Toward quantifying the usage costs of human immunity: Altered metabolic rates and hormone levels during acute immune activation in men
Abstract
There is a paucity of data on the energetic demands of human immune functions, despite the fact that both clinical medicine and evolutionary biology would benefit from further clarification of these costs. To better understand the energetic requirements of mounting a mild immune response, as well as some of the major hormonal changes underlying these metabolic changes, we examined changes in resting metabolic rate (RMR) and hormones during and after respiratory tract infection in young adult men. An epidemiologic passive detection design was used to recruit 25 nonfebrile subjects naturally infected with respiratory tract pathogens. Symptomology, percent body fat, RMR, salivary testosterone and cortisol, and other information were collected at a minimum of three time points during and after convalescence. Comparisons of the differences in RMR, testosterone, and cortisol between sampling days within individual cases were made using paired t‐tests. Participants experienced 8% higher RMR during illness, and a subset of these men experienced a mean increase greater than 14%. The participants also experienced 10% lower testosterone levels during illness, and a subset of these participants experienced a mean decrease of 30%, although cortisol levels did not change significantly. These results document elevated RMR following natural pathogen exposure in adult humans, demonstrating that even mild immune reactions can elicit significant increases in energy expenditure. Understanding the costs of immunity and the immunomodulatory actions of hormones are central to understanding the role of immunity in human life history evolution. Am. J. Hum. Biol. 2010. © 2010 Wiley‐Liss, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Numerous studies have consistently found age-dependent decreases in testosterone.
“Numerous studies have consistently identified age-dependent decreases in T.”
From Challenges in Testosterone Measurement, Data Interpretation, and Methodological Appraisal of Interventional Trials (2016) · cites this paper as [35]
A larger analysis of 3690 community-dwelling elderly males with mean age 77 found similar mean testosterone levels among those describing excellent or very good health compared with the overall cohort, suggesting subjective health may not be a significant factor for testosterone levels.
“A larger analysis (n=3690) of community-dwelling, elderly males (mean age 77 years) which demonstrated similar mean T levels (406 vs 378 ng/dl [14.1 vs 13.1 nmol/L]) among those describing excellent or very good health compared to the overall cohort, suggesting that subjective assessment of overall health may not represent a significant factor for T levels.”
From Challenges in Testosterone Measurement, Data Interpretation, and Methodological Appraisal of Interventional Trials (2016) · cites this paper as [35]
In a community-based sample of 3690 elderly men with mean age 77, calculated free testosterone levels were 24.2 pg/ml, while a separate cohort reporting excellent or very good health had 29.9 pg/ml.
“In a community-based sample of 3,690 elderly men (mean age 77), calculated fT levels were 24.2 pg/ml (83.9 pmol/L), with a separate cohort identifying themselves as being in excellent or very good health reported at 29.9 pg/ml (103.7 pmol/L).”
From Challenges in Testosterone Measurement, Data Interpretation, and Methodological Appraisal of Interventional Trials (2016) · cites this paper as [35]
A study of 3690 elderly community-dwelling men with mean age 77 found a mean total testosterone of 378 ng/dl, with upper and lower reference ranges of 693 and 145 ng/dl.
“A second study evaluating 3690 elderly (mean age 77), community-dwelling men identified a mean TT of 378 ng/dl (13.1 nmol/L), with upper (97.5%) and lower (2.5%) reference ranges of 693 and 145 ng/dl (24 and 5 nmol/L), respectively.”
From Challenges in Testosterone Measurement, Data Interpretation, and Methodological Appraisal of Interventional Trials (2016) · cites this paper as [35]
A subset of patients describing themselves as in excellent or very good health had similar mean, 97.5%, and 2.5% total testosterone levels compared with the entire cohort.
“Of interest, a subset of patients describing themselves as in excellent or very good health had similar mean, 97.5%, and 2.5% TT levels compared to the entire cohort (mean-406, 97.5%–739, 2.5%–184 ng/dl [14.1, 25.6, and 6.4 nmol/L]).”
From Challenges in Testosterone Measurement, Data Interpretation, and Methodological Appraisal of Interventional Trials (2016) · cites this paper as [35]
Cites
(2014) · Medical Entomology and Zoology · Cited by 9,400 · see citing works
Predicting basal metabolic rate, new standards and review of previous work.
Wn, S. (1985) · PubMed · Cited by 2,911 · see citing works
Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology
Sheldon, B. C., & Verhulst, S. (1996) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(96)10039-2 · Cited by 2,568 · see citing works
Trade‐offs in evolutionary immunology: just what is the cost of immunity?
Lochmiller, R. L., & Deerenberg, C. M. (2000) · Oikos · doi:10.1034/j.1600-0706.2000.880110.x · Cited by 2,128 · see citing works
The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men
Bhasin, S., Storer, T. W., Berman, N., Callegari, C., Clevenger, B., Phillips, J., Bunnell, T. J., Tricker, R., Shirazi, A., & Casaburi, R. (1996) · New England Journal of Medicine · doi:10.1056/nejm199607043350101 · Cited by 1,659 · see citing works
Regulation of the Hypothalamic-Pituitary-Adrenal Axis by Cytokines: Actions and Mechanisms of Action
TURNBULL, A. V., & RIVIER, C. L. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.1.1 · Cited by 1,297 · see citing works
Competitiveness, risk taking, and violence: the young male syndrome
WILSON, M. I., & Daly, M. (1985) · Ethology and Sociobiology · doi:10.1016/0162-3095(85)90041-x · Cited by 1,242 · see citing works
Survival for Immunity: The Price of Immune System Activation for Bumblebee Workers
Moret, Y., & Schmid‐Hempel, P. (2000) · Science · doi:10.1126/science.290.5494.1166 · Cited by 1,111 · see citing works
Stress and immunity in humans: a meta-analytic review.
Herbert, T. B., & Cohen, S. (1993) · Psychosomatic Medicine · doi:10.1097/00006842-199307000-00004 · Cited by 1,093 · see citing works
Ecological immunology: life history trade-offs and immune defense in birds
Norris, K. J. (2000) · Behavioral Ecology · doi:10.1093/beheco/11.1.19 · Cited by 905 · see citing works
Immune Defense and Host Life History
Zuk, M., & Stoehr, A. M. (2002) · The American Naturalist · doi:10.1086/342131 · Cited by 773 · see citing works
Variation in immune defence as a question of evolutionary ecology
Schmid‐Hempel, P. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2265 · Cited by 723 · see citing works
Applied body composition assessment
(1996) · Choice Reviews Online · doi:10.5860/choice.34-0910 · Cited by 671 · see citing works
Connectivity and the Governance of Multilevel Social-Ecological Systems: The Role of Social Capital
Brondízio, E. S., Elinor Ostrom, B., & Young, O. R. (2009) · Annual Review of Environment and Resources · doi:10.1146/annurev.environ.020708.100707 · Cited by 662 · see citing works
Gonadal Steroids and Immunity*
Olsen, N. J., & Kovacs, W. J. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-4-369 · Cited by 659 · see citing works
Newsholme, P. (2001) · Journal of Nutrition · doi:10.1093/jn/131.9.2515s · Cited by 619 · see citing works
van Eck, M., Berkhof, H., Nicolson, N., & Sulon, J. (1996) · Psychosomatic Medicine · doi:10.1097/00006842-199609000-00007 · Cited by 617 · see citing works
Energy Metabolism: Tissue Determinants and Cellular Corollaries
Kinney, J. M. (1992) · Medical Entomology and Zoology · Cited by 595 · see citing works
Assessing the Cost of Mounting an Immune Response
Bonneaud, C., Mazuc, J., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B., & Sorci, G. (2003) · The American Naturalist · doi:10.1086/346134 · Cited by 564 · see citing works
Infectious episodes in runners before and after the Los Angeles Marathon.
