Skip to main content

Advertisement

SpringerLink
Log in

Inflammation as Possible Mediator for the Relationship Between Lung and Arterial Function

  • Published:
Lung Aims and scope Submit manuscript

Abstract

Introduction

Reduced lung function is associated with a risk for the development of cardiovascular disease. This association may be due to chronic inflammation which is often present in those with reduced lung function.

Purpose

We investigated the possible role of systemic inflammation as the mediator between lung function and arterial stiffness in 1534 black South Africans.

Methods

Spirometric data including forced expiratory volume in 1 s (FEV1) and forced vital capacity (FVC) were obtained. C-reactive protein (CRP), interleukin-6 (IL-6), blood pressure (BP) and carotid-radial pulse wave velocity (PWV) were determined.

Results

In multivariable-adjusted models, an independent inverse association was found between IL-6 and FEV1 (β = −0.20, p < 0.001) and FVC (β = −0.18, p < 0.001). Similar results were found for CRP. PWV was inversely associated with FEV1 (β = −0.06, p = 0.037). No association was found between inflammatory markers, BP or PWV.

Conclusion

Reduced lung function was associated with increased inflammation and arterial stiffness. The lack of association between arterial stiffness and inflammatory markers suggests that inflammation may not be the mediating link between lung and vascular function in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Engström G, Wollmer P, Valind S et al (2001) Blood pressure increase between 55 and 68 years of age is inversely related to lung function: longitudinal results from the cohort study ‘Men born in 1914’. J Hypertens 19:1203–1208

    Article  PubMed  Google Scholar 

  2. Sparrow D, Weiss ST, Vokonas PS et al (1988) Forced vital capacity and the risk of hypertension. The Normative Aging Study. Am J Epidemiol 127:734–741

    CAS  PubMed  Google Scholar 

  3. Wu Y, Vollmer WM, Buist AS et al (1998) Relationship between lung function and blood pressure in Chinese men and women of Beijing and Guangzhou. PRC-USA Cardiovascular and Cardiopulmonary Epidemiology Research Group. Int J Epidemiol 27:49–56. doi:10.1093/ije/27.1.49

    Article  CAS  PubMed  Google Scholar 

  4. Engstrom G, Lind P, Hedblad B et al (2002) Lung function and cardiovascular risk: relationship with inflammation-sensitive plasma proteins. Circulation 106:2555–2560. doi:10.1161/01.CIR.0000037220.00065.0D

    Article  CAS  PubMed  Google Scholar 

  5. Sin DD, Man SF (2003) Why are patients with chronic obstructive pulmonary disease at increased risk of cardiovascular diseases? The potential role of systemic inflammation in chronic obstructive pulmonary disease. Circulation 107:1514–1519. doi:10.1161/01.CIR.0000056767.69054.B3

    Article  PubMed  Google Scholar 

  6. Eid AA, Ionescu AA, Nixon LS et al (2001) Inflammatory response and body composition in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164:1414–1418. doi:10.1164/ajrccm.164.8.2008109

    Article  CAS  PubMed  Google Scholar 

  7. Wouters EF, Creutzberg EC, Schols AM (2002) Systemic effects in COPD. Chest 121:127S–130S. doi:10.1378/chest.121.5_suppl.127S

    Article  PubMed  Google Scholar 

  8. Barnes P, Celli B (2009) Systemic manifestations and comorbidities of COPD. Eur Respir J 33:1165–1185. doi:10.1183/09031936.00128008

    Article  CAS  PubMed  Google Scholar 

  9. Barr RG, Mesia-Vela S, Austin JH et al (2007) Impaired flow-mediated dilation is associated with low pulmonary function and emphysema in ex-smokers: the Emphysema and Cancer Action Project (EMCAP) Study. Am J Respir Crit Care Med 176:1200–1207. doi:10.1164/rccm.200707-980OC

    Article  PubMed Central  PubMed  Google Scholar 

  10. Yasmin CM, McEniery CM, Wallace S et al (2004) C-reactive protein is associated with arterial stiffness in apparently healthy individuals. Arterioscler Thromb Vasc Biol 24:969–974. doi:10.1161/01.ATV.zhq0504.0173

    Article  CAS  PubMed  Google Scholar 

  11. Mahmud A, Feely J (2005) Arterial stiffness is related to systemic inflammation in essential hypertension. Hypertension 46:1118–1122. doi:10.1161/01.HYP.0000185463.27209.b0

