Reduced Neutrophil Chemotaxis and Infiltration Contributes to Delayed Resolution of Cutaneous Wound Infection with Advanced Age
Open accessAbstract
Advanced age is associated with alterations in innate and adaptive immune responses, which contribute to an increased risk of infection in elderly patients. Coupled with this immune dysfunction, elderly patients demonstrate impaired wound healing with elevated rates of wound dehiscence and chronic wounds. To evaluate how advanced age alters the host immune response to cutaneous wound infection, we developed a murine model of cutaneous Staphylococcus aureus wound infection in young (3–4 mo) and aged (18–20 mo) BALB/c mice. Aged mice exhibit increased bacterial colonization and delayed wound closure over time compared with young mice. These differences were not attributed to alterations in wound neutrophil or macrophage TLR2 or FcγRIII expression, or age-related changes in phagocytic potential and bactericidal activity. To evaluate the role of chemotaxis in our model, we first examined in vivo chemotaxis in the absence of wound injury to KC, a neutrophil chemokine. In response to a s.c. injection of KC, aged mice recruited fewer neutrophils at increasing doses of KC compared with young mice. This paralleled our model of wound infection, where diminished neutrophil and macrophage recruitment was observed in aged mice relative to young mice despite equivalent levels of KC, MIP-2, and MCP-1 chemokine levels at the wound site. This reduced leukocyte accumulation was also associated with lower levels of ICAM-1 in wounds from aged mice at early time points. These age-mediated defects in early neutrophil recruitment may alter the dynamics of the inflammatory phase of wound healing, impacting macrophage recruitment, bacterial clearance, and wound closure.
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Neutrophil numbers do not change with age, but neutrophils show profound functional alterations.
“The number of neutrophils does not change with age, but profound functional alterations have been observed in this cell type [37,38].”
From Aging of the immune system: Focus on inflammation and vaccination (2016) · cites this paper as [38]
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Getting to the site of inflammation: the leukocyte adhesion cascade updated
Ley, K., Laudanna, C., Cybulsky, M. I., & Nourshargh, S. (2007) · Nature Reviews Immunology · doi:10.1038/nri2156 · Cited by 4,354 · see citing works
PERSPECTIVE ARTICLE: Growth factors and cytokines in wound healing
Barrientos, S., Stojadinovic, O., Golinko, M. S., Brem, H., & Tomic‐Canic, M. (2008) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2008.00410.x · Cited by 3,583 · see citing works
Toll-like receptors in innate immunity
Takeda, K. (2004) · International Immunology · doi:10.1093/intimm/dxh186 · Cited by 3,328 · see citing works
Human skin wounds: A major and snowballing threat to public health and the economy
Sen, C. K., Gordillo, G. M., Roy, S., Kirsner, R., Lambert, L., Hunt, T. K., Gottrup, F., Gurtner, G. C., & Longaker, M. T. (2009) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2009.00543.x · Cited by 2,965 · see citing works
Methicillin-Resistant <i>S. aureus</i> Infections among Patients in the Emergency Department
Moran, G. J., Krishnadasan, A., Gorwitz, R. J., Fosheim, G. E., McDougal, L. K., Carey, R. B., & Talan, D. A. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa055356 · Cited by 2,285 · see citing works
Kawai, T., & Akira, S. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401850 · Cited by 1,817 · see citing works
Molecular inflammation: Underpinnings of aging and age-related diseases
Chung, H. Y., Cesari, M., Anton, S., Marzetti, E., Giovannini, S., Seo, A. Y., Carter, C., Yu, B. P., & Leeuwenburgh, C. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2008.07.002 · Cited by 1,203 · see citing works
Takeuchi, O., Hoshino, K., & Akira, S. (2000) · Journal of Immunology · doi:10.4049/jimmunol.165.10.5392 · Cited by 1,156 · see citing works
Surgical Risk Factors, Morbidity, and Mortality in Elderly Patients
Turrentine, F. E., Wang, H., Simpson, V. B., & Jones, R. S. (2006) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2006.08.026 · Cited by 1,062 · see citing works
Gosain, A., & DiPietro, L. A. (2004) · World Journal of Surgery · doi:10.1007/s00268-003-7397-6 · Cited by 1,048 · see citing works
Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4
Yamamoto, M., Sato, S., Hemmi, H., Sanjo, H., Uematsu, S., Kaisho, T., Hoshino, K., Takeuchi, O., Kobayashi, M., Fujita, T., et al. (2002) · Nature · doi:10.1038/nature01182 · Cited by 995 · see citing works
Surgical risk factors, morbidity, and mortality in elderly patients
Turrentine, F. E., Wang, H., Simpson, V. B., & Jones, R. S. (2008) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(08)70016-7 · Cited by 711 · see citing works
Cutting edge: impaired toll-like receptor expression and function in aging
Renshaw, M., Rockwell, J., Engleman, C., Gewirtz, A., Katz, J., & Sambhara, S. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.9.4697 · Cited by 626 · see citing works
Accelerated wound closure in neutrophil-depleted mice
Dovi, J. V., He, L.-K., & DiPietro, L. A. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0802406 · Cited by 525 · see citing works
Scarless Fetal Wound Healing: A Basic Science Review
Larson, B. J., Longaker, M. T., & Lorenz, H. P. (2010) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e3181eae781 · Cited by 455 · see citing works
The phenotype of murine wound macrophages
Daley, J. M., Brancato, S. K., Thomay, A. A., Reichner, J. S., & Albina, J. E. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0409236 · Cited by 452 · see citing works
G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood
Semerad, C. L., Liu, F., Gregory, A. D., Stumpf, K., & Link, D. C. (2002) · Immunity · doi:10.1016/s1074-7613(02)00424-7 · Cited by 450 · see citing works
Butcher, S. K., Chahal, H., Nayak, L., Sinclair, A., Henriquez, N. V., Sapey, E., O'Mahony, D., & Lord, J. M. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.70.6.881 · Cited by 436 · see citing works
Age-Related Alterations in the Inflammatory Response to Dermal Injury
Swift, M. E., Burns, A. L., Gray, K. L., & DiPietro, L. A. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01539.x · Cited by 398 · see citing works
Molecular mechanisms of aging-associated inflammation.