Nieman, D. C., Johanssen, L. M., Lee, J. W., & Arabatzis, K. (1990) · PubMed · Cited by 530 · see citing works
Johnstone, A. M., Murison, S. D., Duncan, J. S., Rance, K. A., & Speakman, J. R. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/82.5.941 · Cited by 514 · see citing works
Martin, L. B., Scheuerlein, A., & Wikelski, M. C. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2185 · Cited by 510 · see citing works
On the evolutionary ecology of specific immune defence
Schmid‐Hempel, P., & Ebert, D. (2003) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)00013-7 · Cited by 488 · see citing works
Testosterone-mediated immune functions and male life histories
Muehlenbein, M. P., & Bribiescas, R. G. (2005) · American Journal of Human Biology · doi:10.1002/ajhb.20419 · Cited by 449 · see citing works
Self-citationReproductive effort decreases antibody responsiveness
Deerenberg, C. M., Arpanius, V., Daan, S., & Bos, N. A. (1997) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1997.0141 · Cited by 442 · see citing works
Reproductive effort reduces specific immune response and parasite resistance
Nordling, D., Andersson, M. S., Zohari, S., & Gustafsson, L. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0432 · Cited by 429 · see citing works
Ketterson, E. D., Nolan, V., Wolf, L., & Ziegenfus, C. (1992) · The American Naturalist · doi:10.1086/285451 · Cited by 423 · see citing works
Elenkov, I. J., Papanicolaou, D. A., Wilder, R. L., & Chrousos, G. P. (1996) · PubMed · Cited by 419 · see citing works
Effects of glucocorticoids on energy metabolism and food intake in humans
Tataranni, P. A., Larson, D. E., Snitker, S., Young, J. B., Flatt, J. P., & Ravussin, É. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.271.2.e317 · Cited by 415 · see citing works
Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice
Demas, G. E., Chefer, V. I., Talan, M. I., & Nelson, R. J. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.5.r1631 · Cited by 367 · see citing works
BAMBINO, T. H., & HSUEH, A. J. W. (1981) · Endocrinology · doi:10.1210/endo-108-6-2142 · Cited by 360 · see citing works
Energetic stress, immunosuppression and the costs of an antibody response
SVENSSON, E. I., Råberg, L., Koch, C., & Hasselquist, D. (1998) · Functional Ecology · doi:10.1046/j.1365-2435.1998.00271.x · Cited by 356 · see citing works
Testosterone and oxidative stress: the oxidation handicap hypothesis
Alonso‐Álvarez, C., Bertrand, S., Faivre, B., Chastel, O., & Sorci, G. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3764 · Cited by 353 · see citing works
Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers
Gustafsson, L., Qvarnström, A., & Sheldon, B. C. (1995) · Nature · doi:10.1038/375311a0 · Cited by 352 · see citing works
Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards
Marler, C. A., & Moore, M. C. (1988) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00303053 · Cited by 349 · see citing works
Ultramarathon running and upper respiratory tract infections. An epidemiological survey.
Peters, E. M., & Bateman, E. D. (1983) · PubMed · Cited by 338 · see citing works
Campbell, D. I., Elia, M., & Lunn, P. G. (2003) · Journal of Nutrition · doi:10.1093/jn/133.5.1332 · Cited by 336 · see citing works
Checkley, W., Epstein, L., Gilman, R. H., Black, R. E., Cabrera, L. Z., & Sterling, C. R. (1998) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009675 · Cited by 329 · see citing works
Gershwin, M. E., Beach, R. S., & Hurley, L. S. (1985) · Cited by 324 · see citing works
Chandra, R. K. (1988) · Liss eBooks · Cited by 311 · see citing works
Nutrition, Immunity, and Infection
Morse, C. G., & High, K. P. (2010) · Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases · doi:10.1016/b978-0-443-06839-3.00010-2 · Cited by 304 · see citing works
Nutritional Aspects of Leukocytic Cytokines
Klasing, K. C. (1988) · Journal of Nutrition · doi:10.1093/jn/118.12.1436 · Cited by 303 · see citing works
Stress hormone and male reproductive function
Hardy, M. P., Gao, H.-B., Dong, Q., Ge, R., Wang, Q., Chai, W. R., Feng, X., & Sottas, C. (2005) · Cell and Tissue Research · doi:10.1007/s00441-005-0006-2 · Cited by 298 · see citing works
Adaptive or Nonadaptive Immunosuppression by Sex Hormones?
Wedekind, C., & Folstad, I. (1994) · The American Naturalist · doi:10.1086/285641 · Cited by 294 · see citing works
Applied body composition assessment
Pintauro, S. J. (2005) · American Journal of Human Biology · doi:10.1002/ajhb.20101 · Cited by 288 · see citing works
Paternal investment affects prevalence of malaria.
Richner, H., Christe, P., & Oppliger, A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.4.1192 · Cited by 277 · see citing works
Metabolic Regulation: A Human Perspective
Frayn, K. N. (1996) · Cited by 276 · see citing works
Oxygen consumption and resting metabolic rate in sepsis, sepsis syndrome, and septic shock
Kreymann, G., GROSSER, S., Buggisch, P., GOTTSCHALL, C., Matthaei, S., & Greten, H. (1993) · Critical Care Medicine · doi:10.1097/00003246-199307000-00015 · Cited by 276 · see citing works
Reproductive ecology and life history of the human male
Bribiescas, R. G. (2001) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10025 · Cited by 273 · see citing works
Regulation of Leydig Cell Steroidogenic Function During Aging1
Zirkin, B. R., & Chen, H. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.4.977 · Cited by 273 · see citing works
Cortisol-Induced Suppression of Plasma Testosterone in Normal Adult Males
Doerr, P., & Pirke, K. M. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-43-3-622 · Cited by 267 · see citing works
Magnitude of the host nutritional responses to infection
Beisel, W. R. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.8.1236 · Cited by 259 · see citing works
Cortisol increases gluconeogenesis in humans: its role in the metabolic syndrome
KHANI, S., & TAYEK, J. A. (2001) · Clinical Science · doi:10.1042/cs1010739 · Cited by 259 · see citing works
Immune challenge affects basal metabolic activity in wintering great tits
Ots, I., Керимов, А. Б., Ivankina, E. V., Ilyina, T. A., & Hõrak, P. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1636 · Cited by 252 · see citing works
DeRijk, R. H., Michelson, D., Karp, B., Petrides, J. S., Galliven, E., Deuster, P., Paciotti, G. F., Gold, P. W., & Sternberg, E. M. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.7.4041 · Cited by 250 · see citing works
Towards a functional explanation for the occurrence of anorexia during parasitic infections
Kyriazakis, I., Tolkamp, B. J., & Hutchings, M. R. (1998) · Animal Behaviour · doi:10.1006/anbe.1998.0761 · Cited by 250 · see citing works
French, S. S., DeNardo, D. F., & Moore, M. C. (2007) · The American Naturalist · doi:10.1086/518569 · Cited by 250 · see citing works
Endocrinologic and metabolic effects of interleukin-6 in humans
Stouthard, J. M., Romijn, J. A., van der Poll, T., Endert, E., Klein, S., Bakker, P. J. M., Veenhof, C. H. N., & Sauerwein, H. P. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.5.e813 · Cited by 247 · see citing works
Stress, testosterone, and the immunoredistribution hypothesis
Braude, S. H., Tang‐Martínez, Z., & Taylor, G. T. (1999) · Behavioral Ecology · doi:10.1093/beheco/10.3.345 · Cited by 244 · see citing works
The energetics of immunity: a neuroendocrine link between energy balance and immune function
Demas, G. E. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.11.002 · Cited by 236 · see citing works
The intricate interface between immune system and metabolism
Matarese, G., & Cava, A. L. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.02.009 · Cited by 225 · see citing works
HORMONAL REGULATION OF HUMAN MUSCLE PROTEIN METABOLISM
Rooyackers, O., & Nair, K. S. (1997) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.17.1.457 · Cited by 225 · see citing works
Tsigos, C., Papanicolaou, D. A., Defensor, R., Mitsiadis, C. S., Kyrou, I., & Chrousos, G. P. (2008) · Neuroendocrinology · doi:10.1159/000127219 · Cited by 223 · cited 1× · see citing works
“Thyroid hormones and several cytokines, particularly tumor necrosis factor-a and interleukin-6, play important roles in altering RMR (de Lange et al., 2001; Freake and Oppenheimer, 1995; Johnstone et al., 2005; Matarese and La Cava, 2004; Stouthard et al., 1995; Tsigos et al., 1997).”
BackgroundA tradeoff between immunocompetence and sexual ornamentation in domestic fowl
Verhulst, S., Dieleman, S. J., & Parmentier, H. K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4478 · Cited by 212 · see citing works
Alternative hypotheses linking the immune system and mate choice for good genes
Westneat, D. F., & Birkhead, T. R. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0400 · Cited by 210 · see citing works
Reproductive axis suppression in acute illness is related to disease severity
Spratt, D. I., Cox, P. M., Orav, E. J., Moloney, J., & Bigos, T. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.6.8501163 · Cited by 208 · see citing works
Effect of cortisol on energy expenditure and amino acid metabolism in humans
Brillon, D. J., Zheng, B., Campbell, R. G., & Matthews, D. E. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.3.e501 · Cited by 206 · see citing works
Sex steroid regulation of autoimmunity
Grossman, C. J., Roselle, G. A., & Mendenhall, C. L. (1991) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90287-f · Cited by 203 · see citing works
Metabolic response to injury and sepsis: changes in protein metabolism
Biolo, G., Toigo, G., Ciocchi, B., Situlin, R., Iscra, F., Gullo, A., & Guarnieri, G. (1997) · Nutrition · doi:10.1016/s0899-9007(97)83044-4 · Cited by 203 · see citing works
Olsen, N. J. (1996) · Endocrine Reviews · doi:10.1210/er.17.4.369 · Cited by 203 · see citing works
Androgen treatment of middle-aged, obese men: effects on metabolism, muscle and adipose tissues.