    Article  CAS  PubMed  Google Scholar 

  12. Willum-Hansen T, Staessen JA, Torp-Pedersen C et al (2006) Prognostic value of aortic pulse wave velocity as index of arterial stiffness in the general population. Circulation 113:664–670. doi:10.1161/CIRCULATIONAHA.105.579342

    Article  PubMed  Google Scholar 

  13. Mattace-Raso FUS, van der Cammen TJM, Hofman A et al (2006) Arterial stiffness and risk of coronary heart disease and stroke. The Rotterdam study. Circulation 113:657–663. doi:10.1161/CIRCULATIONAHA.105.555235

    Article  PubMed  Google Scholar 

  14. Shokawa T, Imazu M, Yamamoto H et al (2005) Pulse wave velocity predicts cardiovascular mortality: findings from the Hawaii-Los Angeles-Hiroshima study. Circulation 69:259–264. doi:10.1253/circj.69.259

    Article  Google Scholar 

  15. Duprez DA, Jacobs DR Jr, Lutsey PL et al (2011) Association of small artery elasticity with incident cardiovascular disease in older adults: the multi-ethnic study of atherosclerosis. Am J Epidemiol 174:528–536. doi:10.1093/aje/kwr120

    Article  PubMed Central  PubMed  Google Scholar 

  16. Lloyd-Sherlock P, Beard J, Minicuci N et al (2014) Hypertension among older adults in low- and middle-income countries: prevalence, awareness and control. Int J Epidemiol 43:116–128. doi:10.1093/ije/dyt215

    Article  PubMed Central  PubMed  Google Scholar 

  17. Duong M, Islam S, Rangarajan S et al (2013) Global differences in lung function by region (PURE): an international, community-based prospective study. Lancet Respir Med 1:599–609. doi:10.1016/S2213-2600(13)70164-4

    Article  PubMed  Google Scholar 

  18. Teo K, Chow CK, Vaz M et al (2009) The Prospective Urban Rural Epidemiology (PURE) study: examining the impact of societal influences on chronic noncommunicable diseases in low-, middle-, and high-income countries. Am Heart J 158:1–7. doi:10.1016/j.ahj.2009.04.019

    Article  PubMed  Google Scholar 

  19. Marfell-Jones M, Olds T, Stewart A, Carter L (eds) (2006) International Standards for Anthropometric Assessment. International Society for the Advancement of Kinanthropometry

  20. Standardization of Spirometry (1994) Update. American Thoracic Society (1995). Am J Respir Crit Care Med 152:1107–1136

    Google Scholar 

  21. Ridker PM (2003) Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107:363–369. doi:10.1161/01.CIR.0000053730.47739.3C

    Article  PubMed  Google Scholar 

  22. Duprez DA, Hearst MO, Lutsey PL, Herrington DM, Ouyang P, Barr RG et al (2013) Associations among lung function, arterial elasticity, and circulating endothelial and inflammation markers: the multiethnic study of atherosclerosis. Hypertension 61(2):542–548

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Gimeno D, Delclos GL, Ferrie JE et al (2011) Association of CRP and IL-6 with lung function in a middle-aged population initially free from self-reported respiratory problems: the Whitehall II study. Eur J Epidemiol 26:135–144. doi:10.1007/s10654-010-9526-5

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Bolton C, Schumacher W, Cockcroft J et al (2011) The CRP genotype, serum levels and lung function in men: the Caerphilly Prospective Study. Clin Sci 120:347–355. doi:10.1042/CS20100504

    Article  PubMed  Google Scholar 

  25. Boulet LP, Chakir J, Dube J et al (1998) Airway inflammation and structural changes in airway hyper-responsiveness and asthma: an overview. Can Respir J 5:16–21

    CAS  PubMed  Google Scholar 

  26. Brunner EJ, Shipley MJ, Witte DR et al (2011) Arterial stiffness, physical function, and functional limitation: the Whitehall II Study. Hypertension 57:1003–1009. doi:10.1161/HYPERTENSIONAHA.110.168864

    Article  CAS  PubMed  Google Scholar 

  27. Bolton CE, Cockcroft JR, Sabit R et al (2009) Lung function in mid-life compared with later life is a stronger predictor of arterial stiffness in men: the Caerphilly Prospective Study. Int J Epidemiol 38:867–876. doi:10.1093/ije/dyn374

