Platelet/lymphocyte ratio is an independent predictor for osteoporosis

Semra Eroglu; Gulsah Karatas

doi:10.15537/smj.2019.4.24009

References

↵
1. Eastell R,
2. O'Neill TW,
3. Hofbauer LC,
4. Langdahl B,
5. Reid IR,
6. Gold DT,
7. et al.
(2016) Postmenopausal osteoporosis. Nat Rev Dis Primers 2:16069.
OpenUrl
↵
1. Curtis EM,
2. Moon RJ,
3. Dennison EM,
4. Harvey NC,
5. Cooper C
(2015) Recent advances in the pathogenesis and treatment of osteoporosis. Clin Med (Lond) 15:s92–s96.
OpenUrl
↵
1. Holm JP,
2. Hyldstrup L,
3. Jensen JB
(2016) Time trends in osteoporosis risk factor profiles:a comparative analysis of risk factors, comorbidities, and medications over twelve years. Endocrine 54:241–255.
OpenUrl
↵
1. Zhen D,
2. Liu L,
3. Guan C,
4. Zhao N,
5. Tang X
(2015) High prevalence of vitamin D deficiency among middle-aged and elderly individuals in northwestern China:its relationship to osteoporosis and lifestyle factors. Bone 71:1–6.
OpenUrl CrossRef PubMed
↵
1. Jamka M,
2. Woźniewicz M,
3. Walkowiak J,
4. Bogdański P,
5. Jeszka J,
6. Stelmach-Mardas M
(2016) The effect of vitamin D supplementation on selected inflammatory biomarkers in obese and overweight subjects:a systematic review with meta-analysis. Eur J Nutr 55:2163–2176.
OpenUrl
↵
1. Gravallese EM,
2. Goldring SR,
3. Schett G
(2016) The role of the immune system in the local and systemic bone loss of inflammatory arthritis. Osteoimmunology (Second edition), 241–256.
↵
1. Jafari T,
2. Faghihimani E,
3. Feizi A,
4. Iraj B,
5. Javanmard SH,
6. Esmaillzadeh A,
7. et al.
(2016) Effects of vitamin D-fortified low fat yogurt on glycemic status, anthropometric indexes, inflammation, and bone turnover in diabetic postmenopausal women:A randomised controlled clinical trial. Clin Nutr 35:67–76.
OpenUrl
↵
1. Harmandar FA,
2. Can H,
3. Cekin AH,
4. Uyar S
Incidence of low bone mineral density and contributing factors in inflammatory bowel disease [Internet]. akademik gastroenteroloji dergisi, Available from: https://pdfs.semanticscholar.org/0ec6/aa740221ea617075f63944fd9bd79d1ad19d.pdf. [Updated 2016;Accessed 2019 January 11].
1. El Maghraoui A,
2. Sadni S,
3. Rezqi A,
4. Bezza A,
5. Achemlal L,
6. Mounach A
(2015) Does Rheumatoid Cachexia Predispose Patients with Rheumatoid Arthritis to Osteoporosis and Vertebral Fractures? J Rheumatol 42:1556–1562.
OpenUrl Abstract/FREE Full Text
↵
1. Salman-Monte TC,
2. Torrente-Segarra V,
3. Muñoz-Ortego J,
4. Mojal S,
5. Carbonell-Abelló J
(2015) Prevalence and predictors of low bone density and fragility fractures in women with systemic lupus erythematosus in a Mediterranean region. Rheumatol Int 35:509–515.
OpenUrl CrossRef PubMed
↵
1. Sponholtz TR,
2. Zhang X,
3. Fontes JD,
4. Meigs JB,
5. Cupples LA,
6. Kiel DP,
7. et al.
(2014) Association between inflammatory biomarkers and bone mineral density in a community-based cohort of men and women. Arthritis Care Res (Hoboken) 66:1233–1240.
OpenUrl
↵
1. Lin CC,
2. Li TC,
3. Liu CS,
4. Yang CW,
5. Lin CH,
6. Hsiao JH,
7. et al.
(2016) Associations of TNF-αand IL-6 polymorphisms with osteoporosis through joint effects and interactions with LEPR gene in Taiwan:Taichung Community Health Study for Elders (TCHS-E). Mol Biol Rep 43:1179–1191.
OpenUrl
↵
1. Berglundh S,
2. Malmgren L,
3. Luthman H,
4. McGuigan F,
5. Åkesson K
(2015) C-reactive protein, bone loss, fracture, and mortality in elderly women:a longitudinal study in the OPRA cohort. Osteoporos Int 26:727–735.
OpenUrl
↵
1. Yan P,
2. Xu Y,
3. Wan Q,
4. Feng J,
5. Yang J,
6. Li H,
7. et al.
(2018) Impact of MPV and PDW on bone mineral density and their relationship with osteoporosis in Chinese patients with type 2 diabetes. Int J Clin Exp Med 11:2337–2349.
OpenUrl
↵
1. Koupenova M,
2. Clancy L,
3. Corkrey HA,
4. Freedman JE
(2018) Circulating Platelets as Mediators of Immunity, Inflammation, and Thrombosis. Circ Res 122:337–351.
