High total homocysteine (tHcy) concentrations contribute to an increased risk of cardiovascular diseases and neurodegenerative disorders. Several investigations have focused on the effect of exercise on tHcy concentrations, but results remain controversial. The differences among the methodologies in the investigations make difficult the interpretation of results. This review differentiates the effects of exercise on tHcy and establishes the relation with the implicated biomarkers on tHcy metabolism related to exercise. The electronic database MEDLINE (http://www.ncbi.nlm.nih.gov) was used for searching studies published between years 2002 and 2015. ‘Homocysteine’, ‘Training ’, ‘Exercise’, ‘Physical Activity’ as well as combinations out of these terms were entered in the database. Articles were grouped in: 1) Acute effect of exercise on tHcy, 2) chronic exercise and tHcy, 3) relationship of physical activity (PA) level and cardiorespiratory fitness with tHcy, and 4) biomarkers related to tHcy and exercise. From a total of 30 articles, most of the studies analyzing the acute effect of exercise showed an increase on tHcy concentrations. Studies analyzing the chronic effect on tHcy concentrations showed contradictory results and no consensus exists probably due to the differences in the methodology, exercise interventions and participants characteristics. Low cardiorespiratory fitness seems to be associated with high tHcy; in contrast, the relation of PA levels and tHcy needs further research. Regarding biomarkers related to tHcy and exercise, some studies showed an increase of folate, vitamin B12, and creatine after acute exercise that could to be due to requirement of protein turnover and an increased metabolic demand of vitamin-B.
Homocysteine is an intermediate sulfur-containing amino acid involved in the methionine cycle . Elevated total serum homocysteine (tHcy) concentrations contribute to plaque formation and consequently to an increased risk of cardiovascular diseases (CVD) and neurodegenerative disorders , but until now, there is no consensus if high tHcy concentrations constitute a risk factor or a risk marker [3, 4]. There are a number of factors that affect homocysteine concentrations such as age, gender, genetics and medication together with lifestyle factors including alcohol intake, smoking habit, nutrition and physical activity . Regarding nutrition, tHcy is driven by several B-complex cofactors. Folate, vitamin B12 and B6 are involved in the transsulfuration pathway and vitamin B6 participates in the remethylation reaction  (Figure 1). The enzyme methionine synthase is involved in the remethylation reaction and conversion of homocysteine to methionine requires both folate and vitamin B12 as coenzymes . Moreover, vitamin B6 acts as a coenzyme for the enzymes cystathionine-β-synthase and cystathionine-γ-lyase in the transsulfuration pathway to convert homocysteine to cysteine. Therefore, an adequate vitamin-B status is critical to maintain the optimal efficiency of the homocysteine-methionine cycle . Methylenetetrahydrofolatereductase (MTHFR) C677T polymorphism is associated with various diseases (vascular, cancers, neurology, diabetes, etc.) and its synthetized enzyme plays a key role in folate metabolism, which is an integral process for DNA and RNA synthesis and in protein methylation. This enzymatic activity process is lowered in subjects with MTHFR 677TT genotype and these individuals might require an increased intake of folate to maintain or control blood levels of plasma folate or tHcy [8, 9].
Physical exercise has been strongly demonstrated to be an important factor to reduce cardiovascular risks . However, it is unclear if exercise or physical activity modify or have an effect on tHcy concentrations . In the last few years, some researches have been focused on the role of exercise on tHcy concentrations; however, results obtained from several studies are contradictory and sometimes inconclusive . Some studies focused on the impact of lifestyle factors, nutrition, physical activity (PA) level, cardiovascular fitness, chronic effect or acute effect of exercise. There is a variety of study population in the different investigations as sedentary, elderly, athletes, obese, women or children. But there is also a huge variety in the methodology applied among all the studies, hence, there is difficulty to reach an agreement . Some researchers have demonstrated reduced tHcy concentrations after a training period [12, 13]; others have related high PA levels and cardiorespiratory fitness with lower homocysteine concentrations [14, 15]. In contrast, some studies have shown higher tHcy concentrations after acute exercise, training period or after a specific sport competition , , . The controversial results may be due, in part, to the lack of standardization among exercise interventions, study population, training programs, or timing and methodology of blood samples collection. In addition, one important aspect is the wrong generalized concept “exercise” as a sole term for huge different exercise responses involved in the physiology of exercise. All in all, it could lead to a possible misunderstanding in the extrapolation of the conclusions from the results. Whereby, altogether makes necessary to interpret carefully previous results and to clarify the different research lines in the context of “exercise effect” on tHcy concentrations.
The exact mechanism by which exercise affects tHcy concentrations continues being unknown. Thus, it is important to discern the kind of exercise and training, and their intensities and durations, in order to know in depth the underlying mechanisms of tHcy variations due to exercise.
