Influence of puberty stage in immune-inflammatory parameters in well-trained adolescent soccer-players, following 8-weeks of pre-seasonal preparation training

Abstract

Aim: The immune system can experience temporary suppression following acute or prolonged strenuous exercise, potentially increasing susceptibility to infections. Young athletes, who must balance school, training, studies, and social life, may further disrupt their immune-inflammatory responses. This study aimed to investigate the effects of an 8-week pre-season training on circulating leukocyte responses in well-trained adolescent soccer-players at different stages of puberty.

Methods: Thirty-six soccer players, divided into two groups based on their biological age-under sixteen (U16) and above sixteen (A16)-underwent two rounds of assessments. These included evaluations of anthropometrics, physical fitness, and immune parameters before and after an 8-week pre-season soccer training program.

Results: No significant treatment or interaction effects were found for erythrocyte sedimentation rate (ESR), platelets, total leucocyte count, immune inflammation markers (IIM), weekly rating of perceived exertion, body composition, sit-and-reach flexibility, or VO_2max (P > 0.05). However, post-intervention neutrophil counts were increased, while lymphocyte counts decreased, and IIM levels rose in both groups ( P < 0.05). Neuromuscular explosiveness and strength endurance were significantly higher in the A16 group compared to the U16 group ( P < 0.05). Body fat was reduced, and all physical fitness parameters improved in both groups over time ( P < 0.05).

Conclusions: The 8-week soccer-specific training program did not lead to different effects on immune-inflammatory parameters between youth soccer players at different stages of puberty. However, training adaptations, including improvements in physical fitness, were observed in both groups. This suggests that when the same training load (frequency, duration, intensity) is applied to adolescents at different stages of puberty, immune-inflammatory responses are not significantly influenced by age, but physical fitness improves regardless of puberty stage. A key limitation of this study is the lack analysis of lymphocyte subpopulations, which could provide a deeper understanding of the cellular effects of training on immune function.

Keywords

Soccer / pre-seasonal training / immune responses / puberty stages / training adaptations

References

[1] Campbell JP, Turner JE. Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan. Front Immunol. 2018; 9: 648.

[2] Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011; 11: 607-15.

[3] Kurowski M, Seys S, Bonini M, Giacco SD, Delgado L, Diamant Z, et al. Physical exercise, immune response, and susceptibility to infections-current knowledge and growing research areas. Allergy. 2022; 77: 2653-64.

[4] Agustiningsih D, Wibawa T. Demystifying roles of exercise in immune response regulation against acute respiratory infections: A narrative review. Sports Med Health Sci. 2024; 6: 139-53.

[5] Pedro FC, de Oliveira MM, Andrade RS, Costa ACTRB, Pereira CR, Rodrigues e Oliveira PF, et al. Resistance Training Improves the Immune Response, Mainly Associated with CD8⁺ T Lymphocytes and B Lymphocytes, in Mice . Braz Arch Biol Technol. 2024; 67: e24220284.

[6] Duggal NA, Niemiro G, Harridge SDR, Simpson RJ, Lord JM. Can physical activity ameliorate immunosenescence and thereby reduce age-related multi-morbidity? Nat Rev Immunol. 2019; 19: 563-72.

[7] Gleeson M, Pyne DB. Respiratory inflammation and infections in high-performance athletes. Immunol Cell Biol. 2016; 94: 124-31.

[8] Kartaram SW, Teunis M, van Norren K, Smits M, M’Rabet L, Verschuren MCM, et al. Markers for Immunological Resilience: Effects of Moderate- and High-Intensity Endurance Exercise on the Kinetic Response of Leukocyte Subsets. Immuno. 2024; 4: 43-56.

[9] Gopalakrishnan J, Dharanirajan K, Petra ZB, Silambanan S, Alwar T, Sivaraman A. Biomarkers of a Football Match-play-Internal load analysis using Technical Soccer Specific Aerobic Field Test (TSAFT⁹⁰) . Int J Med Biochem. 2024; 7: 26-32.

[10] Armstrong N, McManus AM. Physiology of elite young male athletes. Med Sport Sci. 2011; 56: 1-22.

[11] Palmowski J, Boßlau TK, Ryl L, Krüger K, Reichel T. Managing immune health in sports - a practical guide for athletes and coaches. Dtsch Z Sportmed. 2019; 70: 219-26.

[12] Timmons BW, Tarnopolsky MA, Snider DP, Bar-Or O. Immunological changes in response to exercise: influence of age, puberty, and gender. Med Sci Sports Exerc. 2006; 38: 293-304.

[13] de Almeida-Neto PF, Gonçalves CAM, Wilde P, Jaggers JR, Júnior GBC, de Farias Sales VS, et al. Influence of age and fitness level on immune responses of T and NK cells in healthy physically active subjects after strenuous aerobic exercise: a cross-sectional study. Front Immunol. 2023; 14: 1252506.

