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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 4  |  Issue : 3  |  Page : 240-250

Effect of exposure to cadmium on the hippocampus in adult albino rat and the possible role of L-carnitine


Department of Human Anatomy and Embryology, Faculty of Medicine, Assiut University, Assiut, Egypt

Date of Submission30-Jul-2018
Date of Acceptance10-Sep-2018
Date of Web Publication23-Sep-2019

Correspondence Address:
Mariam W Fidal
Department of Human Anatomy and Embryology, Faculty of Medicine, Assiut University, Assiut
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/JCMRP.JCMRP_60_18

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  Abstract 


Background
The hippocampus is an important structure for formation of new memories. Cadmium is one of the most toxic agents that can affect hippocampal neurons. L-carnitine is an antioxidant.
Aim of work
To demonstrate the effects of cadmium on principal cells of hippocampus of adult rats and possible protective role of L-carnitine.
Materials and methods
A total of 42 adult rats aged 1 month were subdivided into four subgroups: group I was the control group, which received no treatment. Group II was administered cadmium given at a dose of 4 mg/kg/day for 1 month. Group III (sham control) was administered L-carnitine given at a dose of 200 mg/kg/day for 1 month. Group IV was administered cadmium and L-carnitine given to the rats at the same previous doses and duration. For each group, six rats were used for light microscopic study (gallocyanin chrom alum stain), and six rats were used for electron microscopy (group III studied only by light microscopy). Principal cell count and thickness were measured and statistically analyzed.
Results
Principal cells in group II showed degenerative changes. Morphometric data showed a significant decrease in measured parameters. In group III, the results were similar to those of the control group. In group IV, semithin sections and the ultrastructure of the principal cells showed obvious improvement of cells. Morphometric data also increased compared with those treated with cadmium.
Conclusion
Cadmium induces changes in the structure of the principal cells of the hippocampus in adult rats. L-carnitine plays an important in protection of the hippocampus.

Keywords: cadmium, hippocampus, L-carnitine


How to cite this article:
Mahmoud FY, El-Hakim AH, El Deen Amer AS, Fidal MW. Effect of exposure to cadmium on the hippocampus in adult albino rat and the possible role of L-carnitine. J Curr Med Res Pract 2019;4:240-50

How to cite this URL:
Mahmoud FY, El-Hakim AH, El Deen Amer AS, Fidal MW. Effect of exposure to cadmium on the hippocampus in adult albino rat and the possible role of L-carnitine. J Curr Med Res Pract [serial online] 2019 [cited 2019 Oct 23];4:240-50. Available from: http://www.jcmrp.eg.net/text.asp?2019/4/3/240/267688




  Introduction Top


The hippocampus plays an important role in the formation of new memories about experienced events [1].

Cadmium is a toxic agent that has many health hazards [2]. Food is the largest source of cadmium exposure through application of phosphate fertilizers [3]. Inhalation is another source of cadmium exposure as it is released in the air during the manufacture of numerous industrial products [4]. Smoking is another important source of cadmium exposure [5]. Cadmium can cross an intact blood barrier [6].

L-carnitine is an antioxidant that can cross an intact blood–brain barrier [7].


  Materials and Methods Top


The experiments were performed at the Human Anatomy and Embryology Department of Assiut University, Faculty of Medicine.

Drugs used in this experiment were as follows: cadmium chloride was dissolved in water and was given orally (4 mg/kg) [8]. The dose is considered sublethal [9]. L-carnitine (200 mg/kg/day) was given orally [10]. A total of 42 adult male rats were subdivided into four subgroups: group I was the control group (12 rats), which received no treatment.

Group II was administered cadmium (12 rats). Cadmium was given to the rats from the age of 30 days and continued daily till the age of 60 days. Group III was administered L-carnitine (sham control) (six rats). L-carnitine was given to the rats from the age of 30 days and continued daily till the age of 60 rats.

Group IV was administered cadmium + L-carnitine (12 rats). Drugs were given as previously described.

Animals were anesthetized by halothane and killed by cervical decapitation. Six rats were used for light microscopic study in each group (gallocyanin chrom alum stain). Moreover, six rats were used in each group for electron microscopy (for group III, only light microscopy was used).