Sarkar, D., & Fisher, P. (2006) · Cancer Letters · doi:10.1016/j.canlet.2005.04.009 · Cited by 379 · see citing works
Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O., & Kinashi, T. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200301133 · Cited by 358 · see citing works
(1999) · PubMed · Cited by 354 · see citing works
Miller, L. S., O’Connell, R. M., Gutiérrez, M. Á., Pietras, E. M., Shahangian, A., Gross, C. E., Thirumala, A., Cheung, A. L., Cheng, G., & Modlin, R. L. (2006) · Immunity · doi:10.1016/j.immuni.2005.11.011 · Cited by 348 · see citing works
G-CSF: a key regulator of neutrophil production, but that's not all!
Roberts, A. W. (2005) · Growth Factors · doi:10.1080/08977190500055836 · Cited by 335 · see citing works
Signal transduction and functional changes in neutrophils with aging
Fülöp, T., Larbi, A., Douziech, N., Fortin, C. F., Guérard, K., Lesur, O., Khalil, A., & Dupuis, G. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00110.x · Cited by 331 · see citing works
Basu, S., HODGSON, G. S., Katz, M., & Dunn, A. R. (2002) · Blood · doi:10.1182/blood.v100.3.854 · Cited by 316 · see citing works
Oxidative stress, inflamm-aging and immunosenescence
Cannizzo, E. S., Clement, C. C., Sahu, R. K., Follo, C., & Santambrogio, L. (2011) · Journal of Proteomics · doi:10.1016/j.jprot.2011.06.005 · Cited by 303 · see citing works
Kim, M. H., Liu, W., Borjesson, D. L., CURRY, F. E., Miller, L. S., Cheung, A. L., Liu, F., Isseroff, R. R., & Simon, S. I. (2008) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5701223 · Cited by 271 · see citing works
Toll-like Receptors and Their Signaling Mechanisms
Akira, S., & Sato, S. (2003) · Scandinavian Journal of Infectious Diseases · doi:10.1080/00365540310015683 · Cited by 264 · see citing works
Ashcroft, G. S., Horan, M. A., & Ferguson, M. W. J. (1997) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12289705 · Cited by 240 · see citing works
Salvioli, S., Capri, M., Valensin, S., Tieri, P., Monti, D., Ottaviani, E., & Franceschi, C. (2006) · Current Pharmaceutical Design · doi:10.2174/138161206777947470 · Cited by 240 · see citing works
Oxidative Stress, Inflammaging, and Immunosenescence
Bauer, M. E., & la Fuente, M. D. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397803-5.00004-6 · Cited by 229 · see citing works
Aging, Longevity, Inflammation, and Cancer
Caruso, C., Lio, D., Cavallone, L., & Franceschi, C. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1322.001 · Cited by 219 · see citing works
Georgel, P., Crozat, K., Lauth, X., Makrantonaki, E., Seltmann, H., Sovath, S., Hoebe, K. H. N., Du, X., Rutschmann, S., Jiang, Z., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.4512-4521.2005 · Cited by 219 · see citing works
Neutrophil Adhesion and Activation under Flow
Zarbock, A., & Ley, K. F. (2008) · Microcirculation · doi:10.1080/10739680802350104 · Cited by 218 · see citing works
Neutrophil function in the healing wound: adding insult to injury?
Dovi, J., Szpaderska, A., & DiPietro, L. (2004) · Thrombosis and Haemostasis · doi:10.1160/th03-11-0720 · Cited by 217 · see citing works
Hillyer, P., Mordelet, E., FLYNN, G., & Male, D. K. (2003) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2003.02323.x · Cited by 174 · see citing works
Boehmer, E. D., Meehan, M. J., Cutro, B. T., & Kovacs, E. J. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.07.009 · Cited by 170 · see citing works
Self-citationSadoun, E., & Reed, M. J. (2003) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540305100902 · Cited by 158 · see citing works
Nguyen-Jackson, H., Panopoulos, A. D., Zhang, H., Li, H. S., & Watowich, S. S. (2010) · Blood · doi:10.1182/blood-2009-08-240317 · Cited by 151 · see citing works
Hinojosa, E., Boyd, A. R., & Orihuela, C. J. (2009) · The Journal of Infectious Diseases · doi:10.1086/600870 · Cited by 143 · see citing works
CXCR2- and E-Selectin–induced Neutrophil Arrest during Inflammation In Vivo
Smith, M. L., Olson, T. S., & Ley, K. F. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040424 · Cited by 138 · see citing works
ICAM-1 and LFA-1 play critical roles in LPS-induced neutrophil recruitment into the alveolar space
Basit, A., Reutershan, J., Morris, M. A., Solga, M. D., Rose, C. E., & Ley, K. F. (2006) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00346.2005 · Cited by 134 · see citing works
Modulation of macrophage recruitment into wounds by monocyte chemoattractant protein‐1
DiPietro, L. A., Reintjes, M. G., Low, Q., Lévi, B., & Gamelli, R. L. (2001) · Wound Repair and Regeneration · doi:10.1046/j.1524-475x.2001.00028.x · Cited by 133 · see citing works
The Effect of Surgical Site Infection on Older Operative Patients
Kaye, K. S., Anderson, D. J., Sloane, R. J., Chen, L. F., Choi, Y., Link, K., Sexton, D. J., & Schmader, K. E. (2008) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2008.02053.x · Cited by 131 · see citing works
Aging of the Innate Immune System: An Update
Mahbub, S., Brubaker, A. L., & Kovacs, E. J. (2011) · Current Immunology Reviews · doi:10.2174/157339511794474181 · Cited by 125 · see citing works
Self-citationNeutrophil depletion delays wound repair in aged mice
Nishio, N., Okawa, Y., Sakurai, H., & Isobe, K. (2008) · AGE · doi:10.1007/s11357-007-9043-y · Cited by 124 · see citing works
Onyszchuk, G., He, Y., Berman, N. E. J., & Brooks, W. M. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2007.0430 · Cited by 120 · see citing works
de Bruyn, K. M. T., Rangarajan, S., Reedquist, K. A., Figdor, C. G., & Bos, J. L. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204990200 · Cited by 114 · see citing works