Mårin, P., Krotkiewski, M., & Björntorp, P. A. (1992) · PubMed · Cited by 196 · see citing works
B-cell kinetics in humans: rapid turnover of peripheral blood memory cells
Macallan, D. C., Wallace, D. L., Zhang, Y., Ghattas, H., Asquith, B., de Lara, C., Worth, A. T., Panayiotakopoulos, G. D., Griffin, G. E., Tough, D. F., et al. (2005) · Blood · doi:10.1182/blood-2004-09-3740 · Cited by 194 · see citing works
Rapid Turnover of Effector–Memory CD4+ T Cells in Healthy Humans
Macallan, D. C., Wallace, D. L., Zhang, Y., de Lara, C., Worth, A. T., Ghattas, H., Griffin, G. E., Beverley, P. C. L., & Tough, D. F. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040341 · Cited by 193 · see citing works
Nutrition, Immunity, and Infection
Chandra, R. K., & Newberne, P. M. (1977) · Springer eBooks · doi:10.1007/978-1-4684-0784-6 · Cited by 189 · see citing works
Marler, C. A., Walsberg, G. E., White, M. L., Moore, M. C., & Marler, C. A. (1995) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00177401 · Cited by 188 · see citing works
Immune response is energetically costly in white cabbage butterfly pupae
Freitak, D., Ots, I., Vanatoa, A., & Hõrak, P. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rsbl.2003.0069 · Cited by 187 · see citing works
Glucocorticoid Induces Apoptosis in Rat Leydig Cells
Gao, H.-B., Tong, M., Hu, Y.-Q., Guo, Q.-S., Ge, R., & Hardy, M. P. (2002) · Endocrinology · doi:10.1210/endo.143.1.8604 · Cited by 185 · see citing works
Thermogenesis and Thyroid Function
Freake, H. C., & Oppenheimer, J. H. (1995) · Annual Review of Nutrition · doi:10.1146/annurev.nu.15.070195.001403 · Cited by 177 · see citing works
The Role of Estrogen Receptors and Androgen Receptors in Sex Steroid Regulation of B Lymphopoiesis
Smithson, G. M., Couse, J. F., Lubahn, D. B., Korach, K. S., & Kincade, P. W. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.1.27 · Cited by 176 · see citing works
Extraction of urban impervious surfaces from an IKONOS image
Lu, D., & Weng, Q. (2009) · International Journal of Remote Sensing · doi:10.1080/01431160802508985 · Cited by 176 · see citing works
McKean, K. A., & Nunney, L. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01800.x · Cited by 176 · see citing works
Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence
McDade, T. W., Beck, M. A., Kuzawa, C. W., & Adair, L. S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.4.543 · Cited by 173 · see citing works
Ahmed, A. M., Baggott, S. L., Maingon, R. D., & Hurd, H. (2002) · Oikos · doi:10.1034/j.1600-0706.2002.970307.x · Cited by 171 · see citing works
Contribution of protein to caloric expenditure following injury.
Duke, J., Jørgensen, S. B., BROELL, J. R., Long, C. L., & Kinney, J. M. (1970) · PubMed · Cited by 170 · see citing works
In Vivo Effects of Sex Steroids on Lymphocyte Responsiveness and Immunoglobulin Levels in Humans
Giltay, E. J., Fonk, J. C. M., Blomberg, B. M. E. V., Drexhage, H. A., Schalkwijk, C., & Gooren, L. J. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.4.6562 · Cited by 170 · see citing works
McDade, T. W., Reyes‐García, V., Tanner, S. N., Huanca, T., & Leonard, W. R. (2008) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20831 · Cited by 160 · see citing works
Nieman, D. C., Austin, M. D., Benezra, L., Pearce, S., McInnis, T., Unick, J. L., & Gross, S. J. (2006) · Research in Sports Medicine · doi:10.1080/15438620600651512 · Cited by 157 · see citing works
Metabolic Response to Injury and Sepsis: Changes in Protein Metabolism
Biolo, G. (1997) · Nutrition · doi:10.1016/s0899-9007(97)00206-2 · Cited by 157 · see citing works
Energy balance and carbohydrate metabolism in infection and sepsis
Long, C. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.8.1301 · Cited by 154 · see citing works
Felten, D. L., & Maida, M. E. (2002) · Elsevier eBooks · doi:10.1016/b0-12-227210-2/00292-2 · Cited by 148 · see citing works
Cytokines, Acute‐Phase Proteins, and Hormones
Burger, D., & Dayer, J.-M. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04248.x · Cited by 146 · see citing works
Malnutrition and Energy Restriction Differentially Affect Viral Immunity
Ritz, B. W., & Gardner, E. M. (2006) · Journal of Nutrition · doi:10.1093/jn/136.5.1141 · Cited by 142 · see citing works
Prenatal Undernutrition and Postnatal Growth Are Associated with Adolescent Thymic Function
McDade, T. W., Beck, M. A., Kuzawa, C. W., & Adair, L. S. (2001) · Journal of Nutrition · doi:10.1093/jn/131.4.1225 · Cited by 138 · see citing works
Sa, B., Ca, M., McEwan, J. C., & Vlassoff, A. (2001) · New Zealand Veterinary Journal · doi:10.1080/00480169.2001.36238 · Cited by 132 · see citing works
Nutrition, immunity, and infection : mechanisms of interactions
Chandra, R. K., & Newberne, P. M. (1977) · Plenum Press eBooks · Cited by 128 · see citing works
Stress, cytokine patterns and susceptibility to disease
Elenkov, I. J., & Chrousos, G. P. (1999) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1053/beem.1999.0045 · Cited by 128 · see citing works
Pharmacology, Biology, and Clinical Applications of Androgens
Silver, R. I. (1996) · The Journal of Urology · doi:10.1097/00005392-199609000-00112 · Cited by 128 · see citing works
Hormonal changes in serum in young men during prolonged physical strain
Aakvaag, A., Sand, T., Opstad, P. K., & Fonnum, F. (1978) · European Journal of Applied Physiology · doi:10.1007/bf00421452 · Cited by 127 · see citing works
Derting, T. L., & Compton, S. (2003) · Physiological and Biochemical Zoology · doi:10.1086/375662 · Cited by 126 · see citing works
de Lange, P., Lanni, A., Beneduce, L., Moreno, M., Lombardi, A., Silvestri, E., & Goglia, F. (2001) · Endocrinology · doi:10.1210/endo.142.8.8303 · Cited by 125 · see citing works
Delayed Puberty Associated with Inflammatory Bowel Disease
Ballinger, A., Savage, M. O., & Sanderson, I. R. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000047510.65483.c9 · Cited by 122 · see citing works
Ardia, D. R., Schat, K. A., & Winkler, D. W. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2424 · Cited by 120 · see citing works
Delayed Puberty Associated with Inflammatory Bowel Disease
Ballinger, A., SAVAGE, A. M. O., & Sanderson, I. R. (2003) · Pediatric Research · doi:10.1203/00006450-200302000-00002 · Cited by 120 · see citing works
Éraud, C., Duriez, O., Chastel, O., & Faivre, B. (2005) · Functional Ecology · doi:10.1111/j.0269-8463.2005.00934.x · Cited by 119 · see citing works
Metabolism of Sepsis and Multiple Organ Failure
MICHIE, H. R. (1996) · World Journal of Surgery · doi:10.1007/s002689900072 · Cited by 118 · see citing works
Chao, T., Alten, P. J. V., & Walter, R. J. (1994) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1994.tb00877.x · Cited by 117 · see citing works
Testosterone signaling in T cells and macrophages
Wunderlich, F. T., Benten, W. P. M., Lieberherr, M., Guo, Z., Stamm, O., Wrehlke, C., Sekeris, C. E., & Mossmann, H. (2002) · Steroids · doi:10.1016/s0039-128x(01)00175-1 · Cited by 115 · see citing works
Immune activation suppresses plasma testosterone level: a meta-analysis
Boonekamp, J. J., Ros, A. F. H., & Verhulst, S. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0347 · Cited by 112 · see citing works
Relationships between resting and total energy expenditure in injured and septic patients
Frankenfield, D. C., Wiles, C. E., Bagley, S. M., & Siegel, J. H. (1994) · Critical Care Medicine · doi:10.1097/00003246-199411000-00015 · Cited by 111 · see citing works
Gomez-Mérino, D., Drogou, C., Chennaoui, M., Tiollier, E., Mathieu, J., & Guézennec, C. Y. (2005) · NeuroImmunoModulation · doi:10.1159/000084849 · Cited by 109 · see citing works
Weinstein, Y., & Berkovich, Z. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.126.3.998 · Cited by 106 · see citing works
Effect of infection on nutrient requirements
Scrimshaw, N. S. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.9.1536 · Cited by 106 · see citing works
Increased resting energy expenditure in cystic fibrosis
Buchdahl, R., Cox, M., Fulleylove, C., Marchant, J. L., Tomkins, A. M., Brueton, M. J., & Warner, J. O. (1988) · Journal of Applied Physiology · doi:10.1152/jappl.1988.64.5.1810 · Cited by 105 · see citing works
Welle, S. L., Józefowicz, R. F., Forbes, G. B., & Griggs, R. C. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.2.1730811 · Cited by 105 · see citing works
House Sparrow (Passer domesticus)