    Article  PubMed  Google Scholar 

  28. Zureik M, Benetos A, Neukirch C et al (2001) Reduced pulmonary function is associated with central arterial stiffness in men. Am J Respir Crit Care Med 164:2181–2185. doi:10.1164/ajrccm.164.12.2107137

    Article  CAS  PubMed  Google Scholar 

  29. Wilk JB, Walter RE, Laramie JM et al (2007) Framingham Heart Study genome-wide association: results for pulmonary function measures. BMC Med Genet 8:S8. doi:10.1186/1471-2350-8-S1-S8

    Article  PubMed Central  PubMed  Google Scholar 

  30. Schutte A, Van Vuuren D, Van Rooyen J et al (2006) Inflammation, obesity and cardiovascular function in African and Caucasian women from South Africa: the POWIRS study. J Hum Hypertens 20:850–859. doi:10.1038/sj.jhh.1002065

    Article  CAS  PubMed  Google Scholar 

  31. Marott SC, Nordestgaard BG, Zacho J et al (2010) Does elevated C-reactive protein increase atrial fibrillation risk? A mendelian randomization of 47,000 individuals from the general population. J Am Coll Cardiol 56:789–795. doi:10.1016/j.jacc.2010.02.066

    Article  PubMed  Google Scholar 

  32. Wensley F, Gao P, Burgess S et al (2011) Association between C reactive protein and coronary heart disease: mendelian randomisation analysis based on individual participant data. Br Med J 15(342):d548. doi:10.1136/bmj.d548

    Google Scholar 

  33. Ridker PM, Hennekens CH, Buring JE et al (2000) C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 342:836–843. doi:10.1056/NEJM200003233421202

    Article  CAS  PubMed  Google Scholar 

  34. Ridker PM, Buring JE, Shih J et al (1998) Prospective study of C-reactive protein and the risk of future cardiovascular events among apparently healthy women. Circulation 98:731–733. doi:10.1161/01.CIR.98.8.731

    Article  CAS  PubMed  Google Scholar 

  35. Ridker PM, Cushman M, Stampfer MJ et al (1998) Plasma concentration of C-reactive protein and risk of developing peripheral vascular disease. Circulation 97:425–428. doi:10.1161/01.CIR.97.5.425

    Article  CAS  PubMed  Google Scholar 

  36. Andoh N, Minami J, Ishimitsu T et al (2006) Relationship between markers of inflammation and brachial-ankle pulse wave velocity in Japanese men. Int Heart J 47:409–420. doi:10.1536/ihj.47.409

    Article  CAS  PubMed  Google Scholar 

  37. Kullo IJ, Seward JB, Bailey KR et al (2005) C-reactive protein is related to arterial wave reflection and stiffness in asymptomatic subjects from the community. Am J Hypertens 18:1123–1129. doi:10.1016/j.amjhyper.2005.03.730

    Article  CAS  PubMed  Google Scholar 

  38. Mattace-Raso FUS, van der Cammen TJM, van der Meer IM et al (2004) C-reactive protein and arterial stiffness in older adults: the Rotterdam Study. Atherosclerosis 176:111–116. doi:10.1016/j.atherosclerosis.2004.04.014

    Article  CAS  PubMed  Google Scholar 

  39. Kasayama S, Saito H, Mukai M et al (2005) Insulin sensitivity independently influences brachial–ankle pulse-wave velocity in non-diabetic subjects. Diabetic Med 22:1701–1706. doi:10.1111/j.1464-5491.2005.01718

    Article  CAS  PubMed  Google Scholar 

  40. Ahluwalia N, Drouet L, Ruidavets J et al (2006) Metabolic syndrome is associated with markers of subclinical atherosclerosis in a French population-based sample. Atherosclerosis 186:345–353. doi:10.1016/j.atherosclerosis.2005.07.021

    Article  CAS  PubMed  Google Scholar 

  41. Nishida M, Moriyama T, Ishii K et al (2007) Effects of IL-6, adiponectin, CRP and metabolic syndrome on subclinical atherosclerosis. Clin Chim Acta 384:99–104. doi:10.1016/j.cca.2007.06.009

    Article  CAS  PubMed  Google Scholar 

  42. Tasaki N, Nakajima M, Yamamoto H et al (2003) Influence of Chlamydia pneumoniae infection on aortic stiffness in healthy young men. Atherosclerosis 171:117–122. doi:10.1016/j.atherosclerosis.2003.08.004

