNA sample was used as a positive control. Bovine papillomaviruses
1 and 2 have homologous DNA, and both types are causative agents of bovine
fibropapillomas. Hybridizations were performed with a BPV-1–cloned DNA
probe labeled by the random primer method24 (Boehringer-Mannheim,
Mannheim, Germany), as previously described.20 Signals
were detected by autoradiography.
RESULTS
All of the laser plume samples for the 3 studied laser parameters contained
substantial amounts of BPV DNA, as revealed by hybridization of the DNA extracts
(Figure 1). Although form II (circular
DNA) was the most prominent in all samples, forms III (linear DNA) and I (supercoiled
DNA) were present. The positions of these DNA forms corresponded exactly to
those obtained with DNA from control BPV virions (Figure 1). This direct correlation is evidence that the plume-collected
viral DNA was intact.
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Figure 1. Collected laser plume samples
contain bovine papillomavirus (BPV) DNA. DNA specimens extracted from plume
samples were electrophoresed in parallel with BPV-2 virion DNA, subjected
to Southern blotting, and probed with phosphorus 32–labeled BPV-1 DNA.
Numbers 1 through 3 correspond to the 3 different sets of laser parameters
described in the "Materials and Methods" section; they are presented in triplicate
(a-c).
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No signal for the naked plasmid DNA was observed in the laser plume
samples treated with deoxyribonuclease, whereas a portion of the BPV DNA in
the sample survived enzyme treatment with concentrations of 0.1 and 1.0 µg
(Figure 2). Because the plasmid
DNA is present in the same mixture, it can be concluded that the enzyme activity
is not inhibited by components of the laser plume sample. Thus, the selective
protection of the collected BPV DNA suggests that part of the viral DNA in
the laser plume is still encapsulated.
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Figure 2. Viral DNA in collected laser plume
samples is resistant to deoxyribonuclease (DNase) I digestion. Laser plume
material containing purified pGEM5 plasmid DNA was digested with varying concentrations
of deoxyribonuclease (DNase) I, as described in the "Materials and Methods"
section. Southern blot hybridization was accomplished with a probe consisting
of bovine papillomavirus (BPV) and plasmid vector sequences.
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Of 3 calves, 2 developed marked lesions in sites of control BPV concentrate
inoculum (Figure 3). The third calf
had only minimal growth. A varying degree of papillomavirus infection susceptibility
occurs in this animal model.25
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Figure 3. Bovine fibropapillomas occurred
at the site of inoculation of control bovine papillomavirus tumor extract,
which was not treated with the laser (full size).
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Lesions developed at laser plume inoculation sites for all 3 laser parameters.
Of the 2 calves with a strong BPV control response, one developed lesions
with material collected using each of the 3 parameters (Figure 4) and the other developed lesions with material collected
from the laser plume, which corresponded to the highest power density and
energy fluence. The calf that had a minor response to the control BPV inoculum
did not develop other lesions.
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Figure 4. Bovine fibropapillomas occurred
at the sites of inoculation of collected laser plume. Numbers 1 through 3
correspond to the 3 different sets of laser parameters described in the "Materials
and Methods" section. The white ring is a freeze brand, used as a marker for
identification of inoculation sites.
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The results of a histological evaluation of the excised laser plume–induced
lesions were typical of BPV fibropapillomas. The epidermis revealed hyperkeratosis,
acanthosis, and papillomatous changes. Foci of large vacuolated cells appeared
in the upper epidermal layers. Sections stained positive for BPV capsid antigen
in all lesions.
DNA extracts from each of the 3 induced tumors also contained high levels
of BPV DNA (Figure 5), confirming
that the lesions arose by BPV infection. The more rapid migration of form
II DNA, relative to the control DNA in extracts from 2 of the tumors, is presumably
due to the presence of large amounts of cellular DNA in those samples. Additional
bands above form II DNA are likely to represent multimeric forms of BPV. Digestion
of a laser plume–induced tumor sample, and a laser plume sample with
the restriction enzyme BamHI, demonstrated only 1
band, thus distinguishing the BPV as type 1 (BPV-2 has 2 BamHI restriction sites).26-27 This
correspondence of viral types in the laser plume, and in induced tumors, provides
additional evidence for a causative role in lesion induction by the laser
plume.
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Figure 5. Laser plume–induced bovine
tumors and the laser plume contain bovine papillomavirus (BPV) type 1 DNA.
Laser plume–induced tumor extracts (1-3), and a tumor extract (T) and
laser plume sample (L) digested with BamHI, were analyzed by
Southern blot hybridization. Numbers 1 through 3 correspond to the 3 different
sets of laser parameters described in the "Materials and Methods" section.