Morphometric studies

In this work, estimation of thickness of the granular cell layer of the dentate gyrus and pyramidal cell layer of CA1 and CA3 fields was done. The thickness was measured after drawing the actual limit of the layer using the following equation: magnification = length in the picture/actual length. Cell count was done by using the Image Analyzer 'soft imaging system-Olympus company' on an area of 12 360 μm 2 for the granule cells and for the pyramidal cells in the CA3 and CA1 fields. Data were presented as mean ± SD. Statistical analysis of data was tested for significance using one-way analysis of variance and post-hoc test 'Tukey' through the computerized statistical package (Social Package of Social Scientists, IBM Incorp., New York, USA) 'SPSS.' Finally, significance was considered according to the P value level of significance: P value more than 0.05 → no significance, P value less than 0.05 → significant, and P value less than 0.01 → highly significant.


  Results Top


Dentate gyrus

In group I: light microscopic study demonstrated that the dentate gyrus appears to be distinguished into three layers: outer molecular layer, intermediate granular cell layer, and inner polymorphic layer [Figure 1]. The granule cells have oval to round nuclei with scanty cytoplasm [Figure 2]. The ultrastructural study shows that it contains a round euchromatic nucleus with prominent nucleolus. The nucleus is surrounded by a thin rim of cytoplasm that contains numerous mitochondria, free ribosomes, and rough endoplasmic reticulum [Figure 3].
Figure 1: A coronal section of hippocampus of an adult control rat. Molecular layer (ML), granular cell layer (GL), polymorphic layer (PL), alveus (A), stratum oriens (SO), stratum pyramidale (SP), stratum radiatum (SR), stratum lacunosum moleculare (LM), and subiculum (S). Gallocyanin, ×40.

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Figure 2: A semithin section of the dentate gyrus of a control adult rat showing the granular cell layer (GL). The granule cells contain large round nuclei (arrow heads). Molecular layer (ML) and polymorphic layer (PL). Toluidine blue, ×400.

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Figure 3: An electron photomicrograph of granule cell of an adult control rat. The cell has a round euchromatic nucleus (N). The nucleus is surrounded with thin rim of cytoplasm containing mitochondria (M), rough endoplasmic reticulum (rER) and free ribosomes (R). ×10 000.

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In group II: light microscopic examination of granule cells shows that most of the cells appeared swollen with faint cytoplasm. Some cells have darkly stained nuclei and vacuolated cytoplasm [Figure 4]. Electron microscopic (EM) examination revealed that the nucleus has peripheral chromatin condensation. The cytoplasm appeared to be rarified with the presence of damaged mitochondria and lysosomes. Marked loss of free ribosomes could be revealed [Figure 5].
Figure 4: A semithin section of the dentate gyrus of an adult rat treated with cadmium. Many of the granule cells appeared to be swollen with faint cytoplasm (open arrow heads). Some cells have darkly stained nuclei and vacuolated cytoplasm (arrows). Toluidine blue, ×400.

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Figure 5: An electron micrograph of granule cell in an adult rat treated with cadmium. The nucleus (N) shows peripheral chromatin condensation. The cytoplasm appears to be rarified with damaged mitochondria (M) and lysosomes (L). ×10 000.

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In group III: light microscopic examination of the granule cells showed that they appeared nearly similar to those of the control [Figure 6].
Figure 6: A coronal section of the dentate gyrus of an adult rat treated only with L-carnitine showing the granule in the granular cell layer (GL) contain large round vesicular nuclei (arrow heads). Molecular layer (ML) and polymorphic layer (PL). Gallocyanin, ×400.

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In group IV: light microscopic examination showed the granule cells similar to those of the control, with a few cells having darkly stained nuclei and vacuolated cytoplasm [Figure 7]. EM examination showed that they have round euchromatic nuclei with prominent nucleoli. The cytoplasm had many free ribosomes, mitochondria, some vacuoles, and dilated rough endoplasmic reticulum [Figure 8].
Figure 7: A semithin section of the dentate gyrus of an adult rat treated with both cadmium and L-carnitine showing most of the granule cells similar to those of the control (arrow heads). Some cells have darkly stained nuclei (arrows). Toluidine blue, ×400.

