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Table 1 | Human peripheral blood studies showing metabolic abnormalities in migraine.

 

Study 

Study population 

Methods 

Finding 

Mitochondrial function 

Littlewood et al., 1984  

48 with migraine, 30 HCs (all male) 

Platelet MAO and SDHactivity 

↓ MAO and SDH activity in migraine compared with HC s 

Montagna et al., 1988  

4 with migraine, 5 with migraine and stroke 

Mitochondrial energy metabolism markers in blood and muscle 

 blood lactate during effort,, ↓ activity of some respiratory chain enzymes in 2 patients and  CCO, SCCR & NADH‐CCR in migraine 

Sangiorgi et al., 1994 

40 with MA, 40 with MO, 24 HCs 

Platelet mitochondrial enzyme activity 

NADH-D and CS in MA and MO compared with HCs, and  NADH-CCR in MA; no alterations in SDH levels  

Okada et al., 1998 

14 with migraine, 12 HCs 

Lactic and pyruvic acid levels in plasma 

 lactic and pyruvic acid levels in migraine compared with HCs 

Oxidative stress 

Shimomura et al., 1994  

30 with MO, 9 with MA, 53 with TTH, 30 HCs 

Concentrations of platelet SOD and activity of platelet SOD  

 platelet SOD in MO and MA, ↓ SOD activity in MA, but not in MO or TTH 

Tozzi-Ciancarelli et al., 1997  

23 with MA, 23 HCs 

Plasma TBARS, in vitro platelet behaviour at rest and after thrombin stimulation 

 TBARS and ↑ membrane rigidity,  cytosolic calcium (at rest  and after thrombin stimulation) and  aggregatory responses to ADP and collagen in platelets in MA  

Ciancarelli et al., 2003  

30 with MO or MA, 20 HCs 

24 h measurement ictal & interictal urinary NOx & TBARS levels 

Interictally:  NOx and TBARS in migraine compared with HCs and  NOx compared with ictal and post-ictal levels 

Ictally:  TBARS compared with interictal levels, no differences between MO and MA 

Bolayir et al., 2004  

11 with MA, 17 with MO, 32 with TTH, 28 HCs 

GPx, catalase and SOD enzyme interictal activities  

 SOD and GPx enzyme activities in MA and MO compared with activities in TTH and HCs  

Ciancarelli et al., 2007  

20 with CM, 20 HCs 

Serum peroxides, NO & SOD  

 NOx levels and SOD activity in CM compared with HCs,  peroxide levels in CM compared with HCs 

Yilmaz et al., 2007  

22 with MO, 14 with MA, 20 HCs 

Platelet levels of NOx, MDA and thiol groups ictally and interictally 

Ictally:  platelet levels of nitrate, nitrite and MDA in migraine compared with HCs  

Interictally: no significant differences  

Tuncel et al., 2008  

37 with MO, 19 with MA, 25 HCs 

Erythrocyte SOD, catalase activity & MDA levels 

 MDA levels in migraine compared with HCs,  SOD activity in MA compared with MO 

Alp et al., 2010  

75 with MO, 65 HCs 

Interictal TAS and TOS of the plasma and the OSI 

¯ TAS and TOS and OSI in MO compared with HC, OSI correlated with disease severity  

Bernecker et al., 2011  

48 with MO, 17 with MA, 48 HCs (all female) 

Interictal levels of MDA, HNE, carbonylated proteins, parameters of associated NO stress, inflammation, lipid metabolism and glucose metabolism  

 HOMA indices and levels of insulin, LDL, triglycerides, oxidized LDL, NOx, nitrate and HNE in migraine compared with HCs; no significant different between migraine and HCs in levels of fasting blood glucose, nitrite, nitrosylated proteins, MDA and carbonylated proteins 

Aytaç et al., 2014  

18 with migraine with WMHs, 14 with migraine without WMH, 17 HCs 

MDA, SOD, GPx and catalase levels in serum 

¯ catalase and MDA levels in all migraine,¯ catalase in migraine with WMHs compared with migraine without WMHs and HCs 

Eren et al., 2015  

74 with MO, 77 with MA, 70 HCs 

TAS, TOS & OSI, and serum thiol levels 

¯ thiol levels in migraine compared with HCs, and levels negatively correlated with migraine-associated disability; no significant differences in TAS, TOS or OSI between migraine and HCs  

Geyik et al., 2016  

39 with MO, 11 with MA, 30 HCs 

TOS, TAS & OSI, and 8-OhdG levels in plasma 

8-OhdG levels in migraine compared with HCs; 8-OHdG was significantly more prominent in MO than in MA; no significant differences in TAS, TOS or OSI between migraine and HCs 

Gumusyayla et al., 2016  

63 with MA or MO, 50 HCs 

Total thiol and native thiol levels in serum 

 total and native thiol levels in migraine compared with HCs 

Tripathi et al., 2018  

136 with MO, 14 with MA, 100 HCs 

GSH, GST & TAC before and after treatment with rTMS (120 with migraine) or amitriptyline (30 with migraine)  