OpenUrl Abstract/FREE Full Text
↵
1. Kapur R,
2. Zufferey A,
3. Boilard E,
4. Semple JW
(2015) Nouvelle cuisine:platelets served with inflammation. J Immunol 194:5579–5587.
OpenUrl Abstract/FREE Full Text
↵
1. Xu ZS,
2. Zhang FP,
3. Zhang Y,
4. Ou-Yang YP,
5. Yu XW,
6. Wang WL,
7. et al.
(2017) Prognostic role of the pre-treatment platelet-lymphocyte ratio in pancreatic cancer:a meta-analysis. Oncotarget 8:99003–99012.
OpenUrl
1. Sato N,
2. Kinoshita A,
3. Imai N,
4. Akasu T,
5. Yokota T,
6. Iwaku A,
7. et al.
(2018) Inflammation-based prognostic scores predict disease severity in patients with acute cholecystitis. Eur J Gastroenterol Hepatol 30:484–489.
OpenUrl
↵
1. Guo J,
2. Wu M,
3. Guo L,
4. Zuo Q
(2018) Pretreatment blood neutrophil/lymphocyte ratio is associated with metastasis and predicts survival in patients with pancreatic cancer. Bull Cancer 105:146–154.
OpenUrl
↵
1. Yu XY,
2. Li XS,
3. Li Y,
4. Liu T,
5. Wang RT
(2015) Neutrophil-lymphocyte ratio is associated with arterial stiffness in postmenopausal women with osteoporosis. Arch Gerontol Geriatr 61:76–80.
OpenUrl CrossRef PubMed
↵
1. Fisher A,
2. Srikusalanukul W,
3. Fisher L,
4. Smith P
(2016) The Neutrophil to Lymphocyte Ratio on Admission and Short-Term Outcomes in Orthogeriatric Patients. Int J Med Sci 13:588–602.
OpenUrl
↵
1. Yilmaz H,
2. Uyfun M,
3. Yilmaz TS,
4. Namuslu M,
5. Inan O,
6. Taskin A,
7. et al.
(2014) Neutrophil-lymphocyte ratio may be superior to C-reactive protein for predicting the occurrence of postmenopausal osteoporosis. Endocr Regul 48:25–33.
OpenUrl CrossRef PubMed
↵
1. Koseoglu SB
(2017) Bone loss &platelet-to-lymphocyte ratio. Biomark Med 11:5–10.
OpenUrl
↵
1. Miller AJ,
2. Jones C,
3. Liss F,
4. Abboudi J,
5. Kirkpatrick W,
6. Beredjiklian P
(2017) Qualitative Evaluation of Digital Hand X-rays Is Not a Reliable Method to Assess Bone Mineral Density. Arch Bone Jt Surg 5:10–13.
OpenUrl
↵
1. Lim HS,
2. Park YH,
3. Kim SK
(2016) Relationship between Serum Inflammatory Marker and Bone Mineral Density in Healthy Adults. J Bone Metab 23:27–33.
OpenUrl
↵
1. Wu ZJ,
2. He JL,
3. Wei RQ,
4. Liu B,
5. Lin X,
6. Guan J,
7. et al.
(2015) C-reactive protein and risk of fracture:a systematic review and dose-response meta-analysis of prospective cohort studies. Osteoporos Int 26:49–57.
OpenUrl
↵
1. Oei L,
2. Campos-Obando N,
3. Dehghan A,
4. Oei EH,
5. Stolk L,
6. van Meurs JB,
7. et al.
(2014) Dissecting the relationship between high-sensitivity serum C-reactive protein and increased fracture risk:the Rotterdam Study. Osteoporos Int 25:1247–1254.
OpenUrl CrossRef PubMed
↵
1. Al-Daghri NM,
2. Aziz I,
3. Yakout S,
4. Aljohani NJ,
5. Al-Saleh Y,
6. Amer OE,
7. et al.
(2017) Inflammation as a contributing factor among postmenopausal Saudi women with osteoporosis. Medicine (Baltimore) 96:e5780.
OpenUrl
↵
1. Huang C,
2. Li S
(2016) Association of blood neutrophil lymphocyte ratio in the patients with postmenopausal osteoporosis. Pak J Med Sci 32:762–765.
OpenUrl
↵
1. Guo L,
2. Gao Z,
3. Ge H
(2017) Effects of serum 25-hydroxyvitaminD level on decreased bone mineral density at femoral neck and total hip in Chinese type 2 diabetes. PLoS One 12:e0188894.
OpenUrl
↵
1. Brincat M,
2. Gambin J,
3. Brincat M,
4. Calleja-Agius J
(2015) The role of vitamin D in osteoporosis. Maturitas 80:329–332.
OpenUrl CrossRef PubMed
↵
1. Akbas EM,
2. Gungor A,
3. Ozcicek A,
4. Akbas N,
5. Askin S,
6. Polat M
(2016) Vitamin D and inflammation:evaluation with neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio. Arch Med Sci 12:721–727.
OpenUrl
↵
1. Tabatabaeizadeh SA,
2. Avan A,
3. Bahrami A,
4. Khodashenas E 4.,
5. Esmaeili H,
6. Ferns GA,
7. et al.
(2017) High Dose Supplementation of Vitamin D Affects Measures of Systemic Inflammation:Reductions in High Sensitivity C-Reactive Protein Level and Neutrophil to Lymphocyte Ratio (NLR) Distribution. J Cell Biochem 118:4317–4322.
OpenUrl