Lowther, P. E., & Cink, C. L. (2006) · The Birds of North America Online · doi:10.2173/bna.houspa.02 · Cited by 105 · see citing works
Warner, C. M., Meeker, D., & Rothschild, M. F. (1987) · Journal of Animal Science · doi:10.2527/jas1987.642394x · Cited by 99 · see citing works
The 3' sequences required for incorporation of an engineered ssRNA into the Reovirus genome
Roner, M. R., & Roehr, J. (2006) · Virology Journal · doi:10.1186/1743-422x-3-1 · Cited by 97 · see citing works
Growth Failure in Children With HIV Infection
Arpadi, S. M. (2000) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/00042560-200010001-00006 · Cited by 97 · see citing works
Role of Cytokines in Regulating Feeding Behaviour
Wong, S., & Pinkney, J. H. (2004) · Current Drug Targets · doi:10.2174/1389450043490532 · Cited by 96 · see citing works
Cortisol increases gluconeogenesis in humans: its role in the metabolic syndrome
KHANI, S., & Tayek, J. A. (2001) · Clinical Science · doi:10.1042/cs20010180 · Cited by 91 · see citing works
Alterations in basal nutrient metabolism increase resting energy expenditure in sickle cell disease
Borel, M. J., Buchowski, M. S., Turner, E., Peeler, B. B., Goldstein, R. E., & Flakoll, P. J. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.2.e357 · Cited by 90 · see citing works
Spratt, D. I., Morton, J. R., Kramer, R. S., Mayo, S. W., Longcope, C., & Vary, C. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00467.2005 · Cited by 88 · see citing works
Sex steroid hormone metabolism and prostate cancer
Soronen, P., Laiti, M., Törn, S., Härkönen, P. K., Patrikainen, L., Li, Y., Pulkka, A. E., Kurkela, R., Herrala, A. M., Kaija, H., et al. (2004) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2004.10.004 · Cited by 86 · see citing works
Testicular dysfunction in human immunodeficiency virus—infected men
Poretsky, L., Can, S., & Zumoff, B. (1995) · Metabolism · doi:10.1016/0026-0495(95)90250-3 · Cited by 86 · see citing works
Growth Failure in Children With HIV Infection
Arpadi, S. M. (2000) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/00126334-200010001-00006 · Cited by 84 · see citing works
Metabolic regulation: a human perspective
(1996) · Choice Reviews Online · doi:10.5860/choice.34-1532 · Cited by 82 · see citing works
DeRijk, R. H. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.7.2182 · Cited by 77 · see citing works
Muehlenbein, M. P., & Ancrenaz, M. (2009) · Journal of Travel Medicine · doi:10.1111/j.1708-8305.2009.00346.x · Cited by 76 · see citing works
Self-citationRevisiting the hierarchy of urban areas in the Brazilian Amazon: a multilevel approach
Guedes, G. R., da Costa, S. M. F., & Brondízio, E. S. (2009) · Population and Environment · doi:10.1007/s11111-009-0083-3 · Cited by 74 · see citing works
Stress-Induced Suppression of Luteinizing Hormone Concentrations in Wild Baboons: Role of Opiates*
Sapolsky, R. M., & Krey, L. C. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-4-722 · Cited by 73 · see citing works
Weng, Q., & Lu, D. (2009) · International Journal of Remote Sensing · doi:10.1080/01431160802552777 · Cited by 72 · see citing works
Shiner, M. (1991) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/j.1536-4801.1991.tb10329.x · Cited by 68 · see citing works
Long, K. Z., & Nanthakumar, N. N. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20064 · Cited by 67 · see citing works
Leptin regulates energetic tradeoffs between body fat and humoural immunity
Demas, G. E., & Sakaria, S. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3126 · Cited by 66 · see citing works
The Caloric Equivalent of Fever
Roe, C. F., & Kinney, J. M. (1965) · Annals of Surgery · doi:10.1097/00000658-196501000-00022 · Cited by 65 · see citing works
National forest carbon inventories: policy needs and assessment capacity
Andersson, K. P., Evans, T. P., & Richards, K. (2008) · Climatic Change · doi:10.1007/s10584-008-9526-6 · Cited by 65 · see citing works
Altered gonadal steroidogenesis in critical illness: is treatment with anabolic steroids indicated?
Spratt, D. I. (2001) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1053/beem.2001.0165 · Cited by 64 · see citing works
Hasselgren, P.-O. J., & Fischer, J. E. (1998) · World Journal of Surgery · doi:10.1007/s002689900370 · Cited by 64 · see citing works
Connors, V. A., & Nickol, B. B. (1991) · Parasitology · doi:10.1017/s0031182000059916 · Cited by 62 · see citing works
Panter‐Brick, C., Lunn, P. G., Baker, R., & Todd, A. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2000225 · Cited by 61 · see citing works
THE REPRODUCTIVE ENDOCRINE RESPONSE TO PLASMODIUM VIVAX INFECTION IN HONDURANS
Muehlenbein, M. P., Alger, J., Cogswell, F. B., James, M. A., & Krogstad, D. J. (2005) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2005.73.178 · Cited by 60 · see citing works
Self-citationMitchell, J. C., Li, X. F., Breen, L., Thalabard, J.-C., & O’Byrne, K. T. (2005) · Endocrinology · doi:10.1210/en.2004-1053 · Cited by 58 · see citing works
Mode of action of interleukin-1 in suppression of pituitary LH release in castrated male rats
Bonavera, J. J., Kalra, S. P., & Kalra, P. S. (1993) · Brain Research · doi:10.1016/0006-8993(93)91637-8 · Cited by 57 · see citing works
Norbiato, G., Bevilacqua, M. T., Vago, T., Taddei, A., & Clerici, M. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.10.4304 · Cited by 56 · see citing works
Gandra, Y. R., & Scrimshaw, N. S. (1961) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/9.2.159 · Cited by 55 · see citing works
Barr, D. P. (1922) · Archives of Internal Medicine · doi:10.1001/archinte.1922.00110050055004 · Cited by 55 · see citing works
Impact of Age on Cortisol Secretory Dynamics Basally and as Driven by Nutrient-Withdrawal Stress
Bergendahl, M., Iranmanesh, A., Mulligan, T., & Veldhuis, J. D. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.6.6628 · Cited by 53 · see citing works
Testosterone correlates with Venezuelan equine encephalitis virus infection in macaques
Muehlenbein, M. P., Cogswell, F. B., James, M. A., Koterski, J. F., & Ludwig, G. V. (2006) · Virology Journal · doi:10.1186/1743-422x-3-19 · Cited by 52 · see citing works
Self-citationRoad impacts in Brazilian Amazonia
Pfaff, A. S. P., Barbieri, A. F., Ludewigs, T., Merry, F. D., Perz, S. G., & Reis, E. J. (2009) · Geophysical monograph · doi:10.1029/2008gm000737 · Cited by 50 · see citing works
Öktenli, Ç. (2004) · Human Reproduction · doi:10.1093/humrep/deh161 · Cited by 50 · see citing works
Infection and Nutritional Status: I. The Effect of Chicken Pox on Nitrogen Metabolism in Children
WILSON, D., Bressani, R., & Scrimshaw, N. S. (1961) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/9.2.154 · Cited by 50 · see citing works
(1985) · Elsevier eBooks · doi:10.1016/b978-0-122-81450-1.x5001-6 · Cited by 50 · see citing works
Detecting subtle land use change in tropical forests
Sirén, A. H., & Brondízio, E. S. (2008) · Applied Geography · doi:10.1016/j.apgeog.2008.08.006 · Cited by 49 · see citing works
Spurlock, M. E., Frank, G. R., Willis, G. M., Kuske, J. L., & Cornelius, S. G. (1997) · Journal of Animal Science · doi:10.2527/1997.753720x · Cited by 46 · see citing works
BRINK, G. R. V. D., van den Boogaardt, D. E. M., van Deventer, S. J. H., & Peppelenbosch, M. P. (2002) · Clinical and Vaccine Immunology · doi:10.1128/cdli.9.1.182-183.2002 · Cited by 46 · see citing works
The effect of environmental temperature on immune response and metabolism of the young chicken
Henken, A. M. (1982) · doi:10.18174/205648 · Cited by 42 · see citing works
Attardi, B., Tsujii, T., Friedman, R., Zeng, Z., Roberts, J. L., Dellovade, T., Pfaff, D. W., Chandran, U. R., Sullivan, M. W., & DeFranco, D. B. (1997) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(97)00102-0 · Cited by 41 · see citing works
Reproductive Function in Human Immunodeficiency Virus Infection
Lo, J. C.-M., & Schambelan, M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7604 · Cited by 41 · see citing works
Hadju, V., Abadi, K., Stephenson, L. S., Noor, N. N., Mohammed, H. O., & Dd, B. (1995) · PubMed · Cited by 40 · see citing works
Muehlenbein, M. P. (2006) · Biodemography and Social Biology · doi:10.1080/19485565.2006.9989113 · Cited by 40 · see citing works
Self-citationThe Effect of Environmental Temperature on Immune Response and Metabolism of the Young Chicken
Henken, A. M., & Brandsma, H. A. (1982) · Poultry Science · doi:10.3382/ps.0611667 · Cited by 39 · see citing works
The nutritional cost of measles in Africa.
