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1. Introduction:- 

       Morphine (C17H19O13N) is one of the forty alkaloids present in opium from Papaver Somniferum and it is one of the strongest known analgesic compounds [1]. Researchers have reported that morphine may play important roles other than analgesia, such as suppression of immune responses [2] and modulation of tumor cell proliferation [3]. Morphine has been suggested to modulate cell death / survival in neurons of the central nervous system [1]. 
                                                                            
         Although opioids are reported to be effective in pain management, their toxic effects should be kept in mind during chronic usage [4] . As one of the addictive drugs, morphine is an increasing cause of death, morbidity, and lost productivity in society [5].

Despite widely known risks, nearly 90% of the drug-abusing women are of childbearing age [6]. Intrauterine morphine exposure is a risk factor for neurological and behavioral deficits in children. Morphine exposure caused a significant reduction of fetal weight and crown-to-rump length. Also, it was associated with premature birth, fetal and neonatal death, chromosomal aberrations, and growth retardation. Intrauterine morphine exposure induced a period of reduced placental blood flow during the second week of pregnancy [7].

           Chronic administration of morphine can induce neuronal apoptosis in the central nervous system [8]. Long term morphine use is considered a risk of increased cerebellum damage. Morphine sulfate induces cell death or necrosis in the rat cerebellum and modulating neurotransmitter system [9]. The cerebellum is characterized by a highly regular circuitry that often regarded as micro processing system [10]. This system plays a recognized role in motor phenomena but a controversial role in pain [11]. The cerebellum underlies the control of posture and balance, fine coordination of motor movement, adaptation of ocular responses, and learning of some conditioned behaviors [12].

       Thus, the purpose of this study was to determine the neurotoxic effect of morphine sulfate administration before and during  pregnancy on the cerebellum of 21-day- old infant mice by both light and transmission electron microscopic (TEM) examinations.
2. Materials & Methods:-
       This work was carried out in the Department of Forensic Medicine and Clinical Toxicology, Faculty of Medicine - Minia University. All aspects of animal care and treatment were carried out according to the local guide line of the Ethical Committee of Faculty of Medicine, Minia University.      
2.1. Drug:- 
       Morphine sulfate was obtained from MISR Company, Egypt as ampoules. Each one is 10 mg/ml morphine sulfate. Each ampoule is diluted by 9 ml normal sterile 0.9% saline. The morphine sulfate was intraperitoneally (i.p.) injected into each rat of the experimental (treated) group at a concentration of 10 mg/kg body weight daily.
2.2. Experimental design:
        Twenty adult female albino rats were used in this work with average weight of (180�20 gm). They were obtained from animal house in Faculty of Science, Minia University. They were housed in standard polypropylene cages (five rats/cage) and maintained under a controlled room temperature with 12:12�h light and dark cycle. All ats were provided with commercially available normal rat diet and water and libitum for two weeks before experiment for acclimatization.      
       Rats were divided into two experimental groups (10 rats each):
Group I: Rats fed on ordinary rat diet and received equivalent volume of saline intraperitoneally (i.p) daily.
Group II: Rats were given morphine sulfate in a dose of 10 mg/kg intraperitoneally (i.p) daily in separate cages for one week before mating (pre-breeding), then mating occurred by admixing female rats with males in the same cage until occurrence of pregnancy. Pregnancy was diagnosed by appearance of a vaginal plug in female vagina. During mating, female rats were treated by morphine sulfate for 2 weeks of breeding (mating). Morphine sulfate was given also for three weeks of pregnancy (GD 0-21) according to Golalipour & Ghafari [13]. The total time of morphine sulfate administration was 6 weeks (1 week of pre-breeding + 2 weeks of breeding + 3 weeks of pregnancy). 
After parturition, postnatal day zero (P0) was defined as the day of parturition. Subsequent postnatal days (e.g. P21) were defined as the number of full days that had elapsed since parturition. Mice offspring of group I mothers were named as group III (control group) and those of group II were named as group IV (experimental group). Both groups (III & IV) were kept alive for three weeks postnatal until complete growth of cerebella occurred. 
At the end of the experimental time, six mice pups of each control and experimental group were randomly selected and sacrificed by decapitation under light halothane anesthesia. Cerebella were rapidly dissected according to the anatomical landmarks and cut conveniently into small pieces. Then, they were processed for light and electron microscopic examinations.  
 
