Molecular and Cellular Biochemistry

, Volume 419, Issue 1–2, pp 193–203 | Cite as

Increased risk of cardiovascular disease in premenopausal female ragpickers of Eastern India: involvement of inflammation, oxidative stress, and platelet hyperactivity

  • Nandan Kumar Mondal
  • Sanghita Roychoudhury
  • Sayali Mukherjee
  • Shabana Siddique
  • Madhuchanda Banerjee
  • Mark S. Slaughter
  • Twisha Lahiri
  • Manas Ranjan Ray


Millions of poor people in the developing world still thrive on ragpicking. In the present study, we have examined whether ragpicking is associated with increased risk of cardiovascular disease. For this, we have enrolled 112 premenopausal female ragpickers (median age 30 years) and 98 age-matched housemaids as control from Kolkata, Eastern India. Venous blood was drawn for routine hematology; flow cytometry was used to measure generation of reactive oxygen species (ROS) by leukocytes, surface expression of CD62P (P-selectin) in platelets and CD11b in leukocytes. Collagen-induced platelet aggregation was evaluated by aggregometer, and erythrocytic superoxide dismutase (SOD) was measured by spectrophotometry. Soluble P-selectin (sP-sel) and CD40L (sCD40L), neutrophil-activating protein-2 (NAP-2), platelet and plasma serotonin, oxidized low-density lipoprotein (oxLDL), and anticardiolipin antibodies (aCL) in plasma were measured by ELISA. Compared with control, the ragpickers had significantly higher prevalence of hypertension and prehypertension, and hypertension was positively associated with ragpicking. The ragpickers also had higher levels of inflammation (elevated NAP-2), oxidative stress (elevated ROS generation with depleted SOD) with oxLDL, platelet activation and aggregability, soluble CD40 ligand, with altered serotonin level (rose in plasma but depleted in platelet). A greater percentage of ragpickers had elevated serum level of aCL of the IgG and IgM isotypes than the controls. The results suggest that the occupation of ragpicking increases the risk of cardiovascular diseases in premenopausal women of Eastern India via inflammation, oxidative stress, platelet hyperactivity, and hypertension.


Ragpickers Hypertension Oxidative stress Platelet function Cardiovascular health India 



