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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 17  |  Issue : 2  |  Page : 145-153

Penicillamine as radiation protector against gamma radiation effect on complete blood count parameters of guinea pigs


1 Department of Tropical Medicine, Faculty of Medicine, Al-Azhar University, Egypt
2 Department of Chemical Engineering, Faculty of Engineering, British University in Egypt (BUE), Cairo, Egypt
3 Department of Environmental Sciences, Faculty of Science, Damietta University, New Damietta City, Damietta Governorate, Egypt

Date of Submission19-Dec-2018
Date of Decision02-Mar-2019
Date of Acceptance25-Mar-2019
Date of Web Publication23-Oct-2019

Correspondence Address:
Yasser M.M El-Dessouky
19 Taher El-Gzaery Street, 7th District, Nasr City, Cairo 11311
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AZMJ.AZMJ_137_18

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  Abstract 


Background and aim The increasing use of nuclear technology has increased the risk of exposure to radiation. Exposure to radiation induces harms to human beings. The blood and blood-forming organs are one of the most sensitive to radiation. People exposed to high radiation doses had blood count changes, and death may occur owing to acute radiation syndromes. Therefore, radioprotective compounds are very important in clinical radiotherapy. The aim of this study was to examine the effect of penicillamine as a radiation protector agent against gamma radiation effects on complete blood count parameters of guinea pigs.
Materials and methods Thirty healthy male guinea pigs were divided into three equal groups: treated irradiated (n=10), irradiated (n=10), and control (n=10) groups. The treated irradiated and irradiated groups were exposed to acute gamma radiation dose (9 kGy). The treated irradiated group received penicillamine (10 mg/kg) 1 h before exposure to radiation. Blood samples were collected soon after radiation and immediately placed in tubes containing EDTA, and these samples were used in the assessment of blood profile.
Results Treated irradiated guinea pigs had significant higher red blood cell count, white blood cell count, hemoglobin concentration, hematocrit, mean corpuscular volume, mean corpuscular hemoglobin, and mean corpuscular hemoglobin concentration (P≤0.05). The treated irradiated guinea pigs had significant lower relative distribution width of red blood cells by volume coefficient of variation (%) and platelet count (P≤0.05). Relative width of the distribution of platelets in volume index of the heterogeneity of platelets (%) had no significant difference between the two groups (P>0.05).
Conclusion Administration of penicillamine reduced radiation damage to red blood cell count, white blood cell count, hemoglobin concentration, hematocrit, mean corpuscular volume, mean corpuscular hemoglobin, and mean corpuscular hemoglobin concentration.

Keywords: complete blood count, gamma radiation, guinea pigs, penicillamine, radiation protector


How to cite this article:
El-Dessouky YM, El-Dessouky MM, El-Batrawy OA. Penicillamine as radiation protector against gamma radiation effect on complete blood count parameters of guinea pigs. Al-Azhar Assiut Med J 2019;17:145-53

How to cite this URL:
El-Dessouky YM, El-Dessouky MM, El-Batrawy OA. Penicillamine as radiation protector against gamma radiation effect on complete blood count parameters of guinea pigs. Al-Azhar Assiut Med J [serial online] 2019 [cited 2019 Nov 15];17:145-53. Available from: http://www.azmj.eg.net/text.asp?2019/17/2/145/269757




  Introduction Top


The increasing use of nuclear technology has increased the risk of exposure to radiation [1]. Gamma radiation causes harms to living tissues owing to generation of free radicals by the action of gamma radiation on water as human tissues contain more than 80% water. The main formed free radicals from radiolysis react with DNA, proteins, RNA, and cell membranes causing disturbance in cell function and mortality. During radiolysis, reactions occur in tumor and normal cells [2]. The blood-forming organs and reproducing cells are most sensitive to radiation. In some cases, bone marrow transplantation is required to produce new blood cells. The presence of oxygen increases sensitivity to radiation [3].

The exposed people to uranium radiation had a decrease in hemoglobin (Hb), white blood cells (WBCs), mean corpuscular hemoglobin (MCH), hematocrit (HCT), mean corpuscular hemoglobin concentration (MCHC), neutrophils, and platelets (PLT). There was an increase in red blood cells (RBCs) and lymphocyte count [4]. Comparison between exposed and unexposed workers to radiation showed significant decrease in MCH, PLT count, HCT, and lymphocytes [5]. At 25–50 Gy dose of radiation, the number of RBCs was not decreased. High radiation dose caused aggregation of membrane proteins and increased permeability of RBCs to water and ions. Exposure to gamma rays or proton radiation induced decreases in total WBCs and lymphocyte counts [6],[7].