Duggan, M. B., Alwar, J., & Milner, R. D. G. (1986) · Archives of Disease in Childhood · doi:10.1136/adc.61.1.61 · Cited by 36 · see citing works
Kalantaridou, S., Makrigiannakis, A., Zoumakis, E., & Chrousos, G. P. (2004) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2004.00155.x · Cited by 34 · see citing works
Metabolic changes following thermal injury
Arturson, M. G. S. (1978) · World Journal of Surgery · doi:10.1007/bf01553553 · Cited by 33 · see citing works
Zwart, D., Brouwer, B. O., van der Hel, W., van den Akker, H. N., & Verstegen, M. W. A. (1991) · Journal of Animal Science · doi:10.2527/1991.6993780x · Cited by 32 · see citing works
Simmons, Z. L., & Roney, J. R. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20837 · Cited by 32 · see citing works
On the dual nature of maternal aggression in rats
Lucion, A. B., & de Almeida, R. M. M. (1996) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(1996)22:5 · Cited by 32 · see citing works
Thermal balance and metabolic rate during upper respiratory tract infection in infants.
Fleming, P., Howell, T., Clements, M., & Lucas, J. S. (1994) · Archives of Disease in Childhood · doi:10.1136/adc.70.3.187 · Cited by 31 · see citing works
Metabolic and febrile responses to typhoid vaccine in humans: effect of beta-adrenergic blockade
Cooper, A. L., Horan, M. A., Little, R., & Rothwell, N. J. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.6.2322 · Cited by 30 · see citing works
Schistosomiasis: Role of endogenous opioids in suppression of gonadal steroid secretion
Isseroff, H., Sylvester, P. W., Bessette, C. L., Jones, P. L., Fisher, W. G., Rynkowski, T. A., & Gregor, K. R. (1989) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(89)90781-0 · Cited by 29 · see citing works
Positive effects of testosterone and immunochallenge on energy allocation to reproductive organs
Derting, T. L., & Virk, M. K. (2005) · Journal of Comparative Physiology B · doi:10.1007/s00360-005-0015-1 · Cited by 27 · see citing works
METABOLIC CONSEQUENCES OF SEPSIS
Crouser, E. D., & Dorinsky, P. (1996) · Clinics in Chest Medicine · doi:10.1016/s0272-5231(05)70312-9 · Cited by 27 · see citing works
Bilateral Communication Between the Endocrine and Immune Systems
(1994) · E&M. Endocrinology and metabolism · doi:10.1007/978-1-4612-2616-1 · Cited by 25 · see citing works
The effect of supplementation with an enriched drink on indices of immune function in frail elderly.
Wouters-Wesseling, W., Vos, A. P., Hal, M. V., de Groot, C. P. G. M., van Staveren, W. A., & BINDELS, J. G. (2005) · PubMed · Cited by 25 · see citing works
Dose-dependent relationships between Nippostrongylus brasiliensis populations and rat food intake
Ovington, K. S. (1985) · Parasitology · doi:10.1017/s0031182000056596 · Cited by 24 · see citing works
Breen, K. M., & Karsch, F. J. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.045898 · Cited by 22 · see citing works
Energy and nitrogen metabolism of chickens infected with eitherEimeria acervulinaorEimeria tenella
Takhar, B. S., & Farrell, D. J. (1979) · British Poultry Science · doi:10.1080/00071667908416569 · Cited by 21 · see citing works
Thermogenic, hormonal and metabolic effects of intravenous glucose infusion in human sepsis
Carlson, G., Gray, P., Arnold, J., Little, R., & Irving, M. H. (1997) · British journal of surgery · doi:10.1111/j.1365-2168.1997.02798.x · Cited by 20 · see citing works
Magnanou, É., Fons, R., Feliú, C., & Morand, S. (2006) · Parasitology Research · doi:10.1007/s00436-005-0063-1 · Cited by 20 · see citing works
Bazar, K. A., Yun, A. J., & Lee, P. Y. (2004) · Medical Hypotheses · doi:10.1016/j.mehy.2004.05.020 · Cited by 19 · see citing works
The Diamond Jubilee of the Nutrition Society
Williams, C. M. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2001266 · Cited by 15 · see citing works
The Role of Sex Steroids in Immune System Regulation
Grossman, C. J. (1994) · E&M. Endocrinology and metabolism · doi:10.1007/978-1-4612-2616-1_1 · Cited by 14 · see citing works
Mattos, L. M., & dos Santos, A. C. C. (2009) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 12 · see citing works
The Pathogenicity of the Avian Tubercle Bacillus
L'Esperance, E. S. (1929) · The Journal of Immunology · doi:10.4049/jimmunol.16.1.27 · Cited by 10 · see citing works
Cooper, A. L., Fitzgeorge, R. B., Baskerville, A., Little, R., & Rothwell, N. J. (1989) · Life Sciences · doi:10.1016/0024-3205(89)90178-1 · Cited by 10 · see citing works
Gash, J. H. C., Keller, M., Bustamante, M., & Dias, P. L. D. S. (2009) · Geophysical monograph · doi:10.1029/2009gm000883 · Cited by 8 · see citing works
EFFECT OF TRAINING ON PHYSICAL EXERCISE-INDUCED CHANGES IN NON-SPECIFIC HUMORAL IMMUNITY
Kumae, T., Kurakake, S., Machida, K., & Sugawara, K. (1994) · 体力科學 · doi:10.7600/jspfsm1949.43.75 · Cited by 5 · see citing works
Proposed biomolecular theory of fasting during fevers due to infection.
Yarnell, E. L. (2001) · PubMed · Cited by 3 · see citing works
Straub, R. H., & Cutolo, M. (2001) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200103)44:3
Flagged first, then by citations
Cited by
Sorted by citations
Impact of Childhood Malnutrition on Host Defense and Infection
Ibrahim, M. K., Zambruni, M., Melby, C. L., & Melby, P. C. (2017) · Clinical Microbiology Reviews · doi:10.1128/cmr.00119-16 · Cited by 359 · see citing works
“, intestinal loss of nutrients during diarrhea), there is a metabolic cost to immune activation that contributes to the increased energy deficit in infected children (327).”
BackgroundNeuronal regulation of immunity: why, how and where?
Schiller, M., Ben-Shaanan, T. L., & Rolls, A. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-0387-1 · Cited by 267 · see citing works
Physical Attractiveness in Adaptationist Perspective.
Sugiyama, L. (2015) · Wiley eBooks · doi:10.1002/9781119125563.evpsych112 · Cited by 218 · see citing works
Trade-offs between acquired and innate immune defenses in humans
McDade, T. W., Georgiev, A. V., & Kuzawa, C. W. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eov033 · Cited by 215 · see citing works
“Prior work on humans has focused almost exclusively on the overall costs of immunity, and the potential for trade-offs with systems or processes related to growth or reproduction [11, 38].”
BackgroundInfluentialEisenberg, D. T. A. (2010) · American Journal of Human Biology · doi:10.1002/ajhb.21127 · Cited by 208 · see citing works
“, 2001; McDade, 2003), and infections can increase basal/resting metabolic rates (e.g. Careau et al., 2010; Cutrera et al., 2010; Hommes et al., 1990; Long et al., 1979; Muehlenbein et al., 2010; Steuber, 2007).”
BackgroundDetection of impervious surface change with multitemporal Landsat images in an urban–rural frontier
Lu, D., Moran, E. F., & Hetrick, S. S. (2010) · ISPRS Journal of Photogrammetry and Remote Sensing · doi:10.1016/j.isprsjprs.2010.10.010 · Cited by 193 · see citing works
Tradeoffs between immune function and childhood growth among Amazonian forager-horticulturalists
Urlacher, S., Ellison, P., Sugiyama, L., Pontzer, H., Eick, G., Liebert, M., Cepon-Robins, T., Gildner, T., & Snodgrass, J. (2018) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1717522115 · Cited by 169 · see citing works
“Severe immunological responses can more than double basal energy expenditure (6), and even mild, nonfebrile immune activity is accompanied by an 8–14% increase in resting metabolic rate (7).”
BackgroundSystemic Immunometabolism: Challenges and Opportunities
Lercher, A., Baazim, H., & Bergthaler, A. (2020) · Immunity · doi:10.1016/j.immuni.2020.08.012 · Cited by 141 · see citing works
“The underlying endogenous regulation of feeding behavior during infection is thought to redistribute energy and balance the energetic demands of the activated immune system with the organism’s core functions of maintenance, growth, and reproduction programs, known as the ‘‘life history programs’’ (Ganeshan et al., 201…”
Wells, J. C. K., & Stock, J. T. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00325 · Cited by 131 · see citing works
Interactions of diarrhea, pneumonia, and malnutrition in childhood
Schlaudecker, E. P., Steinhoff, M. C., & Moore, S. R. (2011) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e328349287d · Cited by 126 · see citing works
Impervious surface mapping with Quickbird imagery
Lu, D., Hetrick, S. S., & Moran, E. F. (2011) · International Journal of Remote Sensing · doi:10.1080/01431161003698393 · Cited by 115 · see citing works
Blackwell, A. D., Snodgrass, J. J., Madimenos, F. C., & Sugiyama, L. S. (2010) · American Journal of Human Biology · doi:10.1002/ajhb.21092 · Cited by 114 · see citing works
“…(Bogin, 1999; McDade et al., 2008; Victora, 1992), and across species the costs associated with mounting an immune response have been found to decrease growth, survival, and reproduction (Adamo, 2001; Klein and Nelson, 1999; Muehlenbein et al., 2010; Sheldon and Verhulst, 1996; Uller et al., 2006).”
