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Hyperbaric oxygen therapy (HBOT) is the use of 100% oxygen at pressures greater than atmospheric pressure. Today several approved applications and indications exist for HBOT. HBOT has been successfully used as adjunctive therapy for wound healing. Non-healing wounds such as diabetic and vascular insufficiency ulcers have been one major area of study for hyperbaric physicians where use of HBOT as an adjunct has been approved for use by way of various studies and trials. HBOT is also indicated for infected wounds like clostridial myonecrosis, necrotising soft tissue infections, Fournier's gangrene, as also for traumatic wounds, crush injury, compartment syndrome, compromised skin grafts and flaps and thermal burns. Another major area of application of HBOT is radiation-induced wounds, specifically osteoradionecrosis of mandible, radiation cystitis and radiation proctitis. With the increase in availability of chambers across the country, and with increasing number of studies proving the benefits of adjunctive use for various kinds of wounds and other indications, HBOT should be considered in these situations as an essential part of the overall management strategy for the treating surgeon.
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Hyperbaric oxygen and wound healing
William A. Zamboni, MD, FACS
a,
*
, Leslie K. Browder, MD
b
,
John Martinez, MD
b
a
Division of Plastic Surgery, University of Nevada School of Medicine, 2040 W. Charleston Blvd., Suite 301,
Las Vegas, NV 89102, USA
b
Department of Surgery, University of Nevada School of Medicine, 2040 W. Charleston Blvd., Suite 301,
Las Vegas, NV 89102, USA
Nonhealing wounds are a major health problem
worldwide. Managing difficult wounds often involves
prolonged hospitalizations, numerous surgical inter-
ventions, and medical wound management, all of
which frequently lead to exuberant costs, morbidity,
and even mortality. A thorough understanding of basic
wound healing, diagnosis, and principles of hyper-
baric oxygen ( HBO) as an adjuvant therapy can
facilitate healing a problem wound.
Wound healing
Phases of wound healing
A wound heals by primary or secondary intention.
A laceration or incision, which is reapproximated, is
an example of wound healing by primary intention.
Most chronic wounds heal by secondary intention via
formation of granulation tissue, contraction, and
central migration of the peripheral epithelium.
The three phases of wound healing are inflam-
mation, repair, and maturation, all of which super-
impose to effectively repair a wound. The inflammation
phase involves vascular and cellular responses. Arte-
rioles constrict, and then dilate. Fibrin congregates,
platelets aggregate, and the coagulation cascade is
initiated. Neutrophils and macrophages invade the
wound, removing tissue debris and bacteria. Macro-
phages attract the fibroblast to the injured site,
stimulating fibroblast proliferation and angiogenesis.
Resolution of the inflammation phase initiates the
repair phase, in which collagen synthesis from fibro-
blast proliferation occurs. During maturation, colla-
genase is present, promoting breakdown and repair of
existing collagen cross-links, and thus contributing to
the wound strength.
Impaired wound healing
Problem wounds are those that fail to heal in
response to standard medical and surgical therapy.
These wounds are frequently found in patients who
have multiple local and systemic factors inhibiting
tissue healing. Advanced ag e, nutritional deficits,
vascular insu fficiency, diabetes, infection, tobacco
use, hypoxia, and immunosupp ressi on are among
some of the important risk factors that interfere with
wound healing. Among these, hypoxia and infection
adversely affect wound healing most frequently. The
consequence of many of these risk factors results in
low oxygen tensions, which adversely effect neutro-
phil, macrophage, and fibroblast functions.
The role of oxygen
The neutrophil, macrophage, and fibroblast
require oxygen to function during inflammation and
repair phases. Both, oxygen-dependent and oxygen-
independent systems are required in order for neu-
trophils and macrophages to kill microorganisms.
0094-1298/03/$ see front matter D 2003, Elsevier Science (USA). All rights reserved.
PII: S 0094-1298(02)00068-8
* Corresponding author.
E-mail address: wzamgboni@med.unr.edu
(W.A. Zamboni).
