The Effect of a Magnesium Deficient Diet and Cortisone on the Growth of the Rat Incisor MICHAEL L. KIELY and L. V. DOMM

Departments of Anatomy, Loyola University of Chicago School of Dentistry and Stritch School of Medicine, Maywood, Illinois 60153, USA Incisors of Mg-deficient rats showed a marked inhibition of eruption and a decrease in mitoses of apical tissues. Cortisone administration resulted in some increase in eruption rate and cell division though these remained below the values of Mg-supplemented controls. An improvement in gross condition and a less severe histopathology of incisor tissues were also observed in cortisone-treated rats. J Dent Res 56(12): 1577-1585, December 1977. It is now well known that cortisone will accelerate the eruption of the rat incisor. In addition to stimulating this rate in the adult rat,' -3 injection of this steroid causes precocious eruption in the newborn4-6 and a further increase in the accelerated rates of amputated incisors.7 The greatly inhibited rates of hypophysectomized and adrenalectomized rats are also very significantly increased following cortisone treatment.'13 Despite these and other similar studies, the mechanism by which cortisone enhances eruption in the rat incisor is not known. Recent studies,89 in which cortisone administration was found to increase the number of colchicine-arrested and 3H-thymidine-labeled cells in the apical tissues of the normal and adrenalectomized rat incisor, indicate a mechanism involving cell renewal. Magnesium (Mg) is an essential requirement for normal tissue growth and function. It activates numerous enzymes including those involved in the synthesis of nucleic acids and protein.'0-'1 Incisors of rats maintained on a Mgdeficient diet reveal a marked reduction in eruption rate. 14.'5 Histologically, these teeth show atrophy of the formative, basal tissues and degenerative changes in the odontoblasts and enamel epithelium with disturbances in calcification.'6 '9 These alterations become more severe as the deficiency progresses. However, Received for publication August 9, 1976. Accepted for publicationi February 22, 1977. This investigatiorn "as supported, in part, bh NIH Research Grant DE-00694 and a NIH General Research Support Grant. *General Biochemicals, Chagrin Falls, Oh.

when the incisor is periodically amputated, thus resulting in an acceleration of eruption similar to that following cortisone injection, these tissue changes are much less apparent.20 The present study evaluates the influence of cortisone on rate of eruption, cell proliferation, and histology of the rat incisor during the prevailing and inhibitory conditions of a Mg deficiency in an effort to gain additional information with respect to the mechanism underlying the eruptive process. Materials and Methods

Thirty-six female rats, age 40 days were employed. They were divided into 3 groups: Group A: 12 rats maintained on a Mg-deficient diet* containing less than 1.0 mg% of Mg (originally prepared for Heggtveit et al2'). They received distilled water ad libitum. Group B: 12 animals maintained on an identical diet supplemented with Mg (63 mg%) and tap water ad libitum. Group C: 12 rats maintained on a standard rat diet containing 260 mg% of Mg and tap water ad libitum. Weekly measurements on eruption rates of maxillary incisors were made for a period of 5 weeks beginning at onset of diet restruction. Eruption rates were determined after a modification of a method described by Baume, Becks, and Evans." At the end of this period, one half of the animals in each group received 6 mg/kg of cortisone in a single daily injection. The injections and measurements were continued for 4 weeks. Three hours prior to sacrifice, all rats were given a single injection of colchicine (1.0 mg/kg). The animals were sacrificed by decapitation, preceded by an intraperitoneal injection of Nembutal (pentobarbital sodium). The maxillary incisors were immediately recovered and fixed for 48 hours in neutral buffered 10% formalin and decalcified in a sodium citrateformic acid solution. They were sectioned sagittally at 5 ,Am and stained with hematoxylin and eosin. Observations were made on the mitotically 1577