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Show more Original Article

[1] ↵
Eastell R,
O'Neill TW,
Hofbauer LC,
Langdahl B,
Reid IR,
Gold DT,
et al.
(2016) Postmenopausal osteoporosis. Nat Rev Dis Primers 2:16069.
OpenUrl

[2] Eastell R,

[3] O'Neill TW,

[4] Hofbauer LC,

[5] Langdahl B,

[6] Reid IR,

[7] Gold DT,

[8] et al.

[9] ↵
Curtis EM,
Moon RJ,
Dennison EM,
Harvey NC,
Cooper C
(2015) Recent advances in the pathogenesis and treatment of osteoporosis. Clin Med (Lond) 15:s92–s96.
OpenUrl

[10] Curtis EM,

[11] Moon RJ,

[12] Dennison EM,

[13] Harvey NC,

[14] Cooper C

[15] ↵
Holm JP,
Hyldstrup L,
Jensen JB
(2016) Time trends in osteoporosis risk factor profiles:a comparative analysis of risk factors, comorbidities, and medications over twelve years. Endocrine 54:241–255.
OpenUrl

[16] Holm JP,

[17] Hyldstrup L,

[18] Jensen JB

[19] ↵
Zhen D,
Liu L,
Guan C,
Zhao N,
Tang X
(2015) High prevalence of vitamin D deficiency among middle-aged and elderly individuals in northwestern China:its relationship to osteoporosis and lifestyle factors. Bone 71:1–6.
OpenUrl CrossRef PubMed

[20] Zhen D,

[21] Liu L,

[22] Guan C,

[23] Zhao N,

[24] Tang X

[25] ↵
Jamka M,
Woźniewicz M,
Walkowiak J,
Bogdański P,
Jeszka J,
Stelmach-Mardas M
(2016) The effect of vitamin D supplementation on selected inflammatory biomarkers in obese and overweight subjects:a systematic review with meta-analysis. Eur J Nutr 55:2163–2176.
OpenUrl

[26] Jamka M,

[27] Woźniewicz M,

[28] Walkowiak J,

[29] Bogdański P,

[30] Jeszka J,

[31] Stelmach-Mardas M

[32] ↵
Gravallese EM,
Goldring SR,
Schett G
(2016) The role of the immune system in the local and systemic bone loss of inflammatory arthritis. Osteoimmunology (Second edition), 241–256.