Clin Plastic Surg 30 (2003) 67 75
Oxygen radicals derived from molecular oxygen are
important in bacterial killing. Leukocytes contain an
enzyme—NADPH-linked oxygenase—that is acti-
vated, resulting in oxidants. After activation, an
oxidative burst allows molecular oxygen to be
reduced to superoxide radicals, thus killing bacteria
by oxidizing cell membranes. The superoxide radi-
cals are reduced to oxygen and peroxide by super-
oxide dismutase. Myeloperoxidase combines with
peroxide and chloride or iodide to form hypochlorite
or hypoiodite. Intracellulary, excess peroxide is
reduced to oxygen by a catalase. If iron is present,
the reaction occurs extracellulary, producing OH
,a
harmful oxygen radical. This oxygen radical kills
bacteria effectively, but also harms surrounding cells.
If cells are hypoxic, the oxygen-dependent pathway is
severely incapacitated, leading to increasing rates of
infection [1].
Collagen synthesis from fibroblasts also requires
oxygen. Fibroblasts follow the macrophages into the
wound environment. Nonhelical procollagen is cre-
ated by protein synthesis involving proline, lysine,
and glycine. Oxygen is an important cofactor re-
quired during hydroxylation of proline and lysine
during formation of procollagen. Next, propeptides
are cleaved off of procollagen to form tropocollagen
via lysyl oxidase. Glycosaminoglyc ans provide a
matrix for cross-linking and aggregation of collagen
molecules to form collagen mature fibers. Mature
collagen synthesis requires prolyl-hydroxylase and
lysyl-hydroxylase, which are enzymes dependent on
oxygen for function. Energy metabolism of the cell
is first priority, occurring through oxidative phos-
phorylation, which then allows enzymes to use
molecular oxygen. If the tissue is hypoxic, procolla-
gen hydroxylation suffers and mature collagen can-
not be formed [2].
The problem wound environment is hypoxic,
acidotic, and contains high levels of lactate. This
environment forms a concentration gradient, largely
responsible for the inward movement of wound
healing cells [3]. Hypoxia is the result of the initial
vascular damage, coagulation, and vasoconstriction.
Furthermore, leukocytes increase oxygen consump-
tion, causing a lower oxygen tension in the wound
[2]. Acidosis results from an increase in oxygen
Fig. 1. Monoplace hyperbaric oxygen chamber. (Courtesy of Sunrise Hospital and Medical Center, Las Vegas, NV.)
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–7568
demand in the face of a decreased oxygen supply. In
wounds, lactate accumulates due to hypoxia. Lactate
accumulation is also caused by leukocytes, fibro-
blasts, and endothelial cells. These cells have few
mitochondria and therefore rely on glycolysis, even
in the presence of oxygen, resulting in high levels of
lactate. Furthermore, lactate stimu lates collagen
secretion and angiogenesis.
Angiogenesis occurs rapidly in wounds across a
gradient of low lactate and high oxygen tension to
areas of high lactate and low oxygen levels [3].
Although profound hypoxia inhibits all wound-
healing processes, moderate low oxygen tensions
initiates angiogenic growth factor production in
vitro and upregulates vascular endothelial growth
factor [2]. Recent data supports lactate as the agent
responsible for initiating these growth factors [3],
but the intricate details of this pathway remain to
be elucidated.
Wound diagnosis
To determine the etiology of a nonhealing wound,
an accurate diagnosis must be made. As with any
medical problem, the evaluation begins with an
adequate history and physical examination. Informa-
tion regarding t he duration, wound environment
(dressings, t opical treatments), surgery (debride-
ments, grafts), and presence of comorbidities (dia-
betes, vascular disease, malnutrition, and so forth) are
important components. Examination of the wound
will provide information such as wound size, loca-
tion, depth, and infection. Peripheral vascular disease
can be diagnosed by the presence of skin changes and
diminished pulses. Venous stasis can also be deter-
mined. Examination of the granulation tissue will
also provide clues as to the etiology of the wound.
If the granulation tissue is beefy red in appearance,
the wound environment is healthy. If the granulation
tissue is pale, friable, or nonexistent, the wound is
likely hypoxic.