2.3. Histological examinations:
        Some pieces were fixed in 10 % neutral buffered formalin (PH 7.2), dehydrated in ascending series of ethanol, cleared in methyl benzoate, embedded in paraffin wax, deparaffinized with xylene, and stained with hematoxylin and eosin for light microscopic examination [14]. 
   Gallyas silver impregnation: 
        Preparation of alkaline silver iodide solution and the developer working solution was prepared according to the method described in Bancroft & Garble [14]. The sections were deparafinized and hydrated to distilled water. The sections were placed in 5% periodic acid for 5 minutes and then washed in distilled for 5 minutes twice. 
         Sections were placed in alkaline silver iodide solution for 1 minute, washed in 0.5% acetic acid for 10 minutes, and placed in developer solution for 5-30 minutes. Then,   they were replaced in 0.5% acetic acid for 10 minutes. The sections were washed again in distilled water and were placed in 0.1 gold chloride for 5 minutes. The sections were rinsed in distilled water and placed in 1% sodium thiosulphate for 5 minutes. Finally, the sections were washed in tap water, dehydrated, cleared, and mounted in DPX.  
Images of some slides were captured using an Olympus computerized microscope in bright-field mode in the Histology Department. 
   Electron Microscopic examination: 
       Smaller pieces; 1�1 mm in size, were fixed in 4% cold gluteraldehyde immediately after dissection of the animal for 24-48 hours. The specimens were then washed in phosphate buffer (PH 7.2) 3-4 times for 20 minutes each and post fixed in 1% OsO4 for 2 hours, after that washed in the same buffer 4 times. Dehydration by ascending grades of alcohol (30, 50, 70, 90, and 100% for 2 hours) was done and embedding in epon araldite mixture. 
        Semithin sections (0.5 um) were prepared and stained with Toluidine blue. Then, ultrathin sections (50-80 nm) were cut using Leica AG ultramicrotome, contrasted with lead citrate and uranyl acetate, to be examined by TEM 100 CX electron microscope, and photographed [14]. 
3. Results:
3.1. H&E results:

Examination of H&E sections of the control group, revealed the normal laminar organization of the cerebellar cortex which characterized by complex folding, which arranged in three successive layers, outer molecular (ML), middle Purkinje (PL) and inner granular layer (GL). The center of the fold showed area of white matter (Fig. 1-a). The ML had sparse population of neurons and formed of nerve cell processes with scanty glial cells. The PL, the middle layer, was formed of single row of large pyriform somata of Purkinje neurons with pale nuclei and prominent nucleoli. The GL was formed of large number of neurons with rounded large nuclei and scanty cytoplasm. Neuropil is a region between  HYPERLINK "http://en.wikipedia.org/wiki/Neuron" \o "Neuron" neuronal  HYPERLINK "http://en.wikipedia.org/w/index.php?title=Cell_body_(biology)&action=edit&redlink=1" \o "Cell body (biology) (page does not exist)" cell bodies in the  HYPERLINK "http://en.wikipedia.org/wiki/Gray_matter" \o "Gray matter" gray matter. It consists of a dense tangle of  HYPERLINK "http://en.wikipedia.org/wiki/Axon_terminal" \o "Axon terminal" axon terminals, dendrites, and  HYPERLINK "http://en.wikipedia.org/wiki/Glial_cell" \o "Glial cell" glial cell processes (Fig. 1-b). In the experimental group, normal laminar organization of the cerebellar cortex was maintained, morphine induced alterations were most pronounced in the PL. In some areas the ML had vacuolations especially in neuropil surrounding the Purkinje cells. The GL appeared darker with darker nuclei. The Purkinje cells lost their specific shaped appearance, decreased in size and numbers. Some Purkinje cell bodies showed irregular outline, shrunken elongated cell bodies, and pyknotic nuclei (Figs. 2a and 2b).