Gamma radiation had great significant effect on WBCs count, MCHC, HCT, Hb concentration, MCH, mean corpuscular volume (MCV), and relative distribution width of red blood cells by volume coefficient of variation (RDW-CV) in male guinea pigs (P≤0.05). The most severe effect of gamma radiation was on WBC count. Gamma radiation had no significant effect on RBCs count, PLT count, or relative width of the distribution of platelets in volume index of the heterogeneity of platelets (PDW-CV) (P>0.05) [8]. Patients with cancer treated by radiation showed significant differences in WBCs and RBCs count. Bone marrow radiation can cause damage of hematopoietic stem cells and produce bone marrow syndrome [2].

To obtain good tumor control with a high dose of radiotherapy, the normal tissues must be protected. Radiation protectors are generally antioxidants and sulfhydryl compounds. Thiol radicals (RS) interact with oxygen at a high rate and may act as an efficient radiation protector. During exposure to radiation, presence of O2 causes formation of peroxyl radical (HO2) which decomposes molecules more than H2O2. Radioprotection effects of thiol compounds (RSH) occur through oxidation reaction with molecular oxygen [9].

Moreover, disulfide (RSSR) has more protective action against radiation than RSH, as S–S bond is weaker and more sensitive to radiation than S–H or S–C bonds [9].

2 RSH+O2⇒RSSR+H2O2.

Radioprotector compounds donate hydrogen atoms to water radicals and any molecules radicals (X) to repair the radical species [9].

2 RSH+2OH⇒RSSR+2H2O,

2 X+2RSH⇒2 XH+RSSR.

Radioprotectors stabilize cellular DNA through formation of disulfides and minimize radiation damage. The mechanism of radiation effect on rats was suggested to be owing to interaction of formed free radicals with cell compounds, with subsequent induced damage [10].

Penicillamine is an antirheumatic drug used in treatment of patients with rheumatoid arthritis. It slows deformities of joints and improves function. Immune system suppression may occur. The empirical formula of penicillamine is C5H11NO2S, giving it a molecular weight of 149.21 [11].

Penicillamine is a metal chelating agent. It is used for treatment of Wilson’s disease (genetic disorder leads to excessive copper deposits in the liver and brain). Normal dosage is 500–1500 mg/day [11]. Penicillamine prevents formation of cystine stones through binding with cysteine. Penicillamine was used for treatment of arsenic poisoning, after dimercaprol (BAL) [12],[13].

Penicillamine oral absorption may be reduced if it is given with iron or other metals, antacids, or food. It reaches maximum concentration in the blood within 1–3 h after absorption [11]. Penicillamine is used as a radioprotective agent in mice to decrease lung damage after pulmonary irradiation [14].

Copper-64 (64Cu) internal radiotherapy was used as a cancer treatment agent, targeting hypoxic regions of tumors. In mice injected by human colon carcinoma cell line, penicillamine (300 mg/kg) decreased radiation damage to bone marrow, ovaries, and liver without decreasing the dose to the tumor [15].

The aim of this study was to examine the radioprotective action of penicillamine against gamma radiation effects on complete blood count (CBC) parameters of male guinea pigs to be utilized as gamma radiation protector in humans.


  Materials and methods Top


Animals

Thirty healthy male guinea pigs were housed in a temperature of 24±3°C, with access to food and water under good supervision. An approval of the study was obtained from the Tropical medicine department and Al- Azhar University ethical committee. Examinations were carried out following the ‘Principles of Laboratory Animal Care’ in the Faculty of Cairo Veterinary Medicine.

The animals were maintained under care conditions. They were divided into three equal groups: treated irradiated (n=10), irradiated (n=10), and control (n=10) groups. Both treated irradiated and irradiated groups were exposed to acute gamma radiation dose (9 kGy). The treated irradiated group received penicillamine at different doses 1 h before exposure to acute gamma radiation (9 kGy). The most effective dose was 10 mg/kg. The source of gamma radiation was cobalt-60 source (Research Model Machine; Atomic Energy of India Ltd, Commercial Products Division). It has dose rate of 9.5 kGy/h. The available chamber volume equals 5 l, and the weight of cell was 5600 kg.

