Study |
Study population |
Methods |
Finding |
Mitochondrial function |
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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 |
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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 |
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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 = cytochrome‐c‐oxidase, 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 = low‐density lipoprotein, M = migraine not otherwise specified; MA = migraine with aura; MAO = monoamine oxidase, MDA = malondialdehyde, MO = migraine without aura, NADH-D = NADH-dehydrogenase, NADH‐CCR= NADH‐cytochrome‐c‐reductase, 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 = succinate‐cytochrome‐c‐reductase, 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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