3.2. Silver impregnation:

The Hematoxylin and Eosin (H&E) stain is adequate for routine study of cellular details of neurons and glial cells, but does not stain the neuronal processes. Axons and dendrites are demonstrated best with silver stains in which ammoniacal silver is deposited on cytoskeletal components and then reduced to black metallic silver. Sections of the control group showed normal faintly stained cell bodies, apical dendrites, and axons (Fig. 3). In experimental group, some of the degenerated Purkinje cells became irregular and smaller, others became shrunken, and strongly argyrophilic, and also their dendrites were more densely argyrophilic. Wallerian-like degeneration was observed in the form of swelling, beading, and segmentation of some dendrites and fibers (Fig.4).

       3.3. Toluidine blue semithin sections: 

        Examination of semithin sections of control group revealed the normal histological structure of the cerebellar cortex. The Purkinje cell layer was formed of single row of large pyriform somata of Purkinje neurons with pale nuclei and prominent nucleoli. The granular layer was formed of large number of neurons with rounded dark nuclei and scanty cytoplasm, fibers and small capillaries (Fig. 5). In experimental group sections, Purkinje cells lost their normal appearance where some Purkinje cell bodies appeared with irregular outline, deeply stained cytoplasm, and hardly identified nuclei. Multilayer disposition of Purkinje cells was observed in some sections. Vacuolation of the cytoplasm of some glial cells and the surrounding neuropil were also observed. Granular cells showed dark stained shrunken cells (Fig. 6).


     3.4. Electron Microscopic Results:
      
           Examination of the cerebella ultrastructurally revealed that, Purkinje cells were distinguished by their position, large size of the somata, euchromatic nuclei, and well defined nucleoli. Intact myelinated axons with compact myelin containing normal mitochondria and neurofilaments were observed (Fig. 7). The cytoplasm was rich in organelles as numerous mitochondria, ribosomes and rough endoplasmic reticulum (Fig. 8). Granular cells were observed with their rounded heterochromatic nuclei and mere shell of cytoplasm containing few organelles. Intact myelinated axons were observed (Fig. 9).

        Morphine administration showed changes in the normal structure. Regarding the Purkinje cells, some cells had electron dense nuclei which contained compact chromatin. The cytoplasm became vacuolated with decreased organelles. Deformation of the plasma membrane with degeneration of the synapses was also observed (Fig. 10). Mitochondrial ultrastructural alterations were observed in the form of swollen degenerated mitochondria with damaged cristae. Some mitochondria appeared with dense matrix (Fig. 11). Abnormally myelinated axons were observed with distorted and decompacted myelin sheath with marked separation between its layers. The axoplasm of the degenerated axons contained abnormal mitochondria with damaged cristae. Degeneration of neurofilaments was observed to the extent that many axons devoided of neurofilaments and the remaining neurofilaments were rarefied and disorganized (Fig.12). Some astrocytes appeared with clear cytoplasm extended to its processes which ensheathed shrunken Purkinje cell which appeared with ill defined nuclear envelope and remnants of the nucleus (Fig. 13). Examination of granular neurons showed some shrunken granular cells with margination and condensation of nuclear chromatin (Fig. 14), or vacuolation of the cytoplasm of other cells (Fig. 15).

4. Discussion:- 

        Morphine abuse during pregnancy is one of the most important risk factors for an array of adverse pregnancy outcomes [15]. Many reports have demonstrated that consumption of morphine during pregnancy has been associated with delay and change in neural tube [16], basal ganglia [17], olfactory bulb (18), premature birth, fetal and neonatal death, chromosomal aberrations, decreased birth weights and growth retardation  [7 , 19].  
   