Saadatian‐Elahi, M., Teyssou, R., & Vanhems, P. (2007) · International Journal of Surgery · doi:10.1016/j.ijsu.2007.05.001 · Cited by 113 · see citing works
Advanced age exacerbates the pulmonary inflammatory response after lipopolysaccharide exposure
Gómez, C. R., Hirano, S. A., Cutro, B. T., Birjandi, S. Z., Baila, H., Nomellini, V., & Kovacs, E. J. (2006) · Critical Care Medicine · doi:10.1097/01.ccm.0000251639.05135.e0 · Cited by 111 · see citing works
Self-citationCellular and Molecular Characteristics of Scarless versus Fibrotic Wound Healing
Satish, L., & Kathju, S. (2010) · Dermatology Research and Practice · doi:10.1155/2010/790234 · Cited by 107 · see citing works
Fossati, G., Moots, R. J., Bucknall, R. C., & Edwards, S. W. (2002) · Arthritis & Rheumatism · doi:10.1002/art.10230 · Cited by 105 · see citing works
Modulation of Macrophage Phenotype by Soluble Product(s) Released from Neutrophils
Daley, J. M., Reichner, J. S., Mahoney, E. J., Manfield, L., Henry, W. L., Mastrofrancesco, B., & Albina, J. E. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.4.2265 · Cited by 101 · see citing works
Roy, S., Khanna, S., Rink, C. L., Biswas, S., & Sen, C. K. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.00045.2008 · Cited by 101 · see citing works
Alterations in Marginal Zone Macrophages and Marginal Zone B Cells in Old Mice
Birjandi, S. Z., Ippolito, J. A., Ramadorai, A. K., & Witte, P. L. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1001271 · Cited by 92 · see citing works
Kim, M. H., CURRY, F. E., & Simon, S. I. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00520.2008 · Cited by 87 · see citing works
Vowden, K., & Vowden, P. (2008) · Journal of Tissue Viability · doi:10.1016/j.jtv.2008.11.002 · Cited by 81 · see citing works
Nomellini, V., Faunce, D. E., Gómez, C. R., & Kovacs, E. J. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.1007672 · Cited by 78 · see citing works
Self-citationPereira, L., de Souza, A. P. D., Borges, T. J., & Bonorino, C. (2011) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.03.005 · Cited by 77 · see citing works
Granulocyte colony-stimulating factor promotes adhesion of neutrophils
Chakraborty, A., Hentzen, E. R., Seo, S. M., & Smith, C. W. (2003) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00165.2002 · Cited by 73 · see citing works
The Effect of Sepsis on Wound Healing
Rico, R. M., Ripamonti, R., Burns, A. L., Gamelli, R. L., & DiPietro, L. A. (2002) · Journal of Surgical Research · doi:10.1006/jsre.2001.6316 · Cited by 72 · see citing works
de la Fuente, M., Hernánz, Á., Guayerbas, N., Alvarez, P., & Alvarado, C. (2004) · PubMed · Cited by 70 · see citing works
Wiekowski, M., Chen, S., Zalamea, P. D., Wilburn, B., Kinsley, D., Sharif, W. W., Jensen, K. K., Hedrick, J. A., Manfra, D. J., & Lira, S. A. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.12.7102 · Cited by 66 · see citing works
Anderson, K. E., Chessa, T. A. M., Davidson, K., Henderson, R. B., Walker, S. A., Tolmachova, T., Grys, K., Rausch, O., Seabra, M. C., Tybulewicz, V. L. J., et al. (2010) · Blood · doi:10.1182/blood-2010-03-275602 · Cited by 62 · see citing works
Bacterial infection profiles in lung cancer patients with febrile neutropenia
Lanoix, J., Pluquet, E., Lescure, F.-X., Bentayeb, H., Lecuyer, E., Boutemy, M., Dumont, P., Jounieaux, V., Schmit, J., Dayen, C., et al. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-183 · Cited by 62 · see citing works
Influence of aging on murine neutrophil and macrophage function againstCandida albicans
Murciano, C., Yáñez, A., O’Connor, J., Gozalbo, D., & Gil, M. L. (2008) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2008.00418.x · Cited by 61 · see citing works
Ming, W., Li, S., Billadeau, D. D., Quilliam, L. A., & Dinauer, M. C. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00985-06 · Cited by 61 · see citing works
Hong, C.-W., Kim, T.-K., Ham, H.-Y., Nam, J., Kim, Y. H., Zheng, H., Pang, B., Min, T.-K., Jung, J., Lee, S.-N., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902814 · Cited by 61 · see citing works
Nomellini, V., Brubaker, A. L., Mahbub, S., Palmer, J. L., Gómez, C. R., & Kovacs, E. J. (2012) · Europe PMC (PubMed Central) · Cited by 57 · see citing works
Self-citationEffect of age on susceptibility to post-traumatic infection in the elderly
Butcher, S. K., Killampalli, V. V., Chahal, H., Alpar, E. K., & Lord, J. M. (2003) · Biochemical Society Transactions · doi:10.1042/bst0310449 · Cited by 57 · see citing works
AGING AND ANIMAL MODELS OF SYSTEMIC INSULT
Nomellini, V., Gómez, C. R., Gamelli, R. L., & Kovacs, E. J. (2008) · Shock · doi:10.1097/shk.0b013e318180f508 · Cited by 55 · see citing works
Self-citationMechanical unloading impairs keratinocyte migration and angiogenesis during cutaneous wound healing
Radek, K. A., Baer, L. A., Eckhardt, J., DiPietro, L. A., & Wade, C. E. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00977.2007 · Cited by 52 · see citing works
Effect of age on susceptibility to Salmonella Typhimurium infection in C57BL/6 mice
Ren, Z., Gay, R., Thomas, A., Pae, M., Wu, D., Logsdon, L. K., Mecsas, J. C., & Meydani, S. N. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.013250-0 · Cited by 51 · see citing works
Reinfection, Rather than Persistent Infection, in Patients with Chronic Granulomatous Disease
Guide, S. V., Stock, F., Gill, V. J., Anderson, V., Malech, H. L., Gallin, J. I., & Holland, S. M. (2003) · The Journal of Infectious Diseases · doi:10.1086/368388 · Cited by 51 · see citing works
Fusté, B., Mazzara, R., Escolar, G., Merino, A., Ordinas, A., & Díaz‐Ricart, M. (2004) · PubMed · Cited by 48 · see citing works
Age-related Dysregulation of Inflammation and Innate Immunity: Lessons Learned from Rodent Models.