[14] Almeida-Neto PF, de Medeiros JA, Jaggers JR, Ferreira ABM, de Assis GG, Cabral BGAT, et al. Exercise Immunology Applied to Pediatric Sport and the Importance of Monitoring Stages of Puberty and Biological Maturation. Sports Health. 2023;19417381231212481.

[15] Ucciferri CC, Dunn SE. Effect of puberty on the immune system: Relevance to multiple sclerosis. Front Pediatr. 2022; 10: 1059083.

[16] Hamlin MJ, Wilkes D, Elliot CA, Lizamore CA, Kathiravel Y. Monitoring Training Loads and Perceived Stress in Young Elite University Athletes. Front Physiol. 2019; 10: 34.

[17] Steidten T, Baumbach P, May R, Gabriel B, Herbsleb M, Markov A, et al. Overnight Immune Regulation and Subjective Measures of Sleep: A Three Night Observational Study in Adolescent Track and Field Athletes. Front Sports Act Living. 2021; 3: 689805.

[18] Nieman DC, Wentz LM. The compelling link between physical activity and the body’s defense system. J Sport Health Sci. 2019; 8: 201-17.

[19] Blume K, Körber N, Hoffmann D, Wolfarth B. Training Load, Immune Status, and Clinical Outcomes in Young Athletes: A Controlled, Prospective, Longitudinal Study. Front Physiol. 2018; 9: 120.

[20] Liu D, Wang R, Grant AR, Zhang J, Gordon PM, Wei Y, et al. Immune adaptation to chronic intense exercise training: new microarray evidence. BMC Genomics. 2017; 18: 29.

[21] Zacher J, Wesemann F, Joisten N, Walzik D, Bloch W, Predel G. Cellular Integrative Immune Markers in Elite Athletes. Int J Sports Med. 2023; 44: 298-308.

[22] Horn PL, Pyne DB, Hopkins WG, Barnes CJ. Lower white blood cell counts in elite athletes training for highly aerobic sports. Eur J Appl Physiol. 2010; 110: 925-32.

[23] Matsuo K, Kubota M, Sasaki H, Toyooka J, Nagatomi R. The Association of the Blood Lymphocytes to Neutrophils Ratio with Overtraining in Endurance Athletes. New Stud Athletics. 2009; 4: 23-9.

[24] Walzik D, Joisten N, Zacher J, Zimmer P. Transferring clinically established immune inflammation markers into exercise physiology: focus on neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio and systemic immune-inflammation index. Eur J Appl Physiol. 2021; 121: 1803-14.

[25] Barale C, Melchionda E, Tempesta G, Morotti A, Russo I. Impact of Physical Exercise on Platelets: Focus on Its Effects in Metabolic Chronic Diseases. Antioxidants (Basel). 2023; 12: 1609.

[26] Hadjicharalambous M. The effects of regular supplementary flexibility training on physical fitness performance of young high-level soccer players. J Sports Med Phys Fitness. 2016; 56: 699-708.

[27] Hadjicharalambous M, Zaras N, Apostolidis A, Tsofliou F. Recreational Soccer, Body Composition and Cardiometabolic Health: A Training-Intervention Study in Healthy Adolescents. Inter J Hum Mov Sports Sci. 2022; 10: 524-33.

[28] Hadjicharalambous MP, Kilduff LP, Pitsiladis YP. Brain serotonergic and dopaminergic modulators, perceptual responses and endurance exercise performance following caffeine co-ingested with a high fat meal in trained humans. J Int Soc Sports Nutr. 2010; 7: 22.

[29] Hadjicharalambous M, Georgiades E, Kilduff LP, Turner AP, Tsofliou F, Pitsiladis YP. Influence of caffeine on perception of effort, metabolism and exercise performance following a high-fat meal. J Sports Sci. 2006; 24: 875-87.

[30] Jackson AS, Pollock ML. Generalized equations for predicting body density of men. Br J Nutr. 1978; 40: 497-504.

[31] Siri WE. Body composition from fluids spaces and density: analysis of methods. In: Brozek J, Henschel A, editors. Techniques for Measuring Body Composition. Washington DC: National Academy of Sciences, National Research Council; 1961. pp. 223-44.

[32] Carskadon MA, Acebo C. A self-administered rating scale for pubertal development. J Adolesc Health. 1993; 14: 190-5.

[33] Cooper S, Baker JS, Tong RJ, Roberts E, Hanford M. The repeatability and criterion related validity of the 20 m multistage fitness test as a predictor of maximal oxygen uptake in active young men. Br J Sports Med. 2005; 39: e19.

[34] Augustsson SR, Bersås E, Magnusson TE, Sahlberg M, Augustsson J, et al. Gender differences and reliability of selected physical performance tests in young women and men. Adv Physiother. 2009; 11: 64-70.