InfluentialAbrams, E. T., & Miller, E. M. (2011) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21621 · Cited by 110 · see citing works
SARS-CoV-2 Pneumonia Affects Male Reproductive Hormone Levels: A Prospective, Cohort Study
Kadıhasanoğlu, M., Aktaş, S., Yardimci, E., Aral, H., & Kadıoğlu, A. (2020) · The Journal of Sexual Medicine · doi:10.1016/j.jsxm.2020.11.007 · Cited by 104 · see citing works
Trost, L. W., & Mulhall, J. P. (2016) · The Journal of Sexual Medicine · doi:10.1016/j.jsxm.2016.04.068 · Cited by 98 · see citing works
Energy Expenditure in Humans and Other Primates: A New Synthesis
Pontzer, H. (2015) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-102214-013925 · Cited by 100 · see citing works
“Work in nonhuman mammals suggests metabolic rate increases of 10–50% are common in response to infection (see Muehlenbein et al. 2010).”
BackgroundHormonal Mechanisms for Regulation of Aggression in Human Coalitions
Flinn, M. V., Ponzi, D., & Muehlenbein, M. P. (2012) · Human Nature · doi:10.1007/s12110-012-9135-y · Cited by 94 · see citing works
“Decreased testosterone levels would also function to prevent immunosuppression and other costs associated with otherwise elevated testosterone levels (Muehlenbein 2008; Muehlenbein et al. 2010).”
BackgroundSelf-citationCoastal wetland vegetation classification with a Landsat Thematic Mapper image
Zhang, Y., Lu, D., Yang, B., Sun, C., & Sun, M. (2011) · International Journal of Remote Sensing · doi:10.1080/01431160903475241 · Cited by 95 · see citing works
Functional significance of men’s testosterone reactivity to social stimuli
Zilioli, S., & Bird, B. M. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.06.002 · Cited by 88 · see citing works
Balancing growth, reproduction, maintenance, and activity in evolved energy economies
Pontzer, H., & McGrosky, A. (2022) · Current Biology · doi:10.1016/j.cub.2022.05.018 · Cited by 88 · see citing works
Lu, D., Li, G., Moran, E. F., Dutra, L. V., & Batistella, M. (2011) · GIScience & Remote Sensing · doi:10.2747/1548-1603.48.3.345 · Cited by 82 · see citing works
Gettler, L. T., McDade, T. W., & Kuzawa, C. W. (2011) · American Journal of Human Biology · doi:10.1002/ajhb.21187 · Cited by 81 · see citing works
Type 2 diabetes and viral infection; cause and effect of disease
Wensveen, T. T., Gašparini, D., Rahelić, D., & Wensveen, F. M. (2021) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2020.108637 · Cited by 80 · see citing works
“[16] Muehlenbein MP, Hirschtick JL, Bonner JZ, Swartz AM.”
BackgroundTrumble, B. C., Cummings, D. K., Rueden, C. R. V., O’Connor, K. A., Smith, E. A., Gurven, M., & Kaplan, H. S. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.0455 · Cited by 80 · see citing works
Measuring testosterone in women and men
Kanakis, G., Tsametis, C. P., & Goulis, D. G. (2019) · Maturitas · doi:10.1016/j.maturitas.2019.04.203 · Cited by 78 · see citing works
Wells, J. C. K. (2016) · Cambridge University Press eBooks · doi:10.1017/cbo9780511972959 · Cited by 81 · see citing works
The brain–body energy conservation model of aging
Shaulson, E. D., Cohen, A. A., & Picard, M. A. (2024) · Nature Aging · doi:10.1038/s43587-024-00716-x · Cited by 76 · see citing works
Land-cover classification in a moist tropical region of Brazil with Landsat Thematic Mapper imagery
Li, G., Lu, D., Moran, E. F., & Hetrick, S. S. (2011) · International Journal of Remote Sensing · doi:10.1080/01431161.2010.532831 · Cited by 74 · see citing works
Lassitude: The emotion of being sick
Schrock, J. M., Snodgrass, J. J., & Sugiyama, L. S. (2019) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2019.09.002 · Cited by 67 · see citing works
Gurven, M., Trumble, B. C., Stieglitz, J., Yetish, G. M., Cummings, D. K., Blackwell, A. D., Beheim, B., Kaplan, H. S., & Pontzer, H. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23040 · Cited by 69 · see citing works
Gurven, M., Trumble, B. C., Stieglitz, J., Blackwell, A. D., Michalik, D. E., Finch, C. E., & Kaplan, H. S. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eow028 · Cited by 67 · see citing works
Gassen, J., Prokosch, M. L., Eimerbrink, M. J., Leyva, R. P. P., White, J. D., Peterman, J. L., Burgess, A., Cheek, D. J., Kreutzer, A., Nicolas, S. C. A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-41437-1 · Cited by 65 · see citing works
Trumble, B. C., Blackwell, A. D., Stieglitz, J., Thompson, M. E., Suarez, I. M., Kaplan, H. S., & Gurven, M. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23054 · Cited by 66 · see citing works
“While it is clear that any energetic stress, whether due to immune activation from infection (Muehlenbein et al., 2010) or caloric restriction (Trumble et al., 2010), results in decreased testosterone production, it is less clear that endogenous testosterone actively down-regulates human immune…”
BackgroundResultInfluentialArchie, E. A. (2013) · Parasite Immunology · doi:10.1111/pim.12048 · Cited by 63 · see citing works
Depression as sickness behavior? A test of the host defense hypothesis in a high pathogen population
Stieglitz, J., Trumble, B. C., Thompson, M. E., Blackwell, A. D., Kaplan, H., & Gurven, M. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.05.008 · Cited by 62 · see citing works
“Even in the absence of fever and chronic disease RMR increases by 8–14% during respiratory infection (Muehlenbein et al., 2010).”
BackgroundRubika, A., Luoto, S., Krama, T., Trakimas, G., Rantala, M. J., Moore, F. R., Skrinda, I., Elferts, D., Krams, R., Contreras-Garduño, J. A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-68217-6 · Cited by 63 · see citing works
García, A. R., Finch, C. E., Gatz, M., Kraft, T. S., Rodriguez, D. E., Charifson, M., Rodríguez, D. E., Buetow, K. H., Beheim, B., Allayee, H., et al. (2021) · eLife · doi:10.7554/elife.68231 · Cited by 61 · see citing works
Simmons, Z. L., & Roney, J. R. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.06.006 · Cited by 56 · see citing works
“…vs. partnered, Gray et al., 2002, 2004; when in the presence of potential mates, Roney et al., 2007, 2010), but declines under conditions of food shortage (Bribiescas, 2001; Trumble et al., 2010) and immune challenge (Muehlenbein et al., 2005; Muehlenbein et al., 2010; Simmons and Roney, 2009).”
DHEA Modulates Immune Function: A Review of Evidence
Prall, S. P., & Muehlenbein, M. P. (2018) · Vitamins and hormones · doi:10.1016/bs.vh.2018.01.023 · Cited by 60 · see citing works
Self-citationUnravelling the role of epigenetics in reproductive adaptations to early-life environment
Bar-Sadeh, B., Rudnizky, S., Pnueli, L., Bentley, G. R., Stöger, R. J., Kaplan, A., & Melamed, P. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0370-8 · Cited by 57 · see citing works
Interleukin-1 beta: a potential link between stress and the development of visceral obesity
Speaker, K. J., & Fleshner, M. (2012) · BMC Physiology · doi:10.1186/1472-6793-12-8 · Cited by 55 · see citing works
“In the case of a non-pathogenic stressor such as tail shock, a tightly regulated innate immune response would benefit the organism not only by conserving energy - an activated immune system can be metabolically demanding [137] but by preserving the life and function of innate immune cells such as neutrophils and monoc…”
BackgroundZerjal, T., Härtle, S., Gourichon, D., Guillory, V., Bruneau, N., Laloë, D., Laan, M.-H. P.-V. D., Trapp, S., Bed’Hom, B., & Quéré, P. (2021) · Genetics Selection Evolution · doi:10.1186/s12711-021-00636-z · Cited by 54 · see citing works
“In humans, even relatively mild immune activity is accompanied by an 8 to 14% increase in metabolic rate [58] and requires the reallocation of energy from storage, growth, and development towards the immune system [59].”