Brubaker, A. L., Palmer, J. L., & Kovacs, E. J. (2011) · Europe PMC (PubMed Central) · Cited by 47 · see citing works
Self-citationGómez, C. R., Nomellini, V., Baila, H., Oshima, K., & Kovacs, E. J. (2009) · Shock · doi:10.1097/shk.0b013e318180feb8 · Cited by 43 · see citing works
Self-citationNeutrophils and natural killer T cells as negative regulators of wound healing
Brubaker, A. L., Schneider, D. F., & Kovacs, E. J. (2011) · Expert Review of Dermatology · doi:10.1586/edm.10.66 · Cited by 35 · see citing works
Self-citationEffects of in vivo administration of G‐CSF on neutrophil and eosinophil adhesion
Håkansson, L., Höglund, M., Jönsson, U., Torsteinsdóttir, I., Xu, X., & Venge, P. (1997) · British Journal of Haematology · doi:10.1046/j.1365-2141.1997.2723093.x · Cited by 35 · see citing works
TLR2 enhances NADPH oxidase activity and killing of Staphylococcus aureus by PMN
Nyffenegger, N., Schmaler, M., Ferracin, F., & Landmann, R. M. (2010) · Immunology Letters · doi:10.1016/j.imlet.2010.09.007 · Cited by 35 · see citing works
Molteni, R., Crespo, C. L., Feigelson, S. W., Moser, C., Fabbri, M., Grabovsky, V., Krombach, F., Laudanna, C., Alon, R., & Pardi, R. (2009) · Blood · doi:10.1182/blood-2008-10-183699 · Cited by 33 · see citing works
Aging Enhances Susceptibility to Cigarette Smoke–Induced Inflammation through Bronchiolar Chemokines
Moriyama, C., Betsuyaku, T., Ito, Y., Hamamura, I., Hata, J., Takahashi, H., Nasuhara, Y., & Nishimura, M. (2009) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2009-0025oc · Cited by 33 · see citing works
Grange-Midroit, M., Garcı́a-Sevilla, J. A., Ferrer‐Alcón, M., Harpe, R. L., Walzer, C., & Guimón, J. (2002) · Molecular Brain Research · doi:10.1016/s0169-328x(02)00144-4 · Cited by 33 · see citing works
Bird, M. D., Morgan, M. O., Ramírez, L., Yong, S. L., & Kovacs, E. J. (2010) · Journal of Burn Care & Research · doi:10.1097/bcr.0b013e3181e4c58c · Cited by 32 · see citing works
Self-citationSchneider, D. F., Palmer, J. L., Tulley, J. M., Kovacs, E. J., Gamelli, R. L., & Faunce, D. E. (2010) · Journal of Surgical Research · doi:10.1016/j.jss.2010.03.030 · Cited by 30 · see citing works
Self-citationKaravitis, J., Murdoch, E. L., Deburghgraeve, C. R., Ramírez, L., & Kovacs, E. J. (2012) · Cellular Immunology · doi:10.1016/j.cellimm.2012.02.002 · Cited by 29 · see citing works
Self-citationGrowth factors G-CSF and GM-CSF differentially preserve chemotaxis of neutrophils aging in vitro
Wolach, B., van der Laan, L. J. W., Mayanskiy, N. A., Tool, A. T. J., van Bruggen, R., Roos, D., & Kuijpers, T. W. (2007) · Experimental Hematology · doi:10.1016/j.exphem.2006.12.008 · Cited by 29 · see citing works
Cj, H. (2009) · PubMed · Cited by 29 · see citing works
Peritoneal macrophages function modulation by L-carnitine in aging rats
Izgut-Uysal, V. N., Ağaç, A., Karadoǧan, Ì., & Derin, N. (2004) · Aging Clinical and Experimental Research · doi:10.1007/bf03324561 · Cited by 22 · see citing works
Differential Recruitment of Activating and Inhibitory FcγRII during Phagocytosis
Syam, S., Mero, P., Pham, T., McIntosh, C., Bruhns, P., & Booth, J. W. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0900016 · Cited by 21 · see citing works
An Appraisal of Trauma in the Elderly
Sharma, O. P., Oswanski, M. F., Sharma, V. S., Stringfellow, K., & Raj, S. S. (2007) · The American Surgeon · doi:10.1177/000313480707300409 · Cited by 21 · see citing works
Li, Y., Howell, E., Lagoo, A. S., Kuchibhatla, M. N., Pan, H., Cohen, H. J., & Lagoo, S. A. (2008) · Shock · doi:10.1097/shk.0b013e3181778ab2 · Cited by 18 · see citing works
Brubaker, A. L., Schneider, D. F., Palmer, J. L., Faunce, D. E., & Kovacs, E. J. (2011) · Journal of Immunological Methods · doi:10.1016/j.jim.2011.08.013 · Cited by 16 · see citing works
Self-citationGuayerbas, N., Puerto, M., Alvarez, P., & la Fuente, M. D. (2004) · PubMed · Cited by 16 · see citing works
Yoshino, T., Tamura, M., Kawabe, M., Nomura, H., Imai, N., & Ono, M. (1992) · British Journal of Haematology · doi:10.1111/j.1365-2141.1992.tb06941.x · Cited by 12 · see citing works
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Age-dependent dysregulation of innate immunity
Shaw, A. C., Goldstein, D. R., & Montgomery, R. R. (2013) · Nature Reviews Immunology · doi:10.1038/nri3547 · Cited by 1,061 · see citing works
Immunosenescence and inflammaging in the aging process: age-related diseases or longevity?
