A Base Científica para o Treinamento de Resistência Quase Isométrica Excêntrica - Uma Revisão Narrativa
A Base Científica para o Treinamento de Resistência Quase Isométrica Excêntrica - Uma Revisão Narrativa
2 A narrative review
3
5 Abstract
6 Eccentric quasi-isometric (EQI) resistance training involves holding a submaximal, yielding
7 isometric contraction until fatigue causes muscle lengthening, then maximally resisting
8 through a range of motion. Practitioners contend that EQI contractions are a powerful tool for
9 the development of several physical qualities important to health and sports performance.
11 performance. Therefore, the primary objective of this review was to synthesize and critically
12 analyze relevant biological, physiological and biomechanical research and develop a rationale
13 for the value of EQI training. Additionally, this review offers potential practical applications
14 and highlights future areas of research. While there is a paucity of research investigating
15 EQIs, the literature on responses to traditional contraction types is vast. Based on relevant
16 literature, EQIs may provide a practical means of increasing total volume, metabolite build-
17 up and hormonal signalling factors while safely enduring large quantities of mechanical
18 tension with low levels of peak torque. Conversely, EQI contractions likely hold little
21 variables with low injury risk. Although speculative due to the limited specific literature,
23
25
1
26 Introduction
28 contractions, also known as yielding, holding, or eccentric isometrics (50, 71, 136), have
29 many variations and proposed applications. However, for this review, EQIs will be defined as
30 “holding a position until isometric failure and maximally resisting the subsequent eccentric
31 phase”. Theoretically, the prolonged quasi-isometric and eccentric component enable a large
33 improvements in work capacity, muscle size and connective tissue health. While traditional
34 high-intensity isometric contractions and eccentric muscle actions are commonly used by
35 practitioners, with well-established value in the modern scientific literature (38, 44, 45, 79,
36 90, 120), EQIs remain relatively unexplored. Therefore, this review aims to synthesize and
37 critically analyze relevant research and subsequently develop a rationale for the value of EQI
39
41 Prior to the EQI contraction, a submaximal (being hereafter relative to one repetition
42 maximum (1RM)) eccentric contraction where the muscle-tendon unit undergoes an active
43 lengthening is performed. Once the prescribed joint position is met, the trainee shifts to
44 yielding isometric muscle action and attempts to hold the position for as long as possible. The
45 final phase occurs as fatigue accumulates, and an eccentric contraction commences while the
46 trainee attempts to resist muscle lengthening maximally. Some practitioners contend that this
47 second lengthening phase places additional stretch and strain on the musculotendinous
49 recommended a wide range of loads, with the goal of holding the quasi-isometric contraction
50 for 5-90 seconds (112, 142). Consistent with traditional resistance training, greater intensities
2
51 and shorter contraction durations are recommended for strength and power athletes while
52 lower loads and longer contractions may be advantageous for oxidative or rehabilitative
53 purposes (112, 142). Anecdotally, increased muscle thickness, improved range of motion
54 (ROM), altered force-angle relationships and improved tendon health, have been reported
55 following EQI training (112, 142). Although quasi-isometric muscle actions have been used
57 sprinting gait (24, 99, 150, 152, 166-169), there is no published empirical data on EQIs, and
59
60 Methods
63 SPORTDiscus, PubMed and CINAHL databases from inception to May 2019. Key terms
64 were searched for within the article title, abstract, and keywords using conjunctions ‘OR’ and
65 ‘AND’ with truncation ‘*.’ Combinations of the following Boolean phrases comprised the
66 search terms: isometric, static, eccentric, contraction, occlusion, blood flow restriction,
67 hypertrophy, strength, power, endurance, muscle, fiber, cross-sectional area, tendon, fascicle,
68 pennation and neuromuscular. Reference lists and books were also utilized.
69
71 Studies were included in the review based on the following criteria: 1) full text
74
75 Statistical analysis
3
76 Percent change and Cohen’s d effect sizes (ES) were calculated wherever possible to
77 indicate the magnitude of the practical effect. Effect sizes were interpreted using the
78 following criteria: trivial <0.2, small 0.2-0.49, moderate 0.5-0.79, large >0.8 (47). All
79 reported ES and percentage changes are pre-post within–group, unless otherwise stated.
80
84 length, and tendon stiffness and elasticity. Functional morphology refers to the structure and
85 function of organisms and their specific structural features. Although morphology affects
86 function in all tissues, this review will focus on the musculoskeletal system, which is often
87 broken down into the three-component model of force transmission (Figure 1) (66). The three
88 component model provides insight into the determinants of force production and transmission
89 - the contractile element (CE), series elastic component (SEC) and parallel elastic component
90 (PEC) (69, 70, 104, 126). The PEC, synonymous with the extracellular matrix, includes the
91 elastic tissues surrounding the myofibrils (the endo, peri and epimysium) as well as the
92 sarcolemma and fascia. These tissues are thought to contribute to sensations of pressure, and
93 although yet to be fully quantified, may play a meaningful role in force transmission between
94 joints and body segments (69, 70, 104). The SEC encompasses the spring-like tissues in
95 series with actin and myosin, the tendon and aponeurosis being most obvious. Controversy
96 exists regarding the exact function of the titin myofilament, which appears to play a role in
97 both active and passive force transmission (41, 64, 68). For example, titin was originally
98 thought to be somewhat innate and only contribute to passive tension in a fully stretched
99 sarcomere (68). However, contemporary research has demonstrated that titin is activated by
100 calcium ions and adenosine triphosphate, contributing to active force transmission (41, 64,
4
101 95). Finally, the CE consists of the myofibril, and more specifically, the myofilaments of
103
105
108 Typically prescribed at long muscle length (LML) and often held through full ROM,
109 EQIs fulfil the scientifically based criteria of mechanical stretch and tension for improving
110 muscular hypertrophy and function. Produced by force generation and stretch, mechanical
111 tension is effective in promoting muscular hypertrophy regardless of contraction type (15, 55,
112 137). In animal models, prolonged mechanical tension has been shown to produce dramatic
113 increases in muscle size. For instance, extreme increases in muscle mass (318%), muscle
114 length (51%), mean fibre thickness (39%) and fibre number (82%) were reported following
115 loaded stretching of avian wings over 28 days (9). Similarly, Tabary et al. (155) reported that
116 cat soleus muscles immobilized in a lengthened position had 20% more serial sarcomeres
117 whereas a shortened soleus group had 40% fewer sarcomeres in series than normal muscle,
119 250% RNA content in four days was observed following electrically induced overload in
120 stretched rabbit tibialis anterior muscles (55). The effect of mechanical tension on skeletal
121 hypertrophy was examined by Ashida et al. (15) utilizing electrically induced contractions in
122 mice. Peak torque and torque-time integrals were highly correlated with increased muscle
123 mass and mTOR regulating p7S6k phosphorylation in isometric contractions and eccentric
124 muscle actions (15). Thus, animal models suggest that loaded stretching may provide a
125 unique stimulus for inducing gene transcription and muscular hypertrophy (55).
