It has been known since the late nineteenth century that repeated mild blows to the head in animal experiments could be lethal even though there was no evidence of structural brain damage [16]. Initial animal models probing the difference between a single versus multiple concussive and subconcussive insults revealed that following a single subconcussive blow there were no behavioral and histologic changes, yet repetitive subconcussive head trauma resulted in permanent injury [17]. In an early experiment looking at concussion in the rat, it was noted that following subconcussive blows, the animals showed signs of “posttraumatic amnesia” [18]. Additionally, Govons et al. [18] reported that subconcussive blows produced convulsions in some of the rats, altered activity for 24 h, and that the impact caused the animal to be momentarily stunned. Additionally, subconcussive head trauma has shown to decrease the polarizability of the cerebrum although not to the extent of a full concussive blow [19]. Tedeschi [16] reported that repetitive subconcussive blows received over a short duration in a rat model elicited a higher incidence of ill effects. Furthermore, postmortem examination of these rats revealed widespread evidence of neuronal injury, myelin loss, and glial proliferation. Other studies of subconcussive head trauma have reported neuropsychological changes and ionic fluctuations and have been hypothesized to leave the brain more vulnerable to a repeated injury [20]. In a recent animal study investigating the effects of subconcussive head trauma induced by a mild lateral fluid percussion, Shultz et al. [8] found that such an injury caused acute neuroinflammation despite any significant axonal injury, or cognitive, emotional, or sensorimotor alterations. Specifically, they documented a short-term increase in microglia, macrophages, and reactive astrogliosis which returned to normal at a 4-week follow-up.

Acute neuroinflammation has also been documented in other animal and human studies of TBI. Repetitive mTBI, similar to neuroinflammation may have cumulative effects leading to neurodegeneration [8] and linked to behavioral impairments after TBI [21]. Conversely it has been thought that neuroinflammation may have a neuroprotective quality [22] and the brain may be better protected following an initial TBI [23]. Complementary to this notion of neuroprotection, it has also been reported that by gradually increasing the amount of brain injury, animals could tolerate trauma that would otherwise kill normal animals. This so-called trauma resistance was attributed to a stabilization of metabolic processes [24] and this idea of preconditioning has been detailed in cerebral ischemia [25]. Fujita et al. [26] reported that subthreshold head trauma did not cause axonal or vascular changes in the rat, even with repetitive blows. Although postmortem studies have identified that repeated subconcussive head trauma may have an accumulative effect and lead to neurodegenerative diseases [8], Slemmer and Weber [25], using a mechanical stretch to simulate an mTBI in hippocampal cell cultures, found that when the tissue was preconditioned they observed a significant decrease in S-100β indicating a positive effect of glial preconditioning. Moreover, Allen et al. [23] reported a rat model of repetitive mTBI preconditioning served to preserve motor function following a severe TBI and also elicited activation of secondary sites in the brain that may aide in recovery. Whether or not this response to repetitive insult is beneficial or detrimental is yet to be determined and is not only limited to animal research. In a recent human study looking at serum nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) levels in soccer players following a session of headers, Bamac et al. [27] reported increased NGF and BDNF from baseline levels. This increase was attributed to the microtrauma caused by the subconcussive impacts from heading the ball. However, this increase is ambiguous as elevated NGF levels could be a sign of neuroprotective or destructive processes in the brain. These studies give evidence that subconcussive blows to the head can cause injury and should not be overlooked as trifle.

Compared to the literature on sports-related concussion, biomechanical studies solely focusing on subconcussive head trauma are scarce, and if any data is presented, it usually limited to the quantification of the number of impacts. Although this not to say that researchers have not tried, and biomechanical studies have shown that significant amount of forces are transmitted to deep midbrain and brainstem structures even in less severe head injury that does not result in concussion or loss of consciousness [28]. Biomechanical studies report that the forces like momentum and energy transfer associated with heading the soccer ball are far less than those found in football, boxing, hockey, and other full contact sports [29]. With the advent of new technologies, like the Head Impact Telemetry System (HITS) that has been employed in football helmets, tracking the number and quantification of forces at impact has become more feasible. In a recent study Broglio et al. [10] used the HITS to measure and record head impacts in 95 high school football players over a 4-year period of time. The results of this study highlighted the number of blows to the head an athlete is exposed to over the course of a season as well as the high degree of linear and rotational accelerations forces sustained during these impacts. Probably the most shocking data to come out of these studies are the sheer quantity of subconcussive impacts endured of the course of a season, let alone an athlete’s career. This number can be upwards of thousands of subconcussive impacts during the course of a single season [1], with one study using accelerometers in football helmets reporting players sustaining over 1,400 subconcussive blows over the course of a season [30]. Consequently, a recent laboratory study of football helmets found that current varsity helmets are less protective to their older leather helmet counterparts when it comes to subconcussive blows [31].

