|Year : 2009 | Volume
| Issue : 3 | Page : 390
|Morphological analysis of second-intention wound healing in rats submitted to 16 J/cm 2 λ 660-nm laser irradiation
Maria Amalia Gonzaga Ribeiro1, Ricardo Luiz Cavalcanti de Albuquerque1, Andre Luiz Santos Barreto2, Vitor Garcia Moreno de Oliveira3, Thalita Barreto Santos3, Carolina Delmondes Freitas Dantas3
1 Laboratory of Morphology and Structural Biology, Science and Technology Institute, University Tiradentes, Aracaju/SE, Brazil
2 Post- Graduation Program in Health and Environment, University Tiradentes, Aracaju/SE, Brazil
3 School of Dentistry, University Tiradentes, Aracaju/SE, Brazil
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|Date of Submission||08-Jan-2008|
|Date of Decision||14-May-2008|
|Date of Acceptance||27-Oct-2008|
|Date of Web Publication||30-Oct-2009|
| Abstract|| |
Background and Objectives : Low-level laser therapy (LLLT) has been extensively applied to improve wound healing due to some biostimulatory properties presented by laser arrays apparently able to accelerate the cicatricial repair of soft tissue injuries. However, many controversial results have been reported in the literature, probably as a result of the wide sort of different protocols of photobiomodulation employed in those experiments. The goal of this study was to investigate the effect of a low-dose protocol of LLT on the intensity of the inflammatory response and the pattern of collagen fibers' deposition during second-intention wound healing in rodents.
Materials and Methods : Standard-sized wounds were carried out in the back of 24 male rats. Half of them underwent LLLT treatment (16 J/cm 2 ) at 660 nm delivered for 7 days. Eight and 14 days after the wounds were performed, the repairing area was removed and stained in HE and Masson's trichrome, and the inflammatory response, epithelization, and collagen fiber depositions were evaluated.
Results : We found that LLLT was able to slightly reduce the intensity of the inflammatory reaction as well as to enhance substantially the epithelization process at both 8 th and 14 th days. In addition, it also appeared to stimulate the deposition of collagen fibers at the final stages of wound healing.
Conclusions : The LLLT protocol tested in this study resulted in some improvements in second-intention wound healing in rodents.
Keywords: Cicatricial repair, laser, photobiomodulation
|How to cite this article:|
Gonzaga Ribeiro MA, Cavalcanti de Albuquerque RL, Santos Barreto AL, Moreno de Oliveira VG, Santos TB, Freitas Dantas CD. Morphological analysis of second-intention wound healing in rats submitted to 16 J/cm 2 λ 660-nm laser irradiation. Indian J Dent Res 2009;20:390
Laser light is a sort of electromagnetic energy which, depending on its source, can be converted into luminous energy, visible or not. Laser arrays are, therefore, a highly concentrated noninvasive kind of non-ionizing radiation that, in contact with different tissues, promotes thermic, photochemical, and nonlinear effects. 
|How to cite this URL:|
Gonzaga Ribeiro MA, Cavalcanti de Albuquerque RL, Santos Barreto AL, Moreno de Oliveira VG, Santos TB, Freitas Dantas CD. Morphological analysis of second-intention wound healing in rats submitted to 16 J/cm 2 λ 660-nm laser irradiation. Indian J Dent Res [serial online] 2009 [cited 2019 Sep 22];20:390. Available from: http://www.ijdr.in/text.asp?2009/20/3/390/57360
Several studies have indicated that laser arrays at low frequencies (low-level laser therapy, LLLT) are quite helpful in modulating different biological activities, such as trophic regenerative,  anti-inflammatory,  and analgesic effects. 
It has been suggested that biological properties of visible spectra of LLLT are probably a result of cellular photoacceptors and signaling pathway stimulation by light. Therefore, the absorption of monochromatic visible radiation by components of the cellular respiratory chain accelerates the transfer of electrons from NADH and FADH2 (produced in the Krebs cycle) to oxygen molecules to form (with the aid of protons) water molecules, harnessing the energy released by this transfer to the pumping of protons (H+) from the matrix to the intermembrane space. This gradient of protons formed across the inner membrane by this process of active transport forms a miniature battery. Consequently, this mechanism increases the mitochondrial ATP production and protein synthesis. Furthermore, it was proposed that cytochrome c oxidase is the primary photoacceptor for both the red and infra-red range in mammalian cells. 