5
126
127 Recently, loaded stretch training with human subjects has grown in popularity (10, 63,
128 148). For example, following six-weeks of loaded (20-45% of maximal voluntary contraction
129 (MVC)) stretching for five, 3-minute sessions per week, fascicle length (25%), ROM
130 (14.9%), and muscle thickness (5.6%) significantly increased, while the pennation angle of
131 the lateral gastrocnemius significantly decreased (7.1%) (148). However, no change (p =
132 0.94, ES = 0.08) in MVIC or voluntary activation (p < 0.05, ES = 0.13) was present (148),
133 despite several cross-sectional investigations supporting the relationship between muscle
134 architecture and performance (3, 7, 23, 89, 118, 163). Yet, the causal relationship between
135 alterations in muscle architecture and muscular strength has become a hot topic in
136 contemporary literature (36, 117). Additionally, the concept of constant-torque versus
137 constant angle-stretching has been recently examined (10, 63). For example, Herda et al. (63)
138 examined the short-term effects of acute knee flexor stretching at a constant-angle, or under
139 constant-torque where the muscle was initially held at a point of mild discomfort followed by
140 additional muscle-tendon unit lengthening via “muscle creep,” and stretch-induced analgesia
141 occurred. While both groups experienced similar improvements in passive ROM and passive
142 torque, only the constant-torque treatment resulted in decreased muscle-tendon-unit stiffness
143 (p < 0.001) (63). Unfortunately, Herda et al. (63) did not report any performance measures, a
144 trend that is common in stretching research (10). From these results, it appears that, in young
145 males, loaded stretching can provide sufficient stimulus to affect musculotendonous
146 architecture, viscoelastic properties and likely, acute pain thresholds (10, 63, 148). As
147 variants of loaded stretching utilize extended periods at or near end ROM, the results of the
148 aforementioned research lend credence to the hypothesis that EQI training may be a valuable
149 training methodology for improving acute and chronic flexibility and musculotendonous
150 function. However, there is a dearth of stretch research elucidating the ideal stretching
6
151 intensity and the efficacy of loaded stretching to improve muscular or athletic performance
152 (10).
153
154 Although eccentric muscle actions have the highest potential for muscular force
155 production, isometric muscle actions are the only contraction type that has no ROM
156 dependent endpoint. Isometric training is also easily implemented as simply flexing (co-
157 contracting the agonists and antagonists of a limb) can increase muscle size and strength in
158 active men (100, 175); though the value of co-contraction training in a well-trained
159 population has yet to be elucidated. Additionally, isometric contractions enable training at
160 specific joint angles and, therefore, muscle-tendon lengths. While strength improvements are
161 joint-angle specific (97), increases in muscular hypertrophy, which is larger following full
162 ROM and LML training, (106), transfer to all joint angles (5, 87, 115, 116). McMahon et al.
163 (106) compared the effects of dynamic resistance training executed with full or partial ROM.
164 The full ROM group experienced significantly greater improvements in the distal anatomical
165 cross-sectional area (59% vs. 16%), fascicle length (23% vs. 10%) and isometric force at all
166 seven (30-90° of flexion) measured knee joint angles (11-30% vs. -1-6%) (106) when
167 compared to the partial ROM group. Although isometric contractions resulted in less muscle
168 damage and less dramatic muscular-tendinous adaptations compared to maximal eccentrics,
169 maximal voluntary isometric contractions (MVICs) at LML increased markers of acute
170 muscle damage and soreness relative to MVICs at short muscle length (SML) despite lower
171 torque outputs (6). Isometric training at LML produces greater hypertrophy, force production
172 at different joint angles, and dynamic performance benefits compared to training at SML
173 following long-term trials (5, 17, 87, 115, 116, 160). In a recent systematic review into the
174 effects of isometric training variations, Oranchuk et al. (120) determined that isometric
175 training at LML produced greater increases in muscular hypertrophy than volume-equated
7
176 SML training, (0.86-1.69%·week-1, ES·week-1 = 0.03-0.09; and 0.08-0.83%·week-1,
177 ES·week-1 = -0.003-0.07, respectively) (120) likely due to increased mechanical tension
179
181
182 The larger architectural and functional adaptations following LML training might be
183 due, at least in part, to the greater degree of fascicle stretch, which results in increased muscle
184 damage, and sarcomere compliance (6, 27) demonstrated by acute optimal angle shifts
185 towards longer muscle lengths. Although more dramatic following eccentric muscle actions,
186 these angle shifts have also been observed following concentric contractions at long fascicle
187 lengths (58). For example, Guex et al. (59) examined the effect of three weeks of maximal
188 eccentric knee flexions at either LML or SML on fascicle length and optimal angle. While
189 fascicle length increased in both groups (SML, 4.9%, ES = 0.57: and LML; 9.3%, ES = 0.89),
190 the SML group only experienced a shift in the optimal concentric angle (8.8°), whereas the
191 LML group experienced optimal angle shifts in both concentric contractions and eccentric
192 muscle actions (17.3° and 10.7°, respectively) (59). There is evidence to support the principle
193 that mechanical tension can increase muscle volume, and that isometric training at LML leads
195
197 Cumulative tension and total workload are key determinants of hypertrophic
198 adaptation, regardless of contraction type (110). Moore et al. (110) found that changes in
199 torque and muscle thickness were not significantly different between load-matched
200 concentric and eccentric resistance training groups, despite the eccentric group requiring 40%
8
201 fewer contractions to match training load. Morphological adaptations to isometric resistance
202 training are similar between work matched high and low-intensity training (120). While much
203 of the literature recommends high-load over low-load resistance training for strength
204 development (102), many periodization models emphasize muscular hypertrophy and general
205 muscular endurance early in a macro and mesocycles (34, 169). Accordingly, EQI training
206 emphasizing time under tension with the application of practitioner-recommended intensities
207 of 30-80% of 1RM may be a useful training method to alter muscle size.
208
210 Total time under tension, acute hypoxia and metabolic stress are mechanisms that
211 contribute to morphological adaptations (25, 49, 51, 120, 123, 140, 157, 158). Several studies
212 have reported significant reductions in oxygen availability from submaximal isometric
213 contractions at 30-50% of MVC (4, 150). Additionally, blood flow does not appear to
214 decrease linearly with intensity (107). Isometric contractions at 60% of MVIC result in
215 greater short-term blood flow restriction relative to 30% and 100% MVIC, as the moderate
216 intensity contraction could be sustained for a significantly greater duration than 100% while
217 the tension created by the 30% contraction was not enough to reduce blood flow and
218 metabolite clearance (107). These occlusive effects have several potential effects, including
219 increased metabolite build-up and post-contraction blood flow, both of which stimulate
220 muscular hypertrophy (98). Several studies have examined the impact of blood flow
221 restriction on hormones and hypertrophic markers in humans (49, 123, 157, 158). Fujita et al.
222 (49) examined the metabolic and hormonal effects of blood flow restriction during low-
223 intensity resistance training and found 46% greater mTOR regulated muscle protein
224 synthesis, via significantly greater S6K1 phosphorylation markers compared to the exercise-
225 only group. Gentil et al. (51) also found that both isometric contractions and vascular
9
226 occlusion resulted in greater blood lactate responses which can increase muscle cell
227 myogenesis, satellite cell activation and phosphorylation of mTOR and P70SK (113).
228 Additionally, acute ischemia combined with low-intensity muscular contraction can
229 significantly increase growth hormone, IGF-1 and mechano-growth factor production (42),
230 which are physiological responses to decreased muscle and blood pH (123, 157, 158).