          It was also reported that morphine causes damage in layer II/III pyramidal neurons morphology in visual cortex [20], neural plate [21], olfactory cortex [22], hippocampus [23] and amygdaloid complex [24]. Moreover, it caused defects in formation and evolution of embryonic visual system, reduces lens development in rat embryos [25]. However, the precise effect of morphine on cerebellum has remained to be elucidated as little is known about it. So this study aimed to detect the effect of prenatal morphine exposure on cerebellum of a neonatal mice offspring.

The present study confirmed that administration of morphine to pregnant rat resulted in marked alterations in neonatal rat cerebellum. The most impressive alterations were located in Purkinje cell layer where Purkinje cells by H &E staining lost their specific shaped appearance, became shrunken, smaller in size, fewer in numbers and elongated with pyknotic nuclei which are in accordance with Bekheet et al. [9], Ghafari et al. [26] & Golalipour &HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/?term=Ghafari%20S%5Bauth%5D"  Ghafari, [13] .

The alterations in Purkinje cells structure can affect their function as Purkinje cells are the pivotal elements around which all the cerebellar circuits are organized by receiving information, processing it, and channeling towards efferent pathways [27]. These changes suggested that prenatal administration of morphine may cause degeneration of myelinated nerve fibers that induce Purkinje cells apoptosis and/or necrosis as morphine produces morphological alterations of astrocytes which increase Ca+2 ions with production of carbonyl oxidation that promote apoptosis and or necrosis in neurons [28]. 

           The resulted cerebellar neurotoxicity arised from the passage of morphine through blood placental barrier as according to the fetal programming hypothesis, the environment of mother�s body and uterus can alter the development of the fetus during particular sensitive periods, with a permanent effect on the set point of physiologic systems and the phenotype in later years [29]. The work examined neonatal rats2  brain on 21th day post-natally. This age was chosen as the neuronal morphology and synaptic connectivity finish developing during the third postnatal weeks, coincident with the final maturation of cerebellar-dependent behaviors [12]. 

Other possible mechanisms underlying the toxic cerebellar morphine effects were postulated. Opioids exposure blocks the proliferation and differentiation of neuroblasts and astroglia of the cerebellum [30] by preventing of DNA synthesis [31]. Additionally, Oehmichen et al. [32] reported reduction in Purkinje cells size and numbers in morphine chronic users. These observations receive a marked support from the reports issued by HYPERLINK "file:///I:\\morphine\\11111.htm" \l "bib23"Hauser et al.  [33] who reported that morphine inhibits Purkinje cell survival and dendritic differentiation in organotypic cultures of mouse cerebellum. 

Silver impregnation revealed degeneration in Purkinje cells which became irregular and smaller. Both cell bodies and their dendrites became strongly argyrophilic. Transmission electron microscopy examination revealed abnormality and changes in all components of Purkinje cells where ultra-structures of nuclei, cytoplasm, plasma membrane, synapses, mitochondria, axons and its myelin sheath, axoplasm, neurofilaments were markedly affected and apparently different from control that highly agree with Bekheet et al.[9].

      Damage of mitochondria usually leads to cell death as it reflects its role as a central organelle mediating cellular death [34]. Destruction of mitochondrial cristae depletes the energy production which leads to release of proapoptotic proteins that activates Caspase-3 and initiates DNA fragmentation [35].�The observed nuclear damage could be interpreted as the beginning of nuclear fragmentation which indicating cell death.

Other marked histological changes in the current work were still observed both in molecular and granular cell layers by different staining and examination techniques that are in line with Bekheet et al. [9] & Golalipour &HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/?term=Ghafari%20S%5Bauth%5D"  Ghafari, [13].  HYPERLINK "file:///I:\\morphine\\11111.htm" \l "bib63"Zagon & McLaughlin,  [36] explained the previous changes by the fact that morphine decreased DNA synthesis that resulted in cell death in granular layer cells neuroblasts in rat cerebellum. 