The foundation of treating a problem wound is the
identification and correction of the underlying etio-
logic and risk factors that may hinder the healing
process. An angiogram should be obtained, if indi-
cated, to determine the presence of vascular abnormal-
ities amenable to surgical intervention. Furthermore,
noninvasive evaluation, consisting of evaluation of
tissue oxygenation and perfusion of the wound, is
essential. Arteriole Doppler studies, consisting of both
segmental and toe pressures, should be obtained to
evaluate perfusion. Transcutaneous oximetry (TcPO
2
)
is used to assess oxygenation of the wound. If both of
these values are normal, a wound should heal sponta-
neously. If they are abnormal, adjunctive therapy may
be needed to aid in healing the wound.
HBO as a therapy
The management o f probl em wound s should
always include correction of perfusion and oxygena-
tion deficiencie s, debrid ement, inf ection con trol,
aggressive wound care, and s urgical closure. In
problem wounds, adjunctive care may also be neces-
sary. When a deficiency in oxygenation of the
wound is found, in the face of nonreconstructable
vascular disease, HBO as an adjunctive therapy
should be considered.
Definition
HBO is defined as a treatment in which 100%
oxygen is delivered to a patient at greater than two
times the normal atmospheric pressure at sea level.
The goal is to increase oxygen delivery to tissues by
increasing the partial pressure of oxygen in plasma.
This is based on Henry’s law, which states that the
Fig. 2. Multiplace hyperbaric oxygen chamber (inside).
(Courtesy of Kindred Hospital, Las Vegas, NV.)
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–75 69
concentration of a gas dissolved in fluid is directly
proportional to the pressure exerted on the gas. In
other words, HBO therapy results in ‘hyperoxic
plasm a, because arteriole PO
2
levels can reach
greater than 2000 mm Hg and tissue PO
2
levels
can reach levels greater than 600 mm Hg.
HBO therapy is accomplished via a monoplace or
multiplace chamber. A monoplace chamber is a
hollow sphere designed to deliver HBO to one patient
without the use of an oxygen mask (Fig. 1). Respira-
tor-dependant patients can be supported on ventila-
tors that are specially designed for the monoplace
chamber. Pertinent vital signs and transcutaneous
oxygen levels can be monitored while the patient is
in the monoplace chamber. Multiplace chambers can
accommodate more than one person (Figs. 2, 3).
Because compressed air is used for pressurization,
patients must wear tight-sealing oxygen masks, or
hoods, that deliver 100% oxygen. Chambers must
also have vacuum reducers to conduct exhaled carbon
dioxide out of the tank. The advantages of a multi-
place chamber are in treating more than one patient at
a time and direct care for patients, including defi-
brillation, suctioning, and chest tube insertion. In
contrast, if patients are in a monoplace chamber, they
must be decompressed before direct patient care can
Fig. 3. Multiplace hyperbaric oxygen chamber (outside). (Courtesy of Kindred Hospital, Las Vegas, NV.)
Fig. 4. TcPO
2
machine.
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–7570
be administered. In addition, there are less claustro-
phobic events in multiplace chambers when com-
pared with monoplace chanbers.
An increase in tissue oxygen tension by HBO
therapy enhances wound healing by a number of
mechanisms. It increases neutrophil bactericidal
capaci ty, kills some anaerobic bacteria, inhibits
toxin formation in some anaerobes, encourages
fibroblast activity, and promotes angiogenesis [4].
Classically, oxygen delivery depends on the
amount of oxygen carried by hemoglobin, rather
than on arterial oxygen content. In wounds, how-
Fig. 5. TcPO
2
evaluation form.
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–75 71
ever, this is not true. Intercapillary distances are
large and oxygen consumption is relatively low in
wounds. Furthermore, microvasculature damage
and peripheral vasoconstriction increase diffusion
distances. Partial pressure is the driving force of
diffusion. A higher PO
2
level is needed to force
oxygen into injured and healing tissues [5,6].
Therefore, HBO creates a steep tissue oxygenation
gradient, providing an even more powerful stimu-
lus than lactate or moderate hypoxia, to initiate
and propel wound healing [5,6].