231 Occlusion may also help to bypass the size principle by reducing the amount of oxygen
232 available for the oxidative type-1 motor units, resulting in preferential recruitment of fast-
233 twitch fibres at relatively low intensities (111). Long-term morphological adaptations to
234 blood flow restriction training include increased muscle thickness and function in a variety of
236
237 Though sparse, a few studies have examined the effect of blood flow and metabolites
238 during isometric training (37, 140). de Ruiter et al. (37) examined the oxygen consumption
240 LML (60° and 90°) consumed significantly greater quantities of blood oxygen compared to
241 SML contractions (30°) at 10%, 30% and 50% of MVC (37). These findings may, in part,
242 explain why long-term isometric training at LML has a greater effect on muscle thickness and
243 strength, compared to SML training at least in “healthy”, or “recreationally active” subjects
244 (5, 17, 87, 97, 115, 116, 120). Schott, McCully and Rutherford (140) compared the metabolic
245 response and adaptations to short (four sets of 10 x three-second contractions) or long (four
246 contractions of 30 seconds) duration isometric contractions at 70% MVC. Although blood
247 flow was not measured, the long-contraction limbs experienced greater changes in
248 metabolites and larger decreases in pH (140). Muscle thickness also significantly increased in
249 the upper (10.1%) and lower (11.1%) portions of the quadriceps in the long-contraction, but
250 not short-contraction limb (140). Although blood flow restriction has many benefits in older
10
251 and injured populations, it does not appear to offer any additional adaptations in healthy well-
252 trained athletes (141). Furthermore, while low intensity single-joint isometric contractions
253 have been found to result in blood flow restriction, the effects of multi-joint isometric and
255
258 hypertrophy (137), emerging research suggests that exercise-induced muscle damage may
259 play some role in morphological adaptations (138). When exposed to a novel stimulus, acute
260 myofibril micro-trauma occurs as an abundance of Ca2+ enters and remains in the myofibril
261 (35). Eccentric muscle actions typically result in a greater degree of acute trauma as
262 evidenced by elevated serum creatine kinase, myoglobin, and skeletal troponin-1 levels, and
263 delayed onset muscle soreness (32). These markers typically coincide with a temporary
264 reduction in muscle force and power (32). While detrimental to short-term performance,
265 exercise-induced muscle damage is associated with changes in a variety of chemokines that
266 attract inflammatory cells, which influence muscle hypertrophy remodelling associated with
267 phagocytosis, free radical production, and circulating cytokines and growth factors (80).
268 Additionally, a novel delayed onset muscle soreness inducing stimulus may lead to increased
269 sarcoplasmic reticulum re-uptake of Ca2+ by altering t-tubule structure (35) and increasing the
270 concentrations of proteins such as calsequestrin (20) and dysferlin (77). These proteins
271 function to promote debris clearance and increased concentrations of IGF-1, fibroblast
272 growth factor, nerve growth factor, and interleukin-6, which increase satellite cell
273 proliferation (16, 18) and rates of protein and collagen synthesis (76). Although acute
274 increases in myofibril protein synthesis do not necessarily correlate with long-term
11
275 hypertrophy (108), these increased synthesis rates, theoretically result in thicker, stronger
277
278 The repeated bout effect refers to the substantial reduction in muscle damage from
279 subsequent training (105). While most commonly observed following eccentric exercise (45,
280 105), the protective effects have also been found to occur following isometric exercise (2),
281 especially at LML (6, 31). Isometric training at LML results in greater delayed onset muscle
282 soreness and acute performance decrements (6) as well as chronic adaptations, compared to
283 isometrics at SML (5, 87, 115, 116, 120, 160). Likewise, greater exercise-induced muscle
284 damage and delayed onset muscle soreness are reported following maximal effort high-
285 velocity (210°·s-1) isokinetic eccentric muscle actions when compared to an equal volume
286 bout at low-velocity (30°·s-1) (29). As a greater number of high vs. low-velocity eccentric
287 muscle actions are needed to equalize volume, the difference in muscle damage and soreness
288 is likely due to increasing the total number of sarcomere bonds and “popping” sarcomeres,
289 which increase Z-disk streaming and subsequent inflammation (39, 146). Similarly, eight
290 weeks of maximal high-velocity (180°·s-1) eccentric training resulted in greater hypertrophic
291 adaptations when compared to maximal low-velocity (30°·s-1) training (44). Conversely,
292 submaximal (70% 1RM) slow velocity (~3 s) eccentric muscle actions during the barbell
293 bench press have been found to stimulate higher blood lactate and recombinant human
294 growth hormone, by promoting a hypoxic environment (28). While EQIs may lead to
295 substantial levels of local fatigue due to a potential lack of blood flow and high metabolite
296 levels, it is unlikely that the low-velocity eccentric component would produce exercise-
298
12
300 Tendon, the primary tissue of the SEC, can undergo morphological and functional
301 adaptations through inactivity, injury, sporting activities and resistance training (14, 86, 101,
302 127). Tendon and other connective tissues comprised of specifically aligned collagen fibres
303 have significant resistance to mechanical strain (101). Optimal performance requires the
304 efficient transfer of force from muscle to bone (101, 114) necessitating transmission via a
305 tendon that is sufficiently stiff to minimize electromechanical delay while avoiding rupture
306 (101). Properly executed dynamic, eccentric and isometric training can improve tendon
307 structure and function (11, 12, 81, 82, 85, 86, 90, 101, 127).
308
310 A single study has directly investigated the effect of joint angle on tendon
311 morphology by comparing volume-equated isometric knee flexion training at LML (100°) or
312 SML (50°) (87). While both SML (10%, ES = 0.82) and LML (11%, ES = 1.06) groups
313 improved quadriceps volume, only LML training resulted in significant tendon stiffness
314 improvements (50.9%, ES = 1.22) (87). While the sparse results of the preceding studies
315 expose a gap in existing literature, they tend to support holding prolonged isometric
316 contractions at LML with near maximal loads if tendon structural adaptations are paramount.
317
318 The titin myofilament, although thought to be a secondary structure to a tendon in the
319 SEC has several important functions and is likely partly responsible for the residual force
320 enhancement following an active stretch (46, 65, 124, 143-145, 147). Titin adds stability,
321 stiffness and passive and active force transmission at LMLs (64, 125) and is a likely factor in
322 injury prevention. Several studies have found titin to regulate muscle force and length in
323 mechanically lengthened fibres (95, 125). Baumert et al. (19) examined the relationship
324 between force production, delayed onset muscle soreness and genotyping related to titin
13
325 stiffness (19). Subjects with the allele linked to greater titin stiffness (TRIM63 A-allele) had
326 greater MVICs (35%, ES = 1.42, p = 0.006) and recovered more quickly (ES = 1.14 , p =
327 0.022) compared to the other subjects (TRIM63 G-allele) (19). Titin protein fragments have
328 been found in the urine of healthy young males following bouts of a dynamic calf-raise
329 exercise and were strongly correlated with traditional markers of exercise-induced muscle
330 damage (75). While the eccentric muscle action following a fatiguing isometric with EQIs is
331 unlikely to produce significant muscle damage due to low velocities (29), it is plausible that
332 titin may be activated. Although occurring at a range of joint angles (143), residual force
333 enhancement magnitude is greater at LMLs (147), suggesting that LML training may
334 preferentially utilize titin (65). Thus, it may be prudent to examine the effects of quasi-
335 isometric holds in the lengthened position on markers of breakdown and expression of titin.
336
338 The SEC appears to be affected differently by movement velocity. The impact of
339 movement velocity on titin is difficult to determine as many questions remain regarding the
340 myofilaments contributions to phenomena such as residual force enhancement (74, 145).
341 While studies have observed the breakdown of titin following resistance training movements,
342 which tend to be relatively slow when compared to activities such as sprinting or jumping
343 (75), there are conflicting data regarding the velocity of stretch and residual force
344 enhancement. Although the majority of residual force enhancement examinations utilize
345 eccentric angular velocities between 30°.s-1 and 60°.s-1 (46, 124, 144, 147), Lee and Herzog
346 (94) compared stretch angular velocities of 10°.s-1, 20°.s-1 and 60°.s-1. While eccentric force
347 during the stretch increased with velocity, there was no significant difference in proceeding
348 isometric force between the three protocols (94). Though the above research is intriguing as
14
349 the effect of velocity on titin is unknown due to several confounding variables, including
350 different neuromuscular strategies and contributions from the CE and PEC (43, 122).
351
352 The relationship between velocity, residual force enhancement and titin are not yet
353 determined; however, the effect of movement velocity on the tendon holds greater clarity.
