The DOI matches its Crossref record; 126 of the 126 references it cites were found in a registry or an index.
Stress-induced redistribution of immune cells–from barracks to boulevards to battlefields: a tale of three hormones–Curt Richter Award winner
Open accessAbstract
Background The surveillance and effector functions of the immune system are critically dependent on the appropriate distribution of immune cells in the body. An acute or short-term stress response induces a rapid and significant redistribution of immune cells among different body compartments. Stress-induced leukocyte redistribution may be a fundamental survival response that directs leukocyte subpopulations to specific target organs during stress, and significantly enhances the speed, efficacy and regulation of an immune response. Immune responses are generally enhanced in compartments (e.g., skin) that are enriched with leukocytes, and suppressed in compartments that are depleted of leukocytes during/following stress. The experiments described here were designed to elucidate the: (1) Time-course, trajectory, and subpopulation-specificity of stress-induced mobilization and trafficking of blood leukocytes. (2) Individual and combined actions of the principal stress hormones, norepinephrine (NE), epinephrine (EPI), and corticosterone (CORT), in mediating mobilization or trafficking of specific leukocyte subpopulations. (3) Effects of stress/stress hormones on adhesion molecule, L-selectin (CD62L), expression by each subpopulation to assess its adhesion/functional/maturation status.Methods Male Sprague Dawley rats were stressed (short-term restraint, 2-120 min), or adrenalectomized and injected with vehicle (VEH), NE, EPI, CORT, or their combinations, and blood was collected for measurement of hormones and flow cytometric quantification of leukocyte subpopulations.Results Acute stress induced an early increase/mobilization of neutrophils, lymphocytes, helper T cells (Th), cytolytic T cells (CTL), and B cells into the blood, followed by a decrease/trafficking of all cell types out of the blood, except neutrophil numbers that continued to increase. CD62L expression was increased on neutrophils, decreased on Th, CTL, and natural killer (NK) cells, and showed a biphasic decrease on monocytes & B cells, suggesting that CD62L is involved in mediating the redistribution effects of stress. Additionally, we observed significant differences in the direction, magnitude, and subpopulation specificity of the effects of each hormone: NE increased leukocyte numbers, most notably CD62L⁻/⁺ neutrophils and CD62L⁻ B cells. EPI increased monocyte and neutrophil numbers, most notably CD62L⁻/⁺ neutrophils and CD62L⁻ monocytes, but decreased lymphocyte numbers with CD62L⁻/⁺ CTL and CD62L⁺ B cells being especially sensitive. CORT decreased monocyte, lymphocyte, Th, CTL, and B cell numbers with CD62L⁻ and CD62L⁺ cells being equally affected. Thus, naïve (CD62L⁺) vs. memory (CD62L⁻) T cells, classical (CD62L⁺) vs. non-classical (CD62L⁻) monocytes, and similarly distinct functional subsets of other leukocyte populations are differentially mobilized into the blood and trafficked to tissues by stress hormones.Conclusion Stress hormones orchestrate a large-scale redistribution of immune cells in the body. NE and EPI mobilize immune cells into the bloodstream, and EPI and CORT induce traffic out of the blood possibly to tissue surveillance pathways, lymphoid tissues, and sites of ongoing or de novo immune activation. Immune cell subpopulations appear to show differential sensitivities and redistribution responses to each hormone depending on the type of leukocyte (neutrophil, monocyte or lymphocyte) and its maturation/functional characteristics (e.g., non-classical/resident or classical/inflammatory monocyte, naïve or central/effector memory T cell). Thus, stress hormones could be administered simultaneously or sequentially to induce specific leukocyte subpopulations to be mobilized into the blood, or to traffic from blood to tissues. Stress- or stress hormone-mediated changes in immune cell distribution could be clinically harnessed to: (1) Direct leukocytes to sites of vaccination, wound healing, infection, or cancer and thereby enhance protective immunity. (2) Reduce leukocyte traffic to sites of inflammatory/autoimmune reactions. (3) Sequester immune cells in relatively protected compartments to minimize exposure to cytotoxic treatments like radiation or localized chemotherapy. (4) Measure biological resistance/sensitivity to stress hormones in vivo. In keeping with the guidelines for Richter Award manuscripts, in addition to original data we also present a model and synthesis of findings in the context of the literature on the effects of short-term stress on immune cell distribution and function.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Immune responses and associated clinical signs require time to respond (40), and the lack of a sizable response in this study could indicate a response in development or a simple reduction in infection potential for these calves.”
From Effect of source and journey on physiological variables in calves transported by road and ferry between Ireland and the Netherlands (2023) · cites this paper as [40]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Monocytes showed a similar but delayed pattern, which was expected as monocyte count typically responds to stress and infection slower than other immune subsets (40).”