Santoro, A., Bientinesi, E., & Monti, D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101422 · Cited by 603 · see citing works
The Role of Chemokines in Wound Healing
Ridiandries, A., Tan, J. T. M., & Bursill, C. A. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103217 · Cited by 479 · see citing works
Aging of the immune system: Focus on inflammation and vaccination
Pinti, M., Appay, V., Campisi, J., Frasca, D., Fülöp, T., Sauce, D., Larbi, A., Weinberger, B., & Cossarizza, A. (2016) · European Journal of Immunology · doi:10.1002/eji.201546178 · Cited by 439 · see citing works
Chronic Wound Repair and Healing in Older Adults: Current Status and Future Research
Gould, L. J., Abadir, P. M., Brem, H., Carter, M. J., Conner‐Kerr, T., Davidson, J., DiPietro, L. A., Falanga, V., Fife, C. E., Gardner, S. E., et al. (2015) · Journal of the American Geriatrics Society · doi:10.1111/jgs.13332 · Cited by 392 · see citing works
Self-citationBao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 389 · see citing works
Sapey, E., Greenwood, H., Walton, G., Mann, E., Love, A., Aaronson, N., Insall, R. H., Stockley, R. A., & Lord, J. M. (2014) · Blood · doi:10.1182/blood-2013-08-519520 · Cited by 358 · see citing works
Phenotypic transitions of macrophages orchestrate tissue repair.
Novak, M. L., & Koh, T. (2013) · American Journal of Pathology · doi:10.1016/j.ajpath.2013.06.034 · Cited by 332 · see citing works
Interconnections between Inflammageing and Immunosenescence during Ageing
Teissier, T., Boulanger, É., & Cox, L. S. (2022) · Cells · doi:10.3390/cells11030359 · Cited by 310 · see citing works
Chronic wound repair and healing in older adults: current status and future research
Gould, L., Abadir, P., Brem, H., Carter, M., Conner‐Kerr, T., Davidson, J., DiPietro, L., Falanga, V., Fife, C., Gardner, S., et al. (2015) · Wound Repair and Regeneration · doi:10.1111/wrr.12245 · Cited by 291 · see citing works
Self-citationDermal adipocyte lipolysis and myofibroblast conversion are required for efficient skin repair
Shook, B. A., Wasko, R. R., Mano, O., Rutenberg-Schoenberg, M. L., Rudolph, M. C., Zirak, B., Rivera-Gonzalez, G. C., López-Giráldez, F., Zarini, S., Rezza, A., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.03.013 · Cited by 265 · see citing works
Avishai, E., Yeghiazaryan, K., & Golubnitschaja, O. (2017) · The EPMA Journal · doi:10.1007/s13167-017-0081-y · Cited by 279 · see citing works
The Confluence of Sex Hormones and Aging on Immunity
Gubbels Bupp, M. R., Potluri, T., Fink, A. L., & Klein, S. L. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01269 · Cited by 277 · see citing works
Biofilm-Innate Immune Interface: Contribution to Chronic Wound Formation
Versey, Z., Nizer, W. S. D. C., Russell, E., Zigic, S., DeZeeuw, K. G., Marek, J. E., Overhage, J., & Cassol, E. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.648554 · Cited by 268 · see citing works
Cunha, L. L., Perazzio, S. F., Azzi, J., Cravedi, P., & Riella, L. V. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01748 · Cited by 239 · see citing works
Hu, M. S.-M., Borrelli, M. R., Lorenz, H. P., Longaker, M. T., & Wan, D. C. (2018) · Stem Cells International · doi:10.1155/2018/6901983 · Cited by 242 · see citing works
Aging and InflammationPreprint
Singh, A., Schurman, S. H., Bektas, A., Kaileh, M., Roy, R., Wilson, D. M., Sen, R., & Ferrucci, L. (2023) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041197 · Cited by 194 · see citing works
Immunosenescence, Inflammaging, and Frailty: Role of Myeloid Cells in Age-Related Diseases
Bleve, A., Motta, F., Durante, B., Pandolfo, C., Selmi, C., & Sica, A. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-021-08909-7 · Cited by 179 · see citing works
Innate immune responses in the ageing lung.
Boe, D. M., Boule, L. A., & Kovacs, E. J. (2016) · Clinical and Experimental Immunology · doi:10.1111/cei.12881 · Cited by 156 · see citing works
Vu, R., Jin, S., Sun, P., Haensel, D., Nguyen, Q., Dragan, M., Kessenbrock, K., Nie, Q. H., & Dai, X. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111155 · Cited by 149 · see citing works
Immunosenescence and inflammaging: Mechanisms and role in diseases
Ajoolabady, A., Praticò, D., Tang, D., Zhou, S., Franceschi, C., & Ren, J. T. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102540 · Cited by 160 · see citing works
Paradoxical changes in innate immunity in aging: recent progress and new directions
Montgomery, R. R., & Shaw, A. C. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.5mr0315-104r · Cited by 147 · see citing works
Abandon the Mouse Research Ship? Not Just Yet!
Osuchowski, M. F., Remick, D. G., Lederer, J. A., Lang, C. H., Aasen, A. O., Aibiki, M., Azevedo, L. C. P., Bahrami, S., Boros, M., Cooney, R. N., et al. (2014) · Shock · doi:10.1097/shk.0000000000000153 · Cited by 144 · see citing works
Neutrophils in aging and aging‐related pathologies
Avondt, K. V., Strecker, J., Tulotta, C., Minnerup, J., Schulz, C., & Soehnlein, O. (2022) · Immunological Reviews · doi:10.1111/imr.13153 · Cited by 146 · see citing works
The Immune Landscape of Visceral Adipose Tissue During Obesity and Aging
Khan, S. M., Chan, Y. T., Revelo, X. S., & Winer, D. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00267 · Cited by 126 · see citing works
An overview of the therapeutic potential of regenerative medicine in cutaneous wound healing
Pang, C., Ibrahim, A., Bulstrode, N. W., & Ferretti, P. (2017) · International Wound Journal · doi:10.1111/iwj.12735 · Cited by 113 · see citing works
Innate immunesenescence: underlying mechanisms and clinical relevance
Hazeldine, J., & Lord, J. M. (2015) · Biogerontology · doi:10.1007/s10522-014-9514-3 · Cited by 104 · see citing works
Autophagy and Immune Senescence
Zhang, H., Puleston, D. J., & Simon, A. K. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.06.001 · Cited by 93 · see citing works
Alcohol, aging, and innate immunity
Boulé, L. A., & Kovacs, E. J. (2017) · Journal of Leukocyte Biology · doi:10.1189/jlb.4ru1016-450r · Cited by 92 · see citing works
Self-citationCutaneous wound healing in aging small mammals: a systematic review
Kim, D. J., Mustoe, T. A., & Clark, R. A. F. (2015) · Wound Repair and Regeneration · doi:10.1111/wrr.12290 · Cited by 90 · see citing works
Cell migration in diabetic wound healing: Molecular mechanisms and therapeutic strategies (Review)
Song, J., Zhao, T., Wang, C., Sun, X., Sun, J., & Zhang, Z. (2025) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2025.5567 · Cited by 86 · see citing works
Cakala, M., Kołodziej, P., & Puzianowska‐Kuźnicka, M. (2021) · Cells · doi:10.3390/cells10113148 · Cited by 77 · see citing works
Contrasting Inflammatory Responses in Severe and Non-severe Community-acquired Pneumonia
Fernandez-Botrán, R., Uriarte, S. M., Arnold, F. W., Rodriquez-Hernandez, L., Rane, M. J., Peyrani, P., Wiemken, T. L., Kelley, R. R., Uppatla, S., Cavallazzi, R., et al. (2014) · Inflammation · doi:10.1007/s10753-014-9840-2 · Cited by 72 · see citing works
Is combined medication with natural medicine a promising therapy for bacterial biofilm infection?