354 Acutely, it appears that isometric contractions provide superior analgesic effects compared to
355 dynamic resistance exercise (128, 130, 161). Rio et al. (128), examined patellar tendon pain
356 during a decline squat exercise in six male volleyball players with tendonitis. The pain was
357 evaluated before and after performing either slow isotonic leg extensions for four sets at an
358 8RM load or five sets of 45s isometric knee extensions at 70% of MVIC (128). While both
359 the isometric (-97%, ES = 3.6) and dynamic (-40%, ES = 0.67) groups significantly reduced
360 pain acutely, pain reduction only remained significant at the 45 minutes mark following
361 isometric exercise (128). Loaded between 30% and 80% of 1RM (136, 169), and maintained
362 for similar periods as Rio et al.’s (128-130), the zero to low-velocity EQI contractions may
363 have potential to reduce tendon pain, despite recent controversy (57).
364
365 Long-term changes in tendon morphology seem minimal in healthy, mature human
366 tissue (79, 101). However, injured tendinous tissue can undergo dramatic adaptations (79,
368 mechanical load threshold is reached (61, 62, 70), which likely explains why traditional
369 exercises with an eccentric emphasis have been found to be superior to dynamic contractions
370 in tendon rehabilitation (81, 90, 101). However, movement velocity is critical as healthy
371 tendon fibres will “spare” the damaged tissue by transmitting a greater portion of the load
372 when high velocities are utilized (13, 101). Conversely, damaged tendon tissue can undergo
373 sufficient loading during slow contractions (13, 101). For example, Kongsgaard et al. (81)
15
374 compared 12 weeks of single-leg decline squats with an eccentric emphasis, bilateral heavy
375 and slow (three second eccentric and concentric phases) resistance training, and
376 corticosteroid injections. While both resistance training groups experienced significant
378 markers, the heavy and slow resistance training group reported greater satisfaction of clinical
379 outcomes (70%) compared to the eccentric (42%) group (81). The researchers theorized that
380 the decreased tendon pain, tendon collagen content and voluntary force production was due to
381 the greater intensity-induced mechanical overload throughout the training period (81). These
382 data demonstrate that tendon adaptation can be achieved via relatively slow movement
383 velocities and that maximal or supramaximal eccentric exercise is not necessarily required.
384 As EQI contractions are slow and submaximal, they may be a viable tool for treating diseased
386
388 Contraction intensity, duration and type have different effects on tendon properties.
389 Kubo et al. (84) compared the effects of 12 weeks of isometric and plyometric training on
390 muscle and tendon stiffness. Active muscle stiffness at 30%, 50% and 70% of MVIC only
391 increased significantly following plyometric training (38.1-69.6%, ES = 1.35-2.57 vs. 12.4-
392 23.6%, ES = 0.46-0.75) whereas ballistic and ramp tendon stiffness increased exclusively
393 following isometric training (23.7-42.1%, ES = 0.92-1.21) (84). Likewise, Burgess and
394 colleagues (26) compared the effects of isometric and plyometric training on the plantar
395 flexors. While no statistically significant difference between groups were present (p < 0.05),
396 the isometric group experienced very large increases (61.6%, ES = 4.91) in tendon stiffness
397 when compared to the plyometric group (29.4%, ES = 1.44) (26). Interestingly, no significant
398 differences between the isometric and plyometric groups were apparent for concentric-only
16
399 jump height (64.3%, ES = 2.87 vs. 58.6%, ES = 2.85), or rate of force development (28.1%,
400 ES = 1.89 vs. 14.6%, ES = 1.38); however, no measures of stretch-shortening cycle function
401 were included (26). These findings demonstrate that while isometric contractions are
402 effective in improving tendon stiffness (thereby reducing electromechanical delay) and
403 improving tendon health (14, 128), improvements in stretch-shortening cycle performance
404 likely require specific training to increase ultrasonically assessed elasticity (86-88),
405 suggesting that isometric contractions are an effective addition to traditional resistance
406 training.
407
408 In regards to contraction intensity, Kongsgaard et al. (82) examined the effect of a 12-
409 week, work-equated dynamic isotonic leg extension training program using either “heavy”
410 (70% 1RM) or light loads. The “heavy” group experienced thickening of the distal (4%, p <
411 0.05) and proximal (6%, p < 0.05) patella tendon, whereas the light group only saw
412 significant proximal hypertrophy (7%, p < 0.05) (82). Additionally, tendon stiffness
413 significantly improved following “heavy” resistance training (14.6%, ES = 1.37), whereas the
414 light load group experienced a non-significant decrease (-9.18%, ES = 0.83) (82). Similarly,
415 Arampatizis et al. (11, 12) compared 14-week training programs consisting of volume
416 equated isometric plantar flexion at low (~55% MVIC) or high (~90% MVIC) intensities.
417 Only the high intensity training groups improved Achilles tendon cross-sectional area and
418 stiffness (17.1-36%, ES = 0.82-1.57, p < 0.05. vs. -5.2-7.9%, ES = 0.26-0.37, p > 0.05) (11,
419 12). Furthermore, tendon elasticity only increased following low intensity training (14-
420 16.1%, ES = 0.56-0.84, p > 0.05. vs. -1.4-3.9%, ES = 0.06-0.20, p > 0.05) intensity training
421 (11, 12). Though the aforementioned studies investigated different tendons, and utilized
422 different training intensities, both point to the superiority of high over low-intensity
423 contractions when an improvement in tendon stiffness is desired. While unlikely to directly
17
424 improve plyometric performance, high-intensity isometric training may be a valuable tool in
425 improving tendon thickness and stiffness which may decrease injury rates, and improve
426 performance when included as a supplement to traditional resistance training (26, 84, 86, 88).
427
429 The effect of resistance training on the PEC and extracellular matrix is lacking, due
430 to the methodological challenge of separating connective tissue from intrafibrillar elements to
431 evaluate their relative contributions to force transmission (131). Subjective measures such as
432 pain and ROM are limited in utility, as they contain confounding variables and often manifest
433 gradually (131). However, we do know that the PEC is comprised primarily of collagen fibres
434 (126) and that adding collagen around the myofibrils leads to an increase in stiffness and
435 transmission of force to the passive structures of the extracellular matrix (52). Thus, it is
436 postulated that the increase in extracellular matrix stiffness is a contributing factor to more
438
439 Several studies have examined resistance training and collagen formation in healthy
440 humans (73, 79, 81, 82, 90, 101). In-situ investigations by Mass et al. (103) and Gomez et al.
441 (56) have reported that damaged tendons and ligaments healing under tension had higher
442 collagen contents compared to passively healing controls. It is understood that damaged
443 tendons experience more efficient healing when factors including transforming growth-factor
444 ß1, platelet-derived growth factor, and IGF-1 are elevated (96). Therefore, resistance training,
445 which places a tissue under tension, increases hormonal and molecular signalling factors,
446 providing optimal extracellular matrix maintenance in the elderly (149). Additionally,
447 resistance training can cause exercise-induced muscle damage and increase local
448 inflammation (32, 149). Muscle damage following unaccustomed loading has been observed
18
449 to acutely increase collagen synthesis and extracellular matrix remodelling (72, 156), while
450 chronic resistance training has resulted in increased intramuscular collagen (73).
451 Interestingly, eccentric and concentric contractions appear equally proficient for increasing
452 collagen synthesis when total work is equated (109). However, eccentric muscle actions
453 enable greater force production or greater work performed at the same load (39) and therefore
454 lead to greater adaptation when total sets and repetitions are equal (67).