From Effect of source and journey on physiological variables in calves transported by road and ferry between Ireland and the Netherlands (2023) · cites this paper as [40]
Experimental — accuracy not yet measuredIn the citing paper
“an acute stressor activates an acquired immune response via mediation by catecholamines and glucocorticoids and locally produced immune mediators; and, yet, a chronic exposure to the same stressor over several weeks has the opposite effect and results in immune suppression.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [5]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Applied Linear Statistical Models
Ziegel, E. R., Neter, J., Wasserman, W., & Kutner, M. (1992) · Technometrics · doi:10.2307/1269588 · Cited by 9,906
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.1.0389 · Cited by 7,541 · cited 2×
“…epinephrine (EPI) and corticosterone (CORT), that exert the widespread physiological effects of an acute stress response (Dhabhar and McEwen, 2001; Sapolsky et al., 2000), are also the major endocrine mediators of specific phases and redistribution profiles of psychological and physical…”
BackgroundSapolsky, R. M. (2000) · Endocrine Reviews · doi:10.1210/er.21.1.55 · Cited by 7,533
Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm
Springer, T. A. (1994) · Cell · doi:10.1016/0092-8674(94)90337-9 · Cited by 7,009 · cited 2×
“The blood is a critical compartment through which immune cells must pass in order to maintain their normal surveillance pathways and to rapidly reach sites of de novo immune activation (e.g., wounding, sterile tissue damage and inflammation, or antigen or pathogen entry) (Springer, 1994).”
BackgroundProtective and Damaging Effects of Stress Mediators
McEwen, B. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801153380307 · Cited by 6,733 · cited 1×
“While stress can be harmful when it is chronic or long lasting (Chrousos and Kino, 2007; Glaser and KiecoltGlaser, 2005; Irwin et al., 1990; McEwen, 1998), it is often overlooked that a stress response has salubrious adaptive effects in the short run (Dhabhar and McEwen, 2007; Dhabhar and…”
BackgroundSelf-citationApplied Linear Statistical Models.
Lorenz, F. O., Neter, J., Wasserman, W., & Kutner, M. (1986) · Journal of the American Statistical Association · doi:10.2307/2289108 · Cited by 5,566
Monocyte and macrophage heterogeneity
Gordon, S., & Taylor, P. R. (2005) · Nature Reviews Immunology · doi:10.1038/nri1733 · Cited by 5,190
Lymphocyte Homing and Homeostasis
Butcher, E. C., & Picker, L. J. (1996) · Science · doi:10.1126/science.272.5258.60 · Cited by 2,846 · cited 2×
“…leukocyte rolling, the first step in the cascade of reactions that leads to leukocyte adhesion and transmigration, critical steps for leukocyte surveillance pathways and leukocyte response to immune activation/inflammation (Butcher and Picker, 1996; Khan et al., 2003; Wedepohl et al., 2011).”
BackgroundStress-induced immune dysfunction: implications for health
Glaser, R., & Kiecolt-Glaser, J. K. (2005) · Nature Reviews Immunology · doi:10.1038/nri1571 · Cited by 2,190 · cited 1×
“This procedure approximates stress that is largely psychological in nature due to the perception of confinement on part of the animal (for review see: Berkenbosch et al., 1991; Glavin et al., 1994).”
Exercise and the immune system: regulation, integration, and adaptation
Pedersen, B. K., & Hoffman-Goetz, L. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.3.1055 · Cited by 1,710 · cited 4×
“Since exercise induces endocrine changes that are similar to stress (Pedersen and Hoffman-Goetz, 2000; Walsh et al., 2011), these findings are also likely to apply to the effects of exercise on immune cell distribution/function.”
BackgroundInfluential
Flagged first, then by citations
Research works printed but not linked: 1
- Ingle, 1936, Resistance of the rat to histamine shock after destruction of the adrenal medulla Merck, Gen. Physiol., 11, 57
Cited by
Sorted by citations
Items 301–400 of 584
Engert, L. C., Weiler, U., Stefanski, V., & Schmucker, S. S. (2017) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2017.04.004 · Cited by 9
“Differences in GR number or affinity might therefore be related to variations found in glucocorticoid responsiveness among different leukocyte types [2,7].”
BackgroundPhotoperiodic Effects on Diurnal Rhythms in Cell Numbers of Peripheral Leukocytes in Domestic Pigs
Engert, L. C., Weiler, U., Pfaffinger, B., Stefanski, V., & Schmucker, S. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00393 · Cited by 9
“Neutrophil counts were found not to be associated with plasma cortisol concentration, which is supported by other studies (39, 49, 55).”
ResultZhou, H., Chanda, B., Chen, Y., Wang, X., You, M.-Y., Zhang, Y., Cheng, R., Yang, Y., & Chen, X.-Q. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2021.728462 · Cited by 9
“In addition, previous studies indicate that GCs can induce an inflammatory response which induces a pro-inflammatory shift in the balance of IL-1β and antiinflammatory secreted IL-1 receptor antagonist (sIL-1Ra) in neutrophils (29), so the target genes of correlative miRNA of the five selected circRNAs may contribute…”
BackgroundZhang, Y., Zeng, L., Lin, D., Chang, G., Zeng, Y., & Xia, Y. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1076521 · Cited by 9
Behind the monocyte’s mystique: uncovering their developmental trajectories and fates
Teh, Y. C., Chooi, M. Y., & Chong, S. Z. (2023) · Discovery Immunology · doi:10.1093/discim/kyad008 · Cited by 12
“Consequently, the lung harbours more monocytes within its vasculature than any other organ [53, 54] and while this marginal pool of monocytes is sequestered from the circulating blood, they can still be rapidly mobilized within the lung parenchyma in times of need [55].”