5. Conclusion & recommendation:

              This study gave a clue that prenatal morphine use by pregnant mothers resulted in detrimental effects on neonatal cerebellum. So this work can predict that the resultant cerebellar changes may be permanent throughout coming years where they were found on 21th days postnatally. Such alterations could affect important physiological functions as cerebellum controls many aspects of behavior as reward, pleasure, instinct, sex drive, food drive, and emotions. If affected; it may cause abnormal behaviors specific to its structure as stumbling and random motion of eyes. So, it is recommended that all females during their birth-bearing age must avoid administration of morphine for any reason.

6. References:

1. Zhang  U, Chen Q,  Yu LC (2008)  Morphine: a protective or destructive role in neurons?. Neuroscientist  14(6): 561-570.

    2. Sacerdote  P  (2006)  Opioids and the immune system. Palliat. Med. 20: 9-15.
 
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4. Bekheet   SH (2010)   Morphine sulphate induced histopathological and histochemical changes in the rat liver. Tissue cell 42(4): 266-72. 

5. Nestler EJ (2004) Historical review: molecular and cellular mechanism of opiate and cocaine addiction. Trends Pharmacol Sci. 25: 210-218. 

6. Vucinovic M, Roje D, Vucinovic Z, Capkun V, Bucat M, et al (2008) Maternal and Neonatal Effects of Substance Abuse during Pregnancy: Our Ten-year Experience. J. Yonsei Med. 49(5): 705�713. 
7. Sadraie SH, Kaka GR, Sahraei H, Dashtnavard H, Bahadoran H, et al (2008) Effect of maternal oral administration of morphine sulphate on developing rat fetal cerebrum: a morphometrical evaluation. Brain Res. 1245: 36-40. 

8. Atici S, Cimel L, Cinel I, Doruk N, Aktekin M, et al  (2004)  Opioid neurotoxicity: comparison of morphine and tramadol in an experimental rat model. Int. J. Neurosci. 114: 1001-1011.

9. Bekheet SH, Saker SA, Abdel-Kader AM , Younis AE  (2010) Histopathological and biochemical changes of morphine sulfate administration on the cerebellum of albino rats. Tissue cell 42(3): 165- 175.

10. Middleton F, Strick P (1998) The cerebellum: an overview. Trends Neurosci  21: 367-369. 

11.  Saab CY, Kawasaki M, Al-Chaer ED, Willis WD (2001) Cerebellar cortical stimulation increases spinal visceral nociceptive responses. Journal of Neurophysiology 85(6): 2359-2363. 

12. McKay BE and Turner RW (2005) Physiological and morphological development of the rat cerebellar Purkinje cell. J Physiol. 567(3): 829�850.

13. Golalipour MJ, Ghafari S (2012) Purkinje cell loss in offspring due to maternal morphine sulfate exposure: a morphometric study. Anat. Cell Biol. 45(2): 121-127. 

14. Bancroft JD, Garble M (2007) Theory and practice of histological techniques, 6th ed. Churchill Livingstone.
15.  Dehghan M,  Jafarpour  M  , Mahmoudian A (2010)  The effect of morphine administration on structure and ultrastructure of uterus in pregnant mice. Iranian Journal of Reproductive Medicine  8 (3): 111-118.
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18. Saeedabadi  S, Sadooghi M, Sahraei H, Bahadoran H, Fahanik B J et al (2008)  Effects of oral morphine on the development of olfactory bulb in rat embryo. The Scientific Journal of Arak Medical University 11: 1-8.