Wound healing is a biological response to tissue injury. This highly controlled repair process is characterized by the movement of specialized cells into the wound site, in order to provide key signaling events required for the influx of connective tissue cells and a new blood supply. 
The healing response is a three-step phenomenon. At first, after the tissue is injured, the critical task of removal of foreign materials, bacteria, and damaged tissues must be performed; thus, as the blood components spill into the site of injury and inflammatory cells, such as neutrophils and macrophages spread out within the tissue, the process of phagocytosis is triggered. Subsequently, after the "cleaning task" is achieved, inflammatory phagocytic cells are replaced by mononuclear leukocytes, lymphocytes, and plasma cells, the vascular component proliferates, and fibroblasts migrate into the area and deposit new extracellular matrix, particularly collagen fibers. At the final stages of the healing process, these fibers become cross-linked and assume a gross thick appearance, characterizing the remodeling phase of the cicatricial repair. 
Despite the fact that wound healing represents a cicatricial reparative response to tissue insult, a long-term or over- induced inflammatory reaction is extensively implicated in promoting atypical patterns of healing, such as fibrosis, strictures, adhesions, and contractures. 
Previous reports have demonstrated that LLLT is efficient in stimulating cellular proliferation and collagen synthesis in biological assays,  the role of LLLT in modulating different steps of the wound-healing process has been widely investigated,  but both positive and negative results have been demonstrated depending on the protocol of irradiation employed in the various experiments reported. 
Variations in the wavelength and dose of phototherapy, as well as optical characteristics inherent to every single tissue, have been pointed out as relevant factors to assure the success of the laser-induced biological modulation. Moreover, the latter variable has been currently considered particularly important to evaluate the extent of the interaction between laser irradiation and cells. 
As there has been an extensive controversy in the literature concerning the role played by phototherapy in stromal and inflammatory cells involved in the wound-healing process, the goal of this study was to investigate the effect of a given protocol of LLLT irradiation on the intensity of the inflammatory response and the pattern of collagen fiber deposition during two different phases of the cicatricial repair in rodents.
| Materials and Methods|| |
The animals used in this study were adult male Rattus norvegicus albinus, Wistar lineage, weighing 250-300 g. The rats were housed in clear plastic cages with solid floors and loose hardwood chip bedding, and supplied with food and water ad libitum in a temperature- and humidity- controlled environment.
Twenty-four rats were anesthetized with intraperitoneal ketamine-xylazine (100 mg/kg, 5 mg/kg) and 1-cm 2 standard-sized wounds were performed on the back of the animals. Animals were handled in accordance with the principles of aseptic chain in order to avoid any possibility of exogenous bacterial contamination. Subsequently, rats were separated into four groups of six animals each, which were randomly assigned to one of the four treatment groups: G1, untreated group sacrificed 8 days after surgical procedures, G2, photo- irradiated group sacrificed 8 days after surgical procedures, G3, untreated group sacrificed 14 days after surgical procedures, and G4, photo-irradiated group sacrificed 14 days after surgical procedures. The sacrifice of the animals was carried out by intramuscular administration of 0.8 ml/kg zoletil, 0.43 ml/kg thiopental and 5 ml/kg potassium chloride (Ariston 19.1%, 2.559 mEq/ml). After death certification, the area corresponding to the wound region in the back of the animals was surgically removed and the specimens were formalin fixed and paraffin embedded according to routine laboratorial techniques.
Animals of G2 and G4 experimental groups were treated with ArGaAl laser arrays of 660-nm wavelength obtained from a laser apparatus Twin LaserÒ (MMOptics, São Paulo, Brazil). The treatment consisted of daily transcutaneous irradiation at 660 nm for 100 s, 40 mW (output power), and an energy density of 100 J/cm 2 during 7 days. Focal spot was 0.04 cm 2 . Laser array was positioned directly over the animal at a vertical distance of 0.3 cm from the edge of the wound and irradiation was performed at four different points equidistant to each other.
After the sacrifice of the animals, the wound area was surgically removed, fixed in buffered 10% formalin, and paraffin embedded. Subsequently, serial 5-µm sections were obtained and stained in hematoxylin-eosin, and Masson's trichrome to assess the intensity of the inflammatory response and collagen deposition (fibroplasia), respectively.