BackgroundGlac, W., Dunacka, J., Grembecka, B., Świątek, G., Majkutewicz, I., & Wrona, D. (2021) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-021-09988-1 · Cited by 9
Walker, D. J., Zimmer, C., Larriva, M., Healy, S. D., & Spencer, K. A. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.187039 · Cited by 15
“Alternatively, (2) prenatal CORT may prolong the immediate immunosuppressive state typically observed in animals exposed to stress in the short term (Dimatelis et al., 2012; Wei et al., 2012).”
BackgroundReel, J. M., Abbadi, J., Bueno, A. J., Cizio, K., Pippin, R., Doyle, D. A., Mortan, L. F., Bose, J. L., & Cox, M. A. (2023) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiad154 · Cited by 8
Farahbakht, E., AL-Sinani, Y., Safari, M., Hofmeister, M., Rezaie, R., Sharifabadi, A., & Jahromi, M. K. (2023) · Noise and Health · doi:10.4103/nah.nah_23_23 · Cited by 8
“[34,35] Stress triggers the secretion of glucocorticoids from the adrenal gland by activating the HPA axis.”
Martínez-Shio, E. B., Marín-Jáuregui, L. S., Ortega-Rodríguez, A. C., Doníz-Padilla, L., González‐Amaro, R., Escobedo-Uribe, C. D., & Monsiváis-Urenda, A. E. (2024) · Clinical & Experimental Immunology · doi:10.1093/cei/uxae014 · Cited by 9
Sayed, S. Z., Hassan, Z. O., Abdelraheem, W. M., Refaat, R. S., & Abuelela, I. S. (2024) · BMC Pediatrics · doi:10.1186/s12887-024-05254-4 · Cited by 9
“…as opposed to other white blood cells, neutrophils have been demonstrated to raise most in mice that have experienced stress and keep on rising hours later, even as other white blood cell numbers begin to decline, showing the long-term effect of stress on neutrophil generation and discharging [33].”
Stress Promotes Lung Metastasis in Breast Cancer by Altering Neutrophil Differentiation
Liu, P., Zheng, J., Ma, W., Lü, J., Zhao, Q., Li, D., Jiang, X., Wang, H., Wang, H., & Yu, Z. (2025) · Cancer Research · doi:10.1158/0008-5472.can-25-1763 · Cited by 8
Inflammation as a mediator of stress-related psychiatric disorders
Flux, M. C., & Lowry, C. A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85654-6.00052-6 · Cited by 10
Rose, C. L., McGuire, H. M., Graham, K., Siegler, J. C., Groth, B. F. D. S., Caillaud, C., & Edwards, K. M. (2022) · European Journal of Applied Physiology · doi:10.1007/s00421-022-05058-3 · Cited by 8
“In terms of recovery from injury or insult to muscle tissue, animal studies have established that when these cells disappear from circulation, they migrate to areas of damage which may expedite recovery processes involving these migrating cells (Dhabhar 2009; Dhabhar et al. 2012; Campbell and Turner 2018).”
BackgroundResultInfluentialYıldırım, Y. E., Umut, G., Evren, C., Yeral, E., & Secerli, H. (2023) · Alcohol · doi:10.1016/j.alcohol.2022.12.004 · Cited by 9
Differential transcriptomic alterations in nasal versus lung tissue of acrolein-exposed rats
Alewel, D. I., Jackson, T. W., Rentschler, K. M., Schladweiler, M. C. J., Astriab‐Fisher, A., Gavett, S. H., Evansky, P., & Kodavanti, U. P. (2023) · Frontiers in Toxicology · doi:10.3389/ftox.2023.1280230 · Cited by 8
Hot metacognition: poorer metacognitive efficiency following acute but not traumatic stress
Smith, A., Bisby, J. A., Dercon, Q., Bevan, A., Kigar, S. L., Lynall, M.-E., Dalgleish, T., Hitchcock, C., & Nord, C. L. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02840-z · Cited by 10
“To con fi rm whether the procedure reliably induced stress, fasting venous blood samples [51] and scores on the Positive and Negative Affect Schedule (PANAS) scale [52] were recorded prior to (between 08:00 am and 10:00 am) and 45 min after completing the stress induction (representing the…”
MethodHuang, X., Le, W., Chen, Q., Chen, J., Zhu, Y., Shi, D., Chen, B., & Cui, Z. (2019) · Stress · doi:10.1080/10253890.2019.1645112 · Cited by 8
“Given the decreased lymphocyte count as a result of immune cell distribution in a similar stress model previously reported, it is possible that cancer risk can be significantly increased by lowering both blood lymphocyte count and the specific CKA (Dhabhar et al., 2012; Guidi et al., 1999).”