[35] Nevill AM, Atkinson G. Assessing agreement between measurements recorded on a ratio scale in sports medicine and sports science. Br J Sports Med. 1997; 31: 314-8.

[36] Qi Q, Zhuang L, Shen Y, Geng Y, Yu S, Chen H, et al. A novel systemic inflammation response index (SIRI) for predicting the survival of patients with pancreatic cancer after chemotherapy. Cancer. 2016; 122: 2158-67.

[37] Jovanovic M. Physical Preparation for Soccer. SOCCERSPECIFIC; 2001.

[38] Foster C, Hector LL, Welsh R, Schrager M, Green MA, Snyder AC. Effects of specific versus cross-training on running performance. Eur J Appl Physiol Occup Physiol. 1995; 70: 367-72.

[39] Impellizzeri FM, Rampinini E, Coutts AJ, Sassi A, Marcora SM. Use of RPE-based training load in soccer. Med Sci Sports Exerc. 2004; 36: 1042-7.

[40] Kirk RE. Practical significance: A concept whose time has come. Educ Psychol Meas. 1996; 56: 746-59.

[41] Zarbock A, Polanowska-Grabowska RK, Ley K. Platelet-neutrophil-interactions: linking hemostasis and inflammation. Blood Rev. 2007; 21: 99-111.

[42] Gleeson M, Ginn E, Francis JL. Salivary immunoglobulin monitoring in an elite kayaker. Clin J Sport Med. 2000; 10: 206-8.

[43] Hellard P, Avalos M, Guimaraes F, Toussaint J, Pyne DB. Training-related risk of common illnesses in elite swimmers over a 4-yr period. Med Sci Sports Exerc. 2015; 47: 698-707.

[44] El-Sayed MS, Ali N, Ali ZE. Haemorheology in exercise and training. Sports Med. 2005; 35: 649-70.

[45] Fallon KE, Fallon SK, Boston T. The acute phase response and exercise: court and field sports. Br J Sports Med. 2001; 35: 170-3.

[46] Harpham C, Harpham QK, Barker AR. The effect of exercise training programs with aerobic components on C-reactive protein, erythrocyte sedimentation rate and self-assessed disease activity in people with ankylosing spondylitis: A systematic review and meta-analysis. Int J Rheum Dis. 2022; 25: 635-49.

[47] Park S, Park I, Lim S, Lee E. Changes in Psychological Anxiety and Physiological Stress Hormones in Korea National Shooters. Brain Sci. 2020; 10: 926.

[48] Tanner A, Day S. The Effects of a 4-Week, Intensified Training, and Competition Period on Salivary Hormones, Immunoglobulin A, Illness Symptoms, and Mood State in Elite Synchronised Swimmers. Sports (Basel). 2017; 5: 64.

[49] Sheykhlouvand M, Khalili E, Gharaat M, Arazi H, Khalafi M, Tarverdizadeh B. Practical Model of Low-Volume Paddling-Based Sprint Interval Training Improves Aerobic and Anaerobic Performances in Professional Female Canoe Polo Athletes. J Strength Cond Res. 2018; 32: 2375-82.

[50] Ambroży T, Rydzik Ł, Obmiński Z, Błach W, Serafin N, Błach B, et al. The Effect of High-Intensity Interval Training Periods on Morning Serum Testosterone and Cortisol Levels and Physical Fitness in Men Aged 35-40 Years. J Clin Med. 2021; 10: 2143.

[51] Boullosa D, Dragutinovic B, Feuerbacher JF, Benítez-Flores S, Coyle EF, Schumann M. Effects of short sprint interval training on aerobic and anaerobic indices: A systematic review and meta-analysis. Scand J Med Sci Sports. 2022; 32: 810-20.

[52] Armstrong N, Barker AR, McManus AM. Muscle metabolism changes with age and maturation: How do they relate to youth sport performance? Br J Sports Med. 2015; 49: 860-4.

[53] Haddad M, Stylianides G, Djaoui L, Dellal A, Chamari K. Session-RPE Method for Training Load Monitoring: Validity, Ecological Usefulness, and Influencing Factors. Front Neurosci. 2017; 11: 612.

[54] Rodríguez-Marroyo JA, Villa G, García-López J, Foster C. Comparison of heart rate and session rating of perceived exertion methods of defining exercise load in cyclists. J Strength Cond Res. 2012; 26: 2249-57.

[55] Egan AD, Winchester JB, Foster C, McGuigan MR. Using Session RPE to Monitor Different Methods of Resistance Exercise. J Sports Sci Med. 2006; 5: 289-95.

[56] Herman L, Foster C, Maher MA, Mikat R, Porcari J. Validity and reliability of the session RPE method for monitoring exercise training intensity. S Afr J Sports Med. 2006; 18: 14-7.