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1578

active cells of the incisors. Cell counts, on four cell layers of the basal, formative loop were made after a method previously described by Domm and Kiely.8 These layers were the stratum intermedium, preameloblast, preodontoblast, and adjacent pulp cells. All prophase and colchicine-arrested metaphase figures were counted. No anaphase or telephase stages were present. The data on eruption rates were statistically analyzed by means of the Student t test. The two-way analysis of variance test was employed to evaluate cell count data. Differences were considered significant at the 5% level of probability. Results GROSS OBSERVATIONS. - The experimental

rats exhibited the classic Mg-deficient syndrome as described elsewhere.2'24 They developed hyperemia of the ears and around the eyes, dull fur with loss of hair, epidermal sores, slow weight gain, and irritability. These conditions became progressively worse. In addition the animals became extremely weak and incoordinate, and they developed spontaneous convulsive seizures with respiratory difficulties usually resulting in death. The cortisone-treated Mg-deficient rats, however, showed a notable improvement. By the end of the first week of treatment, a remission or complete disappearance of the Mg-deficiency syndrome had occurred. The rats were definitely less irritable and convulsions did not occur. All six rats survived the experiment,

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OF Mg-DEFICIENCY & CORTISONE ON RAT INCISOR Voel. 56 No.ENFFECT 12

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Fi(; 3. Section through basal region of a maxillary incisor from a magnesium deficient rat (cf. Fig 2.) the cervical loop (cl), enamel epithelium (ec), and odontoblast layer (o) show severe degenerative changes. Note also the disturbed dentin (d) which is stratified, overgrown and irregular in appearance. Orig mag

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5 and 6), indicating a disturbance in calcificaIt was also folded, overgrown, and irregular in width (Fig 3). In the more severe cases, the odontoblasts were either disorganized and atrophied or completely degenerated with a disturbance in dentin formation. In comparison, the incisors of cortisone-treated deficient rats exhibited dentin with less overgrowth, folds, and irregularity (Fig 4). The odontoblasts, while disorganized and atrophied, did not show the degenerative changes observed in some of the untreated deficient incisors. In the untreated animals, the pulp cavity was greatly reduced in size due to an excessive width of the dentin. Plugs or spurs of dentin or dentin-like material were frequently seen in the pulp cavities of these rats. Ihe dentin of cortisone treated normal or tion.

4

Mg-supplemented rats appeared to be normal. The histology of enamel epithelium in Mgdeficient rats ranged from a slight atrophy to an extreme hypoplasia and degeneration along the length of incisor. In some areas, the cells of enamel epithelium were greatly reduced in height and number so that, even though they were recognizable, it was quite evident that they were severely retarded. Patches of completely degenerated and disorganizedl epithelium were also found. This condition was especially evident apically (Fig 3) although such areas also occurred further coronally (Fig 6). These areas were completely unrecognizable and were filled with connective tissue and epithelial

remnants.

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'I

KIElY & DOMM

1582

filled with an eosin stained amorphous material and vascular elements. This condition may indicate an abortive attempt at enamel formation or simply an accumtulation of degenerative debris. In some of the untreated deficient incisors, extreme degenerative changes were seen along their entire length. While the above-described changes were found in the incisors of the cortisone-treated deficient rats they were very frequently less severe in comparison to the untreated deficients (Figs 4 and 7). The Mg-supplemented animals had essentially normal incisor tissues except for the ameloblasts and the cells of the papillary layer which were slightly reduced in height. I)iscussion The observation on the severe reduction in rate of incisor eruption in Mg-deficient rats is

FIG 6. Section through labial portion of a maxillary inicisor from a magnesium deficient rat (cf. Fig 5.) Note stratification of dentin (d), disorganization of odontoblasts (o), and degeneration of enamel epithelhum (ee). (es) enamel space. Orig

Dent Res December 1977

consistent with the findings of others.'4 '5 However, an acceleration of these rates as the result of cortisone administration has not previously been reported. Nevertheless, a similar result has shown the rate of eruption of unimpeded mandibular incisors to be greater than the impeded rate in Mg-deficient rats.'5 In either case, these results might be anticipated, since numerous studies have reported an acceleration in the rate of both normal and experimental incisors cut out of occlusion or under the influence of cortisone. A less expected result was that the tissues of the incisors of cortisone-treated deficient rats showed much less histopathological change when compared to the untreated deficient ones. Weinreb, Kusner, and Michaeli25 reported a quite similar effect since the unimpeded incisors of Mg-deficient rats had tis-