Collection of blood samples

Blood samples were collected from the external jugular vein soon after radiation and immediately placed in tubes containing EDTA for assessment of blood profile.

The collected blood was mixed well and inserted into Italian Hematology Analyzer machine. The analyzed CBC parameters for the two groups were as follows: RBCs (×106/mm3), Hb (g/dl), WBCs (×103/mm3), PLT count (×103/mm3), HCT (%), MCV (fl), MCH (g/dl), MCHC (%), RDW-CV (%), and PDW-CV (%).

Functional method

Guinea pigs were anesthetized by Ether (Merck, Darmstadt, Germany) in a particular lacuna.

Statistical analysis

Statistical package for social sciences, version 23.0 (IBM, Armonk, New York, USA) was employed for statistical calculations and data analysis. All of 10 CBC parameters obtained in this study were represented as mean±SD (%). Results were analyzed using independent t-test to analyze parameters with significant difference between radiated and treated radiated guinea pigs. Significant level was set at P value less than or equal to 0.05.


  Results Top


Gamma radiation had no significant effect on RBC count in guinea pigs (P=0.229) [8]. Mature non-nucleated RBCs, in comparison with other blood components, are less affected by radiation damage [6]. Radiated guinea pigs after penicillamine treatment had significant higher RBCs count by 118.09% compared with radiated guinea pigs alone (P=0.024).

It was demonstrated that WBC count dropped by more than 30% on exposure to radiation [6]. Radiated guinea pigs had significant severe decrease in the number of WBCs compared with controls owing to radiation injury [8]. Radiated guinea pigs after penicillamine treatment had significant higher WBCs count by 179.24% compared with radiated guinea pigs alone (P=0.004).

Gamma radiation had great significant effect on Hb owing to destructive effect of radiation [8],[16]. Radiated guinea pigs after penicillamine treatment had significant higher Hb concentration by 198.33% compared with radiated guinea pigs alone (P=00.00).

Similar to Hb, gamma radiation had great significant effect on HCT value owing to destructive effect of radiation [5],[8]. Radiated guinea pigs after penicillamine treatment had significant higher HCT value by 159.05% compared with radiated guinea pigs alone (P=00.00).

MCV was significantly decreased in radiated guinea pigs [8]. Radiated guinea pigs after penicillamine treatment had significant higher MCV by 108.80% compared with radiated guinea pigs alone (P=0.008).

MCH was significantly decreased in radiated guinea pigs (P<0.05) [8]. Radiated guinea pigs after penicillamine treatment had significant higher MCH by 176.05% compared with radiated guinea pigs alone (P=00.00).

Gamma radiation had great significant effect on MCHC owing to destructive effect of radiation [5],[8]. Radiated guinea pigs after penicillamine treatment had significant higher MCHC value by 231.27% compared with radiated guinea pigs alone (P=00.00).

There was no significant effect of gamma radiation on PLT count [5],[8],[16]. Radiated guinea pigs after penicillamine treatment had significant lower PLT count by 23.69% compared with radiated guinea pigs alone (P=0.029).

There was no significant effect of gamma radiation on RDW-CV (%) [5],[8]. Radiated guinea pigs after penicillamine treatment had significant lower RDW-CV (%) by 7.11% compared with radiated guinea pigs alone (P=0.045).

There was no significant effect of gamma radiation on PDW-CV (%) [5],[8]. Radiated guinea pigs after penicillamine treatment had no significant difference in RDW-CV (%) compared with radiated guinea pigs alone (P=0.787).

Figure 1 shows that the treated irradiated guinea pigs had significant higher RBCs count, WBCs count, Hb concentration, HCT, MCV, MCH, and MCHC and lower RDW-CV (%) (P≤0.05). There was great significant effect of use of penicillamine as gamma radiation protector on these parameters. The treated irradiated guinea pigs had significant lower PLT count (P≤0.05). This was attributed to the drug effect, as stated by Sweetman [11]. PDW-CV (%) had no significant difference between the two groups (P>0.05).
Figure 1 Comparison between the percentages of mean CBC parameters in treated irradiated to the irradiated Guinea pigs.*P≤0.05. Hb, hemoglobin; HCT, hematocrit; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration; MCV, mean corpuscular volume; PDW-CV, relative width of the distribution of platelets in volume index of the heterogeneity of platelets; PLT, platelet; RBC, red blood cell; RDW-CV, relative distribution width of red blood cells by volume, coefficient of variation; WBC, white blood cell.