Zhang, L., Liang, E., Cheng, Y., Mahmood, T., Ge, F., Zhou, K., Bao, M., Lv, L., Li, L., Yi, J., et al. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110184 · Cited by 73 · see citing works
Regulation of the Wound Healing Response during Aging.
Ding, X.-L., Kakanj, P., Leptin, M., & Eming, S. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2020.11.014 · Cited by 61 · see citing works
Age-related differences in the neutrophil response to pulmonary pseudomonas infection
Chen, M. M., Palmer, J. L., Plackett, T. P., Deburghgraeve, C. R., & Kovacs, E. J. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2013.12.010 · Cited by 68 · see citing works
Self-citationExpanding roles of neutrophils in aging hosts
Tseng, C. W., & Liu, G. Y. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.03.009 · Cited by 70 · see citing works
Cellular senescence in lymphoid organs and immunosenescence
Budamagunta, V., Foster, T. C., & Zhou, D. (2021) · Aging · doi:10.18632/aging.203405 · Cited by 68 · see citing works
Bartlett, D. B., Fox, O., McNulty, C. L., Greenwood, H. L., Murphy, L., Sapey, E., Goodman, M., Crabtree, N. J., Thøgersen‐Ntoumani, C., Fisher, J. P., et al. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.02.024 · Cited by 65 · see citing works
The Prediction and Monitoring of Toxicity Associated with Long-Term Systemic Glucocorticoid Therapy
Harris, E., Tiganescu, A., Tubeuf, S., & Mackie, S. L. (2015) · Current Rheumatology Reports · doi:10.1007/s11926-015-0513-4 · Cited by 63 · see citing works
Roy, R., Zayas, J. P., Singh, S. K., Delgado, K., Wood, S. J., Mohamed, M. F., Frausto, D. M., Albalawi, Y. A., Price, T. P., Estupinian, R., et al. (2022) · eLife · doi:10.7554/elife.72071 · Cited by 64 · see citing works
Management of burns in the elderly.
Abu-Sittah, G. S., Chahine, F., & Janom, H. (2016) · Europe PMC (PubMed Central) · Cited by 60 · see citing works
Inan, S., Torres-Huerta, A., Jensen, L. E., Dun, N. J., & Cowan, A. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172702 · Cited by 58 · see citing works
Quirós, M., & Nusrat, A. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114504 · Cited by 47 · see citing works
The Cutaneous Wound Innate Immunological Microenvironment
Kirchner, S. J., Lei, V., & MacLeod, A. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228748 · Cited by 57 · see citing works
Shin, J. H., High, K. P., & Warren, C. A. (2016) · The Journals of Gerontology Series A · doi:10.1093/gerona/glv229 · Cited by 56 · see citing works
The impact of aging on neutrophil functions and the contribution to periodontitis
Wang, Z., Saxena, A., Yan, W., Uriarte, S. M., de Siqueira, R. A. C., & Li, X. (2025) · International Journal of Oral Science · doi:10.1038/s41368-024-00332-w · Cited by 54 · see citing works
Age-dependent immune and lymphatic responses after spinal cord injury
Salvador, A. F., Dykstra, T., Rustenhoven, J., Gao, W., Blackburn, S. M., Bhasiin, K., Dong, M. Q., Guimarães, R. M., Gonuguntla, S., Smirnov, I., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.04.011 · Cited by 51 · see citing works
An, Y., Wei, W., Jing, H., Ming, L., Liu, S., & Jin, Y. J. (2015) · Scientific Reports · doi:10.1038/srep17036 · Cited by 51 · see citing works
Increased glucocorticoid activation during mouse skin wound healing
Tiganescu, A., Hupe, M., Uchida, Y., Mauro, T. M., Elias, P. M., & Holleran, W. M. (2014) · Journal of Endocrinology · doi:10.1530/joe-13-0420 · Cited by 48 · see citing works
Ebaid, H. (2014) · Diagnostic Pathology · doi:10.1186/1746-1596-9-46 · Cited by 49 · see citing works
Hammer, A. M. (2015) · Alcohol research · doi:10.35946/arcr.v37.2.06 · Cited by 48 · see citing works
Kovacs, E. J., Boe, D. M., Boule, L. A., & Curtis, B. J. (2017) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2017.06.002 · Cited by 49 · see citing works
Self-citationNeuroinflammation and brain–peripheral interaction in ischemic stroke: A narrative review
Cheng, W., Zhao, Q. C., Li, C., & Xu, Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1080737 · Cited by 47 · see citing works
How Inflammation Blunts Innate Immunity in Aging
Goldberg, E. L., Shaw, A. C., & Montgomery, R. R. (2020) · Interdisciplinary topics in gerontology and geriatrics · doi:10.1159/000504480 · Cited by 45 · see citing works
Cellular senescence in cancer: molecular mechanisms and therapeutic targets
Jin, P., Duan, X., Li, L., Zhou, P., Zou, C., & Xie, K. (2024) · MedComm · doi:10.1002/mco2.542 · Cited by 46 · see citing works
Physical plasma and leukocytes – immune or reactive?