This review focuses on the role of exercise and PA, and their different modalities on tHcy concentrations and its possible relation with other implicated biomarkers.
Materials and methods
The electronic database MEDLINE (http://www.ncbi.nlm.nih.gov) was used for searching studies published between 2002 and 2015. ‘Homocysteine’, ‘Training’, ‘Exercise’, ‘Physical Activity’ ‘Sport’ as well as combinations out of these terms were entered in the database. In addition, references found in relevant articles were also used to get further information. Only articles containing data related to homocysteine were chosen. Health status, age and training level of the population was not considered. Reviews, systematic reviews or meta-analysis were excluded. Articles were grouped in four different groups, depending of the factor that seemed to have an effect on tHcy variations: 1) Acute effect of exercise 2) Chronic effect of exercise 3) Relationship of physical activity level and cardiorespiratory fitness with tHcy concentrations and 4) biomarkers implicated on homocysteine concentrations and exercise.
A total of 30 articles were included in this review.
Table 1 summarizes the intervention studies containing the immediate effects of acute exercise on tHcy. From 11 articles, eight studies were performed in athletes, recreational athletes or well-trained participants and three in healthy sedentary or inactive participants for at least 6 months.
Males, ♂; females, ♀; ↑, increase; ↓, dicrease; NS, no statistical differences; B12, vitamin B12; B6, vitamin B6; Hcy, homocysteine; tHcy, total homocysteine.
Nine studies consistently reported a significant increase of tHcy immediately after an acute aerobic or resistance exercise (p<0.05), independently of the type of exercise, duration, intensity, intervention protocol or training level of the subjects. By contrast, two studies showed no significant differences in tHcy after exercise intervention.
The effects of chronic exercise on tHcy concentrations are shown in Table 2. From 10 articles, six studies analyzed aerobic training programs and another four studies, resistance-training programs. Regarding the chronic effect of aerobic training on tHcy, two articles reported a decrease on tHcy, four showed no tHcy changes and two studies observed a tHcy increase after an aerobic training program. On the other hand, from those four studies performing resistance-training programs, two of them showed a decrease in tHcy and the other two showed an increase of tHcy after exercise interventions.
Males, ♂; females, ♀; ↑, increase; ↓, decrease; NS, no statistical differences; B12, vitamin B12; B6, vitamin B6; Hcy, homocysteine; tHcy, total homocysteine.
Table 3 shows the studies analyzing the association between PA and/or cardiorespiratory fitness level with tHcy concentrations. A total of nine studies were categorized into this group. Three of the five studies focused on cardiorespiratory fitness found an inverse association between tHcy concentrations and cardiorespiratory fitness in women. On the other hand, six articles described and analyzed the correlation between PA levels and tHcy. Three of them found lower tHcy concentrations in athletes or in subjects with higher levels of PA compared to sedentary ones. Otherwise, neither intensity nor duration and frequency showed significant associations with tHcy across the nine studies.
Males, ♂; females, ♀; ↑, increase; ↓, decrease; NS, no statistical differences; B12, vitamin B12; Hcy, homocysteine; tHcy, total homocysteine.
Table 4 summarizes those studies that analyze the relation of implicated biomarkers on the homocysteine metabolism with exercise or physical activity. A total of 12 studies were selected into this group. Associations between tHcy and folate before exercise were observed in three studies; two of them also found an inverse correlation before exercise between tHcy and vitamin B12. Three studies showed an inverse correlation after exercise between tHcy and folate, two of these investigations were different than those that found the correlation pre-exercise. Furthermore, most of the studies showed higher values of folate, B12 or B6 depending of exercise, competition or training periods. Regarding creatinine, all the existing studies that analyzed the effect of exercise on creatinine levels, found post-exercise creatinine increase after acute exercise, but not after training periods.
Males, ♂; females, ♀; ↑, increase; ↓, decrease; NS, no statistical differences; B12, vitamin B12; Hcy, homocysteine; tHcy, total homocysteine.
This review attempts to clarify and summarize how tHcy can be affected by exercise or training and its possible consequences regarding health and prevention of cardiovascular risk and other chronic diseases.
Regular exercise affects all the physiological systems in the body. Its benefits on health and prevention of the development of cardiovascular and other chronic diseases are well described in the literature [39, 40]. On the other hand, homocysteine has been studied in depth in the last few years, but the effect of exercise on it remains controversial . The main problem relies in the different physiological effects of exercise on tHcy and the variety of studies with different objectives, methodologies and sample population. This situation makes necessary to distinguish the differences among the terms: ‘acute effect of exercise’, ‘chronic effect of exercise’ ‘cardiovascular fitness’ and ‘physical activity levels’ and its influence on tHcy concentrations.
