Physical Therapy in Sport xxx (2014) 1e6
Contents lists available at ScienceDirect
Physical Therapy in Sport journal homepage: www.elsevier.com/ptsp
Literature review
Immunological effects of massage after exercise: A systematic review ndez a, Miguel Membrilla-Mesa a, Noelia Galiano-Castillo b, Victor Tejero-Ferna Manuel Arroyo-Morales b, * a
Rehabilitation Service, Traumatology Section, Hospital Virgen de las Nieves, Granada, Spain n Biosanitaria de Granada (ibs.GRANADA). University of Granada, Instituto Mixto Universitario “Deporte y Salud” (iMUDS). Instituto de Investigacio Granada, Spain b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 April 2014 Received in revised form 29 May 2014 Accepted 11 July 2014
Objective: The objective of this review was to determine whether immune parameters can be modulated by massage after intense physical activity. Methods: A search was conducted in Pub Med Medline, PEDro, and Cochrane databases, using the key words: “massage”, “myofascial release”, “acupressure”, “recovery”, and “warm up” combined with “exercise”, “exercise-induced muscle damage”, “sport”, “immunology”, and lymphocytes” independently. Only controlled studies published between 1970 and 2012 were selected, with no restrictions regarding publication language. The CONSORT Declaration was applied to assess the quality of the selected studies. Results: The initial search identified 739 publications in the databases, of which only 5 met the review inclusion criteria. A positive relationship between immunological recovery and post-exercise massage was reported by some of these studies but not by others. Conclusion: There is preliminary evidence that massage may modulate immune parameters when applied after exercise, but more research is needed to confirm this possibility. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Massage Immunology Exercise Immunoglobulin A
1. Introduction The practice of massage has long been linked to physical activity, especially in the setting of high-level competitions. It has been defined as the mechanical manipulation of body tissues by means of rhythmically applied strokes and pressure to promote health and wellbeing (Cafarelli & Flint, 1992; Galloway & Watt, 2004). Massage is frequently applied to sportspeople during sport events (Galloway & Watt, 2004), because trainers and athletes believe that it can yield multiple benefits (Weerapong, Hume, & Kolt, 2005) by different biomechanical, physiological, neurological, and psychological mechanisms (De Domenico &Wood, 1997; Hemmings, 2001; Mancinelli, Davis, Abulhosn, & Brady, 2006). However, the role of the immune system in generating the beneficial effects of massage has not been fully elucidated. High-intensity or long-duration exercise can produce immunosuppression, thereby increasing the risk of certain infections (Neville, Gleeson, Folland, 2008), especially in the oral mucosa (Bosch, Ring, Geus, Veerman, & Amerongen, 2002) and upper respiratory tract (Neville, Molley, brooks, Speedy, & Atkinson, 2006). * Corresponding author. Departamento de Fisioterapia, Universidad de Granada, Avda. Madrid s/n, 18014, Granada, Spain. E-mail address: [email protected] (M. Arroyo-Morales).
Both innate and acquired components of the immune system are depressed after prolonged physical activity (Gleeson & Walsh, 2012). Elite sportspeople have evidenced a decrease in the concentration and rate of IgA secretion after a single session of highvolume (Nieman et al., 2002) or maximum-intensity (Fahlman, Engels, Morgan & Kololouri, 2001) physical activity or after prolonged periods of repeated intensive training sessions (Libicz, Mercier, Biguo, Le Gallais, & Castex, 2006). In addition, stressful sports practice can produce an injured area in exercised muscle groups, allowing a large amount of neutrophils to pass through the vascular wall to the focus of the lesion for hours after the physical activity, perpetuating the inflammatory process (Lundberg, Lebel, & Gerdin, 1984; Trowbridge & Emling, 1989). This phenomenon reduces peripheral levels of neutrophils (Smith, McCammon, Smith, Chamness, Israel & O’Brien, 1989). Although all of these events affect the immune system, only a decreased IgA level has been associated with a higher risk of infection (Gleeson & Walsh, 2012). Recovery massage may be useful for reducing the negative repercussions of high-intensity sports practice on the immune system (Arroyo-Morales et al., 2009; Weerapong et al., 2005). In addition, the application of massage as a warm-up procedure may protect against the detrimental effects of high-intensity exercise on the immune system. Various studies have addressed the immunoprotective properties of massage. For example, it has been
http://dx.doi.org/10.1016/j.ptsp.2014.07.001 1466-853X/© 2014 Elsevier Ltd. All rights reserved.