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  Discussion Top


Living organisms are exposed continually to ionizing radiation (IR). Sources of IR in nature may be from testing nuclear weapons, occupations (people working in atomic agency), and in medicine (patients treated by radiotherapy) [8].

Biological tissues damage by IR occurs through excitation or ionization of their atoms and molecules. IR damage may be both directly by affecting DNA integrity and indirectly by intracellular formation of free radicals. It may be prompt (manifested minutes to weeks after exposure) or delayed (manifested several months to years later) depending on the exposed radiation dose [17].

The most sensitive parts of living organism to IR are the blood, blood-forming organs, and reproductive organs. In the blood, WBCs are the key cellular components that are most sensitive to IR. IR damages leukocytes DNA, leading to severe leukocytes drop sharply after exposure to different doses of gamma radiation. RBCs are minimally affected by IR because they have no nuclei [18]. However, IR may affect RBCs concentrates and permeability. It was reported that lymphocyte DNA damage occurred after blood exposure to IR without lethal damage to RBCs [19].

Total body exposure to IR in animals and humans leads to hematopoietic syndrome and eventually death owing to effects on blood cells [20]. So in clinical radiotherapy, to gain better tumor control with a high dose of radiotherapy, we must protect the blood and normal tissues against radiation injury. Thus, it is very important to use radioprotective compounds before exposure to radiotherapy. This study was designed to study the role of penicillamine as a radioprotective compound against gamma radiation effects on CBC parameters of male guinea pigs.

Radiated guinea pigs after penicillamine treatment had significant higher RBCs count by 118.09% compared with radiated guinea pigs alone (P=0.024) ([Table 1] and [Figure 1]). Gamma radiation had no significant effect on RBCs count in guinea pigs [8]. Mature RBCs had no nuclei, unlike other blood components, so RBCs are less affected by radiation damage [6],[18].
Table 1 Comparison between treated radiated and radiated guinea pigs in red blood cell count (normal: 4.5–7.0×106/mm3)

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Irradiation leads to osmotic disturbances and increased permeability of RBCs. At 330 Gy, radiation caused gradual swelling of RBCs with entry of sodium ions into the erythrocytes and exit of potassium ions owing to disturbance of membrane integrity [6]. In addition, WBCs are the most sensitive blood cells to gamma ray irradiation. Leukocyte count dropped sharply after irradiation [7].

Radiated guinea pigs after penicillamine treatment had low WBC count (0.518±0.187×103) compared with controls (7.370±1.870×103), but radiated guinea pigs after penicillamine treatment (10 mg/kg) had significant higher WBCs count (0.518±0.187×103) by 179.24% compared with radiated guinea pigs without treatment (0.289±0.114×103) (P<0.05) ([Table 2] and [Figure 1]). Penicillamine administration decreased the effect of gamma radiation on WBCs. Penicillamine acts as a radioprotective compound owing to thiol bond (RSH), which can decrease the oxidation reaction of molecular oxygen, causing radioprotection.
Table 2 Comparison between treated radiated and radiated guinea pigs in white blood cells count (normal: 4.5–11.0×103/mm3)

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WBCs decreased in a dose-dependent manner on exposure to radiation, and this is considered a health hazard during radiation exposure. The dose-dependent decrease in WBC counts was observed in mice after whole-body exposure to radiation [7].

Although radiation had no significant effect on RBCs count, it had significant effect on RBC size (MCV) and Hb content (MCH and MCHC). Radiated guinea pigs had significant lower MCHC, HCT, Hb concentration, MCH, MCV, and RDW-CV (%) compared with controls (P≤0.05) [8]. Radiation exposure significantly (P<0.001) reduced Hb and HCT in animal model [21]. Another study showed that low-level chronic radiation exposure decreased mean Hb in blood of professional radiation workers [22].