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ever, not as severe as

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Vol. 56 No. 12

EFFECT OF Mg-DEFICIENCY & CORTISONE ON RAT INCISOR

1583

TABLE 4 Two-WAY ANALYSIS OF VARIANCE OF THE DATA SHOWN IN TABLE 3 Source of Variation

Sum of Squares

Degrees of Freedom

Diet Cortisone Within (Error) Totals

2200.01 42.61 4004.14

Stratum Intermedzum 2 1100.01 1 42.61 200 20.02

Diet Cortisone Within (Error) Totals

5058.53 41.09 10776.67

Diet Cortisone Within (Error) Totals

235.99 36.20 1913.75

6246.76

15876.29

2185.94

Mean Squares

203 Preamelo blasts 2 2529.27 1 41.09 200 53.88 203 Preodontoblasts 2 118.00 36.20 200 9.57 203

Variance Ratio (F)

p Value

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Pulp Cells Diet Cortisone Within (Error) Totals

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200

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1

sues that were essentially normal. On the basis

of these findings, they concluded that the histological changes associated with Mg-deficiency are primarily due to an increase in occlusal pressure and not the direct result of Mg deprivation. However, the rates of the unimpeded teeth remained markedly below the impeded rates of the control incisors as did the rates of cortisone-treated deficient rats in the present experiment. It is, therefore, quite apparent that some factor, presumably related to the deficiency, is preventing these incisors from reaching control rates and beyond. Though the prevailing conditions of the Mgdeficiency doubtlessly hinder the incisor tissues from responding fully to cortisone, it seems unlikely that the effect of this hormone on eruption is related to changes in biting forces since the accelerated eruption of incisors periodically amputated shows a further increase following cortisone injection.7 Moreover, a precocious eruption of incisors from fetal and newborn rats occurs as a result of cortisone treatment.4 The dramatic improvement in gross appearance and behavior of the Mg-deficient rats following cortisone administration would suggest a systemic effect exerted by this steroid. A similar phenomenon was observed in young Mg-deficient rats treated with 2.5 mg of cortisone dai-

1265.59 170.86 24.39

51.89

7.01

< 0.001 < 0.01

ly for 12 or 28 days started at the beginning of the deficiency.25 In rats treated daily following the onset of convulsions, these seizures and the accompanying hyperirritability were absent for a period of 10 days. As in the present study, the survival rate was markedly improved in all cortisone-treated groups. It is possible that cortisone therapy brings about a more effective and rapid utilization of skeletal Mg in the deficient rat. Aikawa et a12' reported an increase in uptake of 2"Mg by the heart, appendix, and muscle tissue in the rabbit following cortisone injection. It has been shown that even during an acute deficiency in the rat, bone acts as a reservoir for Mg and apparently supplies this mineral to the soft tissue.27"" As the deficiency progressed, a severe loss of Mg was noted in the skeleton while it remained at a fairly constant level in soft tissues. In the present study, eventual depletion of bone Mg may have occurred in the cortisone-treated deficient rats since a deterioration in their condition and a reduction in eruption rates wre observed by three weeks. The data on mitotic cell counts would seem to support the possibility that the action of cortisone on incisor tissue is a direct one. Not only was there an increase in the average number of mitotic figures in the cortisone-treated Mg-deficient incisors but also in the treated normal and