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Figure 8: An electron photomicrograph of granule cell of an adult rat treated with both cadmium and L-carnitine. The cell has a round achromatic nucleus. The cytoplasm contains free ribosomes (R), mitochondria (M), some vacuoles (V), and dilated rough endoplasmic reticulum (rER). ×10 000.

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Morphometric results

Dentate gyrus

Thickness: there is decrease in the thickness of the granular cell layer of the dentate gyrus in the adult rats treated with cadmium. This decrease in the thickness is statistically highly significant (P < 0.01) [Table 1] and [Histogram 1].
Table 1: Dentate gyrus thickness at the site of the crest in the albino rats (in μm)

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There is increase in the thickness of the granular cell layer of the dentate gyrus in the adult rats treated with L-carnitine. This increase in the thickness is statistically insignificant (P > 0.05) [Table 1] and [Histogram 1].

There is decrease in the thickness of the granular cell layer of the dentate gyrus in the adult rats treated with both cadmium and L-carnitine in comparison with those of the control group. This decrease in the thickness is statistically insignificant (P > 0.05). However, the thickness of the granular cell layer of the dentate gyrus of this group in comparison with those treated with cadmium is increased. This increase in thickness is highly significant (P < 0.01) [Table 1] and [Histogram 1].

Cell count

There is decrease in mean number of the granular cells of the dentate gyrus in adult rats treated with cadmium. This decrease in the mean number is statistically highly significant (P < 0.01) [Table 2] and [Histogram 2].
Table 2: Dentate gyrus cell count (per an area 12 360 μm2)

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There is slight increase in the mean number of the granular cells of the dentate gyrus in the adult rats treated with L-carnitine. This increase in the mean number is statistically insignificant (P > 0.05) [Table 2] and [Histogram 2].

There is decrease in the mean number of the granular cells of the dentate gyrus in the adult rats treated with both cadmium and L-carnitine in comparison with those of the control mothers. This decrease in the mean number is statistically highly significant (P < 0.01). However, the mean number of the granular cells of the dentate gyrus of this group in comparison with those of the cadmium-treated adult rats is increased. This increase in the mean number is statistically highly significant (P < 0.01) [Table 2] and [Histogram 2].

CA3 region

In group I: nissl-stained sections show that the pyramidal cells of the CA3 field have large round nuclei and prominent nucleoli [Figure 9]. The ultrastructural study shows that it has large round nucleus with fine granular chromatin. The surrounding cytoplasm is rich in the rough endoplasmic reticulum, free ribosomes, and mitochondria [Figure 10].
Figure 9: A semithin section of CA3 field of a control adult rat showing the stratum pyramidale (SP). The pyramidal cells are triangular in shape with large round nuclei (arrow heads). Toluidine blue, ×400.

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Figure 10: An electron photomicrograph of the CA3 pyramidal cells of an adult control rat showing a large pyramidal cell containing large round nucleus (N) with fine granular chromatin. The cytoplasm contains mitochondria (M), rough endoplasmic reticulum (rER) and ribosomes (R). ×3600.

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In group II: examination of the pyramidal cells in CA3 field of the hippocampus showed the presence of many cells with darkly stained nuclei and vacuolated cytoplasm [Figure 11]. EM study revealed that the nucleus had fine dispersed chromatin. The cytoplasm showed marked loss of free ribosomes, presence of dilated rough endoplasmic reticulum, and many lysosomes [Figure 12].
Figure 11: A semithin section of CA3 field of an adult rat treated with cadmium. Many of the pyramidal cells in the stratum pyramidale (SP) appear to have darkly stained nuclei and vacuolated cytoplasm (arrows). Toluidine blue, ×400.

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Figure 12: An electron micrograph of CA3 pyramidal cell of adult rat treated with cadmium showing the cytoplasm surrounding the nucleus (N) with marked loss of free ribosomes (R), dilated rough endoplasmic reticulum (rER), and lysosomes (L). ×3600.