¯ GSH, GST and TAC levels in migraine compared with HCs, GSH and TAC levels after treatment irrespective of modality; this increase correlated with treatment success 

Glucose metabolism 

Blau & Cumings, 1966  

12 with migraine 

19 h water fast 

50% developed migraine 11–14 h after start of fasting;¯ BG to 44–65 mg/dl in all of these patients 

Pearce, 1971  

20 with migraine, 10 HCs 

Insulin-induced hypoglycaemia  

¯ blood glucose to 20.4 mg/dl in MA and to 24.3 mg/dl in HCs. 2 of 20 patients with migraine developed an aura (one with headache) within 2 h after insulin administration 

Hockaday et al. ,1971 

10 with migraine with attacks associated with fasting, or undue hunger 

50 g oral GTT after 10 h fast, with 8 h observation 

Migraine attacks in 6 of 10 within 4 h, FFAs and KB in all 10; no difference in glucose or glycerol levels between attack and no attack  

Shaw et al., 1977  

6 with MA 

Ictal and inter-ictal intravenus GTT 

During attacks:  glucose at 30, 45 and 75 min,  KB, FFAs, glycerol, cortiso and, GH levels,  BHB:AcAc ratio and ¯ insulin levels; no significant difference in lactate or pyruvate levels  

Hsu et al.,1977  

13 with early morning onset migraine 

Nocturnal blood analysis 3 hours prior to waking from migraine compared to non-migraine night 

Noradrenaline & adrenalin, glucose, FFA & insulin levels stable 3 h prior to awakening with migraine  

Dexter et al., 1978  

74 with migraine with attacks associated with fasting 

100g oral GTT 

6 patients classified diabetic & 56 patients showed degrees of reactive hypoglycemia, i.e. BG of less than 65 mg/dl or a drop of 75 mg/dl within 1h 

Cavestro et al., 2007  

58 with MO, 6 with MA, 20 with M and non-migraine headache, 25 with non-migraine headache, 26 HCs 

75g oral GTT after 12h fast, 2h observation 

BG at baseline & up to 1 h post GTT in M, insulin levels at all time points compared to HC & other headache, 65% of migraineurs showed IR. 

Sacco et al., 2014  

50 with MA, 50 with MO, 50 HCs 

Fasted BG & insulin analysis, IR calculated with HOMA-IR, HOMA-B, QUICKI  

Fasting BG  in MA & MO, highest in MA, no differences in insulin & measures of IR 

Kokavec 2015  

12 with migraine, 8 HCs 

75g oral STT after 15h overnight fast, insulin, BG & cortisol over 150min period 

cortisol at baseline in M, no sign. difference in fasting insulin & BG,  

following STT: insulin in female M; cortisol in male M 

Siva et al 2017  

83 non-obese women with EM or CM), 36 HCs 

75 g oral GTT 

 Fasting BG in M,  IR in CM compared to EM or HC,  neuropeptide Y in M 

Wang et al., 2017  

86 with migraine, 95 HCs 

75g oralGTT, 2h observation, IR calculated with HOMA-IR, HOMA-B, QUICKI  

No sign. differences in HbA1c,IR & IS between M & HC, only between prediabetic M and prediabetic HC, possible negative association between diabetes & M 

 

8-OHdG = 8-hydroxy-2'-deoxyguanosine, AcAc = acetoacetate, BG = blood glucose, BHB = beta-hydroxybutyrate, CCO = cytochrome-c-oxidase activities, CCO = cytochromecoxidase, CM = chronic migraine, CS = citrate synthase, EM = episodic migraine; FFA = free fatty acids, GH = growth hormone, GPx = Glutathione peroxidase, GSH =glutathione, GST = glutathione-S-transferase, GTT = glucose tolerance test, HC = healthy controls, HNE = 4-hydroxy-2-nonenal, HOMA-B = β-cell function, HOMA-IR = the homeostatic model assessment of insulin resistance, HT = different headache type to migraine, IR = insulin resistance, IS = insulin sensitivity, IV = intravenous, KB = ketones bodies, LDL = lowdensity lipoprotein, M = migraine not otherwise specified; MA = migraine with aura; MAO = monoamine oxidase, MDA = malondialdehyde, MO = migraine without aura, NADH-D = NADH-dehydrogenase, NADHCCR= NADHcytochromecreductase, NO = nitric oxide, NOx = NO stable metabolites, OSI = Oxidative Stress Index, QUICKI = the quantitative insulin sensitivity check index, rTMS = repetitive transcranial magnetic stimulation therapy, SCCR = succinatecytochromecreductase, SDH= succinate dehydrogenase, sign. = statistically significant, SOD = superoxide dismutase, STT = sucrose tolerance test, TAC = total antioxidant activity, TAS = Total Antioxidant Status, TBARS = thiobarbituric acid-reactive substances, TOS = Total Oxidant Status, TTH= tension type headache, WMH = white matter hyperintensities 

 

 

 

 

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