[33] Gravallese EM,

[34] Goldring SR,

[35] Schett G

[36] ↵
Jafari T,
Faghihimani E,
Feizi A,
Iraj B,
Javanmard SH,
Esmaillzadeh A,
et al.
(2016) Effects of vitamin D-fortified low fat yogurt on glycemic status, anthropometric indexes, inflammation, and bone turnover in diabetic postmenopausal women:A randomised controlled clinical trial. Clin Nutr 35:67–76.
OpenUrl

[37] Jafari T,

[38] Faghihimani E,

[39] Feizi A,

[40] Iraj B,

[41] Javanmard SH,

[42] Esmaillzadeh A,

[43] et al.

[44] ↵
Harmandar FA,
Can H,
Cekin AH,
Uyar S
Incidence of low bone mineral density and contributing factors in inflammatory bowel disease [Internet]. akademik gastroenteroloji dergisi, Available from: https://pdfs.semanticscholar.org/0ec6/aa740221ea617075f63944fd9bd79d1ad19d.pdf. [Updated 2016;Accessed 2019 January 11].

[45] Harmandar FA,

[46] Can H,

[47] Cekin AH,

[48] Uyar S

[49] El Maghraoui A,
Sadni S,
Rezqi A,
Bezza A,
Achemlal L,
Mounach A
(2015) Does Rheumatoid Cachexia Predispose Patients with Rheumatoid Arthritis to Osteoporosis and Vertebral Fractures? J Rheumatol 42:1556–1562.
OpenUrl Abstract/FREE Full Text

[50] El Maghraoui A,

[51] Sadni S,

[52] Rezqi A,

[53] Bezza A,

[54] Achemlal L,

[55] Mounach A

[56] ↵
Salman-Monte TC,
Torrente-Segarra V,
Muñoz-Ortego J,
Mojal S,
Carbonell-Abelló J
(2015) Prevalence and predictors of low bone density and fragility fractures in women with systemic lupus erythematosus in a Mediterranean region. Rheumatol Int 35:509–515.
OpenUrl CrossRef PubMed

[57] Salman-Monte TC,

[58] Torrente-Segarra V,

[59] Muñoz-Ortego J,

[60] Mojal S,

[61] Carbonell-Abelló J

[62] ↵
Sponholtz TR,
Zhang X,
Fontes JD,
Meigs JB,
Cupples LA,
Kiel DP,
et al.
(2014) Association between inflammatory biomarkers and bone mineral density in a community-based cohort of men and women. Arthritis Care Res (Hoboken) 66:1233–1240.
OpenUrl

[63] Sponholtz TR,

[64] Zhang X,

[65] Fontes JD,

[66] Meigs JB,

[67] Cupples LA,

[68] Kiel DP,

[69] et al.

[70] ↵
Lin CC,
Li TC,
Liu CS,
Yang CW,
Lin CH,
Hsiao JH,
et al.
(2016) Associations of TNF-αand IL-6 polymorphisms with osteoporosis through joint effects and interactions with LEPR gene in Taiwan:Taichung Community Health Study for Elders (TCHS-E). Mol Biol Rep 43:1179–1191.
OpenUrl

[71] Lin CC,

[72] Li TC,

[73] Liu CS,

[74] Yang CW,

[75] Lin CH,

[76] Hsiao JH,

[77] et al.

[78] ↵
Berglundh S,
Malmgren L,
Luthman H,
McGuigan F,
Åkesson K
(2015) C-reactive protein, bone loss, fracture, and mortality in elderly women:a longitudinal study in the OPRA cohort. Osteoporos Int 26:727–735.
OpenUrl

[79] Berglundh S,

[80] Malmgren L,

[81] Luthman H,

[82] McGuigan F,

[83] Åkesson K

[84] ↵
Yan P,
Xu Y,
Wan Q,
Feng J,
Yang J,
Li H,
et al.
(2018) Impact of MPV and PDW on bone mineral density and their relationship with osteoporosis in Chinese patients with type 2 diabetes. Int J Clin Exp Med 11:2337–2349.
OpenUrl

[85] Yan P,

[86] Xu Y,

[87] Wan Q,

[88] Feng J,

[89] Yang J,

[90] Li H,

[91] et al.