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1584

KIELY & DOMM

Mg-supplemented groups, where sufficient amounts of Mg are presumably available to the tissues in order to activate the enzymes involved in the synthesis of nucleic acids and proteins preparatory to cell division. These results are in agreement with a previous study in which the apical tissues from incisors of cortisone-treated, adrenalectomized rats showed significantly more 3H-thymidine labeled cells than those of untreated adrenalectomized or normal rats.9 Recent results (unpublished) from our laboratory show a marked increase in the uptake of 3H-thymidine by the growing end of mandibular incisors from cortisone-treated normal and Mg-deficient rats as measured by liquid scintillation spectrometry. As in the present study, the values of Mg-deficient incisors were substantially below those of the normal. Ness and Smale29 observed a substantial increase in the mitotic index of pulp cells in rabbit incisors whose eruption was accelerated due to an absence of occlusal contact. The same result was reported for the rat incisor and, in addition, the rate of cell production of the preameloblasts had doubled as had the unimpeded eruption rate.30 These results show a direct correlation between the rate of cell proliferation and the rate of eruption. Our results are in agreement in that we also observed a direct proportionality between the rates of eruption and cell division. Since Mg is an indispensable mineral in basic cellular function, it is not surprising to find significant pathology due to its deficiency in such tissues as the kidney,3' cerebellum,32 bone,33'34 cardiac and skeletal muscle,21'35 gastric muco sa,36 thymus, spleen,37 and erythrocytes.38 Because of these widespread effects, caution must be exercised in the interpretation of its effects on such tissues as the rat incisor. However, since much is known concerning the key role of Mg in biochemical processes, its use as a tool is quite valuable in efforts to gain further insight into the mechanism of tooth eruption. Conclusions Young female rats maintained on a Mg-deficient diet revealed a significant decrease in the rate of eruption of maxillary incisors as compared to rats fed a Mg-supplemented diet or rats given a standard diet. Cortisone administration resulted in a significant increase in eruption rate in each of these three groups. However, the rate in Mg-deficients remained markedly below that of Mg-supplemented rats. Cell count data revealed a marked reduction in number of mitoses in the apical tissues of in-

j Dent

Res December 1977

cisors of Mg-deficient rats. Following cortisone administration, a consistent and significant increase in cell division occurred in each of the three groups studied. Again, the increase in Mg-deficient incisors was of less magnitude than that of Mg-supplemented rats. The deprived rats showed the characteristic manifestations of Mg-deficiency: hyperemia, epidermal sores, hair loss, slow weight gain, diarrhea, soft and chalky incisors, hyperirritability, and convulsive seizures resulting in death. Cortisone administration resulted in a very noticeable improvement in these conditions. Histologically, incisors of Mg-deficient rats showed cellular atrophy and degeneration, disturbances in formation and mineralization of dentin and enamel and calcification of pulp cavity. These changes were most severe in the untreated deficient rats. Cortisone appeared to exert a general ameliorative effect on the tissues of the deficient incisors. The results suggest the effect of cortisone on incisor eruption to be mediated through a stimulation of cell division. The athliors graicnfull acknoMledgc ee tIlichial asiiltancc o'l Mrs. Lucia Snelite anid the is ping of Mlrs. Tinia Shiock.

References 1. DoMM, L. V., and MARZANO, R.: Observations on the Effects of Certain Hormones on the Growth Rate of the Incisor of the Albino Rat, abstract, A nat Rec 118:383, 1954. 2. GARREN, L., and GREEP, R. O.: Effect of Adrenal Cortical Hormones on Eruption Rate of Incisor Teeth in the Rat, Endocrtnol 66:625-628, 1960. 3. DoMM, L. V., and WELLBAND, W. A.: Effects of

Adrenalectomy, Thyroidectomy, Thyro-adrenalectomy and Cortisone on Eruption Rate of Incisors in Adult Female Rats, Proc Soc Exp Bzol Med 107:268-272, 1961. and ANGRIST, A. A.: Comparative Effects of ACTH, Cortisone, Corticosterone, Desoxycorticosterone, Pregnenolone on Growth and Development of Infant Rats, Proc Soc Exp Bzol Med 77:215-218, 1951. LEROY, P., and DoMM, L. V.: Eruption Precoce des Incisives Superieures et Inferieures des Jeunes Rats Traites a la Cortisone, Ann Endocrinol 16:773-784, 1955. GOLDSMI-FH, E. D., and Ross, L.: A Histochemical and Histological Study of the Effects of Cortisone on the Lower Incisors of Fetal and Postnatal Rats, Acta Eodocrinol 22:23-41, 1956. WELLBAND, W. A., and DoMM, L. V.: Effect of Cortisone, Amputation and Food Restriction on Growth of Rat Maxillary Incisors, Proc Soc Exp Bzol Med 116:718-720, 1964. DoMM, L. V., and KIELY, M. L.: The Effect of

4. PARMER, L. G.; KATONAH, F.;

5.