Bekeschus, S., Seebauer, C., Wende, K., & Schmidt, A. (2018) · Biological Chemistry · doi:10.1515/hsz-2018-0224 · Cited by 45 · see citing works
Gut Microbial Changes and their Contribution to Post-Burn Pathology
Luck, M. E., Herrnreiter, C. J., & Choudhry, M. A. (2021) · Shock · doi:10.1097/shk.0000000000001736 · Cited by 42 · see citing works
Self-citationDorschner, R. A., Lee, J., Cohen, O., Costantini, T. W., Baird, A., & Eliceiri, B. P. (2020) · Science Advances · doi:10.1126/sciadv.aay0518 · Cited by 41 · see citing works
Myeloid-derived growth factor regulates neutrophil motility in interstitial tissue damage
Houseright, R. A., Miskolci, V., Mulvaney, O., Bortnov, V., Mosher, D. F., Rindy, J., Bennin, D. A., & Anna Huttenlocher, A. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202103054 · Cited by 40 · see citing works
An interferon gamma response signature links myocardial aging and immunosenescence
Ashour, D., Rebs, S., Arampatzi, P., Saliba, A.-E., Dudek, J., Schulz, R., Hofmann, U., Frantz, S., Cochain, C., Streckfuß-Bömeke, K., et al. (2023) · Cardiovascular Research · doi:10.1093/cvr/cvad068 · Cited by 39 · see citing works
Unveiling mechanisms of lung aging in COPD: A promising target for therapeutics development
Devulder, J. V. (2024) · Chinese Medical Journal - Pulmonary and Critical Care Medicine · doi:10.1016/j.pccm.2024.08.007 · Cited by 41 · see citing works
Cellular Senescence in Immunity against Infections
Marrella, V., Facoetti, A., & Cassani, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911845 · Cited by 37 · see citing works
CNS and peripheral immunity in cerebral ischemia: partition and interaction
Kim, E., & Cho, S. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113508 · Cited by 36 · see citing works
Hornigold, K., Chu, J. Y., Chetwynd, S. A., Machin, P. A., Crossland, L., Pantarelli, C., Anderson, K. E., Hawkins, P. T., Segonds-Pichon, A., Oxley, D., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.888415 · Cited by 35 · see citing works
Age-Related Changes in Immunological and Physiological Responses Following Pulmonary Challenge
Miller, E. J., & Linge, H. M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061294 · Cited by 35 · see citing works
Muthuswamy, S., Viswanathan, A., Yegappan, R., Selvaprithiviraj, V., Vasudevan, A. K., Biswas, R., & Jayakumar, R. (2018) · ACS Applied Bio Materials · doi:10.1021/acsabm.8b00625 · Cited by 35 · see citing works
Innate immune response to bone fracture healing.
Burgan, J., Rahmati, M., Lee, M. A., & Saiz, A. (2024) · Bone · doi:10.1016/j.bone.2024.117327 · Cited by 32 · see citing works
Dynamic interactions between dermal macrophages and Staphylococcus aureus
Feuerstein, R., Kolter, J., & Henneke, P. (2016) · Journal of Leukocyte Biology · doi:10.1189/jlb.3mr0316-097rr · Cited by 32 · see citing works
Lecron, J., Charreau, S., Jégou, J., Salhi, N., Petit-Paris, I., Guignouard, E., Burucoa, C., Favot, L., Bodet, C., Barra, A., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.984016 · Cited by 32 · see citing works
Age-related differences in immune dynamics during SARS-CoV-2 infection in rhesus macaques
Speranza, E. E., Purushotham, J. N., Port, J. R., Schwarz, B. H., Flagg, M., Williamson, B. N., Feldmann, F., Singh, M., Pérez-Pérez, L., Sturdevant, G. L., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202101314 · Cited by 29 · see citing works
Immune aging and infectious diseases
Chen, R., Zou, J., Chen, J., Wang, L., Kang, R., & Tang, D. (2024) · Chinese Medical Journal · doi:10.1097/cm9.0000000000003410 · Cited by 33 · see citing works
Sharma, R., Diwan, B., Sharma, A., & Witkowski, J. M. (2022) · Biogerontology · doi:10.1007/s10522-022-09995-6 · Cited by 29 · see citing works
DAF-16 and SMK-1 Contribute to Innate Immunity During Adulthood in Caenorhabditis elegans
McHugh, D. R., Koumis, E., Jacob, P., Goldfarb, J. A., Schlaubitz-Garcia, M., Bennani, S., Regan, P., Patel, P., & Youngman, M. J. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.120.401166 · Cited by 28 · see citing works
A Porcine Wound Model of Acinetobacter baumannii Infection
Zurawski, D. V., Black, C. C., Alamneh, Y. A., Biggemann, L., Banerjee, J., Thompson, M. G., Wise, M. C., Honnold, C. L., Kim, R. K., Paranavitana, C. M., et al. (2018) · Advances in Wound Care · doi:10.1089/wound.2018.0786 · Cited by 29 · see citing works
Counteracting Immunosenescence—Which Therapeutic Strategies Are Promising?