The authors gratefully acknowledge the financial support received from the Central Pollution Control Board under Ministry of Environment and Forests, Government of India.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Das S, Bhattacharyya BK (2014) Estimation of municipal solid waste generation and future trends in greater metropolitan regions of Kolkata, India. J Indust Eng Manag Inno 1:31–38CrossRefGoogle Scholar
  2. 2.
    Uplap PA, Bhate K (2014) Health profile of women ragpicker members of a nongovernmental organization in Mumbai, India. Indian J Occup Environ Med 18:140–144CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hunt C (1996) Child waste pickers in India: the occupation and its health risks. Environ Urban 8:111–118CrossRefGoogle Scholar
  4. 4.
    Ray MR, Roychoudhury S, Mukherjee S, Siddiqe S, Banerjee M, Akolkar AB, Sengupta B, Lahiri T (2009) Airway inflammation and upregulation of b2 Mac-1 integrin expression on circulating leukocytes of female ragpickers in India. J Occup Health 51:232–238CrossRefPubMedGoogle Scholar
  5. 5.
    Ray MR, Mukherjee G, Roychoudhury S, Lahiri T (2004) Respiratory and general health impairments of ragpickers in India: a study in Delhi. Int Arch Occup Environ Health 77:595–598CrossRefPubMedGoogle Scholar
  6. 6.
    Robb AO, Din JN, Mills NL, Smith IB, Blomberg A, Zikry MN, Raftis JB, Newby DE, Denison FC (2010) The influence of the menstrual cycle, normal pregnancy and pre-eclampsia on platelet activation. Thromb Haemostat 103:372–378CrossRefGoogle Scholar
  7. 7.
    Ripoche J (2011) Blood platelets and inflammation: their relationship with liver and digestive diseases. Clin Res Hepatol Gastrenterol 35:353–357CrossRefGoogle Scholar
  8. 8.
    Tang YQ, Yeaman MR, Selsted ME (2002) Antimicrobial peptides from human platelets. Infect Immun 70:6524–6533CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Li Z, Yang F, Dunn S, Gross AK, Smyth SS (2011) Platelets as immune mediators: their role in host defense responses and sepsis. Thromb Res 127:184–188CrossRefPubMedGoogle Scholar
  10. 10.
    McNicol A, Israels SJ (2008) Beyond hemostasis: the role of platelets in inflammation, malignancy and infection. Cardiovasc Hematol Disord: Drug Targets 8:99–117CrossRefGoogle Scholar
  11. 11.
    Yee J, Sadar MD, Sin DD, Kuzyk M, Xing L, Kondra J, McWilliams A, Man SF, Lam S (2009) Con 233 nective tissue-activating peptide III: a novel blood biomarker for early lung cancer detection. J Clin Oncol 27:2787–2792CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Lam FW, Burns AR, Smith CW, Rumbaut RE (2011) Platelets enhance neutrophil transendothelial migration via P-selectin glycoprotein ligand-1. Am J Physiol Heart Circ Physiol 300:H468–H475CrossRefPubMedGoogle Scholar
  13. 13.
    Senchenkov E, Khoretonenko MV, Leskov IL, Ostanin DV, Stokes KY (2011) P-selectin mediates the microvascular dysfunction associated with persistent cytomegalovirus infection in normocholesterolemic and hypercholesterolemic mice. Microcirculation 18:452–462CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Katz JN, Kolappa KP, Becker RC (2011) Beyond thrombosis: the versatile platelet in critical illness. Chest 139:658–668CrossRefPubMedGoogle Scholar
  15. 15.
    Assinger A, Koller F, Schmid W, Zellner M, Koller E, Volf I (2010) Hypochlorite-oxidized LDL induces intraplatelet ROS formation and surface exposure of CD40L-a prominent role of CD36. Atherosclerosis 213:129–134CrossRefPubMedGoogle Scholar
  16. 16.
    Kaufman J, Spinelli SL, Schultz E, Blumberg N, Phipps RP (2007) Release of biologically active CD154 during collection and storage of platelet concentrates prepared for transfusion. J Thromb Haemost 5:788–796CrossRefPubMedGoogle Scholar
  17. 17.
    Siess W (2006) Platelet interaction with bioactive lipids formed by mild oxidation of low-density lipoprotein. Pathophysiol Haemost Thromb 35:292–304CrossRefPubMedGoogle Scholar
  18. 18.
    Sherer Y, Shemesh J, Tenenbaum A, Praprotnik S, Harats D, Fisman EZ, Blank M, Motro M, Shoenfeld Y (2000) Coronary calcium and anti-cardiolipin antibody are elevated in patients with typical chest pain. Am J Cardiol 86:1306–1311CrossRefPubMedGoogle Scholar
  19. 19.