The intensity of the inflammatory response was assessed as follows: + (inflammatory cells representing less than 10% of the cell population observed within the wound area), ++ (inflammatory cells representing between 10 and 50% of the cell population observed within the wound area), and +++ (inflammatory cells representing more than 50% of the cell population observed within the wound area). Moreover, depending on the predominant leukocyte subset, the inflammatory reaction was typed as acute (neutrophil- rich inflammation), subacute (neutrophils and mononuclear cells are equivalent), chronic nonspecific (lymphocyte and/or plasma cell-rich inflammation), and chronic granulomatous (macrophage and giant cell-rich inflammation).
Moreover, the degree of epithelization of the wound surface was also assessed according to the following criteria: + (epithelization recovering less than 10% of the wound surface), ++ (epithelization recovering between 10 and 50% of the wound surface), and +++ (epithelization recovering more than 50% of the wound surface).
The analysis of the intensity and pattern of fibroplasia was performed according to the disposition and appearance of the collagen fibers deposited in the wound site. These fibers were then categorized into + (thin, delicate, loosely arranged collagen fibers seen throughout the wound area), ++ (thin, delicate, loosely arranged collagen fibers seen in the deeper regions and margins of the wound area, but thicker and gross at the center), and +++ (thick, gross, densely arranged collagen fibers seen throughout the wound area).
Before the beginning of any experimental procedure, this study was approved by the institution's animal care and use committee.
| Results|| |
As showed in [Table 1], the intensity of the inflammatory response was severe in absolutely all the cases of G1. Besides, the leukocyte infiltrate was predominantly composed of neutrophils and lymphocytes, characterizing an acute inflammatory reaction. In general, neutrophils were distributed along the wound surface, particularly within the fibrinous exudate membrane [Figure 1]a, whereas lymphocytes were observed in the deeper regions of the specimens. Plasma cells were also an important component of the infiltrate, but these cells comprised less than 10% of the leukocytes in any case. Some fusiform cells, with indistinct cytoplasm and large, pale nuclei consistent with macrophages were also observed, but they always represented less than 10% of the leukocyte population. Eosinophils and giant cells were not observed.
The wounds of the irradiated animals of G2 presented a severe inflammatory response (+++) in 50% of the cases and moderate in the other half. Neutrophils and lymphocytes were also the most frequently observed leukocytic cells, but they appeared to be less abundant in this group than in G1, particularly neutrophils [Figure 1]b. Notwithstanding, the response was categorized as acute, as long as the neutrophil population was clearly more conspicuous than that of the mononuclear cells. However, the pattern of distribution of these leukocytes throughout the wound was pretty similar to that seen in G1. In addition, the satellite leukocyte population (macrophages, eosinophils, and giant cells) of G2 presented the very same profile verified in G1 [Table 1].
At the 14 th day, the intensity of the inflammatory response in G3 was predominantly moderate, although it still presented severely in two cases. Besides, lymphocytes were the most abundant leukocyte population and on that account, the infiltrate was classified as chronic nonspecific (lymphocytic). Plasma cells were frequently observed but not as copiously as lymphocytes [Table 1]. Moreover, a remarkable neoformation of capillary blood vessels, mainly in the deeper regions of the healing area, was also observed [Figure 1]c.
The inflammatory response persisted in G4 [Table 1], although it had been classified as chronic nonspecific and in moderate intensity, and some blood vessels in formation were observed spread out in the connective tissue, but this vascular component was not as copious as in G3. Regarding the profile of the inflammatory infiltrate, most of the specimens presented slight infiltration of plasma cells and, less conspicuously, lymphocytes [Figure 1]d. Even though the presence of neutrophils could still be verified in some cases, their presence was not remarkable in any case.
As indicated in the [Table 2], epithelization was seen to be inconspicuous at the eighth day of surgery. In G1, it was absolutely absent [Figure 2]a and in G2, although new epithelial formation right under the fibrinous exudate [Figure 2]b was seen in all the specimens, it had recovered more than 10% of the wound surface in only a single case. On the 14 th day, epithelial neoformation was extremely irregular in G3, despite the fact that in the absolute majority of cases, it had recovered close to 50% of the wound surface [Figure 2]c. On the other hand, significant neoformation of the recovering epithelial tissue (pattern +++) was observed in almost all the animals of G4, but it was seen to be complete in only one of the six specimens [Figure 2]d.