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In group III: light microscopic examination of the pyramidal cells of CA3 field showed that they appeared nearly similar to those of the control [Figure 13].
Figure 13: A coronal section of CA3 field of an adult rat treated with L-carnitine showing the stratum pyramidale (SP) with its pyramidal cells contain round vesicular nuclei (arrow heads). Gallocyanin, ×400.

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In group IV: examination of the pyramidal cells of CA3 field of the hippocampus showed normal appearance of most cells. A few cells had darkly stained nuclei [Figure 14]. EM study showed that the cells had normal appearance [Figure 15].
Figure 14: A semithin section of CA3 field of adult rat treated with both cadmium and L-carnitine. It shows normal appearance of most of the pyramidal cells (arrow heads) in the stratum pyramidale (SP). Few cells have darkly stained nuclei (arrow). Toluidine blue, ×400.

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Figure 15: An electron photomicrograph of CA3 pyramidal cell of an adult rat treated with cadmium and L-carnitine. It has a rounded nucleus (N) with fine chromatin. The cytoplasm contains mitochondria (M), dilated rough endoplasmic reticulum (rER), ribosomes (R), and vacuoles (V). ×3600.

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CA3 field

Thickness: there is decrease in the thickness of the stratum pyramidale of CA3 field in the adult rats treated with cadmium. This decrease in the thickness is statistically highly significant (P < 0.01) [Table 3] and [Histogram 3].
Table 3: CA3 thickness in the albino rats (in μm)

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There is increase in the thickness of the stratum pyramidale of CA3 field in the adult rats treated with L-carnitine. This increase in the thickness is statistically insignificant (P > 0.05) [Table 3] and [Histogram 3].

There is decrease in the thickness of the stratum pyramidale of CA3 field in the adult rats treated with both cadmium and L-carnitine in comparison with those of the control group. This decrease in the thickness is statistically insignificant (P > 0.05). However, the thickness of the stratum pyramidale of CA3 field of this group in comparison with those treated with cadmium is increased. This increase in thickness is highly significant (P < 0.01) [Table 3] and [Histogram 3].

Cell count

There is decrease in mean number of the pyramidal cells of CA3 in adult rats treated with cadmium. This decrease in the mean number is statistically highly significant (P < 0.01) [Table 4] and [Histogram 4].
Table 4: CA3 cell count (per an area 12 360 μm2)

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There is increase in the mean number of the pyramidal cells of CA3 in the adult rats treated with L-carnitine. This increase in the mean number is statistically highly significant (P < 0.01) [Table 4] and [Histogram 4].

This decrease in the mean number is statistically highly significant (P < 0.01). However, the mean number of the pyramidal cells of CA3 of this group in comparison with those of the cadmium-treated adult rats is increased. This increase in the mean number is statistically highly significant (P < 0.01) [Table 4] and [Histogram 4].

CA1 region

In group I: examination of the pyramidal cells of CA1 field shows that they are less sized than those of CA3 field and are characterized by their elongated cell bodies and oval nuclei [Figure 16]. The ultrastructural study shows that it has an oval nucleus with fine granular chromatin and prominent nucleolus. The surrounding cytoplasm contains rough endoplasmic reticulum, many free ribosomes, and mitochondria [Figure 17].
Figure 16: A semithin section of CA1 field of a control adult rat. The pyramidal cells of the stratum pyramidale (SP) are rounded with oval nuclei (arrow heads). Apical dendrites (D) pass toward stratum radiatum (SR). Stratum oriens (SO). Toluidine blue, ×400.

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Figure 17: An electron photomicrograph of CA1 pyramidal cells of an adult control rat having oval nuclei (N) with fine granular chromatin. The cytoplasm contains mitochondria (M), rough endoplasmic reticulum (rER), and free ribosomes (R). ×3600.