    Article  CAS  PubMed  Google Scholar 

  43. Schumacher W, Cockcroft J, Timpson NJ et al (2009) Association between C-reactive protein genotype, circulating levels, and aortic pulse wave velocity. Hypertension 53:150–157. doi:10.1161/HYPERTENSIONAHA.108.117622

    Article  CAS  PubMed  Google Scholar 

  44. Sabit R, Bolton CE, Edwards PH et al (2007) Arterial stiffness and osteoporosis in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 175:1259–1265. doi:10.1164/rccm.200701-067OC

    Article  PubMed  Google Scholar 

  45. Stewart S, Libhaber E, Carrington M et al (2011) The clinical consequences and challenges of hypertension in urban-dwelling black Africans: insights from the Heart of Soweto Study. Int J Cardiol 146:22–27. doi:10.1016/j.ijcard.2009.05.061

    Article  PubMed  Google Scholar 

  46. Vorster HH, Bourne LT, Venter CS et al (1999) Contribution of nutrition to the health transition in developing countries: a framework for research and intervention. Nutr Rev 57:341–349. doi:10.1111/j.1753-4887.1999.tb06911

    Article  CAS  PubMed  Google Scholar 

  47. Lemogoum D, Van Bortel L, Leeman M et al (2006) Ethnic differences in arterial stiffness and wave reflections after cigarette smoking. J Hypertens 24:683–689. doi:10.1097/01.hjh.0000217850.87960.16

    Article  CAS  PubMed  Google Scholar 

  48. Schutte AE, Schutte R, Huisman HW et al (2012) Are behavioural risk factors to be blamed for the conversion from optimal blood pressure to hypertensive status in Black South Africans? A 5-year prospective study. Int J Epidemiol 41:1114–1123. doi:10.1093/ije/dys106

    Article  PubMed  Google Scholar 

  49. Boreham CA, Ferreira I, Twisk JW et al (2004) Cardiorespiratory fitness, physical activity, and arterial stiffness: the Northern Ireland Young Hearts Project. Hypertension 44:721–726. doi:10.1161/01.HYP.0000144293.40699.9a

    Article  CAS  PubMed  Google Scholar 

  50. Barinas-Mitchell E, Kuller LH, Sutton-Tyrrell K et al (2006) Effect of weight loss and nutritional intervention on arterial stiffness in type 2 diabetes. Diabetes Care 29:2218–2222. doi:10.2337/dc06-0665

    Article  CAS  PubMed  Google Scholar 

  51. Mahmud A, Feely J (2003) Effect of smoking on arterial stiffness and pulse pressure amplification. Hypertension 41:183–187. doi:10.1161/01.HYP.0000047464.66901.60

    Article  CAS  PubMed  Google Scholar 

  52. Mahmud A, Feely J (2002) Divergent effect of acute and chronic alcohol on arterial stiffness. Am J Hypertension 15:240–243. doi:10.1016/S0895-7061(01)02315-9

    Article  CAS  Google Scholar 

  53. Laurent S, Boutouyrie P, Asmar R et al (2001) Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37:1236–1241. doi:10.1161/01.HYP.37.5.1236

    Article  CAS  PubMed  Google Scholar 

  54. London GM, Blacher J, Pannier B et al (2001) Arterial wave reflections and survival in end-stage renal failure. Hypertension 38:434–438. doi:10.1161/01.HYP.38.3.434

    Article  CAS  PubMed  Google Scholar 

  55. Stefanadis C, Dernellis J, Tsiamis E et al (2000) Aortic stiffness as a risk factor for recurrent acute coronary events in patients with ischaemic heart disease. Eur Heart J 21:390–396. doi:10.1053/euhj.1999.1756

    Article  CAS  PubMed  Google Scholar 

  56. Chaturvedi N, Bulpitt CJ, Leggetter S et al (2004) Ethnic differences in vascular stiffness and relations to hypertensive target organ damage. J Hypertens 22:1731–1737. doi:10.1097/00004872-200409000-00017

    Article  CAS  PubMed  Google Scholar 

  57. Din-Dzietham R, Couper D, Evans G et al (2004) Arterial stiffness is greater in African Americans than in whites: evidence from the Forsyth County, North Carolina, ARIC cohort. Am J Hypertens 17:304–313. doi:10.1016/j.amjhyper.2003.12.004