Fibroplasia was assessed by analyzing the appearance and disposition of collagen fibers stained in blue by Masson's trichrome, as shown in [Table 3]. In G1 and G2, thin collagen fibers arranged in delicate intertwined bundles were observed within a loose connective tissue (pattern +) in the entire cases studied [Figure 3]a. G3 presented morphological features corresponding to the ++ pattern of fibroplasia in the absolute majority of the cases [Figure 3]b. In most of the cases of G4, cicatricial repair was observed to be well developed, with thick, gross collagen fibers densely arranged in parallel bundles (+++ pattern) [Figure 3]c and d, although in two cases the pattern ++ of collagen deposition had persisted. However, collagen fibers appeared to be less abundant and thicker in G3 than in G4.
| Discussion|| |
The induction of cicatricial repair in wounds with loss of tissue characterizes a particular sort of cicatrization phenomenon known as second-intention wound healing. The inflammatory reaction represents the earliest event to take place after tissue injury, whose main function is to eliminate eventual microorganisms and provide wound cleaning. Subsequently, biological events, such as formation of new capillary blood vessels associated with progressive deposition and remodeling of collagen fibers will culminate in a complete cicatricial repair of the injured area.  Inflammatory response is absolutely required to provide wound healing, but its long-term persistence has been considered one of the most important reasons of delay in the healing process. 
Despite recent advances in improving the wound-healing process, many studies have still been performed looking at new strategies to stimulate the biological events that comprise the cicatricial repair phenomenon. 
Studies have demonstrated that laser arrays present some biostimulatory properties apparently able to accelerate wound healing of soft tissue injuries. [13,14] Wavelengths in the 600-700 nm range have been employed in treating superficial tissues, such as cutaneous or mucosal wounds, whereas wavelengths between 780 and 950 nm have been applied in deep seated tissue insults, like bone fracture healing.  However, both positive and negative results have been reported in the literature, probably as a result of different protocols of photobiomodulation employed in as in vitro and in vivo biological assays.
The beneficial effects of adequate protocols of photobiomodulation on wound healing can be explained by considering its ability to stimulate several biological mechanisms responsible for triggering many phases of cicatricial repair of soft tissue injuries, including the induction of cytokines and expression of growth factors by keratinocytes and stromal cells.  On the other hand, negative responses can be a result of an unsuitable interaction between laser light and tissue components of the wound-healing process due to the application of inappropriate protocols of photoirradiation. 
The dosage of energy applied in the photobiomodulation procedure is currently considered as an extremely relevant parameter to provide a significant improvement in cicatricial repair. 
A specific protocol of laser irradiation at 660 nm (total energy dose of 24 J/cm 2 ) has been previously reported which showed to be truly effective in improving the wound-healing process, possibly by promoting photostimulation of a variety of cell subsets, such as fibroblasts, myofibroblasts, and epithelial cells, at the same time modulating the inflammatory response. 
In this study, we investigated the effectiveness of a reduced energy dosage of laser irradiation in stimulating wound healing. We made use of the very same general protocol employed in a previous work  in order to afford subsequent reliable comparisons between our findings and those recently reported.
Within the protocol of photobiomodulation applied in this study, LLLT was able to induce a certain decrease in the intensity of the inflammatory reaction at both 8 th and 14 th days after surgical procedures, but this reduction did not appear to be very substantial. In fact, a remarkable anti- inflammatory activity of LLLT has been previously reported within other different protocols. , In addition, we have found that the inhibitory effect promoted by LLLT on the inflammatory reaction in this work was not as meaningful as that obtained in our previous investigations using a total dose of 24 J/cm 2 .  These findings suggest that, despite the fact that this protocol of LLLT had shown some ability to modulate negatively the inflammatory response, it cannot be reliably asserted that this effect might truly favor the acceleration of the healing process.
However, this protocol of LLLT appeared to be successful in influencing the immunoinflammatory response, i.e., once it reduced the amount of neutrophils at the earlier stages of the wound-healing process and unexpectedly induced switching of the leukocyte infiltration pattern from lymphocyte into plasma cell-rich irradiated wounds. This modulatory effect of LLLT over the acute inflammatory response might be a result of an important inhibitory role played by laser arrays, on the synthesis of prostaglandin, a chemical mediator widely supposed to provide chemotactic signals for polymorphonuclear neutrophils.  Therefore, LLLT might provide a short term acute inflammatory response in earlier stages of wound healing, which certainly would favor the process of cicatricial repair.