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In group II: nissl-stained sections showed that many of pyramidal cells in CA1 field had darkly stained nuclei. It also showed the presence of some cells with pyknotic nuclei and vacuolated cytoplasm [Figure 18]. EM examination showed peripheral chromatin condensation in the nucleus. The cytoplasm had many vacuoles and damaged mitochondria. Marked loss of the free ribosomes could be revealed [Figure 19].
Figure 18: A semithin section of CA1 field of an adult rat treated with cadmium. It shows that many of the pyramidal cells in the stratum pyramidale (SP) have darkly stained nuclei (arrows). Some cells have pyknotic nuclei (open arrows). Toluidine blue, ×400.

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Figure 19: An electron micrograph of CA1 pyramidal cell in adult rat treated with cadmium showing the nucleus (N) with peripheral chromatin condensation and marked loss of free ribosomes (R) and damaged mitochondria (M) in the vacuolated cytoplasm (V). ×3600.

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In group III: light microscopic examination of the pyramidal cells of CA3 field showed that they appeared nearly similar to those of the control [Figure 20].
Figure 20: A coronal section of CA1 field of an adult rat treated with L-carnitine showing the stratum pyramidale (SP) with its pyramidal cells are large rounded (arrow heads) with prominent nucleoli. Stratum oriens (SO) and stratum radiatum (SR). Gallocyanin, ×400.

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In group IV: light microscopic examination of the CA1 pyramidal neurons revealed that most cells had normal appearance. Few cells with darkly stained nuclei and vacuolated cytoplasm were found to be present [Figure 21]. EM examination revealed that the cell had an oval nucleus with fine granular chromatin. The cytoplasm contained a lot of free ribosomes, mitochondria, and rough endoplasmic reticulum [Figure 22].
Figure 21: A semithin section of CA1 field of an adult rat treated with both cadmium and L-carnitine. It shows normal pyramidal neurons (arrow heads) in the stratum pyramidale (SP). Some cells with vacuolated cytoplasm and darkly stained nuclei (arrows). Toluidine blue, ×400.

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Figure 22: An electron photomicrograph of CA1 pyramidal cells of an adult rat treated with both cadmium and L-carnitine. The pyramidal cell has oval nucleus (N) with fine chromatin. The cytoplasm contains mitochondria (M), ribosomes (R), and dilated rough endoplasmic reticulum (rER). ×3600.

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EM study of synaptic terminals

In group I: EM examination of the presynaptic terminals making contact with pyramidal neurons revealed that it is filled with synaptic vesicles and mitochondria [Figure 23].
Figure 23: An electron photomicrograph showing synaptic contact (arrow head) on the pyramidal cells of the hippocampus of an adult control rat. The presynaptic terminal (arrow) has a lot of synaptic vesicles (SV) and mitochondria (M). ×14 000.

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In group II: ultrastructural study of the presynaptic terminal making contact with pyramidal cells showed marked loss of synaptic vesicles and the presence of damaged mitochondria [Figure 24].
Figure 24: An electron micrograph of the pyramidal cell in an adult rat treated with cadmium. It shows synaptic contact (arrow head) between the pyramidal cells and presynaptic terminal (arrow). Note damaged mitochondria (M) and marked loss of the synaptic vesicles (SV). ×14 000.

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In group IV: ultrastructural study of the presynaptic terminal making synaptic contact with the pyramidal neuron showed the presence of numerous synaptic vesicles and mitochondria with well-defined cristae [Figure 25].
Figure 25: An electron photomicrograph showing synaptic contact (arrow head) between presynaptic terminal (arrow) and pyramidal cell in an adult rat that was treated with both cadmium and L-carnitine. Note the presence of mitochondria (M) and numerous synaptic vesicles (SV). ×14 000.

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CA1 field

Thickness: there is decrease in the thickness of the stratum pyramidale of CA1 field in the adult rats treated with cadmium. This decrease in the thickness is statistically highly significant (P < 0.01) [[Table 5] and [Histogram 5].
Table 5: CA1 thickness in the albino rats (in μm)

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There is decrease in the thickness of the stratum pyramidale of CA1 field in the adult rats treated with L-carnitine. This decrease in the thickness is statistically insignificant (P > 0.05) [Table 5] and [Histogram 5].