[92] ↵
Koupenova M,
Clancy L,
Corkrey HA,
Freedman JE
(2018) Circulating Platelets as Mediators of Immunity, Inflammation, and Thrombosis. Circ Res 122:337–351.
OpenUrl Abstract/FREE Full Text

[93] Koupenova M,

[94] Clancy L,

[95] Corkrey HA,

[96] Freedman JE

[97] ↵
Kapur R,
Zufferey A,
Boilard E,
Semple JW
(2015) Nouvelle cuisine:platelets served with inflammation. J Immunol 194:5579–5587.
OpenUrl Abstract/FREE Full Text

[98] Kapur R,

[99] Zufferey A,

[100] Boilard E,

[101] Semple JW

[102] ↵
Xu ZS,
Zhang FP,
Zhang Y,
Ou-Yang YP,
Yu XW,
Wang WL,
et al.
(2017) Prognostic role of the pre-treatment platelet-lymphocyte ratio in pancreatic cancer:a meta-analysis. Oncotarget 8:99003–99012.
OpenUrl

[103] Xu ZS,

[104] Zhang FP,

[105] Zhang Y,

[106] Ou-Yang YP,

[107] Yu XW,

[108] Wang WL,

[109] et al.

[110] Sato N,
Kinoshita A,
Imai N,
Akasu T,
Yokota T,
Iwaku A,
et al.
(2018) Inflammation-based prognostic scores predict disease severity in patients with acute cholecystitis. Eur J Gastroenterol Hepatol 30:484–489.
OpenUrl

[111] Sato N,

[112] Kinoshita A,

[113] Imai N,

[114] Akasu T,

[115] Yokota T,

[116] Iwaku A,

[117] et al.

[118] ↵
Guo J,
Wu M,
Guo L,
Zuo Q
(2018) Pretreatment blood neutrophil/lymphocyte ratio is associated with metastasis and predicts survival in patients with pancreatic cancer. Bull Cancer 105:146–154.
OpenUrl

[119] Guo J,

[120] Wu M,

[121] Guo L,

[122] Zuo Q

[123] ↵
Yu XY,
Li XS,
Li Y,
Liu T,
Wang RT
(2015) Neutrophil-lymphocyte ratio is associated with arterial stiffness in postmenopausal women with osteoporosis. Arch Gerontol Geriatr 61:76–80.
OpenUrl CrossRef PubMed

[124] Yu XY,

[125] Li XS,

[126] Li Y,

[127] Liu T,

[128] Wang RT

[129] ↵
Fisher A,
Srikusalanukul W,
Fisher L,
Smith P
(2016) The Neutrophil to Lymphocyte Ratio on Admission and Short-Term Outcomes in Orthogeriatric Patients. Int J Med Sci 13:588–602.
OpenUrl

[130] Fisher A,

[131] Srikusalanukul W,

[132] Fisher L,

[133] Smith P

[134] ↵
Yilmaz H,
Uyfun M,
Yilmaz TS,
Namuslu M,
Inan O,
Taskin A,
et al.
(2014) Neutrophil-lymphocyte ratio may be superior to C-reactive protein for predicting the occurrence of postmenopausal osteoporosis. Endocr Regul 48:25–33.
OpenUrl CrossRef PubMed

[135] Yilmaz H,

[136] Uyfun M,

[137] Yilmaz TS,

[138] Namuslu M,

[139] Inan O,

[140] Taskin A,

[141] et al.

