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Comparison of protective effect of melatonin and amifostine on acute renal damage caused by ionizing radiation


Alaattin OZEN1, Ebru TASTEKIN2, Suat CAKINA1, Sule PARLAR1, Nukhet KURKCU1, Necdet SUT3, M. Cem UZAL1


1Trakya University Faculty of Medicine Department of Radiation Oncology, Edirne (22030), Turkey
2Trakya University Faculty of Medicine Department of Pathology, Edirne (22030), Turkey
3Trakya University Faculty of Medicine Department of Biostatistics (22030), Edirne, Turkey



This study has been accepted as a poster at the 2nd ESTRO FORUM in 2013.










Corresponding author: Alaattin OZEN, M.D.
Address:	Trakya University Faculty of Medicine,
Department of Radiation Oncology,
Edirne (22030), TURKEY
E-mail: dralovettin@gmail.com
Phone/Fax: 00902842361074
Abstract
Introduction: The aim of this study is to compare the protective effect of melatonin and amifostine on radiation induced renal damage in early phase. 
Methods: 50 female albino rats were divided into five groups: control (Cont), radiotherapy alone (RT), radiotherapy + amifostine (RT+AMI), radiotherapy + melatonin (RT+MEL), radiotherapy + amifostine + melatonin (RT+AMI+MEL). Intraperitoneal amifostine (200 mg/kg) was administered to the rats in the RT+AMI and RT+AMI+MEL groups 30 minutes before irradiation. Intraperitoneal melatonin (10 mg/kg) was administered to the rats in the RT+MEL and RT+AMI+MEL groups 30 minutes before irradiation. RT, RT+AMI, RT+MEL and RT+AMI+MEL groups were irradiated individually with a single dose of 8 Gy on whole body. At the end of the follow-up period paraffin embedded kidney tissue samples were analyzed and percentage of damaged glomeruli was determined by counting damaged glomeruli of kidney cortex as segmental or total necrosis for each animal. 
Results: The protective effect of amifostine, melatonin, and amifostine plus melatonin on radiation induced renal toxicity is statistically meaningful (p < 0.001, = 0.003, < 0.001, respectively). There is an advantage in favor of melatonin when compared with amifostine (p = 0.005). Although there is not an advantage of adding amifostine to melatonin when compared with melatonin alone (p = 0.243), there is statistically significant better protective effect in amifostine plus melatonin group when compared with amifostine alone group (p = 0.003). 
Conclusions: In this study, it has shown histopathologically that the protective effect of melatonin on radiation induced acute renal toxicity is better than amifostine.
Keywords
Amifostine, melatonin, acute renal damage, ionizing radiation










Text
Introduction
The aim of radiation therapy is to deliver sufficient dose to tumor tissue to provide cure without of inducing damage in surrounding normal tissue. Kidneys can be exposed to radiation during radiation therapy of gastrointestinal tumors, and total-body irradiation in preparation for bone marrow transplantation. Radiation induced nephropathy includes vascular permeability, perfusion disturbance, inflammatory reactions and fibrosis [1-3]. Segmental fibrinoid necrosis of the glomerular tufts, occlusive intracapillary accumulations of periodic acid positive material with enmeshed erythrocytes, mesangiolysis, endothelial swelling, and splitting of glomerular capillary basement membranes, fibrinoid changes of the terminal afferent arterioles are the abnormalities seen by light microscopy [4-6]. 
Amifostine, an amino thiol, is a pro-drug that is dephosphorylated by alkaline phosphatase to the active metabolite into the cell. It prevents radiation induced cellular injury through free-radical scavenging, hydrogen donation, and inhibition of DNA damage [3]. Several studies have demonstrated its protective effect on normal tissues against the toxic effects of radiation [7-9]. Melatonin (N-acetyl-5-methoxytryptamine), an endogenous compound synthesized by pineal gland, is a potent antioxidant as in scavenging hydroxyl radicals and increases some antioxidant enzymes such as superoxide dismutase and glutathione peroxidase [10,11].
In this study, we aimed to compare histopathologically the protective effect of melatonin and amifostine on radiation induced renal damage in early phase. And also no functional endpoints were tested.

Materials and Methods

Animals and experimental design
All experiments were conducted adhering to the guidelines of the institutional animal ethics committee. 50 female albino rats, 3�4 months old, weighing 200 � 25 g, maintained under standard temperature and humidity conditions, were used in the study. The animals had free access to sterile water and food, and were housed in a polypropylene cage containing sterile paddy husk for bedding throughout the experiment.
The animals were divided into five groups (with ten rats each) and treated as follows:
� Group 1: control (Cont),
� Group 2: radiotherapy alone (RT),
� Group 3: radiotherapy + amifostine (RT+AMI),
� Group 4: radiotherapy + melatonin (RT+MEL),
� Group 3: radiotherapy + amifostine + melatonin (RT+AMI+MEL).
Animals in the RT group were treated with 0.9% saline solution (SS) 30 minutes before irradiation. Amifostine was administered to the rats in the RT+AMI and RT+AMI+MEL groups 30 minutes before irradiation. Animals in the RT+AMI group received amifostine (200 mg/kg, ER-KIM Ilac, Istanbul, Turkey) by intraperitoneal injection before irradiation. Melatonin was administered to the rats in the RT+MEL and RT+AMI+MEL groups 30 minutes before irradiation. Animals in the RT+MEL and RT+AMI+MEL groups received melatonin (100 mg/kg, Sigma Chemical Co, St. Louis, USA) by intraperitoneal injection before irradiation. All experimental procedures were performed on anesthetized rats. Anesthesia was maintained via intramuscular ketamine (100 mg/kg, Pfizer Ilac, Istanbul, Turkey) and xylazine (3.9 mg/kg, Interhas A.S., Istanbul, Turkey) during irradiation. The follow-up period was 72 hours in all groups.