There is decrease in the thickness of the stratum pyramidale of CA1 field in the adult rats treated with both cadmium and L-carnitine in comparison with those of the control group. This decrease in the thickness is statistically highly significant (P < 0.01). However, the thickness of the stratum pyramidale of CA1 field of this group in comparison with those treated with cadmium is increased. This increase in thickness is highly significant (P < 0.01) [Table 5] and [Histogram 5].

Cell count

There is decrease in mean number of the pyramidal cells of CA1 in the adult rats treated with cadmium. This decrease in the mean number is statistically highly significant (P < 0.01) [Table 6] and [Histogram 6].
Table 6: CA1 cell count (per an area 12 360 μm2)

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There is increase in the mean number of the pyramidal cells of CA1 in the adult rats treated with L-carnitine. This increase in the mean number is statistically highly significant (P < 0.01) [Table 6] and [Histogram 6].

There is increase in the mean number of the pyramidal cells of CA1 in the adult rats treated with both cadmium and L-carnitine in comparison with those of the control mothers. This increase in the mean number is statistically insignificant (P > 0.05). However, the mean number of the pyramidal cells of CA1 of this group in comparison with those of the cadmium-treated adult rats is increased. This increase in the mean number is statistically highly significant (P < 0.01) [Table 6] and [Histogram 6].


  Discussion Top


In this work, cadmium was studied because it is one of the most toxic heavy metals [11]. On entering the body, cadmium has detrimental effects on lung [12], reproductive system [13], liver [14], bone [15], blood [16], nervous system [16], and kidney [17].

For the control group of the adult age, our results were similar to that reported by El-Sokkary and Awadalla [18].

Electron microscopic examination revealed the normal structure of the granule and pyramidal cells. These results came in accordance with Helal et al. [19]. The synaptic terminals appeared to contain numerous vesicles responsible for neurotransmitters release as reported by Afifi and Embaby [20] and Chen et al. [21].

Histologic examination of the cadmium-treated group revealed the presence of degenerative changes in the principal cells and could be explained by the ability of cadmium to cross an intact blood barrier, and this agree with Goncalves et al. [6].

The mitochondrial damage was closely connected with a massive and rapid influx of calcium into the cells [22]. Vacuolations could be explained through lipid peroxidation theory, as stated by Afifi and Embaby [20]. The presence of dilated rough endoplasmic reticulum is attributed to lipid peroxidation, and this came in agreement with Afifi and Embaby [20].

In the hippocampal neurons synapses of rats treated with cadmium, it was observed marked decrease in the number of presynaptic vesicles and degeneration of the mitochondria. This came in accordance with Chen et al. [21].

On reaching the central nervous system, cadmium can induce microvessel injury which is attributed to oxidative stress [11]. In mitochondria, cadmium affects phosphorylation-oxidative enzymes and disrupts energy cycles [23]. Cadmium interferes with other metals such as calcium and zinc [11].

In addition, cadmium can impair neurogenesis, resulting in markedly reduced neuronal differentiation and axonogenesis, leading to neuronal cell death [24].

In this work, L-carnitine was given alone to the third experimental group (sham control), and by histological examination of this group, it was found that the results were more or less similar to those of the control group. This came in accordance with El-Masry et al. [10].

In this study, using L-carnitine together with cadmium revealed the protective effect of L-carnitine through histological study that revealed the normal appearance of the majority of the principal cells. The study of the ultrastructure of the principal cells revealed the improvement of the cells and in the synaptic terminals, and this agreed with Pettegrew et al. [25].

L-carnitine had an antioxidant effect, and this is attributed to its capability of fatty acid oxidation. This agreed with Ozmen et al. [26]. These findings are also supported by reports of others [7],[27],[10].

The present morphometric study demonstrates that the thickness of the principal cell layers of the three studies areas of the adult group came in accordance with Hussein and George [28]. The morphometric results support the histologic studies coming in agreement with Ramezani et al. [27].

Acknowledgements

Drug source: imported from India.

The authors thank Assiut University for financial support for electron microscopic studies.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14], [Figure 15], [Figure 16], [Figure 17], [Figure 18], [Figure 19], [Figure 20], [Figure 21], [Figure 22], [Figure 23], [Figure 24], [Figure 25]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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