ndez, V., et al., Immunological effects of massage after exercise: A systematic review, Physical Please cite this article in press as: Tejero-Ferna Therapy in Sport (2014), http://dx.doi.org/10.1016/j.ptsp.2014.07.001
Genome expression profile Metabolite concentration Muscle damage Mitochondrial biogenesis (a) (b) (c) (d) Anaerobic Intervention after cycloergometric exercise until exhaustion RCT Crane et al. (2012)
11 healthy young males
Anaerobic Intervention after Wingate test RCT Arroyo et al. (2009)
60 university students (37 males and 23 females)
RCT
18 male and females (n ¼ 9 in each group)
(a) 40 min of myofascial induction protocol (b) Control
(a) 10 min of effleurage, petrissage, and tapotement on quadriceps (b) Control (no massage on contralateral quadriceps)
(a) Both groups: NS: Y salivary flow rate S: [ cortisol in saliva (b) Group with massage: S: [ Ig A in saliva (in females) NS: [ total proteins in saliva Muscle biopsy after massage: S: [ mitochondrial biogenesis S: Y proinflammatory cytokine production
Group with massage: S: Y pain 48 h after exercise
Catecholamines in blood Lactic acid in blood Lymphocytes and leukocytes in blood EEG activity Profile of mood states (POMS) Range of movement (ROM) Maximal contraction peak Descriptor differential scale (DDS) Neutrophils Salivary flow rate Cortisol in saliva Immunoglobulin A in saliva Total proteins in saliva (a) (b) (c) (b) (a) (b) (c) (d) (e) (a) (b) (c) (d) (a) Water jet system on latex bench (b) Control
(a) 20 min of Swedish techniques (effleurage, petrissage, and tapotement (b) Control
Group with massage: S: Y DOMS and CK S: [ neutrophils Delayed onset muscle soreness (DOMS) CK in blood Neutrophils in blood Cortisol in blood (a) (b) (c) (d) (a) 30 min of effleurage, petrissage, and tapotement (b) Control
S ¼ statistically significant; NS ¼ not statistically significant; RCT: randomized controlled trial.
Fig. 1. Flow chart of the systematic review process.
Hilbert et al. (2003)
1 Terms used: massage, myofascial release, acupressure, recovery, warm up, exercise-induced muscle damage, exercise, sport, immunology, and lymphocytes
RCT
5 articles included
Stock et al. (1996)
20 articles excluded for not meeting the inclusion criteria
RCT
25 full-text arƟcles reviewed
Design
714 arƟcles excluded for not addressing the topic of the systemaƟc review
Smith et al. (1994)
739 articles retrieved froms electronic databases (including Pubmed, Medline, pEDRO, and Cochrane) using relevant terms1
Study
2.1.1. Study selection A first selection of studies was made by two reviewers [V.T.F and M.M.M] based on the abstracts, ruling out studies unrelated to the issue in question. In the next stage, the variables considered in the selected studies were examined, and only randomized controlled trials relating to massage as a post-exercise recovery method were included for further review (Table 1).
Table 1 Effects of massage on the immune system after physical activity.
Pubmed Medline, PEDro, and Cochrane databases were searched using the following key words: massage, myofascial release, acupressure, recovery, warm up, exercise-induced muscle damage, exercise, sport, immunology, and lymphocytes. Only controlled studies carried out between 1970 and 2012 were gathered; there were no restrictions on the language of the publications (Fig. 1).
Sample
2.1. Search strategy
10 healthy male physical education students (crossgroup design)
Main results Parameters measured Intervention
Resistance Intervention at 2 hour after eccentric biceps and triceps contractions of the nondominant arm. Resistance Intervention after three series of a five-exercise sequence for upper and lower body Resistance Intervention at 2 hour after eccentric hamstring contractions
This study used a systematic review design to describe potential immune effects of massage as a recovery method. Different local and general effects of massage after exercise have been postulated but there is scarce information about role of different immune markers during recovery processes after exercise involving massage procedures.