Irradiation
Rats were anesthetized and fixed on their blocks across a blue Styrofoam (Med-Tec, Orange City, IA, USA) treatment couch in prone position. RT, RT+AMI, RT+MEL and RT+AMI+MEL groups were irradiated individually with a single dose of 8 Gy using a 60Co treatment unit (Cirus, cis-Bio Int., Gif-sur-Yvette, France). Dose rate was 1.15 Gy/min.

Histopathologic analysis
Tissue specimens were prefixed in formaldehyde for 24 h. All tissues were embedded in paraffin wax and processed through hematoxylin-eosin, in 4-�m sections. Tissue samples were evaluated by a light microscope. All samples were analyzed and percentage of damaged glomeruli was determined by counting damaged glomeruli of kidney cortex as segmental or total necrosis for each animal.

Statistical analysis
Conventional methods were used to generate descriptive statistics. Data between groups were compared using Mann-Whitney U-test (post hoc with Bonferoni correction). p-values < 0.05 were considered significant between compared two groups.

Results
The percentage of damaged glomeruli is presented in Table I. We demonstrated pathological changes which concentrate in focal areas of the cortex of the kidney glomeruli in radiotherapy group. The main finding was a significant segmental glomerular necrosis (mesangiolysis). In addition to this, fibrinoid changes in the glomeruli and accumulation of fibrinous material in Bowman's space was detected (Figure 1). There was no significant pathological change in tubules. The protective effect of amifostine, melatonin, and amifostine plus melatonin on radiation induced renal toxicity is statistically meaningful (p < 0.001, = 0.003, < 0.001, respectively). There is an advantage in favor of melatonin when compared with amifostine (p = 0.005). Although there is not an advantage of adding amifostine to melatonin when compared with melatonin alone (p 0.243), there is statistically significant better protective effect in amifostine plus melatonin group when compared with amifostine alone group (p = 0.003). As there was no significant damage following 8 Gy whole body irradiation on the kidney tubules, the protective effect of any agent could not be assessed.

Discussion
The capillary endothelium and the tubular epithelium in the kidneys are conditional cell renewal systems, but they have a limited proliferation potential when they are stimulated by injury. The histopathological findings depend on the time interval between the radiation and the tissue examination. Tissue damage can be seen in both the glomeruli and the tubules. Glomerular capillary endothelial damage is seen within a few days after radiation. Chronic mesangiocapillary or membranoproliferative glomerular injury is the most consistently observed changes in kidney after radiation. Segmental fibrinoid necrosis of the glomerular tufts, occlusive intracapillary accumulations of periodic acid-Schiff-positive material with enmeshed erythrocytes, mesangiolysis, endothelial swelling, and splitting of glomerular capillary basement membranes, fibrinoid changes of the terminal afferent arterioles are the abnormalities seen by light microscopy [4-6].
Tubular changes are late findings, observed after months [12,13]. Tubular loss and atrophy may occur in the absence of glomerular solidification in animals subjected to irradiation. Nonspecific accumulations of mononuclear leukocytes can be seen. The interstitium may show no changes or only a slight apparent increase may occur in interstitial tissue. Tubular cell vacuolization and desquamation are other nonspecific change. Some studies have suggested an important and perhaps primary toxic effect on the tubules by radiation as the basis for subsequent radiation nephropathy [14-18]. Evidence indicates an acute tubular injury corresponding to acute tubular necrosis that may occur after high-dose irradiation [6]. We showed radiation damage on glomeruli using histopathological examination after 72 hours after irradiation. Our main finding was mesangiolysis but we could not find any damage on kidney tubules.
Amifostine and melatonin have similar action mechanisms [11,19]. There are lots of studies in literature which show the protective effects of amifostine and melatonin on different tissues. Although experimental examinations were done in first three days after radiation in molecular studies, they were done after first week in histophatological studies. We think that our study is very important, because we showed the protective effect of each amifostine and melatonin against radiation on kidney tissue using histopathological examination after a very short time from irradiation such as three days [8,20-23].
There is no study in literature which compares the protective effect of amifostine and melatonin on radiation induced renal toxicity. Also, this is another importance of this study. Topkan et al. has observed a superior radioprotective function of�melatonin�over�amifostine�in preventing radiation-induced epiphyseal growth plate injury, without any increase in radioprotective effect by adding�amifostine�to�melatonin [24]. Similar to this study, we found that there is an advantage in favor of melatonin when compared with amifostine. In addition to this result, there is not an advantage of adding amifostine to melatonin when compared with melatonin alone and there is statistically significant better protective effect in amifostine plus melatonin group when compared with amifostine alone group.
In conclusion, this study is really important because it detected that melatonin is more effective when compared with amifostine which is commonly used as a radioprotective agent. For using melatonin like amifostine in clinical experience in the future, further studies which investigate primarily the functional protective effect of melatonin against radiation damage on the kidney.

Conflict of interest 
We have no personal or financial conflict of interest and have not entered into any agreement that could interfere with our access to the data on the research, or upon our ability to analyze data independently, to prepare manuscripts, and publish them.





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