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COMMENT
The CO2 laser is an effective instrument in many medical
specialties. Water within the tissue absorbs the laser energy, converting
it to heat that produces the desired effect and a thick plume of vapor and
debris that must be removed by suction. Analysis of the plume has revealed
various components besides the water vapor,28 which
can be irritating to the eyes and respiratory tract and are known animal or
human mutagens and carcinogens. Laser smoke condensates, from control animal
tissue in modified Ames tests, have produced mutagenicity.29
The size of the mainly homogeneous particulate matter present in the
plume debris can easily spread into the surrounding environment and reach
the entire respiratory system, producing, in study animals, pathologic changes.30-33 Cellular
elements are also recovered with the CO2 laser, most cells are
carbonized or distorted, and intact cells have not been viable after placement
into tissue culture.34-36 However,
with other laser systems, viable cells have been found.37
Since an earlier study5 of animal and
HPV lesions treated with the CO2 laser revealed intact viral DNA
in the generated plume, viral DNA has been detected in subsequent studies
from bovine fibropapillomas (BPV), plantar warts,6 and
genital verrucae (HPV).7-8 A bioassay
of the plume detected infectious BPV.6 In a
tissue culture study11 using the CO2 laser,
proviral human immunodeficiency virus DNA was recovered from the suction tubing
used to remove the plume. However, no sustained infection occurred in cultured
cells inoculated by the laser plume–contaminated tubing.
In the present study, BPV viral DNA was again readily detected in the
laser aerosol. In addition, a portion of this DNA was not sensitive to deoxyribonuclease
treatment, suggesting that whole virion particles were present in the laser
plume. Most important, when the collected plume produced from a wide range
of various laser parameters was used as an inoculum, lesions were induced.
Based on histopathological and viral typing criteria, the laser plume–induced
lesions were identical to the original tumors.
This study addresses the use of the CO2 laser, either in
a continuous mode or pulsed at 100 milliseconds. Lasers used for tissue resurfacing,
such as the CO2 or the Er:YAG laser, are pulsed for short exposures,
from 10 to generally less than 1 millisecond. These rapid pulses produce a
more explosive response with greater tissue ablation.
A study38 analyzing CO2 laser
plume captured during resurfacing cases revealed viable bacteria. The filter
size used in the study was too porous to capture viruses, and there was no
indication of viral infection in these patients. An Er:YAG laser used in resurfacing
verrucae vulgaris did not find any HPV DNA in material collected on the laser
handpiece.39 This material may have represented
desiccated debris, and perhaps material directly collected in the plume would
have revealed HPV DNA. Ziegler et al,18 using
the Er:YAG laser, did demonstrate, through in vitro methods, viable cells,
viral genes, and infectious viruses. Therefore, it seems that short-pulsed
resurfacing lasers also have the potential of liberating infectious material.
Another type of laser that has a short pulse duration, and is used in
ophthalmology for tissue ablation (photorefractive keratectomy), is the excimer
laser. At 193 nm, and nanosecond pulse durations, it was able to experimentally
disrupt the fairly large (180-200 nm) attenuated varicella-zoster virus, with
only fragments present in the laser plume.40 However,
as the researchers themselves comment, it is unknown whether smaller viruses
(ie, papillomavirus, hepatitis, and retrovirus) would be undamaged and liberated
into the plume. More important, the UV wavelength of the excimer laser immediately
disrupts surface cells, allowing for little tissue penetration. The Er:YAG
laser at 2940 nm and the CO2 laser at 10 600 nm have greater
tissue penetration, producing a deeper ablative effect, potentially expelling
much more intact material.
These studies and the findings in the present study increase the concern
surrounding the use of aerosol-producing lasers in the treatment of virally
induced lesions and virally infected (or potentially infected) patients. With
HPV and the human immunodeficiency virus already detected in laser plume,
it is possible that other viruses, such as hepatitis, may also be liberated
in the plume during laser use. Fortunately, most HPV lesions, particularly
those of genital origin, contain fewer particles than those studied in the
bovine fibropapilloma model,41 and the direct
inoculation of the laser plume in our study onto the animals may not equal
routine clinical exposure. However, there is already a report42 of
a surgeon, who treats anogenital condylomas with the Nd:YAG laser, developing
laryngeal papillomatosis containing HPV DNA types 6 and 11.
It is even more relevant, with the proved potential for disease transmission,
that safety precautions during laser surgery be strictly maintained. These
include limiting the use of aerosol-producing lasers to patients for whom
there is a strong therapeutic advantage over other modalities, protection
of skin surfaces with gloves and gowns, eye protection, and the use of masks
and smoke suction systems that have high flow volume and good filtration.43
AUTHOR INFORMATION
Accepted for publication February 26, 2002.
This study was supported by a grant from the J. P. Wilmot Foundation;
a grant from the Stackhouse Inc, Palm Springs, Calif; and the Dr Guy G. Graham
Fund.
We thank John P. Sundberg, DVM, PhD, for immunoperoxidase BPV identification;
Robert O. Olson, PhD, for production and use of the BPV papillomas; and Yasmeen
S. Salem, MD, for technical assistance.
Corresponding author: Jerome M. Garden, MD, Department of Dermatology,
150 E Huron, Suite 910, Chicago, IL 60611 (e-mail: j_garden{at}northwestern.edu).
From the Departments of Dermatology (Drs Garden and Bakus) and Biomedical
Engineering (Dr Garden), Northwestern University, the Divisions of Dermatology
and Plastic Surgery, The Children's Memorial Hospital, (Dr Garden) Chicago,
Ill; the Department of Medicine, University of Rochester, Rochester, NY (Dr
O'Banion); and the Department of Veterinary Science, University of Wisconsin,
Madison (Dr Olson).
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