19. Nettleton R, Wallisch M , Olsen G (2008)  Respiratory effects of chronic in utero methadone or morphine exposure in the neonatal guinea pig. Neurotoxicology and Teratology 30: 448�454.
20. HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Mei%20B%5BAuthor%5D&cauthor=true&cauthor_uid=19670310"Mei B, HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Niu%20L%5BAuthor%5D&cauthor=true&cauthor_uid=19670310"Niu L, HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Cao%20B%5BAuthor%5D&cauthor=true&cauthor_uid=19670310"Cao B, HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Huang%20D%5BAuthor%5D&cauthor=true&cauthor_uid=19670310"Huang D , HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou%20Y%5BAuthor%5D&cauthor=true&cauthor_uid=19670310"Zhou Y (2009)  Prenatal morphine exposure alters the layer II/III pyramidal neurons morphology in lateral secondary visual cortex of juvenile rats. HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/19670310" \o "Synapse (New York, N.Y.)."Synapse 63(12): 1154-61.
21. Nasiraei-Moghadam S, Bahadoran H, Saeedabady S, Shams J, Sahraei H (2009): Oral administration of morphine delay neural plate development of rat embryos. Physiology and Pharmacology 12: 314-319.
22. Fahanik-babaei J, sadooghi M, zardooz H, sahraei H (2010) maternal oral morphine consumption delays olfactory cortex development in Wistar rats during embryonic period. Journal of rafsanjan university of medical sciences 9 (1): 3-14.
23. Ramazani M, Hamidi E, Haji M, Bahadoran H,  Sahraei H (2010) The effect of oral morphine consumption on hippocampus development in Wistar rats embryo. Kowsar Medical Journal 1(1): 11-15.

24. Ramazani  M,  Ameli H, Hakimi G, Bahadoran H, Sahraei H (2010) Reduction of cell size in amygdaloid complex of the Wistar rat embryos after oral morphine consumption. Physiology and Pharmacology 14 (2): 181 -190.

25. Kazemi M, Tekieh E, Sadeghi-Gharachdaghi S, Ghoshoni H, Zardooz H, et al (2012)  Oral morphine consumption reduces lens development in rat embryos. Basic and Clinical neuroscience 3 (3): 16-23.

26. Ghafari S, Roshandel D , Golalipour M (2011)  Effect of intrauterine morphine sulfate exposure on cerebellar histomorphological changes in neonatal mice. Folia Neuropathol. 49(4): 328�334.

27. Biran V, Verney C, Ferriero DM (2012) Perinatal cerebellar injury in human and animal models. Neurology Research International 3 (3): 1-9.

28. Hauser KF, Harris-White ME, Jackson JA, Opanashuk LA, Carney JM (1998)  Opioids disrupt Ca2+ homeostasis and induce carbonyl oxyradical production in mouse astrocytes in vitro: transient increases and adaptation to sustained exposure. Exp. Neurol. 151:70�76.

29. Gutteling B, De Weerth C,  uttelaar J (2007)  Prenatal stress and mixed-handedness. Pediatric Res. 62 (5): 586-590.

30. Hammer RP, Jr R,  Seatriz JV (1989)  Effects of opiates on brain development. Neurotoxicology 10: 475�483.

31. Hauser KF, Houdi AA, Turbek CS, Elde RP , Maxson W (2000) 3rd Opioids intrinsically inhibit the genesis of mouse cerebellar granule neuron precursors in vitro: differential impact of mu and delta receptor activation on proliferation and neurite elongation. Eur. J. Neurosci. 12: 1281�1293.

32. Oehmichen M, Meissner C, Reiter A, Birkholz M (1996) Neuropathology in non-human immunodeficiency virus-infected drug addicts: hypoxic brain damage after chronic intravenous drug abuse. Acta Neuropathol. 91: 642-6.
33. Hauser KF, Gurwell JA, Turbek CS (1994)  Morphine inhibits Purkinje cell survival and dendritic differentiation in organotypic cultures of the mouse cerebellum. Exp. Neurol. 130: 95�105.
34. Dmbska M, Gajkowska B (2002) Hypoxic damage of the cerebellum in 7-day-old rats. Ultrastructural and histochemical study. Acta Neurobiol. Exp. 62: 45�49.
35. Gajkowska B, Motyl T, Olszewska-Bdarczuk H, Gniadecki R,  Koronkiewicz M (2000)  Structural association of Bax with nuclear matrix and cytomatrix revealed by embedment-free immunogold electron microscopy. Cell Biol. Monogr. 24: 649�656.

36. Zagon IS , McLaughlin PJ (1991) Identification of opioid peptides regulating proliferation of neurons and glia in the developing nervous system. Brain Res. 542: 318�323.






 














                                                                 



 


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