Type of exercise
2. Methods
14 healthy untrained Caucasian males, (n ¼ 7 in each group)
reported that 10 min of massage increases IgA levels in the elderly (Groer et al., 1994) and that massage enhances parasympathetic activity (Arroyo-Morales, Olea, Martinez, Moreno-Lorenzo, DíazRodríguez, & Hidalgo-Lozano, 2008), increasing salivary secretion and levels of alpha-amylase, the enzyme responsible for neutralizing bacteria in the oral cavity (Scannapieco, Torres, & Levine, 1993). Massage was also found to relocate peripheral blood neutrophil levels through its effect on muscle blood flow (Galloway & Watt, 2004), which reduced extravasation of neutrophils towards the focus of the muscle injury (Garcia-Leme, 1991). Hence, massage can prolong the time during which the blood contains an adequate concentration of neutrophils (Calun, Burnstein, Assia, Tur-Kaspa, Rosenblum, Epstein, 1987). We hypothesized that the ability of massage to induce relaxation can facilitate immune system stimulation in active healthy individuals, reducing the deleterious effects of exercise on the immune system. The purpose of this paper was to describe and review the current literature on massage and its role in modulating immune parameters when applied after intense physical activity.
Group with massage: S: Y power density in beta 1 in central and frontal EEG leads
ndez et al. / Physical Therapy in Sport xxx (2014) 1e6 V. Tejero-Ferna
2
ndez, V., et al., Immunological effects of massage after exercise: A systematic review, Physical Please cite this article in press as: Tejero-Ferna Therapy in Sport (2014), http://dx.doi.org/10.1016/j.ptsp.2014.07.001
ndez et al. / Physical Therapy in Sport xxx (2014) 1e6 V. Tejero-Ferna
2.2. Assessment of methodological quality The methodological quality of the papers included in the review was determined by evaluating whether the study complied with the 22 items of the CONSORT Declaration (Moher, Schulz, & Altman, 2003), assigning 1 [Yes] or 0 [NO] for each item and generating a score ranging from 0 to 22 points; a score 11 points was considered to denote high quality and a score < 11 points low quality, following a previously reported method (Balasubramanian, Wiener, Alshameeri, Tiruvoipati, Elbourne, & Reed, 2006; HuwilerMuntener, Juni, Junker, & Egger, 2002). The methodology was based on the approach taken by two reviews published in 2012 on other topics (Silva, Serrao, Driusso, Mattiello, 2012; van Beijsterveldt, van de Port, Verijken, & Backx, 2013). The scoring was done by two of the authors [V.T.F and M.M.M]; when their scoring of a paper differed, a consensus was reached on the score by all three authors of the present study. The inclusion criteria were as follows: massage is the main intervention; control subjects receive a placebo treatment; immunological variables are measured, and all study participants are healthy individuals. Exclusion criteria were: intense exercise in the previous four months, history of systemic disease,
Contents lists available at ScienceDirect
Physical Therapy in Sport journal homepage: www.elsevier.com/ptsp
Literature review
Immunological effects of massage after exercise: A systematic review ndez a, Miguel Membrilla-Mesa a, Noelia Galiano-Castillo b, Victor Tejero-Ferna Manuel Arroyo-Morales b, * a
Rehabilitation Service, Traumatology Section, Hospital Virgen de las Nieves, Granada, Spain n Biosanitaria de Granada (ibs.GRANADA). University of Granada, Instituto Mixto Universitario “Deporte y Salud” (iMUDS). Instituto de Investigacio Granada, Spain b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 9 April 2014 Received in revised form 29 May 2014 Accepted 11 July 2014
Objective: The objective of this review was to determine whether immune parameters can be modulated by massage after intense physical activity. Methods: A search was conducted in Pub Med Medline, PEDro, and Cochrane databases, using the key words: “massage”, “myofascial release”, “acupressure”, “recovery”, and “warm up” combined with “exercise”, “exercise-induced muscle damage”, “sport”, “immunology”, and lymphocytes” independently. Only controlled studies published between 1970 and 2012 were selected, with no restrictions regarding publication language. The CONSORT Declaration was applied to assess the quality of the selected studies. Results: The initial search identified 739 publications in the databases, of which only 5 met the review inclusion criteria. A positive relationship between immunological recovery and post-exercise massage was reported by some of these studies but not by others. Conclusion: There is preliminary evidence that massage may modulate immune parameters when applied after exercise, but more research is needed to confirm this possibility. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Massage Immunology Exercise Immunoglobulin A
1. Introduction The practice of massage has long been linked to physical activity, especially in the setting of high-level competitions. It has been defined as the mechanical manipulation of body tissues by means of rhythmically applied strokes and pressure to promote health and wellbeing (Cafarelli & Flint, 1992; Galloway & Watt, 2004). Massage is frequently applied to sportspeople during sport events (Galloway & Watt, 2004), because trainers and athletes believe that it can yield multiple benefits (Weerapong, Hume, & Kolt, 2005) by different biomechanical, physiological, neurological, and psychological mechanisms (De Domenico &Wood, 1997; Hemmings, 2001; Mancinelli, Davis, Abulhosn, & Brady, 2006). However, the role of the immune system in generating the beneficial effects of massage has not been fully elucidated. High-intensity or long-duration exercise can produce immunosuppression, thereby increasing the risk of certain infections (Neville, Gleeson, Folland, 2008), especially in the oral mucosa (Bosch, Ring, Geus, Veerman, & Amerongen, 2002) and upper respiratory tract (Neville, Molley, brooks, Speedy, & Atkinson, 2006). * Corresponding author. Departamento de Fisioterapia, Universidad de Granada, Avda. Madrid s/n, 18014, Granada, Spain. E-mail address: [email protected] (M. Arroyo-Morales).