[142] ↵
Koseoglu SB
(2017) Bone loss &platelet-to-lymphocyte ratio. Biomark Med 11:5–10.
OpenUrl

[143] Koseoglu SB

[144] ↵
Miller AJ,
Jones C,
Liss F,
Abboudi J,
Kirkpatrick W,
Beredjiklian P
(2017) Qualitative Evaluation of Digital Hand X-rays Is Not a Reliable Method to Assess Bone Mineral Density. Arch Bone Jt Surg 5:10–13.
OpenUrl

[145] Miller AJ,

[146] Jones C,

[147] Liss F,

[148] Abboudi J,

[149] Kirkpatrick W,

[150] Beredjiklian P

[151] ↵
Lim HS,
Park YH,
Kim SK
(2016) Relationship between Serum Inflammatory Marker and Bone Mineral Density in Healthy Adults. J Bone Metab 23:27–33.
OpenUrl

[152] Lim HS,

[153] Park YH,

[154] Kim SK

[155] ↵
Wu ZJ,
He JL,
Wei RQ,
Liu B,
Lin X,
Guan J,
et al.
(2015) C-reactive protein and risk of fracture:a systematic review and dose-response meta-analysis of prospective cohort studies. Osteoporos Int 26:49–57.
OpenUrl

[156] Wu ZJ,

[157] He JL,

[158] Wei RQ,

[159] Liu B,

[160] Lin X,

[161] Guan J,

[162] et al.

[163] ↵
Oei L,
Campos-Obando N,
Dehghan A,
Oei EH,
Stolk L,
van Meurs JB,
et al.
(2014) Dissecting the relationship between high-sensitivity serum C-reactive protein and increased fracture risk:the Rotterdam Study. Osteoporos Int 25:1247–1254.
OpenUrl CrossRef PubMed

[164] Oei L,

[165] Campos-Obando N,

[166] Dehghan A,

[167] Oei EH,

[168] Stolk L,

[169] van Meurs JB,

[170] et al.

[171] ↵
Al-Daghri NM,
Aziz I,
Yakout S,
Aljohani NJ,
Al-Saleh Y,
Amer OE,
et al.
(2017) Inflammation as a contributing factor among postmenopausal Saudi women with osteoporosis. Medicine (Baltimore) 96:e5780.
OpenUrl

[172] Al-Daghri NM,

[173] Aziz I,

[174] Yakout S,

[175] Aljohani NJ,

[176] Al-Saleh Y,

[177] Amer OE,

[178] et al.

[179] ↵
Huang C,
Li S
(2016) Association of blood neutrophil lymphocyte ratio in the patients with postmenopausal osteoporosis. Pak J Med Sci 32:762–765.
OpenUrl

[180] Huang C,

[181] Li S

[182] ↵
Guo L,
Gao Z,
Ge H
(2017) Effects of serum 25-hydroxyvitaminD level on decreased bone mineral density at femoral neck and total hip in Chinese type 2 diabetes. PLoS One 12:e0188894.
OpenUrl

[183] Guo L,

[184] Gao Z,

[185] Ge H

[186] ↵
Brincat M,
Gambin J,
Brincat M,
Calleja-Agius J
(2015) The role of vitamin D in osteoporosis. Maturitas 80:329–332.
OpenUrl CrossRef PubMed

[187] Brincat M,

[188] Gambin J,

[189] Brincat M,

[190] Calleja-Agius J

[191] ↵
Akbas EM,
Gungor A,
Ozcicek A,
Akbas N,
Askin S,
Polat M
(2016) Vitamin D and inflammation:evaluation with neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio. Arch Med Sci 12:721–727.
OpenUrl

[192] Akbas EM,

[193] Gungor A,

[194] Ozcicek A,

[195] Akbas N,

[196] Askin S,

[197] Polat M

[198] ↵
Tabatabaeizadeh SA,
Avan A,
Bahrami A,
Khodashenas E 4.,
Esmaeili H,
Ferns GA,
et al.
(2017) High Dose Supplementation of Vitamin D Affects Measures of Systemic Inflammation:Reductions in High Sensitivity C-Reactive Protein Level and Neutrophil to Lymphocyte Ratio (NLR) Distribution. J Cell Biochem 118:4317–4322.
OpenUrl

[199] Tabatabaeizadeh SA,

[200] Avan A,

[201] Bahrami A,

[202] Khodashenas E 4.,

[203] Esmaeili H,

[204] Ferns GA,

[205] et al.

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Platelet/lymphocyte ratio is an independent predictor for osteoporosis

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