455
456 In summary, EQI training appears to offer a time and energy efficient means of
458 Therefore, EQI training should be implemented when increasing muscle size and improving
460
463 low, but not high velocities. Although a few acute studies are examining and describing EQI
464 exercise on musculotendinous (24, 99, 150, 152) and neuromuscular adaptations (4, 166), the
465 lack of any long-term investigations makes any definitive conclusions problematic. However,
466 there is a significant amount of research examining fatiguing contractions (107, 135),
467 yielding isometrics (4, 50, 71, 132-134, 136), slow tempo resistance training (159, 170-172,
468 174) and joint angle (37, 115, 116, 135, 154) that allow conjecture and identify areas for
470
472 Contraction intent is an important factor to consider when evaluating the effect of
473 resistance training (33). Although the intent of the trainee during EQIs is to maintain a
19
474 movement velocity of zero, once isometric failure occurs at low velocity, lengthening follows
475 despite maximal effort due to accumulated fatigue (112, 142). Though a variety of isometric
476 training and exercise methods have been described (50, 71, 136), the vast majority of
477 experiments have utilized maximal contractions against an immovable object. While maximal
478 isometrics serve as a valuable and highly reliable means of evaluating neuromuscular
479 function (40, 119), results from these studies are difficult to apply to EQI exercise. Recently,
480 researchers have demonstrated that “yielding” (resisting an external force) isometrics, with
481 the intent of preventing eccentric muscle action, create different fatigue and neuromuscular
483 isometrics (50, 71, 132-134, 136). Hunter et al. (71) compared time to task failure and
484 neuromuscular function when maintaining a constant force (pushing) of 15% of MVIC, or by
485 supporting an equivalent inertial load while maintaining a constant joint angle (holding).
486 Pushing resulted in significantly greater time to failure (1402 ± 728 s) than holding (702 ±
487 582 s) (71). Similarly, Schaefer et al. (136) examined pushing and holding isometric actions
488 at 80% of MVIC and found that subjects could maintain the target force for twice as long
489 when pushing (41 ± 24 s vs. 19 ± 8 s). Hunter et al. (71), Schaefer et al. (136) and other
490 investigators (50, 132-134) have also demonstrated that agonist activation at failure is greater
491 when pushing, while co-activation of antagonist and synergist muscles are greater when
492 holding (50, 132-134, 136). While the increased co-activation during position tasks are a
493 likely cause of the decreased endurance time (50, 71, 133, 136), it is plausible that position
494 task training may lead to superior joint stabilization and thus carry value in rehabilitative
495 settings (132). Additionally, several activities and sporting actions involve bracing to avoid
496 dynamic muscle action (93, 167). Therefore, while pushing isometrics likely allow for greater
497 morphological adaptations, due to larger forces and time under tension, training with the
498 intent to maintain specific positions instead of exerting force against an immovable object
20
499 may provide improved carry over to specific tasks that involve maintaining specific joint
500 angles or postures due to the similarity of neural characteristics (93, 168).
501
502 Ballistic and ramp contractions are additional means of distinguishing movement
503 intent (120). When comparing the result of several isometric training studies directly
504 comparing contraction intents, Oranchuk et al. (120) determined that training with ballistic
505 intent resulted in constantly greater improvements in muscular activation (3/4 studies) (1.04-
506 10.5%·week-1, ES = 0.02-0.31 vs. 1.64-5.53%·week-1, ES·week-1 = 0.03-0.20) and rapid (0-
507 150 ms) force production (3/3 studies) (1.2-13.4%·week-1, ES·week-1 = 0.05-0.61 vs. 1.01-
508 8.13%·week-1, ES·week-1 = 0.06-0.22). Furthermore, Behm and Sale (21) compared the
509 effects of isometric contractions performed with ballistic intent, and high angular velocity
510 (240°.s-1) concentric contractions. Both concentric and isometric training lead to similar (all p
511 < 0.01) improvements in peak isometric force, rate of force development and relaxation and
512 peak torque at 14.9°.s-1, 29.8°.s-1, 59.6°.s-1, 88.8°.s-1, 173°.s-1 and 240°.s-1 (21). These results
513 highlight the importance of contraction intent, and not necessarily movement velocity, on
514 neurological qualities and performance alterations. Although comparing the above results
515 with EQI training is difficult, given that EQIs are non-ballistic, it is reasonable to suggest that
517 progressive resistance training program to improve explosive performance would avoid
518 incorporating EQIs in late training cycles; they may be best positioned early in a periodized
520
522 While research on isometric contraction intensity is emerging, the only long-term
21
524 isometrics. Investigations directly comparing isometric training intensity have determined
525 that little difference in morphological or performance adaptations exist if the total volume is
526 equated (120). While little evidence exists regarding different isometric contraction
527 intensities on neurological adaptations, the wealth of data on dynamic contractions may
528 provide insight. High load dynamic training has been found to increase coordination (162)
529 and reduce neuromuscular inhibition (1), which is valuable when optimal performance is
530 desired (33). Additionally, a significant portion of the existing literature has determined that
531 high-intensity dynamic resistance training is superior for improving neuromuscular function
532 and sports performance when compared to lower intensity methods (33).
533
535 Motor-unit activation and muscle inhibition are strongly affected by the joint angle
536 (114, 135, 154). The strain sensing organelles of the Golgi tendon organ and muscle spindles
537 undergo different levels of stimulation at varying muscle-tendon lengths (114, 135). For
538 example, Suter and Herzog (154) examined muscle inhibition and joint angle by comparing
539 voluntary force and force produced by superimposed femoral nerve stimulation at 15°, 30°,
540 45°, 60° and 90° of knee flexion. While muscle inhibition was present at all assessed joint
541 angles, the largest superimposed twitches were present at LMLs (154). Greater muscular
542 stretch, patellofemoral pressure and ligament strain at knee angles between 45° and 60° of
543 flexion are theorized to underpin the greater degree of muscle inhibition (154); however,
544 these observations are not necessarily applicable for all joints or movements to differing
545 tendon structural properties, fascicle lengths and co-contraction dynamics (8, 22, 60, 78, 92,
546 173). Although muscle inhibition is necessary for extreme situations, improving muscular
547 activity is important when returning to activity or when optimizing performance (33, 114).
548
22
549 Advantages of LML isometric training for improving muscle size and force
550 production throughout a full ROM exist (5, 17, 87, 115, 116, 120, 160). Interestingly, studies
551 investigating the effect of restricted ROM resistance training have determined that limiting
552 dynamic contractions to LML does not result in meaningful changes in the length-tension
553 relationship (164, 165). While EQI contractions utilize a full ROM, they are inherently low
554 velocity. Therefore, EQI training should be implemented early in a yearly training plan to
556
558 Performance
560 methodologies have differing utility and value depending on the type of sport, proximity to
561 competition, individual training age and a multitude of additional factors. With few
562 exceptions (93, 168, 169), quasi-isometric and EQI contractions have not been widely
563 utilized in training plans. However, although no direct investigations on EQI contraction or
564 training exist, relevant research, (e.g. isometric, eccentric, time under tension, blood flow
565 restriction) suggest that EQIs may have a place in intelligently designed programs. The
566 theoretical potential of EQIs in relation to dynamic (eccentric and concentric), eccentric only
567 and isometric resistance training are summarized in Table 1 (based on (153)).
568
570
572 A systematic increase in the exposure to the total volume that a muscle or muscle-
573 group undergoes is a common means of improving muscular endurance (83, 169). Training
23
574 with EQIs may have the potential to provide a unique stimulus for promoting muscular
575 endurance, as a primary aim is to increase the amount of time that the prescribed position is
577 commonly employed to improve muscular endurance, the constant muscular tension present
578 in isometric and quasi-isometric contractions can alter blood flow and muscle oxygenation (4,
579 150). Although far from conclusive, this mild, and temporary alteration in oxygenation may
580 lead to alterations in aerobic and anaerobic enzymes and significant, yet temporary increases
581 in several anabolic signalling factors (111, 158). Furthermore, muscular endurance training
582 may lead to adaptations to the t-tubule structure and increase Ca2+ re-uptake (35), therefore
583 offering a protective effect from delayed onset muscle soreness and short-term performance
584 decrements that may occur from future high-load training (30, 31).
585
586 Eccentric quasi-isometric training may also offer a novel sport-specific training
587 stimulus to athletes that undergo regular, sustained quasi-isometric contractions. While actual
588 sports participation offers the greatest level of sport-specific adaptation, utilizing quasi-
589 isometric or EQI contractions in a controlled environment such, as a weight-room, offers the
590 ability to apply focused overload. For example, a speed skater wishing to increase lower-
591 body muscular endurance in a skating specific ROM, via morphological adaptations, may
592 wish to experiment with quasi-isometric or EQI training by utilizing a leg-press (Figure 3).