BackgroundLuo, D., Li, H., Heng, Y., Zhang, M., Hu, J., Jin, C., Chua, M., & Han, B. (2020) · Journal of Surgical Oncology · doi:10.1002/jso.26195 · Cited by 8
Wells, A., Varanoske, A. N., Coker, N., Kozlowski, G. J., Frosti, C. L., Boffey, D., Harat, I., Jahani, S., Gepner, Y., & Hoffman, J. (2020) · Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000003809 · Cited by 6
Innate Immunity in Cardiovascular Diseases—Identification of Novel Molecular Players and Targets
Poller, W. C., Heidecker, B., Ammirati, E., Kuss, A. W., Tzvetkova, A., Poller, W. C., Skurk, C., & Haghikia, A. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12010335 · Cited by 8
Beattie, U. K., Rosen, E. S., Fefferman, N. H., & Romero, L. M. (2023) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2692 · Cited by 8
Testosterone immunomodulation in free-living and captive Rhinella icterica male toads
Titon, S. C. M., Titon, B., Assis, V. R., de Figueiredo, A. C., Floreste, F. R., Lima, A. S., & Gomes, F. R. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0118 · Cited by 7
Modified Aloe Polysaccharide Restores Chronic Stress-Induced Immunosuppression in Mice
Lee, Y. J., Im, S., Kim, J., Lee, S., Kwon, J., Lee, H., Kong, H., Song, Y., Shin, E., Do, S., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17101660 · Cited by 8
“Chronic stress is known to contribute significantly to the development of various diseases such as ulcer, cancer metastasis, and cardiovascular disease [20–22], which has been explicated with its detrimental effects on host immune systems [23,24].”
BackgroundBiomolecules from Plants as an Adaptogen
Singh, M. K., Jain, G., Das, B. K., & Patil, U. K. (2018) · Medicinal & Aromatic Plants · doi:10.4172/2167-0412.1000307 · Cited by 8
Horikawa, I., Nagai, H., Taniguchi, M., Chen, G., Shinohara, M., Suzuki, T., Ishii, S., Katayama, Y., Kitaoka, S., & Furuyashiki, T. (2024) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2024.02.010 · Cited by 8
Cui, X., Xu, P., Tian, T., Song, M., Qin, X., Gong, D., Wang, Y., Zhang, X., Xing, B., Li, M., et al. (2024) · Fishes · doi:10.3390/fishes9060217 · Cited by 7
“This buildup may subsequently interfere with other essential biological processes, such as feeding and reproductive behaviors in fish [51].”
Ansofaxine suppressed NSCLC progression by increasing sensitization to combination immunotherapy
Gui, H., Nie, Y., 袁, 豪., Wang, M., Li, L., Zhu, L., Chen, S., Jing, Q., Wan, Q., Lv, H., et al. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.113918 · Cited by 7
The stress-immune system axis: Exploring the interplay between stress and immunity
Raza, M. L. (2025) · Progress in brain research · doi:10.1016/bs.pbr.2025.01.003 · Cited by 8
Keeler, J. L., Xu, C., Morris, R. C., Hartland, H., Treasure, J. L., & Himmerich, H. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.12.045 · Cited by 7
Kiseleva, I., Larionova, N. V., Grigorieva, E., Дмитриевич, К. А., Farroukh, M. A., & Георгиевна, Р. Л. (2021) · Russian Journal of Infection and Immunity · doi:10.15789/2220-7619-sfo-1662 · Cited by 8
Carbillet, J., Hollain, M., Rey, B., Palme, R., Pellerin, M., Régis, C., Geffré, A., Duhayer, J., Pardonnet, S., Débias, F., et al. (2022) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2022.114141 · Cited by 7
Association between immune cells in peripheral blood and psychiatric symptoms
Yang, J., Wang, Q., & Jiang, W. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1198734 · Cited by 7
Maggio, M. C., Miniaci, A., Gallizzi, R., & Civino, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713192 · Cited by 7
“Stress hormones play a pivotal role in the redistribution of immune cells: noradrenaline and adrenaline mobilize cells into the bloodstream, while adrenaline and cortisol activate cells traffic to lymphoid tissues and tissues with damage or inflammation [88].”
BackgroundVasilieva, N. Y., Хрущова, А. М., KUPTSOV, A. V., Shekarova, O. N., Sokolova, O. V., Wang, D., & Rogovin, K. A. (2019) · Integrative Zoology · doi:10.1111/1749-4877.12419 · Cited by 7
Clinical tolerance of dexamethasone in New Zealand white rabbits
Mayer, J., Aguilar, L. A. B., Walth, G. B., Appleton, K., Holladay, S. D., Howerth, E. W., Meichner, K., & Gogal, R. M. (2021) · Research in Veterinary Science · doi:10.1016/j.rvsc.2021.02.015 · Cited by 7
Immune factors and health of Antarctic explorers
Zabara, D., Kozeretska, I. A., Deineko, I., Anoshko, Y., Shapovalenko, N., Stamboli, L. V., & Dons’koi, B. V. (2021) · Ukrainian Antarctic Journal · doi:10.33275/1727-7485.2.2021.680 · Cited by 7
“However, prolonged action of stress hormones and chronic stress causes a decrease in the circulating leukocytes counts and negatively impacts their ability to migrate (Dhabhar et al., 2013).”