These subconcussive hits are not only relegated to the contact sports that immediately come to mind when we think of concussion like football, ice-hockey, and rugby. Soccer is a contact sport and chronic traumatic brain injury (CTBI) has been well documented in the literature [32]. During an average game, a soccer player heads the ball 6–12 times which is estimated to be over 5,000 headers for a 15-year career [9, 29]. However, most of the documented cases of concussion in soccer occur due to the players head contacting another player’s head, the ground, or the goal post, not from purposeful heading [33]. However, repeated subconcussive blows that are incurred from heading the soccer ball account for many clinical symptoms that span the spectrum from headache to brain damage and can also lead to alterations in acute and chronic cognitive function [9]. It has long been known that heading of the soccer ball could produce “footballer’s migraine” [34]. There are few biomechanical studies on subconcussive head trauma and implementing such studies requires highly technical and intricate technology and knowledge. Furthermore, biomechanical studies of full blown concussive episodes have gone to great lengths to quantify and identify a threshold of concussion to no avail [35], as this is very difficult given the fact that each concussion is different [36].

These subconcussive impacts that are below the threshold of concussion and do not result in any clinically identifiable signs or symptoms are a controversial topic as researchers and clinicians are divided on their true effect. Some research has shown that subconcussive head trauma may have minimal impact on cognitive functions [37] although there is mounting evidence that subconcussive blows have detrimental effects on cognitive and cerebral functions [5, 14]. It has been hypothesized that exposure to repeated and multiple subconcussive blows throughout an athlete’s career may compromise cognitive function [38]. It is becoming ever more apparent that brain injury does not only come from concussive episodes, but that the accumulation of these subconcussive blows may be detrimental [13]. A history of multiple concussions and subconcussive blows is known to result in depression, cognitive deficits, and progressive neuropathologies that include neurofibrillary tangles and deposits of amyloid plaques seen in Alzheimer’s disease [39].

A majority of the literature that exists on acute and chronic sports-related subconcussive head trauma has been focused on soccer as purposeful heading represents a form of repetitive subthreshold mild brain injury [29]. In a preliminary study, it was found that out of 77 retired Norwegian professional soccer players, 50 % reported symptoms linked to heading, and 75 % suffered from disorientation, headache, and nausea [40]. Further studies by Tysvaer et al. used electroencephalograph (EEG) to evaluate professional soccer players. They found that 35 % of the participants had abnormal EEGs and 70 % displayed some form of neurological impairment [41, 42]. In addition to these findings, neuropsychological testing (Wechsler Adult Intelligence Scale) of the same soccer players revealed significant differences compared to controls with one-third of participants’ scores low enough to suggest evidence of organic brain damage [43]. Matser et al. [44] reported significant deficits in neuropsychological assessment of amateur soccer players associated with heading. Specifically, they reported impaired performance in memory, planning, and visual perception processing that was exacerbated by the number of previous concussions a player had sustained. Downs and Abwender [45] reported that subjects with a long history of soccer heading demonstrated slower patterns of motor speed and reaction time. Another study looking at purposeful heading by Witol and Webbe [7] revealed that players with the most reported number of headers had the lowest attention, concentration, and IQ scores. Decreased reaction time and reduced speed performing a motor task have been documented when assessing the effects of subconcussive head trauma in soccer [45], as well as in athletes following a concussion [46], suggesting that reaction time is impaired following repeated subconcussive and concussive head trauma [38]. Although there is evidence that a long career which accounts to many instances of heading the soccer ball can lead to impaired brain function, it is not clear whether or not this increased likelihood is caused by numerous subconcussive blows or from full blown concussive episodes [33]. Jordan et al. [47] found that there was a correlation between a history of concussion with increased symptoms in the United Stated national soccer team players and may suggest that full blown concussions as compared to repetitive subconcussive impacts may be the cause of encephalopathic changes. But it seems evident in the literature that a long soccer career, which amounts to a higher frequency of heading and accumulation of subconcussive blows, contributes to impairments in cognitive function [33, 48]. Whereas, in a review by Rutherford et al. [15] on neuropsychological testing and purposeful heading in soccer literature, they raise certain methodological concerns with a majority of the studies. They conclude that there is preliminary evidence that full blown concussive episodes can have deleterious effects based upon neuropsychological examination, whereas the effects of subconcussive impacts on neuropsychological tests awaits more supporting evidence. Not all studies on heading in soccer have reported neuropsychological deficits [34]. In a recent study, Kontos and colleagues [49] used computerized testing in the form of Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT) to test 63 adolescent soccer players. All subjects under study had no current (less than 3 months) history of concussion and were placed into one of the three groups based upon the number of documented headers as observed by the researchers over the course of two practices and games. Their results showed no significant differences between the low, moderate, and high frequency heading groups on computerized neuropsychological assessment. However, the authors did note that the males showed lower scores on verbal memory, visual memory, and motor processing compared to female participants. This decreased performance was attributed to differences based upon sex despite the fact that males headed the ball more often than females.