Both innate and acquired components of the immune system are depressed after prolonged physical activity (Gleeson & Walsh, 2012). Elite sportspeople have evidenced a decrease in the concentration and rate of IgA secretion after a single session of highvolume (Nieman et al., 2002) or maximum-intensity (Fahlman, Engels, Morgan & Kololouri, 2001) physical activity or after prolonged periods of repeated intensive training sessions (Libicz, Mercier, Biguo, Le Gallais, & Castex, 2006). In addition, stressful sports practice can produce an injured area in exercised muscle groups, allowing a large amount of neutrophils to pass through the vascular wall to the focus of the lesion for hours after the physical activity, perpetuating the inflammatory process (Lundberg, Lebel, & Gerdin, 1984; Trowbridge & Emling, 1989). This phenomenon reduces peripheral levels of neutrophils (Smith, McCammon, Smith, Chamness, Israel & O’Brien, 1989). Although all of these events affect the immune system, only a decreased IgA level has been associated with a higher risk of infection (Gleeson & Walsh, 2012). Recovery massage may be useful for reducing the negative repercussions of high-intensity sports practice on the immune system (Arroyo-Morales et al., 2009; Weerapong et al., 2005). In addition, the application of massage as a warm-up procedure may protect against the detrimental effects of high-intensity exercise on the immune system. Various studies have addressed the immunoprotective properties of massage. For example, it has been
http://dx.doi.org/10.1016/j.ptsp.2014.07.001 1466-853X/© 2014 Elsevier Ltd. All rights reserved.
ndez, V., et al., Immunological effects of massage after exercise: A systematic review, Physical Please cite this article in press as: Tejero-Ferna Therapy in Sport (2014), http://dx.doi.org/10.1016/j.ptsp.2014.07.001
Genome expression profile Metabolite concentration Muscle damage Mitochondrial biogenesis (a) (b) (c) (d) Anaerobic Intervention after cycloergometric exercise until exhaustion RCT Crane et al. (2012)
11 healthy young males
Anaerobic Intervention after Wingate test RCT Arroyo et al. (2009)
60 university students (37 males and 23 females)
RCT
18 male and females (n ¼ 9 in each group)
(a) 40 min of myofascial induction protocol (b) Control
(a) 10 min of effleurage, petrissage, and tapotement on quadriceps (b) Control (no massage on contralateral quadriceps)
(a) Both groups: NS: Y salivary flow rate S: [ cortisol in saliva (b) Group with massage: S: [ Ig A in saliva (in females) NS: [ total proteins in saliva Muscle biopsy after massage: S: [ mitochondrial biogenesis S: Y proinflammatory cytokine production
Group with massage: S: Y pain 48 h after exercise
Catecholamines in blood Lactic acid in blood Lymphocytes and leukocytes in blood EEG activity Profile of mood states (POMS) Range of movement (ROM) Maximal contraction peak Descriptor differential scale (DDS) Neutrophils Salivary flow rate Cortisol in saliva Immunoglobulin A in saliva Total proteins in saliva (a) (b) (c) (b) (a) (b) (c) (d) (e) (a) (b) (c) (d) (a) Water jet system on latex bench (b) Control
(a) 20 min of Swedish techniques (effleurage, petrissage, and tapotement (b) Control
Group with massage: S: Y DOMS and CK S: [ neutrophils Delayed onset muscle soreness (DOMS) CK in blood Neutrophils in blood Cortisol in blood (a) (b) (c) (d) (a) 30 min of effleurage, petrissage, and tapotement (b) Control
S ¼ statistically significant; NS ¼ not statistically significant; RCT: randomized controlled trial.
Fig. 1. Flow chart of the systematic review process.