Supporting data
The effects of HBO on wound healing have been
shown in several clinical trials. Conditions such as
osteomyelitis, necrotizing infections, ischemia reper-
fusion, and thermal injuries have been studied with
promising results [7 9]. Perhaps the most inform-
ative studies have been in diabetic lower extremity
wounds. Overall, several studies have shown
decreased wound size [1012], decreased rates of
amputation [10, 1316], and increased numbers of
healed wounds [15, 17, 18] among patients receiving
HBO therapy as an adjunctive treatment.
Baroni et al [10] conducted a nonrandomized
study of 18 hospitalized diabetics and 10 diabetic
control patients. They reported that a significant
number of subjects who received HBO went on to
heal their wound when compared with subjects who
had not received HBO. In a continuation of this study
[16], a significant decrease in amputations was found
among patients who underwent HBO, when com-
pared with the control group. The same researchers
published a third study [17] that involved 151 dia-
betic patients with wounds of the lower extremity
(there was no control group in this study). One
hundred and thirty of the patients completely healed
their wounds with adjunctive HBO. Furthermore, the
authors of a prospective randomized trial [14] invol-
ving 35 subjects who received HBO and 33 patients
who were controls reported a significan tly lower
incidence of major amputations among Wagner grade
IV ulcers. Wattel et al [18] conducted a noncontrolled
study consisting of 59 diabetic patients with wounds.
Fifty-two patients who received HBO went on to heal
their wounds. Doctor et al [13] showed a significant
decrease in amputation rate in 30 patients who were
Fig. 6. Initial evaluation of a 58-year-old insulin-dependent
diabetic patient with a limb-threatening foot wound. The
patient had a normal perfusion pressure and a low
transcutaneous oxygen measurement.
Fig. 7. Wound after surgical debridement.
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–7572
subjected to HBO when compared with the control
group during a prospective randomized study. Ham-
merlund et al [11] found a significant reduction in
wound size among nondiabetic patients who received
HBO in a prospective randomized study. Zamboni
et al [12] followed nonhealing diabetic ulcers in a
prospective nonrandomized study, and found a sig-
nificant reduction in wound size for HBO patients
when compared with non-HBO patients. Kalani et al
[15] followed chronic diabetic foot wounds for 3 years
in a prospective randomized study. When compared
with conventionally treated wounds, HBO patients
had an accelerated rate of healing, reduced rate of
amputation, and an increased rate of completely
healed wounds on a long-term basis.
Many factors play an important role in wound
healing. Diabetic control, circulatory problems, pres-
ence of infection, and wound size or depth may
adversely affect wound healing. Many of these
studies fail ed to compare these variables during
analysis of their data. Nonetheless, the results are
promising and should serve as a stimulus for the
development of double-blinded prospective random-
ized studies in the future.
Patient evaluation
Proper patient selection for HBO therapy is cru-
cial. The etiology of the problem wound ensures
successful management. A vascular surgery consul-
tation is the first priority, to determine if a recon-
structible lesion exists. If the patient has
nonreconstructable vascular disease, HBO therapy
may be indicated. Tissue oxygenation and perfusion
must be evaluated in each wound. Noninvasive
arteriole Doppler studies, consisting of s egmental
and toe pressures, are used to evaluate perfusion,
whereas TcPO
2
is used to evaluate oxygenation.
Currently, TcPO
2
is the best tool available to
evaluate tissue hypoxia, wound-healing potential,
and patient selection for HBO therapy, and to monitor
progress during therapy (Figs. 4, 5) [19]. A trans-
cutaneous oxygen tension greater than 50 mm Hg
indicates that the wound should heal spontaneously.
Values between 30 and 50 mm Hg are marginal, and
values below 30 mm Hg indicate that the wound
will not heal without adjunctive therapy. HBO
therapy will accelerate tissue repair in hypoxic
wounds in which oxygen tension can be elevated
to therapeutic levels [19]. Therefore, if a patient has
been found to have TcPO
2
levels below 40 mm Hg,
Fig. 8. Wound after 15 hyperbaric treatments.
Fig. 9. Wound after 30 hyperbaric treatments and prior to
successful skin graft.
