Possible Involvement of Histamine in Muscular Fatigue in Temporomandibular Disorders: Animal and Human Studies

Abstract

As an approach to clarifying the molecular basis of pain and fatigue in muscles involved in temporomandibular disorders, we examined the activity of histidine decarboxylase (HDC), the enzyme which forms histamine, in the masseter muscles of mice. In the resting muscle, HDC activity was very low. Direct electrical stimulation of the muscle markedly elevated HDC activity. HDC activity rose within 3 hrs of the electrical stimulation, peaked at 6 to 8 hrs, and then gradually declined. Intraperitoneal injection of a small amount of interleukin-1 (IL-1) (from 1 to 10 μg/kg) produced a similar elevation of HDC activity in the masseter muscle. We also examined the effect of an antihistamine, chlorphenylamine (CP), on temporomandibular disorders in humans and compared it with that of an antiinflammatory analgesic, flurbiprofen (FB). Two groups received one or the other of the drugs daily for 7 days, and they were asked about their signs and symptoms before and after the treatment. A positive evaluation of their treatment was made by 74% of the CP group, but by only 48% of the FB group. Although the effects of CP on the limitation of mouth-opening and on joint noise were negligible, about 50% of the CP group answered positively concerning the drug's effect on spontaneous pain or pain induced by chewing or mouth-opening. The positive evaluation for CP (50%) in relieving associated symptoms (headache or shoulder stiffness) was significantly greater than for FB (13%). FB showed effectiveness similar to but sometimes weaker than that of CP on several symptoms. On the basis of these and previous results and the known actions of histamine, we propose that the histamine newly formed following the induction of HDC activity, which is itself mediated by IL-1, may be involved in inducing pain and, possibly, stiffness in muscles in temporomandibular disorders.

Keywords

histidine decarboxylase histamine antihistamine interleukin-1 (IL-1)masseter muscle temporomandibular disorder

Get full access to this article

View all access options for this article.

References

Beaven MA (1978). Histamine: its role in physiological and pathological processes. In: Monographs in allergy. Vol. 13. Basel: S. Karger, pp. 1-113.

Bross IDJ (1958). How to use ridit analysis. Biometrics 14:18-38.

Campbell WB (1990). Lipid-derived autacoid. In: Goodman and Gilman's The pharmacological basis of therapeutics. 8th ed. Gilman AG , Rail TW , Nies AS , Taylor P , editors. New York: Pergamon Press, pp. 600-617.

Cannon JG , Evans WJ , Hughes VA , Meredith CN , Dinarello CA (1986). Physiological mechanisms contributing to increased interleukin-1 secretion. J Appl Physiol 61:1869-1874.

Cannon JG , Fielding RA , Fiatarone MA , Orencole SF , Dinarello CA , Evans WJ (1989). Increased interleukin 1β in human skeletal muscle after exercise. Am J Physiol 257:R451-R455.

Dinarello CA (1991). Interleukin-1 and interleukin-1 antagonism. Blood 77:1627-1652.

Duner H. , Pernow B. (1958). Histamine and leukocytes in blood during muscular work. Scand J Clin Lab Invest 10:394-396.

Ekberg E-C. , Kopp S. , Akerman S. (1996). Diclofenac sodium as an alternative treatment of temporomandibular joint pain. Acta Odontol Scand 54:154-159.

Endo Y. ( 1979). Elevation of histamine in rat and mouse tissues by the deacetylation of administered N-acetylhistamine. Eur J Pharmacol 60:299-305.

10.

Endo Y. ( 1982). Simultaneous induction of histidine and ornithine decarboxylases and changes in their product amines following the injection of Escherichia coli lipopolysaccharide into mice. Biochem Pharmacol 31:1643-1647.

11.

Endo Y. ( 1983a). A simple method for the determination of polyamines and histamine and its application to the assay of ornithine decarboxylase and histidine decarboxylase activities. Meth Enzymol 94:42-47.

12.

Endo Y. ( 1983b). Induction of histidine decarboxylase in mouse tissues by mitogens in vivo. Biochem Pharmacol 32:3835-3838.

13.

Endo Y. ( 1989). Induction of histidine and ornithine decarboxylase activities in mouse tissues by recombinant interleukin-1 and tumor necrosis factor. Biochem Pharmacol 38:1287-1292.

14.

Endo Y. , Suzuki R. , Kumagai K. (1986). Macrophages can produce factors capable of inducing histidine decarboxylase, a histamine-forming enzyme, in vivo in the liver, spleen, and lung of mice. Cell Immunol 97:13-22.