Radiated guinea pigs after penicillamine treatment had significant higher Hb concentration by 198.33% ([Table 3] and [Figure 1]), higher HCT value by 159.05% ([Table 4] and [Figure 1]), higher MCH by 176.05% ([Table 5], [Figure 1]), and higher MCHC value by 231.27% ([Table 6] and [Figure 1]) compared with radiated guinea pigs alone (P<0.05). Penicillamine protects Hb from destruction by radiation.
Table 3 Comparison between treated radiated and radiated guinea pigs in hemoglobin concentration (normal: 11–15 g/dl)

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Table 4 Comparison between treated radiated and radiated guinea pigs in hematocrit value (normal: 37–48%)

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Table 5 Comparison between treated radiated and radiated guinea pigs in mean corpuscular hemoglobin (normal:14.2–20.1 pg)

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Table 6 Comparison between treated radiated and radiated guinea pigs in mean corpuscular hemoglobin concentration (normal: 31.7–40.4 g/dl)

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Heydarheydari et al. [22] showed that low-level chronic radiation exposure leads to decreased MCV in blood of professional radiation workers. Radiated guinea pigs had significant lower MCV compared with controls (P≤0.05) [8]. This was attributed to direct radiation damage of the cell membrane of RBCs.

Radiated guinea pigs after penicillamine treatment had significant higher MCV by 108.80% ([Table 7] and [Figure 1]) and lower RDW-CV (%) by 7.11% ([Table 8] and [Figure 1]) compared with radiated guinea pigs alone (P<0.05). Significant higher MCV in radiated guinea pigs after penicillamine treatment may be attributed to several factors. Penicillamine protects RBC membrane from damage by radiation, increased permeability of RBCs to water and ions with subsequent swelling of RBCs and preservation of the Hb content of RBCs from destruction by radiation. The variation in RBCs size was decreased after penicillamine treatment owing to lower RDW-CV (%) in treated irradiated guinea pigs.
Table 7 Comparison between treated radiated and radiated guinea pigs in mean corpuscular volume (normal:37.8–56.0 fl)

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Table 8 Comparison between treated radiated and radiated guinea pigs in relative distribution width of red blood cells by volume, coefficient of variation (%)

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Free radicals produced in-vivo system by gamma radiation alter the structure and function of cell membranes, lipids, and protein through lipid peroxidation, hydrolysis of membrane phospholipids, formation of lipid-lipid cross-links, disulfide bridge formation, damage of amino acid residues in the membrane proteins, formation of lipid-protein cross-links, and ultimately loss of the membrane deformability and increased membrane rigidity. Lipid peroxidation by radiation inhibits the activity of membrane enzymes and transport proteins. This effect may arise owing to conformational changes of protein structure and/or oxidation of thiol groups, which are most susceptible to oxidation by radiation [1].

Radiation did not affect PLT count, aggregation of PLTs, and expression of PLT factor [3]. Similarly, PLTs’ survival was not affected by a 50-Gy radiation dose. Even at high radiation doses, PLTs were not affected [6]. These data are consistent with findings reported by El-Dessouky and El-Dessouky [8] who concluded that gamma radiation had no significant effect on PLT count or PDW-CV (%) (P>0.05).

Radiated guinea pigs after penicillamine treatment (10 mg/kg) had significant lower PLT count (277±69.62×103) by 23.69% compared with radiated guinea pigs alone (363±90.00×103) (P<0.05) with no significant effect of gamma radiation on PDW-CV (%) (P= 0.787). ([Table 9] and [Table 10] and [Figure 1]). Hematological adverse effects of penicillamine have included thrombocytopenia and, less frequently, leucopenia; these are usually reversible. In humans, incidence of 12–27% has been reported for penicillamine induced thrombocytopenia in patients with rheumatoid arthritis, possibly owing to bone marrow suppression and a reduced PLT production rate [11].
Table 9 Comparison between treated radiated and radiated guinea pigs in platelet count (normal:250–850×103/mm3)

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Table 10 Comparison between treated radiated and radiated guinea pigs in relative width of the distribution of platelets in volume index of the heterogeneity of platelets (%)

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In this study, penicillamine was used in a dose of 10 mg/kg to reduce the effect of external gamma radiation to male guinea pigs owing to existence of thiol bond. In a study done by Yoshii et al. [15], during 64Cu internal radiotherapy (PET) in mice injected with cancer colon cells, administration of penicillamine (single dose of 300 mg/kg) reduced radiation doses to critical organs without decreasing the dose to the tumor owing to its chelating action with 64Cu.


  Conclusion Top


Administration of penicillamine reduced radiation damage to RBCs count, WBCs count, Hb concentration, HCT, MCV, MCH, and MCHC.

Acknowledgements

The authors like to express their deepest appreciation to British University in Egypt (BUE) and Military Technical College who provided us the possibility to complete this work.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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