593
595
596 Hypertrophy
597 Muscle mass is highly related to strength (53) and is, therefore, an important factor in
598 sports performance. While heavy loading, including supra-maximal eccentric training, offers
24
599 a strong stimulus, total work and training volume are the most important determinants of
600 hypertrophic adaptation (91, 110, 137, 139). While moderate resistance training allows for a
602 circumstances. Depending on the intensity, initial joint angle and other factors, EQI
603 contractions can expose a muscle group to substantial total load in a relatively short period.
604 Eccentric quasi-isometric contractions also offer a likely advantage over dynamic training
605 when it comes to accumulating volume as shortening contractions are less energetically and
606 mechanically efficient (110). While a non-linear, inverse relationship exists between intensity
607 and time under tension (83, 169), exclusion of the less efficient concentric phase allows for
608 higher intensities for throughout a set duration, or more work at the same intensities (38,
609 110). Therefore, a single EQI contraction would likely impart greater time under tension than
610 a similarly loaded set of dynamic contractions when both are taken to failure. Likewise,
611 similar set durations could be met with a greater external load applied to an EQI contraction
612 compared to a dynamic alternative. Additionally, EQIs are likely to reduce muscle
613 oxygenation and metabolite clearance (4, 150) which may lead to preferential recruitment of
614 type-II muscle fibres with increased capacity to increase cross-sectional area and force
615 production, and signal anabolic hormones known to contribute to the hypertrophic response
617
619 A variety of morphological and neurological factors including muscle size, muscle
620 fiber type and motor-unit recruitment characteristics determine strength and power (7, 33, 34,
621 38, 43, 48, 93, 114, 153, 163, 172, 175). While EQI contractions may be a viable tool for
622 improving total hypertrophy, an abundance of evidence supports the use of high-velocity
623 contractions and maximal to supra-maximal loads for preferentially targeting type-II muscle
25
624 fibers (48, 121). From a neurological perspective, the ability to express maximal force and
625 power is contingent on several factors. While isometric and eccentric resistance training can
626 lead to the neurological and neuromuscular adaptations of rate-coding, agonist, antagonist
627 and synergist activation and co-activation, the adaptations above are highly specific (1). As
628 EQI contractions are inherently submaximal and intentionally low-velocity, it is likely that
629 direct carry over to high threshold activities would be minimal. However, the slow, relatively
630 high accumulated loading synonymous with EQI contractions, may potentially lead to
631 improved rates of collagen synthesis and stiffness of the SEC and PEC (81, 90, 101). There is
632 reason to believe that these morphological adaptations may improve force transmission by
633 decreasing the electromechanical delay, therefore improving the rate of force development
634 and stretch-shortening cycle function (52, 101). Quasi-isometric and EQI contractions are
635 postulated to build position-specific strength and potentially reduce injury risk (167, 168).
636 Verkhoshansky and Siff (169), described weightlifters utilizing EQI training to strengthen
637 key positions in their weightlifting pulls. For example, a weightlifter who struggles to
638 maintain an ideal position throughout the “first pull” (151) may wish to experiment with EQI
640
642
643 Rehabilitation
644 Injuries to any of the three components of force transmission require mechanical
645 overload at some point in the rehabilitation process (101). Isometric and quasi-isometric
646 exercises are already commonplace in the initial phases of muscular and tendon rehabilitation
647 protocols as they enable tight control over ROM and intensity (54, 83, 128-130, 161).
648 Sustained submaximal isometric contractions avoid large peak forces and acutely reduce
26
649 tendon pain, potentially allowing for periods of pain-free dynamic exercise (129, 130, 161).
650 Furthermore, while progressive mechanical tension is crucial (79, 81), slow movement
651 velocities should be prescribed to stimulate damaged fibers (13). Therefore, the combined
652 static and lengthening phases of EQI contractions may provide an analgesic effect while
653 stimulating connective tissue reformation. In the case of serious injuries, such as bone
654 fractures or severe connective tissue strains, patients may undergo a period of full or partial
655 immobilization. These periods of immobilization often result in significant muscle atrophy
656 and fascicle shortening (155). Eccentric quasi-isometric exercise may offer a submaximal
657 means of improving tendon morphology, work capacity, muscle thickness, and
658 neuromuscular function while returning fascicles to a normal length (101). Eccentric quasi-
659 isometric contractions can be performed with a wide range of loads and can be easily
660 implemented through a specific ROM. For example, a patient may experiment with EQI
661 contractions by performing an EQI elbow flexion, with the torso inclined, until the elbow
662 reaches the end ROM (Figure 4). At this point, a second EQI with a focus on the shoulder
663 flexors can be initiated to impart further mechanical loading, metabolic stress to the target
664 tissues (Figure 5). While currently highly speculative, a hypothetical training plan including
665 EQIs for an athlete recovering from patellar tendonitis is provided in table 2.
666
669
670 Limitations
671 Due to the lack of any long-term investigations regarding EQI or quasi-isometric
672 resistance training, limitations are abundant in this review. Like many methods of resistance
673 training, EQIs can be applied with an endless combination of variables including intensity,
27
674 contraction duration, repetitions, sets, rest periods, frequencies and exercise selection. Any
675 adjustment to the aforementioned parameters will alter the resemblance of EQI to traditional
676 methods. Similarly, much is left to be determined regarding established training methods
677 such as isometrics. For example, while the characteristics of “pushing” and “holding”
678 isometric contractions differ (50, 71, 132-134, 136), there is a paucity of research examining
679 long-term consequences to such altered loading parameters. Researchers and practitioners
680 need to progress the knowledge and understanding of the acute and short-term
681 neuromuscular, biomechanical and metabolic effects of quasi-isometric and EQI contractions
682 (50, 71, 132-134, 136). Furthermore, long-term investigations are needed to compare the
684
686 It is common for “novel” training methods to precede evidence-based practice. While
687 there are limited data on long-term adaptations, short-term investigations, anecdotal evidence
688 and relevant scientific knowledge make a strong case for the investigation of EQI loading and
689 training. Based on the existing literature, the value of EQIs appears to relate most strongly to
690 triggering morphological rather that neuromuscular adaptations and are likely best applied
691 early in a periodized training plan, distal to high threshold neuromuscular work. Quasi-
692 isometric and EQI training may also hold value in pre and rehabilitation contexts to modify
693 muscle-tendon structures, provide analgesic effects, and closely match functional movements
694 from a neurological perspective. Finally, EQIs appear to have the potential to provide an
695 efficient means of increasing total load and volumes in specific positions.
696
697 Examination of EQI muscle actions and training are required due to the complete lack
698 of direct empirical evidence investigating this area. As such, several foci for potential
28
699 research exist. From an acute standpoint, EQI contractions may involve unique
700 neuromuscular activation and muscular contraction dynamics that would be worthy of
701 investigation. Researchers may also wish to compare the short-term effects of EQI exercise
702 with volume equated modalities such as dynamic or isokinetic contractions on neuromuscular
703 fatigue, delayed onset muscle soreness or the repeated bout effect. Furthermore, long-term
704 training studies are required to determine optimal loading parameters and exercise selection,
706
707 References
708 1. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Halkjaer-Kristensen J, and
709 Dyhre-Poulsen P. Neural inhibition during maximal eccentric and concentric
710 quadriceps contraction: Effects of resistance training. J Appl Physiol 89: 2249-2257,
711 2000.
712 2. Abdulaziz A, McGuigan MR, and Nosaka K. Less indication of muscle damage in the
713 second than initial electrical muscle stimulation bout consisting of isometric
714 contractions of the knee extensors. Eur J Appl Physiol 108: 709-717, 2010.