15.

Endo Y. , Kikuchi T. , Takeda Y. , Nitta Y. , Rikiishi H. , Kumagai K. (1992a). GM-CSF and G-CSF stimulate the synthesis of histamine and putrescine in the hematopoietic organs in vivo. Immunol Lett 33:9-14.

16.

Endo Y. , Kikuchi T. , Nakamura M. (1992b). Ornithine and histidine decarboxylase activities in mice sensitized to endotoxin, interleukin-1 or tumor necrosis factor by D-galactosamine. Br J Pharmacol 107:888-894.

17.

Endo Y. , Kikuchi T. , Nakamura M. , Shinoda H. (1992c). Determination of histamine and polyamines in calcified tissues of mice: contribution of mast cells and histidine decarboxylase to the amount of histamine in the bone. Calcif Tissue Int 51:67-71.

18.

Endo Y. , Nakamura M. , Nitta Y. , Kumagai K. (1995). Effects of macrophage depletion on the induction of histidine decarboxylase by lipopolysaccharide, interleukin-1 and tumor necrosis factor. Br J Pharmacol 114:187-193.

19.

Endo Y. , Tabata T. , Kuroda H. , Tadano T. , Matsushima K. , Watanabe M. (1998). Induction of histidine decarboxylase in skeletal muscle in mice by electrical stimulation, prolonged walking and interleukin-1 . J Physiol 509:587-598.

20.

Federspil G. , Baggio B. , De Palo C. , De Carlo E. , Borsatti A. , Vettor R. (1987). Effect of prolonged physical exercise on muscular phospholipase A2 activity in rats. Diabet Metab 13:171-175.

21.

Fielding RA , Manfredi TJ , Ding W. , Fiatarone MA , Evans WJ , Cannon JG (1993). Acute phase response in exercise. III. Neutrophil and IL-1β accumulation in skeletal muscle. Am J Physiol 265:R166-R172.

22.

Friden J. , Seger J. , Sjostrom M. , Ekblom B. (1983). Adaptive response in human skeletal muscle subjected to prolonged eccentric training. Int J Sports Med 4:177-183.

23.

Furutani Y. , Notake M. , Yamanishi M. , Yamagishi J. , Nomura H. , Ohue M. , et al. (1985). Cloning and characterization of the cDNAs for human and rabbit interleukin-1 precursor. Nucleic Acids Res 13:5869-5882.

24.

Garrison JC (1990). Histamine, bradykinin, 5-hydroxytryptamine, and their antagonists. In: Goodman and Gilman's the pharmacological basis of therapeutics. 8th ed. Gilman AG , Rail TW , Nies AS , Taylor P , editors. New York: Pergamon Press, pp. 575-599.

25.

Graham P. , Kahlson G. , Rosengren E. (1964). Histamine formation in physical exercise, anoxia and under the influence of adrenaline and related substances. J Physiol 172:174-188.

26.

Kahlson G. , Rosengren E. (1968). New approaches to the physiology of histamine . Physiol Rev 48:155-196.

27.

Kikuchi H. , Watanabe M. , Endo Y. ( 1997). Induction by interleukin-1 of the mRNA of histidine decarboxylase, the histamine-forming enzyme, in the lung of mice in vivo and the effect of actinomycin D. Biochem Pharmacol 53:1383-1388.

28.

Morganroth ML , Young EW , Sparks HV (1977). Prostaglandin and histaminergic mediation of prolonged vasodilatation after exercise. Am J Physiol 233:H27-H33.

29.

Oppenheim JJ , Elizabeth JK , Matsushima K. , Durum SK (1986). There is more than one interleukin 1. Immunol Today 7:45-56.

30.

O'Reilly KP , Warhol MJ , Fielding RA , Frontera WR , Meredith CN , Evans WJ (1987). Eccentric exercise-induced muscle damage impairs muscle glycogen repletion. J Appl Physiol 63:252-256.

31.

Reilly MA , Schayer RW (1968). Further studies on the histidine-histamine relationship in vivo: effects of endotoxin and of histidine decarboxylase inhibitors. Br J Pharmacol 34:551-563.

32.

Schayer RW (1974). Histamine and microcirculation. Life Sci 15:391-401.

33.

Schayer RW (1978). Metabolism and excretion of histamine. In: Handbook of experimental pharmacology. XVIII ed. (Part 2). Berlin: Springer-Verlag , pp. 109-129.