BackgroundEvolving the neuroendocrine physiology of human and primate cooperation and collective action
Trumble, B. C., Jaeggi, A. V., & Gurven, M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0014 · Cited by 50 · see citing works
Wildfire smoke impacts activity and energetics of wild Bornean orangutans
Erb, W. M., Barrow, E. J., Hofner, A. N., Utami-Atmoko, S. S., & Vogel, E. R. (2018) · Scientific Reports · doi:10.1038/s41598-018-25847-1 · Cited by 49 · see citing works
Lu, D., Li, G., Moran, E. F., Batistella, M., & Freitas, C. C. (2011) · ISPRS Journal of Photogrammetry and Remote Sensing · doi:10.1016/j.isprsjprs.2011.08.004 · Cited by 48 · see citing works
Rödel, H. G., & Dekker, J. (2012) · European Journal of Wildlife Research · doi:10.1007/s10344-012-0635-1 · Cited by 46 · see citing works
“2002), may restrict the allocation of energy to other physiological functions such as to the animals’ immune defence (Muehlenbein et al. 2010), thus favouring the outbreak of diseases.”
BackgroundBhutta, M. F. (2015) · Human Biology · doi:10.13110/humanbiology.87.2.0092 · Cited by 45 · see citing works
Coccidian Infection Causes Oxidative Damage in Greenfinches
Sepp, T., Karu, U., Blount, J. D., Sild, E., Männiste, M., & Hõrak, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036495 · Cited by 45 · see citing works
Mohamed, R. S., Pettifor, J. M., & Norris, S. A. (2017) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23340 · Cited by 44 · see citing works
Testosterone and Immune Function in Primates: A Brief Summary with Methodological Considerations
Prall, S. P., & Muehlenbein, M. P. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9752-x · Cited by 41 · see citing works
Self-citationWensveen, F. M., Šestan, M., Wensveen, T. T., & Polić, B. (2019) · European Journal of Immunology · doi:10.1002/eji.201847895 · Cited by 41 · see citing works
Immunological Mechanisms of Sickness Behavior in Viral Infection
Krapić, M., Kavazović, I., & Wensveen, F. M. (2021) · Viruses · doi:10.3390/v13112245 · Cited by 41 · see citing works
“Following infection, therefore, up to 30% of all nutrients in the body can be directed towards the activated immune system [54,55].”
BackgroundSystems Immunology Approaches to Metabolism
Mogilenko, D. A., Sergushichev, A., & Artyomov, M. N. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101220-031513 · Cited by 39 · see citing works
Fractional forest cover mapping in the Brazilian Amazon with a combination of MODIS and TM images
Lu, D., Batistella, M., Moran, E. F., Hetrick, S. S., Alves, D. S., & Brondízio, E. S. (2011) · International Journal of Remote Sensing · doi:10.1080/01431161.2010.519004 · Cited by 39 · see citing works
Mechanisms for survival: vagal control of goal-directed behavior
Teckentrup, V., & Kroemer, N. B. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.11.001 · Cited by 40 · see citing works
Patterns and processes of human life history evolution
Muehlenbein, M. P., & Flinn, M. V. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199568765.003.0012 · Cited by 36 · see citing works
“Resting metabolic rates are elevated by more than 8% in young adult men during acute respiratory tract infections, even in the absence of fever ( Muehlenbein et al. 2010 ).”
BackgroundSelf-citationKsiążek, A., & Konarzewski, M. (2012) · Physiological and Biochemical Zoology · doi:10.1086/663696 · Cited by 34 · see citing works
“…with an immune challenge (Demas et al. 1997; Demas and Sakaria 2005; Li et al. 2007; Ilmonen et al. 2008; Cai et al. 2009; Cutrera et al. 2010; Muehlenbein et al. 2010), several others found those costs difficult to quantify (Lochmiller and Deerenberg 2000; Råberg et al. 2002; Derting and…”
BackgroundHughes, F. M., Odom, M. R., Cervantes, A., Livingston, A. J., & Purves, J. T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032821 · Cited by 33 · see citing works
“Implementation of a full-scale systemic immune response utilizes approximately 25–30% of the basal metabolic rate [61,62] and is therefore a significant stressor to the organism when activated.”
BackgroundTestosterone, Immune Function, and Life History Transitions in Filipino Males (Homo sapiens)
Gettler, L. T., McDade, T. W., Agustin, S. S., Feranil, A. B., & Kuzawa, C. W. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9749-5 · Cited by 32 · see citing works
“Men with greater cold/flu symptomology also had lower testosterone, which is potentially consistent with previous research suggesting that active infection suppresses testosterone (Muehlenbein 2006; Muehlenbein et al. 2005, 2010; Simmons and Roney 2009).”
ResultCentennial perspective on human adaptability
Leonard, W. R. (2018) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23401 · Cited by 32 · see citing works
EMAS position statement: Testosterone replacement therapy in older men
Kanakis, G., Pofi, R., Goulis, D. G., Isidori, A. M., Armeni, E., Erel, C. T., Fistonić, I., Hillard, T., Hirschberg, A. L., Męczekalski, B., et al. (2023) · Maturitas · doi:10.1016/j.maturitas.2023.107854 · Cited by 32 · see citing works
“Finally, physical and psychological stressors may significantly impact T concentrations; therefore, T evaluation should be avoided during the acute phase of an illness [28].”
BackgroundMerlo, J. L., Cutrera, A., Luna, F., & Zenuto, R. R. (2014) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2014.05.021 · Cited by 29 · see citing works
Make New Friends and Keep the Old? Parasite Coinfection and Comorbidity in Homo sapiens
Martin, M. A., Blackwell, A. D., Gurven, M., & Kaplan, H. S. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7181-3_12 · Cited by 27 · see citing works
“…coinfection may increase investment in immune function (Bordes and Morand 2009 ), which may divert energy away from other fi tness-enhancing allocations, such as growth and reproduction (Sheldon and Verhulst 1996 ; Adamo 2001 ; Uller et al. 2006 ; Blackwell et al. 2010 ; Muehlenbein et al. 2010 ).”
BackgroundShattuck‐Heidorn, H., Reiches, M. W., Prentice, A. M., Moore, S. E., & Ellison, P. T. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eow034 · Cited by 27 · see citing works
“Pyrogenic and non-febrile immune responses are associated with approximately 10% increases metabolic rate [1, 2], and acute immune responses are associated with reductions in activity, body mass and reproductive success in a wide range of animals [3].”
BackgroundWarburton, E. M., Pearl, C. A., & Vonhof, M. J. (2016) · Parasitology Research · doi:10.1007/s00436-016-4957-x · Cited by 26 · see citing works
Naim, N., Amrit, F. R. G., McClendon, T. B., Yanowitz, J. L., & Ghazi, A. (2020) · BioEssays · doi:10.1002/bies.202000103 · Cited by 27 · see citing works
“increase in BMR in young adult human males infected with a respiratory virus,[10] but as with pregnancy, energy needs and metabolic”
BackgroundBlackwell, A. D. (2022) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-101819-110236 · Cited by 25 · see citing works
Sustained Inflammation Induced by LPS Leads to Tolerable Anorexia and Fat Loss via Tlr4 in Mice
Yang, Y., Zhong, W., Zhang, Y., Cheng, Y., Lai, H., Yu, H., Feng, N., Han, Y., Huang, R., & Zhai, Q. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s358518 · Cited by 27 · see citing works
Sarma, M. S., Boyette, A. H., Lew‐Levy, S., Miegakanda, V., Kilius, E., Samson, D. R., & Gettler, L. T. (2020) · American Journal of Physical Anthropology · doi:10.1002/ajpa.24075 · Cited by 24 · see citing works
Prall, S. P., Ambu, L. N., Nathan, S. K. S. S., Alsisto, S., Saldivar, D. A. R., & Muehlenbein, M. P. (2015) · American Journal of Primatology · doi:10.1002/ajp.22387 · Cited by 23 · see citing works
Self-citationAn Overview of Sex Hormones in Relation to SARS-CoV-2 Infection
Naz, M. S. G., Banaei, M., Dashti, S., & Tehrani, F. R. (2021) · Future Virology · doi:10.2217/fvl-2021-0058 · Cited by 23 · see citing works
Urlacher, S. S. (2023) · American Journal of Biological Anthropology · doi:10.1002/ajpa.24719 · Cited by 23 · see citing works
Metabolism, bioenergetics and thermal physiology: influences of the human intestinal microbiota
Armstrong, L. E., Casa, D. J., & Belval, L. N. (2019) · Nutrition Research Reviews · doi:10.1017/s0954422419000076 · Cited by 21 · see citing works
“Fever, for example, results in a 10–15 % increase of RMR for every 1°C rise of internal body temperature(117), and a respiratory tract infection with no fever can potentiate RMR 8–14 %(118).”
BackgroundA positive relationship between body height and the testosterone response to physical exercise
Kowal, M., Sorokowski, P., Żelaźniewicz, A., Nowak, J., Orzechowski, S., Żurek, A., & Żurek, G. (2020) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2020.08.012 · Cited by 20 · see citing works
Applications of Dried Blood Spots in General Human Health Studies
Brindle, E., O’Connor, K. A., & Garrett, D. (2014) · Wiley eBooks · doi:10.1002/9781118890837.ch9 · Cited by 20 · see citing works
Adiposity, CVD risk factors and testosterone
Gettler, L. T., Sarma, M. S., Gengo, R. G., Oka, R., & McKenna, J. J. (2017) · Evolution Medicine and Public Health · doi:10.1093/emph/eox005 · Cited by 19 · see citing works
“While T’s interfaces with the immune system have been extensively reviewed elsewhere, various lines of evidence suggest that elevated T tends to suppress or dampen certain immune functions, such as aspects of the inflammatory response, B-cell development and differentiation, and costly forms of T cell-mediated immune…”
BackgroundTrade-offs between immunity and testosterone in male African ground squirrels
O'Brien, K. A., Waterman, J. M., Anderson, W. G., & Bennett, N. C. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.177683 · Cited by 18 · see citing works
“Adult male humans have significantly lower testosterone levels during illness (Muehlenbein et al., 2010).”