Acute effect of exercise on tHcy concentrations
Many experimental studies have examined the acute effects of exercise on tHcy concentrations, by varying the degree of intensity, duration and type of exercise. Most of the reviewed articles from this category found a tHcy increase immediately after acute exercise. Konig et al. , found higher tHcy concentrations after 1 and 24 h of a triathlon competition. Herrmann et al.  found the same response after various modalities of aerobic exercises [17, 18]. These effects are in line with those found by several investigations [11, 19, 20, 22, 23, 24, 26, 41]. The study of Herrmann et al. , speculates that intensity and duration of exercise could determine the tHcy response, due that only marathon runners showed significant tHcy increment both, from baseline and comparing by groups. These authors suggested that the high intensity sustained by the runners comparing to the 100 km run and mountain bike race, can have more rest periods during trials, being a possible answer of this response. In contrast, other research studies including different intensities showed that the tHcy increase is independent of the intensity of the exercise [11, 24] or type of exercise .
Sotgia et al. , who compared athletes and non-athletes subjects, found no changes in tHcy after acute exercise but a decrease in the Homocysteine reduced form . On the other hand, Hammouda et al. , did not found any change in tHcy concentrations after acute exercise . This probably relies on the fact that the intervention was performed only by a 30 s Wingate test, not long enough to stimulate the methionine synthesis. Moreover, Konig et al. , concluded that although acute exercise significantly increases tHcy, chronic endurance exercise was not associated with higher plasma tHcy concentrations . Health status from individuals can also influence the metabolic pathways . But in the reviewed investigations, when analyzing active and sedentary people, acute effects had the same tHcy increment-response. Authors have suggested that intense exercise accelerates protein turnover catabolism and the pool of amino acids in the muscles . As a consequence, it may lead to an increase in the catabolism of the intermediary metabolism and homocysteine formation .
From these results it could be observed that acute exercise generally induces an increase immediately after exercise, independently of the previous training level, intensity and duration.
Effect of chronic exercise on tHcy concentrations
Regarding the studies analyzing the effect of chronic exercise programs on tHcy concentrations, it is difficult to reach an agreement due to the variety of type of exercises and training programs. Some researchers highlighted an exercise-induced-fall in tHcy after training: the investigations of Randeva et al.  and Choi et al.  included aerobic modalities and Vincent et al.  and  performed resistance programs [12, 13, 27, 30]. Thus, we did not find the common point among these results, due to the differences in the type of exercise, training duration and sample studied.
On the other hand, three of the studies reported an increase in tHcy concentrations, although the training interventions were also different, using both aerobic and resistance exercises. The investigations of Molina-López et al.  and Guzel  found increased tHcy after training but both of them were within reference values (<15 μmol/L) [31, 32]. Interestingly, Okura et al.  found different responses depending on the baseline tHcy status . An increased tHcy was observed after training in those within normal tHcy concentrations at baseline; in contrast, the contrary effect was observed in subjects with hyperhomocysteinemia at baseline, where tHcy decreased after training exercise programs.
On the other hand, some studies provided data that training does not alter tHcy concentrations .
Furthermore, health status could provoke different responses in the homocysteine metabolism than the effect on general or healthy population, as shown by Randeva et al.  in overweight polycystic women and by Vincent et al.  in elderly people [12, 27].
In summary, the studies of the effect of chronic exercise did not show a consistent effect on tHcy, neither in active nor sedentary samples, nor type, duration and intensity of exercises. Unfortunately, these observations could not be used to discuss the effect of chronic exercise on tHcy in healthy individuals or athletes. It could be observed that the intervention exercise programs used different intensities, duration of training intervention, type of exercise and study population. This could be the reason for the variability in the results and in sight of these studies; the question about the relationship between tHcy and chronic exercise remains unclear.
Relation of physical activity levels and/or cardiorespiratory fitness with tHcy concentrations
Poor cardiovascular fitness is another important risk factor for cardiovascular disease and is a predictor of morbidity and all-cause mortality . Kuo et al. , found that tHcy concentrations were inversely associated to cardiovascular fitness in adult women but not in men, independently of body mass index (BMI), age, race, vitamins B, creatinine levels and physical activity among other factors .