BackgroundUtilization of Mind–Body Intervention for Integrative Health Care of COVID-19 Patients and Survivors
Yang, H., Setou, N., & Koh, E. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19116618 · Cited by 7
“Psychological stress-induced secretions of hormones and neurotransmitters, such as cortisol, epinephrine, and norepinephrine, affect immune cells, causing changes in the immune system during stress [95,96].”
BackgroundNeuroendocrine regulations in tissue-specific immunity: From mechanism to applications in tumor
Liu, S., Li, B., Li, J., Sun, S., Sun, S., & Wu, Q. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.896147 · Cited by 7
“Studies have shown that chronic stress causes a large-scale alteration of immune cells in tissues and induces suppression or dysregulation of immune function (Dhabhar et al., 2012; Dhabhar, 2014).”
BackgroundAl-Hatamleh, M. A. I., Baig, A. A., Simbak, N., Nadeem, M. I., Khan, S. U., & Ariff, T. M. (2017) · Pakistan Journal of Biological Sciences · doi:10.3923/pjbs.2017.478.488 · Cited by 7
Jin, Y., Zhang, X., Badgery, W. B., Li, P., & Wu, J. (2019) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.18.0966 · Cited by 7
“As the stress response continues, stress hormones induce leukocytes to exit the blood and redistribute in the lungs, liver and lymph nodes in preparation for immune challenges [16], which results in a decrease in blood leukocyte numbers [17].”
BackgroundCardiovascular Risk Factors in Parents of Food-Allergic Children
Walker, S. O., Mao, G., Caruso, D., Hong, X., Pongracic, J. A., & Wang, X. (2016) · Medicine · doi:10.1097/md.0000000000003156 · Cited by 7
Investigating relationships among stress, reproduction, and immunity in three species of watersnake
Field, E. K., Terry, J., Hartzheim, A. M., Krajcir, K. J., Mullin, S. J., & Neuman‐Lee, L. A. (2023) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2023.114350 · Cited by 6
Effects of divergent selection upon adrenocortical activity on immune traits in pig
Hervé, J., Terenina, E. E., Haurogné, K., Bacou, E., Kulikova, E., Allard, M., Billon, Y., Bach, J., Mormède, P., & Lieubeau, B. (2019) · BMC Veterinary Research · doi:10.1186/s12917-019-1809-9 · Cited by 6
“In particular, GCs induce lymphocyte sequestration into tissues thereby reducing their number in the circulation [16, 17].”
BackgroundLeal, F. J. V., Ramos‐Fuentes, M. I., Guisado, J. A., Espárrago‐Llorca, G., Redondo‐Rodríguez, C., Bajo‐Cabello, B., & Santos, L. R. (2020) · International Journal of Eating Disorders · doi:10.1002/eat.23278 · Cited by 6
Sood, A., Chaudhari, P. R., Tiwari, P., Shah, S. A., & Vaidya, V. A. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136871 · Cited by 6
Etzel, L. C., Apsley, A. T., Mattern, B. C., Hastings, W. J., Heller, T., Ram, N., Siegel, S. R., & Shalev, I. (2022) · Stress · doi:10.1080/10253890.2022.2148100 · Cited by 6
“…we observed a significant increase in total WBCs due to the TSST across both ELA and control groups which is consistent with literature finding an increase in mobilization of immune cells overall due to acute stress in both animal models and humans (Schedlowski et al., 1993; Dhabhar et al., 2012).”
Rapid and delayed stress effects on recognition of female and male faces
Pötzl, L., Wolf, O. T., & Merz, C. J. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106043 · Cited by 7
Effects of stress and mindfulness on epigenetics
Househam, A. M. (2023) · Vitamins and hormones · doi:10.1016/bs.vh.2022.11.003 · Cited by 6
Kristanto, D., & Septiyani, S. (2023) · Jurnal Medik Veteriner · doi:10.20473/jmv.vol6.iss2.2023.237-243 · Cited by 6
Emerson, D. J., Mulley, C., & Bliemer, M. C. J. (2016) · Research in Transportation Economics · doi:10.1016/j.retrec.2016.05.007 · Cited by 6
Commentary: Sex Differences in the Peripheral Immune System in Patients with Depression
Breidenstein, J., Przyborowski, C., & Walther, A. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00145 · Cited by 6
Lange, L. J., Ames, S. C., Ames, G. E., Heckman, M. G., White, L. J., Roy, V., & Foran, J. M. (2024) · BMC Psychology · doi:10.1186/s40359-024-01535-w · Cited by 5
Pereira-Figueiredo, I., Rosa, I., & Sancho, C. (2024) · Animals · doi:10.3390/ani14050784 · Cited by 6
“A significant increase in neutrophil counts in peripheral blood has been reported in several species just after 6 min of a stressful event, exercise, or inflammation of the muscle tissues [50].”