715 3. Abe T, Fukashiro S, Harada Y, and Kawamoto K. Relationship between sprint
716 performance and muscle fascicle length in female sprinters. J Physiol Anthropol 20:
717 141-147, 2001.
718 4. Akima H and Ryosuke A. Oxygenation and neuromuscular activation of the
719 quadriceps femoris including the vastus intermedius during a fatiguing contraction.
720 Clin Physiol Funct Imaging 37: 750-758, 2017.
721 5. Alegre LM, Ferri-Morales A, Rodriguez-Casares R, and Aguado X. Effects of
722 isometric training on the knee extensor moment–angle relationship and vastus lateralis
723 muscle architecture. Eur J Appl Physiol 114: 2437-2446, 2014.
724 6. Allen TJ, Jones T, Tsay A, Morgan DL, and Proske U. Muscle damage produced by
725 isometric contractions in human elbow flexors. J Appl Physiol 124: 388-399, 2018.
726 7. Ando R, Saito A, Umemura Y, and Akima H. Local architecture of the vastus
727 intermedius is a better predictor of knee extension force than that of the other
728 quadriceps femoris muscle heads. Clin Physiol Funct Imaging 35: 376-382, 2014.
729 8. Andrade RJ, Lacourpaille L, Freitas SR, McNair PJ, and Nordez A. Effects of hip and
730 head position on ankle range of motion, ankle passive torque, and passive
731 gastrocnemius tension. Scand J Med Sci Sports 26: 41-47, 2016.
732 9. Antonio J and Gonyea WJ. Progressive stretch overload of skeletal muscle results in
733 hypertrophy before hyperplasia. J Appl Physiol 75: 1263-1271, 1993.
734 10. Apostolopoulos N, Metsios GS, Flouris AD, Koutedakis Y, and Wyon MA. The
735 relevance of stretch intensity and position-A systematic review. Front Psychol 6: 1-
736 25, 2015.
737 11. Arampatzis A, Karamanidis K, and Albracht K. Adaptational responses of the human
738 Achilles tendon by modulation of the applied cyclic strain magnitude. J Exp Biol 210:
739 2743-2753, 2007.
29
740 12. Arampatzis A, Peper A, Bierbaum S, and Albracht K. Plasticity of human Achilles
741 tendon mechanical and morphological properties in response to cyclic strain. J
742 Biomech 43: 3073-3079, 2010.
743 13. Arnoczky SP, Lavagnino M, and Egerbacher M. The mechanobiological
744 aetiopathogenesis of tendinopathy: Is it the over-stimulation or the under-stimulation
745 of tendon cells? Int J Exp Pathol 88: 217-226, 2007.
746 14. Arya S and Kulig K. Tendinopathy alters mechanical and material properties of the
747 Achilles tendon. J Appl Physiol 108: 670-675, 2010.
748 15. Ashida Y, Himori K, Tatehayashi D, Yamada R, Ogasawara R, and Yamada T.
749 Effects of contraction mode and stimulation frequency on electrical stimulation-
750 induced skeletal muscle hypertrophy. J Appl Physiol 124: 341-348, 2017.
751 16. Bamman MM, Shipp JR, Jaing J, Gower BA, Hunter GR, Goodman A, and
752 McLafferty CL. Mechanical load increased muscle IGF-I and androgen receptor
753 mRNA concentrations in humans. Am J Physiol 280: E383-E390, 2001.
754 17. Bandy WD and Hanten WP. Changes in torque and electromyographic activity of the
755 quadriceps femoris muscles following isometric training. Phys Ther 73: 455-465,
756 1993.
757 18. Barton-Davis ER, Shoturma DI, and Sweeney HL. Contribution of satellite cells to
758 IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 167: 301-305,
759 1999.
760 19. Baumert P, Lake MJ, Drust B, Stewart C, and Erskine RM. TRIM63 (MuRF-1) gene
761 polymorphism is associated with biomarkers of exercise-induced muscle damage.
762 Physiol Genomics 50: 142-143, 2017.
763 20. Beard NA, Laver DR, and Dulhunty AF. Calsequestrin and the calcium release
764 channel of skeletal and cardiac muscle. Prog Biophys Mol Biol 85: 33-69, 2004.
765 21. Behm DG and Sale DG. Intended rather than actual movement velocity determines
766 velocity-specific training response. J Appl Physiol 74: 359-368, 1993.
767 22. Billot M, Simoneau EM, Ballay Y, Van Hoecke J, and Martin A. How the ankle joint
768 angle alters the antagonist and agonist torques during maximal efforts in dorsi- and
769 plantar flexion. Scand J Med Sci Sports 21: 273-281, 2011.
770 23. Blazevich AJ, Coleman DR, Horne S, and Cannavan D. Anatomical predictors of
771 maximum isometric and concentric knee extensor moment. Eur J Appl Physiol 105:
772 869-878, 2009.
773 24. Bojsen-Moller J, Larsson B, and Aagaard P. Physical requirements in Olympic
774 sailing. Eur J Sport Sci 15: 220-227, 2015.
775 25. Burd NA, Andrews RJ, West DW, Little JP, Cochran AJ, Hector AJ, Cashaback JG,
776 Gibala MJ, Potvin JR, Baker SK, and Phillips SM. Muscle time under tension during
777 resistance exercise stimulates differential muscle protein sub-fractional synthetic
778 responses in men. J Physiol 590: 351-362, 2012.
779 26. Burgess KE, Connik MJ, Graham-Smith P, and Pearson SJ. Plyometric vs isometric
780 training influences on tendon propertied and muscle output. J Strength Cond Res 21:
781 986-989, 2007.
782 27. Butterfield TA and Herzog W. Is the force-length relationship a useful indicator of
783 contractile element damage following eccentric exercise? J Biomech 38: 1932-1937,
784 2005.
785 28. Calixto RD, Verlengia R, Crisp AH, Carvalho TB, Crepaldi MD, Pereira AA,
786 Yamada AK, da Mota GR, and Lopes CR. Acute effects of movement velocity on
787 blood lactate and growth hormone responses after eccentric bench press exercise in
788 resistance-trained men. Biol Sport 31: 289-294, 2014.
30
789 29. Chapman D, Newton M, Sacco P, and Nosaka K. Greater muscle damage induced by
790 fast versus slow velocity eccentric exercise. Int J Sports Med 27: 591-598, 2006.
791 30. Chen H, Nosaka K, Pearce A, and Chen TC. Two maximal isometric contractions
792 attenuate the magnitude of eccentric exercise-induced muscle damage. Appl Physiol
793 Nutr Metab 37: 680-689, 2012.
794 31. Chen TC, Lin MJ, Chen HL, Lai JH, Yu HI, and Nosaka K. Muscle damage
795 protective effect by two maximal isometric contractions on maximal eccentric
796 exercise of the elbow flexors of the contralateral arm. Scand J Med Sci Sports 28:
797 1354-1360, 2018.
798 32. Clarkson PM, Nosaka K, and Braun B. Muscle function after exercise-induced muscle
799 damage and rapid adaptation. Med Sci Sports Exerc 24: 512-520, 1992.
800 33. Cormie P, McGuigan MR, and Newton RU. Developing maximal neuromuscular
801 power: Part 1 - Biological basis of maximal power production. Sports Med 41: 17-38,
802 2011.
803 34. Cormie P, McGuigan MR, and Newton RU. Developing maximal neuromuscular
804 power: Part 2 - Training considerations for improving maximal power production.
805 Sports Med 41: 125-146, 2011.
806 35. Cully TR, Murphy RM, Roberts L, Truls R, Fassett RG, Coombes JS, Jayasinghe ID,
807 and Launikonis BS. Human skeletal muscle plasmalemma alters its structure to
808 change its Ca2+ handling following heavy-load resistance exercise. Nat Commun 8: 1-
809 10, 2016.