Hieber, C., Grabbe, S., & Bros, M. (2023) · Biomolecules · doi:10.3390/biom13071085 · Cited by 28 · see citing works
Sepsis in elderly patients: the role of neutrophils in pathophysiology and therapy
Ramoni, D., Tirandi, A., Montecucco, F., & Liberale, L. (2024) · Internal and Emergency Medicine · doi:10.1007/s11739-023-03515-1 · Cited by 27 · see citing works
Dysregulation of leukocyte trafficking in ageing: Causal factors and possible corrective therapies
Hopkin, S. J., Lord, J. M., & Chimen, M. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105323 · Cited by 25 · see citing works
Jones, R. A., Feng, Y., Worth, A. J. J., Thrasher, A. J., Burns, S. O., & Martin, P. B. (2013) · Journal of Cell Science · doi:10.1242/jcs.128728 · Cited by 26 · see citing works
Burn wounds in the young versus the aged patient display differential immunological responses
Farinas, A. F., Bamba, R., Pollins, A. C., Cardwell, N. L., Nanney, L. B., & Thayer, W. P. (2018) · Burns · doi:10.1016/j.burns.2018.05.012 · Cited by 26 · see citing works
The phagocytic fitness of leucopatches may impact the healing of chronic wounds
Thomsen, K., Trøstrup, H., Christophersen, L., Lundquist, R., Høiby, N., & Moser, C. E. (2016) · Clinical & Experimental Immunology · doi:10.1111/cei.12773 · Cited by 25 · see citing works
Serre-Miranda, C., Roque, S., Barreira‐Silva, P., Nóbrega, C., Vieira, N., Costa, P., Palha, J. A., & Correia‐Neves, M. (2021) · The Journals of Gerontology Series A · doi:10.1093/gerona/glab330 · Cited by 24 · see citing works
Amini, N., Hivechi, A., Asadpour, S., Ebrahimzadeh, K., Kargozar, S., Gholipourmalekabadi, M., Nasrolahi, A., Ghasemian, M., Shafaat, A., Mozafari, M., et al. (2023) · Drug Delivery and Translational Research · doi:10.1007/s13346-023-01292-0 · Cited by 24 · see citing works
Asunama, A. S. R., Nambi, N., Radhakrishnan, L., Prasad, M. K., & Ramkumar, K. M. (2024) · Current Vascular Pharmacology · doi:10.2174/0115701611308960241014155413 · Cited by 24 · see citing works
The gastrointestinal-brain-microbiota axis: a promising therapeutic target for ischemic stroke
Wei, Y., Bi, R., Qiu, Y., Zhang, C., Li, J., Li, Y., & Hu, B. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1141387 · Cited by 25 · see citing works
Cell and Molecular Biology of Wound Healing
Häkkinen, L., Koivisto, L., Heino, J., & Larjava, H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397157-9.00054-0 · Cited by 22 · see citing works
Therapeutic evaluation of immunomodulators in reducing surgical wound infection
Mahmud, F., Roy, R., Mohamed, M. F., Aboonabi, A., Moric, M. M., Ghoreishi, K., Bayat, M., Kuzel, T. M., Reiser, J., & Shafikhani, S. H. (2021) · The FASEB Journal · doi:10.1096/fj.202101019r · Cited by 23 · see citing works
The complex role of neutrophils in healthy aging, inflammaging, and frailty
Abdullah, G. A., Akpan, A., Phelan, M. M., & Wright, H. L. (2025) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiaf117 · Cited by 20 · see citing works
Nagaraja, S., Chen, L., Zhou, J. P., Zhao, Y. H., Fine, D., DiPietro, L. A., Jaques Reifman, A., & Mitrophanov, A. Y. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601273 · Cited by 20 · see citing works
Boe, D. M., Hulsebus, H. J., Najarro, K. M., Mullen, J. E., Kim, H., Tan, A. C., McMahan, R. H., & Kovacs, E. J. (2022) · Journal of Leukocyte Biology · doi:10.1002/jlb.3hi0620-399rr · Cited by 20 · see citing works
Self-citationMechanisms and Points of Control in the Spread of Inflammation: A Mathematical Investigation
Bayani, A., Dunster, J. L., Crofts, J. J., & Nelson, M. R. (2020) · Bulletin of Mathematical Biology · doi:10.1007/s11538-020-00709-y · Cited by 19 · see citing works
Bayani, A., Dunster, J. L., Crofts, J. J., & Nelson, M. R. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008413 · Cited by 17 · see citing works
Ye, T., Wu, Z., Liu, X., Wu, J., Fu, Q., Cao, J., Zhang, D., & Shi, P. (2025) · Science Advances · doi:10.1126/sciadv.adt7387 · Cited by 16 · see citing works
The Roles of Myeloid Cells in Aging-related Liver Diseases
Yao, J., Li, Y., & Wang, H. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.82352 · Cited by 15 · see citing works
Belboul, A., Ashworth, J., Fadel, A., Mcloughlin, J., Mahmoud, A. M., & Mohtadi, M. E. (2025) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2025.104971 · Cited by 15 · see citing works
Magri, S., Masetto, E., Solito, S., Francescato, S., Belluzzi, E., Pozzuoli, A., Berizzi, A., Ruggieri, P., & Mandruzzato, S. (2020) · Immunity & Ageing · doi:10.1186/s12979-020-00199-5 · Cited by 15 · see citing works
Pantoja, P. D. S., Schmitt, B. L., Maurmann, R. M., & Pence, B. D. (2025) · Molecules · doi:10.3390/molecules30051178 · Cited by 14 · see citing works
Immunosenescence and the Geriatric Giants: Molecular Insights into Aging and Healthspan
Fetarayani, D., Kahdina, M., Waitupu, A., Pratiwi, L., Ningtyas, M. C., Adytia, G. J., & Sutanto, H. (2025) · Medical Sciences · doi:10.3390/medsci13030100 · Cited by 14 · see citing works
Stromal senescence contributes to age-related increases in cancer
Ye, J., Melam, A., & Stewart, S. A. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-025-00840-9 · Cited by 14 · see citing works
Rottmann, B. G., Singh, P. K., Singh, S., Revankar, S. G., Chandrasekar, P. H., & Kumar, A. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.11.31 · Cited by 13 · see citing works
- Authors
- Brubaker, A. L., Rendon, J. L., Ramirez, L., Choudhry, M. A., & Kovacs, E. J.
- Affiliations
- Loyola University Chicago (US)
- Burn and Shock Trauma Institute, Loyola University Chicago Health Sciences Division , Maywood, IL 60153
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-02
- Volume
- 190
- Issue
- 4
- Pages
- 1746-1757
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC3563860
- OpenAlex
- W1865977598
- Cited by
- 181
- References
- 97
- Citations by year
- 2026: 10 · 2025: 17 · 2024: 11 · 2023: 18 · 2022: 15 · 2021: 16 · 2020: 19 · 2019: 12 · 2018: 11 · 2017: 12 · 2016: 15 · 2015: 8 · 2014: 11 · 2013: 6
- FWCI
- 14.23
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Dr. Ralph and Marian Falk Medical Research Trust
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (F30AA020167, T32AA013527)
- National Institute on Aging (R01AG018859, T32AG031780)
- Topics
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Keywords
- aging, neutrophil chemotaxis, neutrophil infiltration, Staphylococcus aureus, wound healing, KC chemokine, ICAM-1, macrophage recruitment, TLR2, FcγRIII, chronic wounds, elderly patients, innate immune dysregulation
- MeSH terms
- Aging, Animals, Chemotaxis, Leukocyte, Disease Models, Animal, Neutrophils, Skin, Staphylococcal Infections, Wound Healing, Down-Regulation, Neutrophil Infiltration, Mice
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