BackgroundAcute high-intensity exercise enhances T cell proliferation compared to moderate-intensity exercise
Siedlik, J. A., Deckert, J. A., Dunbar, A. J., Bhatta, A., Gigliotti, N. M., Chan, M. A., Benedict, S. H., Bubak, M. P., Vardiman, J. P., & Gallagher, P. M. (2025) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2024-0420 · Cited by 5
Characterizing Primary Immune Responses Against Three Antigens in a Reptile
Terry, J., Davis, I. V., Rolland, V., & Neuman‐Lee, L. A. (2025) · Integrative and Comparative Biology · doi:10.1093/icb/icaf053 · Cited by 5
Hao, X., Gao, M., He, L., Ye, X., Yang, J., Zhang, F., Liu, R., & Wei, H. (2020) · Toxicology · doi:10.1016/j.tox.2020.152411 · Cited by 5
Immunoglobulin-A (IgA) Improvement through Sports and Frirage Massage
Priyonoadi, B., Ndayisenga, J., Sutopo, P., & Graha, A. S. (2020) · International journal of human movement and sports sciences · doi:10.13189/saj.2020.080516 · Cited by 5
“Interestingly, research and other research groups have shown sympathetic nerves which innervate lymphoid tissue as one of the main pathways of the nervous and immune systems communicating to maintain body homeostasis [23, 24] Most importantly according to [26, 27] the evidence suggests that the homeostatic cross-talk…”
BackgroundSurgical Site Infections and Perioperative Optimization of Host Immunity by Selection of Anesthetics
Yuki, K., & Shibamura‐Fujiogi, M. (2021) · BioMed Research International · doi:10.1155/2021/5576959 · Cited by 6
“Epinephrine and norepinephrine induce a redistribution of neutrophils, monocytes, and T cells from the marginated pool such as spleen, lungs, lymph nodes, and bone marrows into the bloodstream and temporarily increase blood leukocyte counts [52].”
BackgroundGenome-Wide mRNA Expression Analysis of Acute Psychological Stress Responses
Logan, J. G., Yun, S., Teachman, B. A., Bao, Y., Farber, E., & Farber, C. R. (2022) · MEDICC Review · doi:10.37757/mr2022.v24.n2.6 · Cited by 5
Immediate and Delayed Salivary Cytokine Responses during Repeated Exposures to Cold Pressor Stress
Larra, M. F., Capellino, S., Schwendich, E., von Haugwitz, L., Reinders, J., & Wascher, E. (2023) · NeuroImmunoModulation · doi:10.1159/000529625 · Cited by 6
“It is indeed well described that acute stressors lead to the recruitment of immune cells in the blood stream [7] and to a systemic increase of proin fl ammatory cytokines [6, 8].”
BackgroundGilstrap, S. R., Hobson, J. M., Owens, M. A., White, D. M., Sammy, M. J., Ballinger, S. W., Sorge, R. E., & Goodin, B. R. (2023) · Molecular Pain · doi:10.1177/17448069231195975 · Cited by 16
Belić, M., Sopić, M., Milenković, M. R., Krstić, V. Ć., Guzonijić, A., Vukašinović, A., Ostanek, B., Dimić, N., Jovanović, D. M., & Kotur‐Stevuljević, J. (2023) · Folia Biologica · doi:10.14712/fb2023069020059 · Cited by 5
Psychoneuroimmunology in the Daily Clinic is Only Possible Within a Contextual Frame
Pruimboom, L., Rocio, F. A., & Ledesma, S. N. (2024) · Integrated science · doi:10.1007/978-3-031-73061-0_16 · Cited by 5
The Brain on Stress: The Good and the Bad
McEwen, B. S. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_1 · Cited by 5
Self-citationKemmerling, J., Fehlert, E., Kuper, C. F., Rühl-Fehlert, C., Stropp, G. D., Vogels, J., Krul, C. A. M., & Vohr, H.-W. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.03.032 · Cited by 5
Benbenishty, A., Segev‐Amzaleg, N., Shaashua, L., Melamed, R., Ben‐Eliyahu, S., & Blinder, P. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.02.012 · Cited by 5
Nishioka, R., Nishi, Y., Choudhury, M. E., Miyaike, R., Shinnishi, A., Umakoshi, K., Takada, Y., Sato, N., Aibiki, M., Yano, H., et al. (2022) · Journal of Immunotoxicology · doi:10.1080/1547691x.2022.2029630 · Cited by 5
“Acute stress elevates Ad and NA levels in circulation while increasing the number of PMN (van de Wouw et al. 2020) and decreasing the number of B-cells (Dhabhar et al. 2012).”
BackgroundDirani, E., Khalil, R. B., Raad, G., & Richa, S. (2022) · Journal of Dual Diagnosis · doi:10.1080/15504263.2022.2090650 · Cited by 5
“For example, stress might activate the cytokine pathway, leading to a shift toward granulocytes in comparison to lymphocytes (Dhabhar et al., 2012).”