Similar to the studies looking at the chronic effects of repetitive subconcussive head trauma, initial research looking at the acute effects has reported mixed results. Schmitt et al. [33] tested postural control and recorded subjects’ self-reported symptoms immediately and at 24 h following a controlled session of intentional soccer ball heading. They found that prior to, immediately following, and at 24 h after the 40 min session of heading, there were no differences in postural control as assessed by center of pressure (COP) area and velocity between the heading group and a control kicking group. In spite of not finding any significant difference in postural control after an acute bout of heading, an increase in concussion-related symptoms were found immediately following the heading session, but not at 24 h after in the heading cohort. The main complaints were headache, dizziness, and feeling lethargic. This reported finding was similar to Tysvaer [50] who found that 10 min following a session of purposeful heading, all subjects reported suffering from a headache. Consistent with these findings, Mangus et al. [51] also reported no differences in balance following an acute bout of soccer ball heading. Additionally, Broglio et al. [52] found no significant acute changes in postural control following a study that looked at the effects that purposeful heading in soccer can have on balance. In a recent study by Rieder and Jansen [53], they took subjects and divided them into three groups to investigate the effects that a bout of acute heading would have on neuropsychological exam. The three groups consisted of subjects exposed to aerobic training and purposeful heading drills, the second group consisted of subjects only doing the aerobic training, and the third group did not exert themselves physically before neuropsychological testing. Neuro-psychological testing was performed 1 week prior to training session and immediately after. The results showed no differences between groups and or any deficits caused by heading drills. However, there was a higher incidence of headache during and after in the heading cohort which the authors attributed to the most minor form of head trauma, cranial contusion, which is associated with local or diffuse transient headache. However, Putukian et al. [54] did not report any differences in self-reported symptoms and cognitive function in a pilot study after a soccer training session that included heading. Therefore, symptoms from subconcussive blows may be shorter lived and only detectable immediately after insult as the training session was substantially longer and less focused on heading than the Schmitt et al. [33] study. Employing the use of a computerized tablet, Zhang et al. [55] devised a variant of common eye tracking research, prosaccade, and antisaccade by having participants point towards a target (Pro-Point) or point to the opposite target (Anti-Point). Eye tracking research has been shown to be more sensitive in picking up cognitive and functional deficits compared to standard neuropsychological testing [56–58]. In their study, Zhang et al. [55] tested 12 female high school soccer players following practice that included heading of the soccer ball. No difference was seen between the soccer group compared to sex and age matched control group on the Pro-Point task. Although the Anti-Point task, similar to the antisaccade task used in eye tracking studies, showed that subjects in the soccer group that were exposed to heading demonstrated significantly slower response times compared to the control group.

In an early study of boxers, Heilbronner and colleagues [59] were the first to demonstrate changes in cognitive function immediately following a fight when compared to a prefight assessment. Specifically they noted a decline in verbal and incidental memory, and noted that numerous subconcussive blows may be more deleterious than less frequent full blown concussions as the number of rounds a boxer fights better predicts the development of encephalopathy compared to the number of knockouts. In a study by Ravdin et al. [60] investigating the effects of subconcussive blows, boxers were administered neuropsychological examinations before a fight, after the fight, and at a 1-month follow-up session. Their results were interesting and questioned the validity of a return-to-baseline as an appropriate criterion for return-to-play decisions. They noted that at 1-month post-fight, neuropsychological performance had increased beyond baseline assessment taken prior to the fight and was believed to be caused by the repeated subconcussive blows the boxers received while training for the fight. Repetitive subconcussive head trauma has been hypothesized to be the main cause of neurocognitive dysfunction in boxers and that the accumulation of subconcussive blows may lead to cognitive deterioration of brain function [61].

Shuttleworth-Edwards and Radloff [62] investigated the differences between rugby players and athletes involved in non-contact sports and found that rugby players had a poorer performance on visuomotor processing speed. Additionally, they subdivided the rugby players into two groups based upon the frequency of the positions to be exposed to subconcussive head trauma. This within group analysis revealed that the group that regularly receives more subconcussive impacts displayed lower scores on the digit symbol substitution visuomotor task. Interestingly enough, it has been reported that despite a five times greater frequency of head injuries, rugby players out perform soccer players on neuropsychological testing [63]. Additionally, Parker et al. [38] found that subjects exposed to repeated subconcussive blows in football, rugby, and lacrosse showed increased medial–lateral sway in their gaits. In a study by Killam et al. [64] examining athletes with and without a history of concussion and athletes recovering from concussion to a control group without any history of head trauma, researchers concluded that subconcussive head trauma seen in contact sports produces subclinical cognitive impairments. Similarly, Stephens et al. [65] performed neuropsychological testing on adolescent soccer and rugby players in addition to a group of noncontact athletes. They reported no evidence of neurological dysfunction in both the soccer and rugby players when compared to their noncontact counterparts. Although no individual has suffered a recent (within the past 3 years) head injury, those with a previous concussion showed poorer performance on attention measures.