    Sherer Y, Tenenbaum A, Praprotnik S, Shemesh J, Blank M, Fisman EZ, Harats D, George J, Levy Y, Peter JB, Motro M, Shoenfeld Y (2001) Coronary artery disease but not cornary calcification is associated with elevated levels of cardiolipin, beta-2-glycoprotein-1, and oxidized LDL antibodies. Cardiology 95:20–24CrossRefPubMedGoogle Scholar
  20. 20.
    Roell A, Schueller P, Schultz A, Losel R, Wehling M, Christ M, Feuring M (2007) Effect of oral contraceptives and ovarian cycle on platelet function. Platelets 18:165–170CrossRefPubMedGoogle Scholar
  21. 21.
    O’Brien E, Petrie J, Littler WA, De Swiet M, Padfield P, Dillon MJ (1997) Blood Pressure Measurement: Recommendations of the British Hypertension Society, 3rd edn. BMJ Publishing Group, LondonGoogle Scholar
  22. 22.
    Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr et al (2003) Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension 42:1206–1252CrossRefPubMedGoogle Scholar
  23. 23.
    Whitworth JA (2003) World Health Organization (WHO)/International Society of Hypertension (ISH) statement on management of hypertension. J Hypertens 21:1983–1992CrossRefPubMedGoogle Scholar
  24. 24.
    Rothe G, Valet G (1990) Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′-dichlorofluorescein. J Leukoc Biol 47:440–448PubMedGoogle Scholar
  25. 25.
    Paoletti F, Aldinucci D, Mocali A, Caparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541CrossRefPubMedGoogle Scholar
  26. 26.
    Banerjee A, Mondal NK, Das D, Ray MR (2012) Neutrophilic inflammatory response and oxidative stress in premenopausal women chronically exposed to indoor air pollution from biomass burning. Inflammation 35:671–683CrossRefPubMedGoogle Scholar
  27. 27.
    Mondal NK, Mukherjee B, Das D, Ray MR (2010) Micronucleus formation, DNA damage and repair in premenopausal women chronically exposed to high level of indoor air pollution from biomass fuel use in rural India. Mutat Res 697:47–54CrossRefPubMedGoogle Scholar
  28. 28.
    Mondal NK, Roy A, Mukherjee B, Das D, Ray MR (2010) Indoor air pollution from biomass burning activates Akt in airway cells and peripheral blood lymphocytes: a study among premenopausal women in rural India. Toxicol Pathol 38:1085–1098CrossRefPubMedGoogle Scholar
  29. 29.
    Mondal NK, Sorensen E, Hiivala N, Feller E, Griffith B, Wu ZJ (2013) Oxidative stress, DNA damage and repair in heart failure patients after implantation of continuous flow left ventricular assist devices. Int J Med Sci 10:883–893CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Türkoğlu O, Bariş N, Kütükçüler N, Senarslan O, Güneri S, Atilla G (2008) Evaluation of serum anti-cardiolipin and oxidized low-density lipoprotein levels in chronic periodontitis patients with essential hypertension. J Periodontol 79:332–340CrossRefPubMedGoogle Scholar
  31. 31.
    Blann AD, Draper Z (2011) Platelet activation as a marker of heart attack. Clin Chim Acta 412:841–842CrossRefPubMedGoogle Scholar
  32. 32.
    Silverstein RL (2009) Inflammation, atherosclerosis, and arterial thrombosis: role of the scavenger receptor CD36. Clevel Clin J Med 76:S27–S30CrossRefGoogle Scholar
  33. 33.
    Chen K, Febbraio M, Li W, Silverstein RL (2008) A specific CD36-dependent signaling pathway is required for platelet activation by oxidized low-density protein. Circ Res 102:1512–1519CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Relou IA, Hackeng CM, Akkerman JW, Malle E (2003) Low-density lipoprotein and its effect on human blood platelets. Cell Mol Life Sci 60:961–971PubMedGoogle Scholar
  35. 35.
    Yıldırım ZK, Orhan MF, Büyükavcı M (2011) Platelet function alterations and their relation to P-selectin (CD62P) expression in children with iron deficiency anemia. Blood Coagul Fibrinolysis 22:98–101CrossRefPubMedGoogle Scholar
  36. 36.
    Fusegawa Y, Goto S, Handa S, Kawada T, Ando Y (1999) Platelet spontaneous aggregation in platelet-rich plasma is increased in habitual smokers. Thromb Res 93:271–278CrossRefPubMedGoogle Scholar
  37. 37.
    Rubenstein D, Jesty J, Bluestein D (2004) Differences between mainstream and sidestream cigarette smoke extracts and nicotine in the activation of platelets under static and flow conditions. Circulation 109:78–83CrossRefPubMedGoogle Scholar
  38. 38.