BackgroundAnand, G., Lahariya, R., Sarfraz, A., & Tiewsoh, J. B. A. (2025) · American Journal of Infection Control · doi:10.1016/j.ajic.2025.08.020 · Cited by 4
Stress Suppresses Systemic Th17/Treg Imbalance in Rats with Experimental Autoimmune Uveitis
Song, J., Guo, D., Tian, Q., Wu, Q., Zhang, X., & Bi, H. (2021) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2021.1970778 · Cited by 4
Mind-body techniques on stress-induced gut microbiota dysbiosis in Asthmatics: A narrative review
Das, M., Thajuddin, N., Patra, S., & Pundir, M. (2023) · Brain Behavior and Immunity Integrative · doi:10.1016/j.bbii.2023.100040 · Cited by 4
Huang, Y.-C., Ko, P., & Wu, L. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.114848 · Cited by 4
“ARS is also known to induce significant changes in the distribution of immune cells[11,12], affecting populations such as macrophages and T cells[8].”
Öznur, Ö., Utz, S., Schlee, C., & Langhorst, J. (2025) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2025.101006 · Cited by 4
“The drop of leucocyte levels in the recovery phase of the TSST might represent leucocyte traffic out of the blood and into tissues (Dhabhar et al., 2012).”
Srebnik, N., Michaeli, J., Shalev, L., Ruchlemer, R., Farkash, R., & Grisaru‐Granovsky, S. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.12.032 · Cited by 4
Ji, S., Li, Z., Li, M., Lu, Y., Ma, T., Qi, H., Cui, Y., Du, B., Huang, Q., Zhang, K., et al. (2023) · PubMed Central · Cited by 4
Swart, P., Plessis, M. D., Rust, C., Womersley, J. S., van den Heuvel, L. L., Seedat, S., & Hemmings, S. M. J. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15919 · Cited by 3
Interaction of Allostatic Load With Immune, Inflammatory, and Coagulation Systems
Hassanpour, H. (2023) · Immunoregulation · doi:10.32598/immunoregulation.5.2.4 · Cited by 4
González, M. H., Hernández‐Arteaga, E., Almanza-Sepúlveda, M. L., & Guevara, M. Á. (2015) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2015.57023 · Cited by 4
Pukhalsky, A. L., Шмарина, Г. В., & Aleshkin, V. A. (2014) · Annals of the Russian academy of medical sciences · doi:10.15690/vramn.v69i5-6.1038 · Cited by 4
Berg, F., Köper, E., Limberg, A., Mattonet, K., Budeus, B., Kumsta, R., Hummel, E. M., & Moser, D. (2025) · Epigenomics · doi:10.1080/17501911.2025.2479423 · Cited by 3
“The blood cell composition also fluctuates based on factors such as time of day, menstrual cycle, and stress [11].”
van Heijningen, J., van der Pluijm, L. H. M., Schaaf, M. J. M., & Faught, E. (2025) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2025.114815 · Cited by 2
Age affects the immune system more than a moderate surgical trauma and anesthesia
Kraus, R. F., Rastorfer, I., Sixt, S., Hundhammer, T., Dejaco, A., Rimboeck, J., Gruber, M. A., & Petermichl, W. (2025) · Scientific Reports · doi:10.1038/s41598-025-26401-6 · Cited by 3
“An animal test study by Dhabhar et al. showed leukocytosis followed by a steady decrease in the total leukocyte count as early as 6 min after rats were exposed to an acute stress stimulus 28 .”
Decreased exercise-induced natural killer cell redistribution in multiple sclerosis
Munteis, E., Vera, A., Llop, M., Moreira, A., Oviedo, G. R., Javierre, C. F., & Rodríguez, J. (2024) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2024.105634 · Cited by 3
Melanocyte-dependent macrophage redistribution enhances skin immunity upon acute stress
Faught, E. L., & Schaaf, M. J. M. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2511358122 · Cited by 3
“When there is no additional inflammatory stimulus, the animal still mounts a robust immune response, which we postulate is preparatory in nature, corresponding to previous hypotheses that acute stress will act to prepare the animal for any subsequent challenges ( 42 ).”
The Selfish Immune System when the Immune System Overrides the ‘Selfish’ Brain
Pruimboom, L. (2020) · DergiPark (Istanbul University) · Cited by 3
Lester, A. B., Vickers, G. L., Macro, L., Gudgeon, A., Bonham‐Carter, A., Campbell, J. P., & Turner, J. E. (2021) · Physiological Reports · doi:10.14814/phy2.15010 · Cited by 3
“, 2018), due to cells mobilizing from the endothelium, spleen and bone marrow which is thought to be an important part of immune surveillance (Dhabhar, 2014; Dhabhar et al., 2012).”