Hilbert et al. (2003)
1 Terms used: massage, myofascial release, acupressure, recovery, warm up, exercise-induced muscle damage, exercise, sport, immunology, and lymphocytes
RCT
5 articles included
Stock et al. (1996)
20 articles excluded for not meeting the inclusion criteria
RCT
25 full-text arƟcles reviewed
Design
714 arƟcles excluded for not addressing the topic of the systemaƟc review
Smith et al. (1994)
739 articles retrieved froms electronic databases (including Pubmed, Medline, pEDRO, and Cochrane) using relevant terms1
Study
2.1.1. Study selection A first selection of studies was made by two reviewers [V.T.F and M.M.M] based on the abstracts, ruling out studies unrelated to the issue in question. In the next stage, the variables considered in the selected studies were examined, and only randomized controlled trials relating to massage as a post-exercise recovery method were included for further review (Table 1).
Table 1 Effects of massage on the immune system after physical activity.
Pubmed Medline, PEDro, and Cochrane databases were searched using the following key words: massage, myofascial release, acupressure, recovery, warm up, exercise-induced muscle damage, exercise, sport, immunology, and lymphocytes. Only controlled studies carried out between 1970 and 2012 were gathered; there were no restrictions on the language of the publications (Fig. 1).
Sample
2.1. Search strategy
10 healthy male physical education students (crossgroup design)
Main results Parameters measured Intervention
Resistance Intervention at 2 hour after eccentric biceps and triceps contractions of the nondominant arm. Resistance Intervention after three series of a five-exercise sequence for upper and lower body Resistance Intervention at 2 hour after eccentric hamstring contractions
This study used a systematic review design to describe potential immune effects of massage as a recovery method. Different local and general effects of massage after exercise have been postulated but there is scarce information about role of different immune markers during recovery processes after exercise involving massage procedures.
Type of exercise
2. Methods
14 healthy untrained Caucasian males, (n ¼ 7 in each group)
reported that 10 min of massage increases IgA levels in the elderly (Groer et al., 1994) and that massage enhances parasympathetic activity (Arroyo-Morales, Olea, Martinez, Moreno-Lorenzo, DíazRodríguez, & Hidalgo-Lozano, 2008), increasing salivary secretion and levels of alpha-amylase, the enzyme responsible for neutralizing bacteria in the oral cavity (Scannapieco, Torres, & Levine, 1993). Massage was also found to relocate peripheral blood neutrophil levels through its effect on muscle blood flow (Galloway & Watt, 2004), which reduced extravasation of neutrophils towards the focus of the muscle injury (Garcia-Leme, 1991). Hence, massage can prolong the time during which the blood contains an adequate concentration of neutrophils (Calun, Burnstein, Assia, Tur-Kaspa, Rosenblum, Epstein, 1987). We hypothesized that the ability of massage to induce relaxation can facilitate immune system stimulation in active healthy individuals, reducing the deleterious effects of exercise on the immune system. The purpose of this paper was to describe and review the current literature on massage and its role in modulating immune parameters when applied after intense physical activity.
Group with massage: S: Y power density in beta 1 in central and frontal EEG leads
ndez et al. / Physical Therapy in Sport xxx (2014) 1e6 V. Tejero-Ferna
2
ndez, V., et al., Immunological effects of massage after exercise: A systematic review, Physical Please cite this article in press as: Tejero-Ferna Therapy in Sport (2014), http://dx.doi.org/10.1016/j.ptsp.2014.07.001
ndez et al. / Physical Therapy in Sport xxx (2014) 1e6 V. Tejero-Ferna
2.2. Assessment of methodological quality The methodological quality of the papers included in the review was determined by evaluating whether the study complied with the 22 items of the CONSORT Declaration (Moher, Schulz, & Altman, 2003), assigning 1 [Yes] or 0 [NO] for each item and generating a score ranging from 0 to 22 points; a score 11 points was considered to denote high quality and a score < 11 points low quality, following a previously reported method (Balasubramanian, Wiener, Alshameeri, Tiruvoipati, Elbourne, & Reed, 2006; HuwilerMuntener, Juni, Junker, & Egger, 2002). The methodology was based on the approach taken by two reviews published in 2012 on other topics (Silva, Serrao, Driusso, Mattiello, 2012; van Beijsterveldt, van de Port, Verijken, & Backx, 2013). The scoring was done by two of the authors [V.T.F and M.M.M]; when their scoring of a paper differed, a consensus was reached on the score by all three authors of the present study. The inclusion criteria were as follows: massage is the main intervention; control subjects receive a placebo treatment; immunological variables are measured, and all study participants are healthy individuals. Exclusion criteria were: intense exercise in the previous four months, history of systemic disease,