    Article  PubMed  Google Scholar 

  58. Heffernan KS, Jae SY, Fernhall B (2007) Racial differences in arterial stiffness after exercise in young men. Am J Hypertens 20:840–845. doi:10.1016/j.amjhyper.2007.03.015

    Article  PubMed  Google Scholar 

  59. Zheng Z, Rosamond WD, Chambless LE et al (2005) Lower extremity arterial disease assessed by ankle-brachial index in a middle-aged population of African Americans and whites: the Atherosclerosis Risk in Communities (ARIC) Study. Am J Prev Med 29:42–49. doi:10.1016/j.amepre.2005.07.019

    Article  PubMed  Google Scholar 

  60. Mayosi BM, Flisher AJ, Lalloo UG et al (2009) The burden of non-communicable diseases in South Africa. Lancet 374:934–947. doi:10.1016/S0140-6736(09)61087-4

    Article  PubMed  Google Scholar 

  61. Rees D, Murray J (2007) Silica, silicosis and tuberculosis. Int J Tuberc Lung Dis 11:474–484. doi:10.1186/1745-6673-9-2

    CAS  PubMed  Google Scholar 

  62. Chronic diseases of lifestyle in South Africa: 1995–2005. In: Ehrlich R, Jithoo A (eds) Medical Research Council—technical report. Cape Town: South African Medical Research Council; 2006. pp 1–266

  63. Schutte AE, Huisman HW, Schutte R et al (2011) Arterial stiffness profiles: investigating various sections of the arterial tree of African and Caucasian people. Clin Exp Hypertens 33:511–517. doi:10.3109/10641963.2011.561897

    Article  PubMed  Google Scholar 

  64. Grey E, Bratteli C, Glasser SP et al (2003) Reduced small artery but not large artery elasticity is an independent risk marker for cardiovascular events. Am J Hypertens 16:265–269. doi:10.1016/S0895-7061(02)03271-5

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank all supporting staff and the participants of the PURE study and in particular: PURE-South Africa: The PURE-NWP-SA research team, field workers and office staff in the Africa Unit for Transdisciplinary Health Research (AUTHeR) and the Hypertension in Africa Research Team (HART), Faculty of Health Sciences, North-West University, South Africa. PURE International: Dr. S Yusuf and the PURE project office staff at the Population Health Research Institute (PHRI), Hamilton Health Sciences and McMaster University. ON, Canada.

Author information

Authors and Affiliations

  1. Hypertension in Africa Research Team (HART), North-West University (Potchefstroom Campus), Private Bag X6001, Potchefstroom, 2520, South Africa

    Yolandi van Rooyen, Aletta E. Schutte, Hugo W. Huisman & Johannes M. van Rooyen

  2. Occupational Hygiene and Health Research Initiative (OHHRI), North-West University, Potchefstroom, South Africa

    Fritz C. Eloff & Johan L. Du Plessis

  3. Africa Unit for Transdisciplinary Health Research (AUTHeR), North-West University, Potchefstroom, South Africa

    Annamarie Kruger

  4. MRC Research Unit for Hypertension and Cardiovascular Disease, North-West University, Potchefstroom, South Africa

    Aletta E. Schutte & Annamarie Kruger

Authors
  1. Yolandi van Rooyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aletta E. Schutte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hugo W. Huisman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fritz C. Eloff
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Johan L. Du Plessis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Annamarie Kruger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Johannes M. van Rooyen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes M. van Rooyen.

Ethics declarations

Statement of Financial Disclosure

This work was supported by the South Africa Netherlands Research Programme on Alternatives in Development, South African National Research Foundation [GUN numbers 2069139 and FA2006040700010], North-West University, Roche Diagnostics South Africa, Population Health Research Institute and South African Medical Research Council. Lastly, we thank South Africa’s National Research Fund (NRF) Thuthuka grant for financial assistance provided in carrying out this study. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors, and therefore, the NRF do not accept any liability in regard thereto.

Conflict of interest

All authors have declared no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van Rooyen, Y., Schutte, A.E., Huisman, H.W. et al. Inflammation as Possible Mediator for the Relationship Between Lung and Arterial Function. Lung 194, 107–115 (2016). https://doi.org/10.1007/s00408-015-9804-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00408-015-9804-9

Keywords

Search

Navigation