BackgroundHe, W., Ma, P., Li, X., Wang, Y., & Zhang, Y. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1165614 · Cited by 4
Stress-induced enhancement of immune function
Dhabhar, F. S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-817558-3.00013-5 · Cited by 3
Self-citationHIIT Induces Stronger Shifts within the Peripheral T Cell Compartment Independent of Sex
Proschinger, S., Schenk, A., Metcalfe, A. J., & Zimmer, P. (2023) · International Journal of Sports Medicine · doi:10.1055/a-2197-0882 · Cited by 5
“This redistribution pattern represents a well-known concept in the stress-immune research field [45] and has been translated to the exercise context [46].”
BackgroundTiton, B., Barsotti, A. M. G., Titon, S. C. M., Vaz, R. I., de Figueiredo, A. C., Vasconcelos‐Teixeira, R., Navas, C. A., & Gomes, F. R. (2024) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2024.114517 · Cited by 3
Prado, D. M. D. A., de Figueiredo, A. C., Lima, A. S., Gomes, F. R., & Madelaire, C. B. (2024) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2024.111712 · Cited by 3
Walther, L.-M., Gideon, A., Sauter, C., Leist, M., & Wirtz, P. H. (2024) · Cells · doi:10.3390/cells13231941 · Cited by 3
“(1 ) Immune cell count increases: in addition to the above-described effect of stress hemoconcentration [12,13,29], it has been proposed that the stress-induced release of the catecholamines NEP and EP mobilizes the rapid trafficking of leukocytes from storage organs into the blood stream [9].”
InfluentialPeters, E. M. J. (2016) · JDDG Journal der Deutschen Dermatologischen Gesellschaft · doi:10.1111/ddg.12957_g · Cited by 3
Thymus mast cells as a component of neuro-endocrine-immune interactions under stress
Artashyan, O. S., & Khramtsova, Y. S. (2023) · Medical Immunology (Russia) · doi:10.15789/1563-0625-tmc-2774 · Cited by 2
Music enrichment improves the behavior and leukocyte profile of dairy cattle
Contreras-Torres, E. G., Hernández‐Chávez, J. F., Quiroz, C. A. D., Barrios, R. M. M., Millán, P. A., & Ulloa‐Mercado, G. (2024) · Open Agriculture · doi:10.1515/opag-2022-0289 · Cited by 2
Minias, P., Markowski, M., Słaba, M., Chyb, A., Drzewińska‐Chańko, J., Jedlikowski, J., Bańbura, J., & Włodarczyk, R. (2025) · Environmental Pollution · doi:10.1016/j.envpol.2025.126046 · Cited by 2
Methods for telomere length measurement: an update on current technologies and emerging approaches
Makarova, J. A., Belova, U. D., Zvereva, M. I., Shkurnikov, M. Y., & Tonevitsky, A. (2025) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2025.1725112 · Cited by 3
Sabry, M. O., Seleem, M. M., Ebrahim, Y. M., Hussien, S. G., Ahmed, R., Hassan, H. E., Bahr, A., Alsadany, M. A., El-Shiekh, R. A., & Ali, D. E. (2025) · Revista Brasileira de Farmacognosia · doi:10.1007/s43450-025-00729-6 · Cited by 2
“…evidence through literature that exposure to chronic stressors triggers apoptosis in mononuclear cells, decreases immune cell mobilization from the blood to other tissue compartments, and inhibits cell-mediated immunity (Dhabhar et al. 2012; Sarjan and Yajurvedi 2018; Balakin et al. 2025).”
McEwen, B. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-398270-4.00034-3 · Cited by 2
Self-citation
Metadata
- Authors
- Dhabhar, F. S., Malarkey, W. B., Neri, E., & McEwen, B. S.
- Affiliations
- Stanford Medicine (US)
- The Ohio State University (US)
- Rockefeller University (US)
- Corresponding author
- Dhabhar, Firdaus S.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 37
- Issue
- 9
- Pages
- 1345-1368
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3412918
- OpenAlex
- W2042565214
- Cited by
- 589
- References
- 126
- Citations by year
- 2026: 45 · 2025: 38 · 2024: 46 · 2023: 52 · 2022: 53 · 2021: 69 · 2020: 50 · 2019: 51 · 2018: 36 · 2017: 34 · 2016: 38 · 2015: 33 · 2014: 27 · 2013: 13 · 2012: 4
- FWCI
- 10.22
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- The John D. & Catherine T. MacArthur Foundation
- The DeWitt Wallace Foundation Fellowship
- The Dana Foundation
- NIH (AI48995, AR46299, CA107498)
- Carl & Elizabeth Naumann Fund
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- immune cell trafficking, norepinephrine, epinephrine, corticosterone, neutrophils, monocytes, B cells, T cells, natural killer cells, adrenalectomy, acute restraint stress, stress hormones, leukocyte mobilization, adhesion molecules, rats
- MeSH terms
- Adrenalectomy, Animals, Catecholamines, Cell Movement, Corticosterone, Epinephrine, Immune System, Leukocyte Count, Leukocytes, Male, Restraint, Physical, Stress, Physiological, Stress, Psychological, Rats, Sprague-Dawley, L-Selectin, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