6.

7.

8.

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VOl. 56 NO. 12

EFFECT OF Mg-DEFICIENCY & CORTISONE ON RAT INCISOR

Cortisone on Mitotic Activity in the Rat Incisor, Proc Soc Exp Biol Med 129:912-916, 1968. 9. KIELY, M. L., and DoMM, L. V.: Circadian Uptake of 3H-thymidine in the Rat Incisor Under the Influence of Cortisone, Proc Soc Exp Blol Med 143:844-849, 1973. 10. AIKAWA, J. K.: The Role of Magnesium in Biologic Processes, 1st ed, Springfield: Charles C Thomas, 1963, pp 49-51. 11. AIKAWA, J. K.: The Relationship of Magnesium to Disease in Domestic Animals and zn Humans, 1st ed, Springfield: Charles C Thomas, 1971, pp 10-36. 12. WACKER, W. E. C.: The Biochemistry of Magnesium, Ann NY Acad Sci 162:717-726, 1969. 13. TROWBRIDGE, H. O., and JENKS, P.: Magnesium Deficiency,J Calff Dent Assoc 44:444-448, 1968. 14. GAGNON, J.; SCHOUR, I.; and PA-rRAS, M. C.: Effect of Magnesium Deficiency on Dentin Apposition and Eruption in Incisor of Rat, Proc Soc Exp Biol Med 49:662-666, 1942. 15. KUSNER, W.; MICHAELlI, Y.; and WEINREB, M. M.: Role of Attrition and Occlusal Contact in the Physiology of the Rat Incisor: VI. Impeded and Unimpeded Eruption in Hypophysectomized and Magnesium-Deficient Rats, J Dent Res 52:65-73, 1973. 16. KLEIN, H.; ORENT, E. R.; and MCCOLLUM, E. V.: The Effects of Magnesium Deficiency on the Teeth and Their Supporting Structures in Rats, AmJPhySiol 112:256-262, 1935. 17. BECKS, H., and FURUTA, W. J.: Effect of Magnesium Deficient Diets on Oral and Dental Tissues 1. Changes in the Enamel Epithelium, JADA 26:883-891, 1939. 18. BECKS, H., and FURUTA, W. J.: Effect of Magnesium Deficient Diets on Oral and Dental Tissues II. Changes in the Enamel Structure, JADA 28:1083-1088, 1941. 19. BECKS, H., and FURUTA, W. J.: The Effect of Magnesium-Deficient Diets on Oral and Dental Structures III. Changes in the Dentine and Pulp Tissue, A mJ Ortho Oral Surg 28(oral surg): 1 14, 1942. 20. WEINREB, M. M.; KUSNER, W.; and MICHAELI, Y.: Role of Attrition and Occlusal Contact in the Physiology of the Rat Incisor: VII. Formation of Impeded and Unimpeded Incisors in Magnesium-Deficient Rats,J Dent Res 52:498-507, 1973. 21. HEGGTVEIr, H. A.; HERMAN, L.; and MISHRA, R. K.: Cardiac Necrosis and Calcification in Experimental Magnesium Deficiency. A Light and Electron Microscopic Study, Am J Path 45:757-782, 1964. 22. BAUME, L. J.; BECKS, H.; and EVANS, H. M.: Hormonal Control of Tooth Eruption. I. The Effect of Thyroidectomy on the Upper Rat Incisor and the Response to Growth Hormone, Thyrox-

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The effect of a magnesium deficient diet and cortisone on the growth of the rat incisor.

The Effect of a Magnesium Deficient Diet and Cortisone on the Growth of the Rat Incisor MICHAEL L. KIELY and L. V. DOMM Departments of Anatomy, Loyol...
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