BackgroundValeggia, C. R., & la Mora, A. N. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802652-6.00021-9 · Cited by 18 · see citing works
Snodgrass, J. J. (2012) · Human Biology · doi:10.1002/9781118108062.ch8 · Cited by 18 · see citing works
Haavik, H., Niazi, I. K., Kumari, N., Amjad, I., Duehr, J., & Holt, K. R. (2021) · Medicina · doi:10.3390/medicina57060536 · Cited by 17 · see citing works
Müller, W., Heylen, D., Eens, M., Rivera‐Gutiérrez, H. F., & Groothuis, T. G. G. (2013) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-013-1586-6 · Cited by 16 · see citing works
“Our study adds, therefore, to the growing number of studies showing negative effects of immune activation and parasites on circulating testosterone levels in birds and mammals (Weatherhead et al. 1993; Ros et al. 2009; Greiner et al. 2010; Muehlenbein et al. 2010; Casagrande and Groothuis 2011; reviewed in Boonekamp e…”
InfluentialAging US males with multiple sources of emotional social support have low testosterone.
Gettler, L., & Oka, R. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.003 · Cited by 19 · see citing works
Gassen, J., Nowak, T. J., Henderson, A. D., & Muehlenbein, M. P. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.10.001 · Cited by 14 · see citing works
Self-citationLower testosterone levels are associated with higher risk of death in men
Muehlenbein, M. P., Gassen, J., Shattuck, E. C., & Sparks, C. S. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac044 · Cited by 15 · see citing works
“Further, in the context of infectious illness, increasing the energy allocated toward immune function and somatic repair is likely to yield greater fitness benefits than enhanced investment in reproduction [8, 9].”
BackgroundSelf-citationBuffered or impaired: Maternal anemia, inflammation and breast milk macronutrients in northern Kenya
Fujita, M., Ruvalcaba, N. P., Wander, K., Corbitt, M., & Brindle, E. (2018) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23752 · Cited by 15 · see citing works
Hagen, E. H., Blackwell, A. D., Lightner, A. D., & Sullivan, R. J. (2023) · American Journal of Biological Anthropology · doi:10.1002/ajpa.24718 · Cited by 14 · see citing works
“…investments, such as growth and reproduction (Blackwell et al., 2010; Demas et al., 1997; Garcia et al., 2020; Martin et al., 2011; McDade et al., 2016; Muehlenbein et al., 2010; Nystrand & Dowling, 2020; Schulenburg et al., 2009; Shattuck-Heidorn et al., 2017; Urlacher et al., 2018).”
BackgroundHuman Energy Expenditure in Anthropology and Beyond
Ocobock, C. J. (2020) · American Anthropologist · doi:10.1111/aman.13392 · Cited by 12 · see citing works
Alvarado, L. C., Valeggia, C. R., Ellison, P. T., Lewarch, C. L., & Muller, M. N. (2019) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-019-00116-1 · Cited by 11 · see citing works
“For instance, pathogen burden can affect both metabolic rate and testosterone levels (Muehlenbein and Bribiescas 2005; Muehlenbein et al. 2010; Trumble et al. 2016).”
BackgroundInfant growth and the thymus: Data from two South American native societies
Veile, A. J., Winking, J., Gurven, M., Greaves, R. D., & Kramer, K. L. (2012) · American Journal of Human Biology · doi:10.1002/ajhb.22314 · Cited by 11 · see citing works
“Immune function is an important component of survival effort and entails physiological trade-offs with growth and reproduction (Lochmiller and Deerenberg, 2000; Muehlenbein et al., 2010; Norris and Evans, 2000; Sheldon and Verhulst, 1996).”
BackgroundImmunity, Hormones, and Life History Trade-Offs
Muehlenbein, M. P., Prall, S. P., & Peck, H. N. (2017) · Springer eBooks · doi:10.1007/978-1-4939-4038-7_7 · Cited by 10 · see citing works
“For example, in a sample of 25 nonfebrile young men naturally infected with respiratory tract pathogens, resting metabolic rate was elevated by 14 % compared to samples taken after convalescence (Muehlenbein et al. 2010).”
ResultSelf-citationCepon‐Robins, T. J. (2020) · American Journal of Human Biology · doi:10.1002/ajhb.23544 · Cited by 10 · see citing works
Wander, K., Shell‐Duncan, B., Brindle, E., & O’Connor, K. A. (2013) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22250 · Cited by 10 · see citing works
“…investigated variability in immune function, as well as predictors and outcomes associated with this variability (Shell-Duncan, 1993, 1995, 1997; Shell-Duncan and Wood, 1997; McDade, 2001, 2002; McDade et al., 2000a, 2001a, 2008; Gurven et al., 2008; Muehlenbein et al., 2010; Wander et al., 2012a).”
BackgroundWang, A. Z., & Husak, J. F. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.232132 · Cited by 10 · see citing works
Książek, A., & Konarzewski, M. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.129312 · Cited by 9 · see citing works
“…complex molecule synthesis during antigen presentation in cell-mediated and humoral responses (Demas et al., 1997; Ots et al., 2001; Ksia ̨żek et al., 2003; Martin et al., 2003; Li et al., 2007; Ilmonen et al., 2008; Cai et al., 2009; Cutrera et al., 2010; Muehlenbein et al., 2010).”
BackgroundBar-Sadeh, B., Amichai, O. E., Pnueli, L., Begum, K., Leeman, G., Emes, R. D., Stöger, R. J., Bentley, G. R., & Melamed, P. (2022) · BMC Biology · doi:10.1186/s12915-021-01219-6 · Cited by 9 · see citing works
“The energetic costs of immune challenges arising from childhood in Bangladesh or prepubertal colitis in mice likely force trade-offs with other physiological systems [84, 85].”
BackgroundCumulative host energetic costs of soil-transmitted helminth infection
Gildner, T. E., Cepon‐Robins, T. J., & Urlacher, S. S. (2022) · Trends in Parasitology · doi:10.1016/j.pt.2022.04.007 · Cited by 10 · see citing works
Tradeoffs in milk immunity affect infant infectious disease risk
Wander, K., Fujita, M., Mattison, S. M., Duris, M., Gauck, M., Hopt, T., Lacy, K., Foligno, A., Ulloa, R., Dodge, C., et al. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac020 · Cited by 9 · see citing works
“In addition, both immune activity and immuno-tolerance are energetically expensive [26], and evolved mechanisms that optimize energy allocation may not minimize disease risk [27–29].”
Sild, E. (2011) · DSpace repository (University of Tartu) · Cited by 9 · see citing works
Energy constraint on human health
Behnke, A., Shaulson, E. D., Pontzer, H., Kempes, C. P., & Picard, M. A. (2026) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2026.02.010 · Cited by 12 · see citing works
Sarma, M. S., Ocobock, C. J., Martin, S., Rochelle, S. G., Croom, B. P., & Gettler, L. T. (2021) · American Journal of Human Biology · doi:10.1002/ajhb.23634 · Cited by 8 · see citing works
“…fat and potentially muscle during an expedition could lead to poor individual performance but may also lead to other downstream negative health consequences related to depleted energy resources, such as fatigue or dysregulated immune function (Marconi et al., 2005; Muehlenbein et al., 2010).”
Background
- Authors
- Muehlenbein, M. P., Hirschtick, J. L., Bonner, J. Z., & Swartz, A. M.
- Affiliations
- Indiana University Bloomington (US)
- University of Wisconsin–Milwaukee (US)
- Corresponding author
- Muehlenbein, Michael P.
- Venue
- American Journal of Human Biology
- Publisher
- Wiley
- Published
- 2010-03-22
- Volume
- 22
- Issue
- 4
- Pages
- 546-556
- ISSN
- 1042-0533 (ISSN-L)
- 1520-6300
- OpenAlex
- W2118187515
- Cited by
- 178
- References
- 187
- Citations by year
- 2026: 9 · 2025: 4 · 2024: 7 · 2023: 12 · 2022: 9 · 2021: 32 · 2020: 15 · 2019: 10 · 2018: 11 · 2017: 7 · 2016: 13 · 2015: 11 · 2014: 7 · 2013: 4 · 2012: 12
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Human Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Wisconsin-Milwaukee
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Keywords
- resting metabolic rate, energy expenditure, respiratory infections, testosterone, cortisol, salivary hormones, immunomodulation, life history evolution, convalescence
- MeSH terms
- Adolescent, Adult, Energy Metabolism, Humans, Hydrocortisone, Immunity, Male, Respiratory Tract Infections, Rest, Saliva, Testosterone, Adiposity, Young Adult
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