The apparent role played by LLLT in stimulating plasma cell differentiation in the final stages of the wound-healing process is harder to be explained. In fact, this sort of data was not observed in our previous experiments, when the dose of 24 J/cm 2 was employed.  A possible explanation could lie in the fact that low doses of LLLT might be more effective to stimulate the differentiation of B cells, a class of lymphocytes, into plasma cells, a class of lymphoid cells able to synthesize and release antibodies. However, in spite of our data, other investigations are firmly recommended to clarify the nature of this biological effect.
Epithelization is the process where epithelial cells on the edges of the wound or in residual skin appendages lose contact inhibition and migrate into the wound area. Simultaneously, additional epithelial cells are provided by the proliferation of immature keratinocytes in the basal layer. 
As keratinocytes are supposed to be a source of a variety of cytokines involved in remodeling the collagen fibers deposited at the final stages of cicatricial repair, the development of epithelial lining is considered a relevant step of wound healing. Furthermore, the epithelial bridge is also responsible for removal of scab by dissolution of its attachments to the underlying connective tissue. 
In this study, the process of wound surface epithelization was enhanced by LLLT in both stages of wound healing, although the advances in epithelial neoformation had been less apparent in 8 than in 14 days. These findings are supported by previous studies asserting that LLLT was shown to be effective in stimulating the migration of keratinocyte along the healing wound surface, probably as a result of the release of growth factors such as EGF (epidermal growth factor) and TGF-á (transforming growth factor alpha) by irradiated macrophages. ,, Furthermore, LLLT was recently proved to act directly on keratinocyte-promoting epithelial cell proliferation in vitro. 
The reason for stimulus for epithelization being more intense in final than in early stages of the healing process is unclear, although similar findings have already been reported.  The persistence of more intense inflammatory infiltration at the eighth day of the cicatricial repair might probably be related to these findings, but the exact nature of this relationship remains uncertain.
Once the wound is "cleaned," the inflammatory phase of the cicatricial repair is gradually substituted by the proliferating phase as the healing process takes place. The latter is characterized by migration of fibroblasts into the wound area and consequent deposition of the collagen fibers required for the cicatricial repair of tissue injury.  In normal tissues, collagen fibers provide strength, integrity, and structure; so, when tissues are disrupted following an injury, collagen deposition is essential for replacing the lost tissue and restoring anatomic structure and function. 
In this study, LLLT appeared to stimulate the deposition of collagen fibers at the final stages of wound healing. This improvement of the collagen deposition promoted by LLLT can be closely related to the fact that low-energy laser is able to upregulate the release of some cytokines responsible for fibroblast proliferation and collagen synthesis, such as FGF-β and TGF, respectively. ,, Moreover, it has been suggested that LLLT increases ATP synthesis and consequently, the cell enzymatic activity. , Thus, it seems rational to suppose that laser arrays might upregulate the activity of enzymes responsible for the synthesis of collagen fibers. However, further investigations are required to clarify this mechanism and prove this theory right.
Surprisingly, we found no beneficial effects on the collagen fiber deposition on the eighth day, which is not in agreement with some previous findings. , These findings might be indirectly interpreted as a result of the protocol of dosage used in this study. Thus, the low dose could lead to an underexposition of stromal and inflammatory cells to the irradiation, which would minimize the biological effects of the laser arrays on both fibroblasts and leukocytes of the damaged tissue, minimizing the potential to stimulate the fibroplasia process and to inhibit the inflammatory response, respectively.
Despite the fact that the extent of the results obtained in this study by using a dose of 16 J/cm 2 had not been as advantageous as in previous investigations using higher doses, we can assert that this protocol of photobiomodulation was successful in improving certain steps of second- intention wound healing, such as inflammatory profile and epithelization.
| Conclusion|| |
The LLLT protocol tested in this study improved wound healing in vivo. Nevertheless, further investigations are necessary to provide data about possible extrapolations of its effectiveness in cicatricial repair in human beings.
| Acknowledgment|| |
We would like to thank the CNPq (Conselho Nacional de Pesquisa) for the financial support.
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Ricardo Luiz Cavalcanti de Albuquerque
Laboratory of Morphology and Structural Biology, Science and Technology Institute, University Tiradentes, Aracaju/SE
Source of Support: None, Conflict of Interest: None
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]
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