The study conducted by Ruiz et al. , reported no association of tHcy with any measure of physical activity as cardiovascular fitness or physical activity level when controlling for MTHFR genotype in children. In contrast, a further study by Ruiz et al.  showed that cardiovascular fitness was negatively associated with homocysteine levels in young women when controlling for MTHFR genotype [15, 36]. These results are in accordance with those found by Kuo et al. . Ruiz et al.  suggested that this negative association could be due to sex hormones modulation. Differences in rates of homocysteine remethylation  and estrogen concentrations  may contribute to the homocysteine sex dimorphism. In another investigation conducted by Dankner et al. , results did not show association between tHcy and cardiorespiratory fitness in adult males . The review of Joubert and Manore , concluded that tHcy could be dependent on the individual fitness level of participants . Dankner et al.  found a negative correlation between PA levels and tHcy in elderly, independently of the vitamin-B status and MTHFR genotype . Moreover, in an investigation conducted by Nygård et al. , results showed that physical inactivity was associated to higher tHcy . This author suggests that exercise exerts most favorable effects in subjects with hyperhomocysteinemia, as shown by Unt et al. , who found higher tHcy concentrations in ex-athletes returning to a sedentary lifestyle comparing to those who continued being active . In this study, vitamin status or dietary habits did not reveal any difference. In contrast, Joubert and Manore  did not found any association between PA levels and tHcy concentrations . Furthermore, they reported that individuals who had higher levels of PA had also higher tHcy concentrations and may need a vitamins B supplementation to keep blood tHcy concentrations as low as possible . The intervention studies analyzing the relationship between tHcy and PA levels show some limitations as the low accuracy of the measurement of PA level by questionnaires.
Implicated biomarkers related to homocysteine concentrations and exercise
The literature has studied the relation of the known factors that influence homocysteine metabolism and its implication with exercise [6, 35]. These factors include B vitamins, such as folate, vitamin B12 and vitamin B6 blood levels as cofactors of several enzymes involved in homocysteine metabolism [7, 45]. Some authors have speculated that proper intake of vitamin B6, B12 and folate can help to maintain low tHcy concentrations and support the increased demand on metabolism during high intensity exercise . The inverse correlation among serum vitamin B12, and folate is well established in the literature, but this interaction may be modulated by exercise or training. The literature shows a great variability in the correlations with folate, vitamin B12 or B6 and tHcy concentrations due, among other factors, to the lack of control in the methodology analyzing dietary intake and blood levels of vitamins B. The correlation between blood vitamin B12 and folate with tHcy before exercise has been observed in various studies [18, 46]. However, results are less clear and sometimes controversial regarding exercise or training program. Moreover, it seems that there is some consensus about the increase of folate, vitamin B12 after acute exercise, competition or training programs [11, 46]. Vitamin B6 is required as coenzyme of transaminases, decarboxylases and glycogen phosphorylase in metabolic pathways of energy production, but in contrast, results from the study of Iglesias-Gutierrez et al. , did not reported any relationship between vitamin B6 and substrate utilization during different intensities throughout the trials . On the other hand, Herrmann et al. , suggest that endurance athletes had a higher prevalence of B vitamin deficiency due to the high necessity of vitamin B6 and folate not only during exercise but also during training  because vitamin B6 is necessary to fuel working muscles and to repair damaged tissue .
The C677T polymorphism of the MTHFR gene, has been established as an important genetic determinant of elevated tHcy . There is evidence that physical activity may also alter homocysteine metabolism by increasing protein and/or methyl group turnover . Another implicated parameter is creatine, which is responsible for a considerable consumption of S-adenosylmethionine in the liver for homocysteine formation . During high intensity exercise, creatine-phosphate is required as an immediate energy source for muscle contraction. The increase in creatine synthesis demand can be a key factor in the methyl balance modulation and one of the most important factors related to increased tHcy . The increased creatinine after acute exercise has been observed in different studies [21, 50]. Creatine production is parallel to tHcy elevation and in addition to the need of vitamin B6. Some authors have studied the effects of creatine supplementation followed by exercises interventions . Deminice et al. reported that 0.3 g/kg of creatine supplementation during 7 days were unable to lower tHcy concentrations either at rest or after acute exercise . Surprisingly, some animal research showed opposite results, founding a decrease in plasma tHcy after creatine supplementation [41, 51]. These contradictory data suggest that inhibition of the endogenous methylation demand by creatine supplementation can reduce tHcy levels in animals, but not in humans . However, more studies are necessary to examine activities of key enzymes on creatine synthesis after acute exercise.
In summary, this review identifies that acute exercise usually induces increases in tHcy. In contrast, no consensus exists regarding training effect due a large variety of exercise interventions, with different intensities, duration and mode of exercise. Additionally, the population and their characteristics differ among studies and make it difficult to reach a consistent conclusion. Low cardiorespiratory fitness seems to be associated with high tHcy concentrations, in contrast, results analyzing physical activity levels and its relation to tHcy concentrations; needs further research. Regarding biomarkers implicated on tHcy response with exercise, there is a consensus about the increase of folate vitamin B12, vitamin B6 and creatine during acute exercise probably due to increased requirement of protein turnover and increased metabolic demand, while the exact reactions and effect on tHcy during prolonged training need to be investigated in depth. Finally, due to the accepted results about the increase of tHcy concentrations after acute exercise, it could be necessary to improve the B-vitamin status of the athletes in order to ensure the requirements of the methionine-homocysteine metabolism during acute exercise.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
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