    Dewitte A, Tanga A, Villeneuve J, Lepreux S, Ouattara A, Desmoulière A, Combe C, Ripoche J (2015) New frontiers for platelet CD154. Exp Hematol Oncol 4:6. doi: 10.1186/s40164-015-0001-6.eCollection CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Ge H, Zhou Y, Liu X, Nie X, Wang Z, Guo Y, Chen W, Yang Q (2012) Relationship Between Plasma Inflammatory Markers and Platelet Aggregation in Patients With Clopidogrel Resistance After Angioplasty. Angiol 63:62–66CrossRefGoogle Scholar
  40. 40.
    Yacoub D, Hachem A, Théorêt JF, Gillis MA, Mourad W, Merhi Y (2010) Enhanced levels of soluble CD40 ligand exacerbate platelet aggregation and thrombus formation through a CD40-dependent tumor necrosis factor receptor-associated factor-2/Rac1/p38 mitogen-activated protein kinase signaling pathway. Arterioscler Thromb Vasc Biol 30:2424–2433CrossRefPubMedGoogle Scholar
  41. 41.
    Schonbeck U, Varo N, Libby P, Buring J, Ridker PM (2001) Soluble CD40L and cardiovascular risk in women. Circulation 104:2266–2268CrossRefPubMedGoogle Scholar
  42. 42.
    Blann AD, Tan KT, Tayebjee MH, Davagnanam I, Moss M, Lip GY (2005) Soluble CD40L in peripheral artery disease. Relationship with disease severity, platelet markers and the effects of angioplasty. Thromb Haemost 93:578–583PubMedGoogle Scholar
  43. 43.
    Balija M, Bordukalo-Niksic T, Mokrovic G, Banovic M, Cicin-Sain L, Jernej B (2011) Serotonin level and serotonin uptake in human platelets: a variable interrelation under marked physiological influences. Clin Chim Acta 412:299–304CrossRefPubMedGoogle Scholar
  44. 44.
    Pracharová L, Okénková K, Lojek A, Cíz M (2010) Serotonin and its 5-HT(2) receptor hydrochloride inhibit the oxidative burst in total leukocytes but not in isolated neutrophils. Life Sci 86:518–523CrossRefPubMedGoogle Scholar
  45. 45.
    Camacho A, Dimsdale JE (2000) Platelets and psychiatry: lessons learned from old and new studies. Psychosom Med 62:326–336CrossRefPubMedGoogle Scholar
  46. 46.
    Piletz JE, Zhu H, Madakasira S, Pazzaglia P, Lindsay DeVane C, Goldman N, Halaris A (2000) Elevated P-selectin on platelets in depression: response to bupropion. J Psychiatr Res 34:397–404CrossRefPubMedGoogle Scholar
  47. 47.
    Brandt E, Van Damme J, Flad HD (1991) Neutrophils can generate their activator neutrophil-activating peptide 2 by proteolytic cleavage of platelet-derived connective tissue-activating peptide III. Cytokine 3:311–321CrossRefPubMedGoogle Scholar
  48. 48.
    Goel N, Tuli A, Choudhry R (2006) The role of aspirin versus aspirin and heparin in cases of recurrent abortions with raised anticardiolipin antibodies. Med Sci Monit 12:CR132–CR136PubMedGoogle Scholar
  49. 49.
    De Angelis V, Scurati S, Raschi E, Liutkus A, Belot A, Borghi MO, Meroni PL, Cimaz R (2009) Pro-inflammatory genotype as a risk factor for aPL-associated thrombosis: report of a family with multiple anti-phospholipid positive members. J Autoimmun 32:60–63CrossRefPubMedGoogle Scholar
  50. 50.
    Marai I, Shechter M, Langevitz P, Gilburd B, Rubenstein A, Matssura E, Sherer Y, Shoenfeld Y (2008) Anti-cardiolipin antibodies and endothelial function in patients with coronary artery disease. Am J Cardiol 101:1094–1097CrossRefPubMedGoogle Scholar
  51. 51.
    Orshal JM, Khalil RA (2004) Gender, sex hormones, and vascular tone. Am J Physiol Regul Integ Comp Physiol 286:R233–R249CrossRefGoogle Scholar
  52. 52.
    Pepine CJ (2004) Ischemic heart disease in women: facts and wishful thinking. J Am Coll Cardiol 43:1727–1730CrossRefPubMedGoogle Scholar
  53. 53.
    Labana S, Cervellione KL, Mangla M, Virk Z, Cheema A, Edasery D, Bhasin N, Jauhar R (2009) Further evidence that smaller coronary artery diameter in Asian-Indians is a risk factor for development of coronary artery disease. Chest. doi: 10.1378/chest.134.4 Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Nandan Kumar Mondal
    • 1
    • 2
  • Sanghita Roychoudhury
    • 1
  • Sayali Mukherjee
    • 1
  • Shabana Siddique
    • 1
  • Madhuchanda Banerjee
    • 1
  • Mark S. Slaughter
    • 2
  • Twisha Lahiri
    • 1
  • Manas Ranjan Ray
    • 1
  1. 1.Department of Experimental HematologyChittaranjan National Cancer InstituteKolkataIndia
  2. 2.Department of Cardiovascular and Thoracic Surgery, Cardiovascular Innovation InstituteUniversity of Louisville School of MedicineLouisvilleUSA

Personalised recommendations