W.A. Zamboni et al. / Clin Plastic Surg 30 (2003) 67–75 73
and these levels have been shown to increase to
greater than 100 mm Hg while brea thing 100%
oxygen or to greater than 200 mm Hg at 2.5 atmo-
spheres absolute, the patient may be a candidate for
HBO. Repeated TcPO
2
with the patient breathing
room air for at least 12 hours after an HBO treatment
is documented on a weekly basis. Importantly, there is
often a 2-week period in which there is no improve-
ment in wound appearance, despite HBO. These
patients may eventually respond to HBO, and there-
fore amputation should be delayed. When healthy
granulation tissue is present—which usually occurs
after 15 to 30 treatments—TcPO
2
should be measured
at room air. If TcPO
2
levels are above 40 mm Hg,
HBO should be discontinued and proper wound care
should be continued until the wound heals.
The diabetic patient poses a challenge during
evaluation of tissue perfusion and oxygenation.
Diabetic patients may have normal or falsely ele-
vated noninvasive Doppler studies and low TcPO
2
levels, implying satis factory perfusion a nd inad-
equate oxygenation of the wound. Many factors
unique to diabete s may contribute to dec reased
oxygen delivery to the wound, such as red blood
cell membrane stiffness and glycosylated hemo-
globin. In general, a diabetic patient with normal
noninvasive Doppler and low TcPO
2
level responds
best to HBO (Figs. 69).
Presently, the use of HBO therapy is necessary in
only 15% to 20% of patients [19]. HBO therapy in
compromised diabetic wounds is usually reserved for
wounds with tendon or bone exposed, as well as
those wounds with impending gangrene that do not
respond to traditional management of debridement,
antibiotics, and general wound care, including vas-
cular reconstruction. HBO therapy increases wound
oxygen tension, enhancing host antibacterial mecha-
nisms and promoting wound healing [19]. Overall,
HBO is reserved for wounds in which hypoxia and
infection are the etiology. Rarely, HBO is indicated
for other wounds such a venous ulceration or decu-
bitus ulcers [7].
HBO treatment protocols
Protocols for administering HBO vary depending
on the wound severity and chamber type. Oxygen
pressure, duration, periodicity, and total number of
sessions may vary from center to center. Typically,
treatments are delivered at 2.0 to 2.4 atmospheres for
90 to 120 minutes once or twice daily in multiplace
chambers [7]. Treatments in monoplace chambers are
typically performed at 2.0 atmospheres [7]. When
serious infections are present, patients are typically
hospitalized, and given both IV antibiotics and hyper-
baric treatments twice daily. HBO is an adjuvant
treatment ; therefore, diabetic control, debridement,
and aggressive wound treatment are given first pri-
ority. When the wound bed has adequate granulation
tissue, appl ication of grafts can shorten morbidity,
hospital stay, and health care costs.
Summary
Problem wounds, which fail to respond to tra-
ditional medical and surgical therapy, can be chal-
lenging to the plastic surgeon. Surgical, outpatient,
and inpatient wound care costs can be exorbitant.
Indirect costs, su ch as those rel ated to p atient
productivity, disability, a nd premature death, can
also be significant. The underlying problem in
failure of a wound to heal is usually hypoxia and
infection. HBO treatments in selected patients can
facilitate healing by increasing tissue oxygen ten-
sion, thus providing the wound with a more favor-
able environment for repair. Therefore, HBO therapy
can be an important component to any comprehen-
sive wound care program.
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... 8.9 Dari 128 kasus yang menggunakan TOHB sebagai modalitas terapi tambahan di RSUP Prof. Dr. R. D. Kandou selama periode tahun 2011-2016 tercatat bahwa penggunaan TOHB terbanyak untuk decompression sickness (46,87%), diikuti thermal burns (22,65%) dan diabetic ulcer (14,84%), crush injury, skin graft dan pre-post amputation masingmasing sebanyak 6 kasus (4,68%), dan gangrene gas (1,56%). 1,8,9 Pada beberapa laporan dan penelitian, pasien dapat diobati dengan 1-3 sesi TOHB setiap hari. Studi menggunakan model hewan juga menemukan TOHB bermanfaat dalam beberapa kondisi untuk penyembuhan tulang. ...
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... Reference: (Sahni et al., 2003;Bhutani and Vishwanath, 2012). ...
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... Reference: (Sahni et al., 2003;Bhutani and Vishwanath, 2012). ...
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