810 36. Dankel SJ, Buckner SL, Jessee MB, Grant Mouser J, Mattocks KT, Abe T, and
811 Loenneke JP. Correlations do not show cause and effect: Not even for changes in
812 muscle size and strength. Sports Med 48: 1-6, 2018.
813 37. de Ruiter CJ, de Boer MD, Spanjaard M, and de Haan A. Knee angle-dependent
814 oxygen consumption during isometric contractions of the knee extensors determined
815 with near-infrared spectroscopy. J Appl Physiol 99: 579-586, 2005.
816 38. Douglas J, Pearson S, Angus R, and McGuigan M. Chronic adaptations to eccentric
817 training: A systematic Review. Sports Med 47: 917-941, 2017.
818 39. Douglas J, Pearson S, Ross A, and McGuigan M. Eccentric exercise: Physiologicaly
819 characteristics and acute responses. Sports Med 47: 663-675, 2017.
820 40. Drake D, Kennedy R, and Wallace E. The validity and responsiveness of isometric
821 lower body multi-joint tests of muscular strength: A systematic review. Sports Med 3:
822 1-11, 2017.
823 41. DuVall MM, Gifford JL, Amrein M, and Herzog W. Altered mechanical properties of
824 titin immunoglobulin domain 27 in the presence of calcium. Eur Biophys J 42: 301-
825 307, 2013.
826 42. Ehrnborg C and Rosen T. Physiological and pharmacological basis for the ergogenic
827 effects of growth hormone in elite sports. Asian J Androl 10: 373-383, 2008.
828 43. Enoka RM and Duchateau J. Rate coding and the control of muscle force. Cold Spring
829 Harb Perspect Med 7: pii: a029702, 2017.
830 44. Farthing JP and Chilibeck PD. The effects of eccentric and concentric training at
831 different velocities on muscle hypertrophy. Eur J Appl Physiol 89: 578-586, 2003.
832 45. Fernandez-Gonzalo R, Bresciani G, Souza-Teixeira Fd, Hernandez-Murua JA,
833 Jimenez-Jimenez R, Gonzalez-Gallego J, and de Paz JA. Effects of a 4-week eccentric
834 training program on the repeated bout effect in young active women. J Sports Sci Med
835 10: 692-699, 2011.
836 46. Fortuna R, Power GA, Mende E, Seiberl W, and Herzog W. Residual force
837 enhancement following shortening is speed-dependent. Sci Rep 6, 2016.
31
838 47. Fritz CO, Morris PE, and Richler JJ. Effect size estimates: Current use, calculations,
839 and interpretation. J Exp Psychol Gen 141: 2-18, 2012.
840 48. Fry AC, Schilling BK, Staron RS, Hagerman FC, Hikida RS, and Thrush JT. Muscle
841 fiber characteristics and performance correlates of male Olympic-style weightlifters. J
842 Strength Cond Res 17: 746-754, 2003.
843 49. Fujita S, Abe T, Drummond MJ, Cadenas JG, Dreyer HC, Sato Y, Volpi E, and
844 Rasmussen BB. Blood flow restriction during low-intensity resistance exercise
845 increases S6K1 phosphorylation and muscle protein synthesis. J Appl Physiol 103:
846 903-910, 2007.
847 50. Garner JC, Blackburn T, Wiemar W, and Campbell B. Comparison of
848 electromyographic activity during eccentrically versus concentrically loaded isometric
849 contractions. J Electromyogr Kinesiol 18: 466-471, 2008.
850 51. Gentil P, Oliveira E, and Bottaro M. Time under tension and blood lactate response
851 during four different resistance training methods. J Physiol Anthropol 25: 339-344,
852 2006.
853 52. Gillies AR and Lieber RL. Structure and function of the skeletal muscle extracellular
854 matrix. Muscle Nerve 44: 318-311, 2011.
855 53. Gilliver SF, Degens H, Rittweger J, Sargeant AJ, and Jones DA. Variation in the
856 determinants of power of chemically skinned human muscle fibres. Exp Physiol 94:
857 1070-1078, 2009.
858 54. Goldman RJ, Reinbold KA, Iglarsh ZA, Neustadter LM, Oatis CA, and Schumacher
859 HR. Phase I design and evaluation of an isometric muscle reeducation device for knee
860 osteoarthritis rehabilitation. J Rehabil Res Dev 40: 95-107, 2003.
861 55. Goldspink G, Scutt A, Martindale J, Jaenicke T, Turay L, and Gerlach GF. Stretch
862 and force generation induce rapid hypertrophy and myosin isoform gene switching in
863 adult skeletal muscle. Biochem Soc Trans 19: 368-373, 1991.
864 56. Gomez MA, Woo SL, Amiel D, Harwood F, Kitabayashi L, and Matyas JR. The
865 effects of increased tension on medial collateral ligaments. Am J Sports Med 19: 347-
866 354, 1991.
867 57. Gravare Silbernagel K, Vicenzio BT, Rathleff MS, and Thorborg K. Isometric
868 exercise for acute pain relief: is it relevant in tendinopathy management? Br J Sports
869 Med Ahead of print, 2019.
870 58. Guex K, Degache F, Gremion G, and Millet GP. Effect of hip flexion angle on
871 hamstring optimum length after a single set of concentric contractions. J Sports Sci
872 31: 1545-1552, 2013.
873 59. Guex K, Degache F, Morisod C, Sailly M, and Millet GP. Hamstring architectural and
874 functional adaptations following long vs. short muscle length eccentric training. Front
875 Physiol 7: 1-9, 2016.
876 60. Hahn D, Olvermann M, Richtberg J, Seiberl W, and Schwirtz A. Knee and ankle joint
877 torque-angle relationships of multi-joint leg extension. J Biomech 44: 2059-2065,
878 2011.
879 61. Heinemeier KM, Olesen JL, Haddad F, Langberg H, Kjaer M, Baldwin KM, and
880 Schjerling P. Expression of collagen and related growth factors in rat tendon and
881 skeletal muscle in response to specific contraction types. J Physiol 582: 1303-1316,
882 2007.
883 62. Heinemeier KM, Olesen JL, Schjerling P, Haddad F, Langberg H, Baldwin KM, and
884 Kjaer M. Short-term strength training and the expression of myostatin and IGF-1
885 isoforms in rat muscle and tendon: Differential effects of specific contraction types. J
886 Appl Physiol 102: 573-581, 2007.
32
887 63. Herda TJ, Costa PB, Walter AA, Ryan ED, and Cramer JT. The time course of the
888 effects of constant‐angle and constant‐torque stretching on the muscle–tendon unit.
889 Scand J Med Sci Sports 24: 62-67, 2012.
890 64. Herzog W, Duvall M, and Leonard TR. Molecular mechanisms of muscle force
891 regulation: A role for titin? Exerc Sport Sci Rev 40: 50-57, 2012.
892 65. Herzog W, Schappacher G, DuVall M, Leonard TR, and Herzog JA. Residual force
893 enhancements following eccentric contractions: A new mechanism involving titin.
894 Physiology 31: 300-312, 2016.
895 66. Hoffman BW, Lichtwark GA, Carroll TJ, and Cresswell AG. A comparison of two
896 Hill-type skeletal muscle models on the construction of medial gastrocnemius length-
897 tension curves in humans in vivo. J Appl Physiol 113: 90-96, 2012.
898 67. Holm L, Rahbek SK, Farup J, Vendelbo MH, and Vissing K. Contraction mode and
899 whey protein intake affect the synthesis rate of intramuscular connective tissue.
900 Muscle Nerve 55: 128-130, 2017.
901 68. Horowits R. Passive force generation and titin isoforms in mammalian skeletal
902 muscle. Biophys J 61: 392-396, 1992.
903 69. Huijing PA. Muscular force transmission: A unified, dual or multiple system? A
904 review and some explorative experimental results. Arch Physiol Biochem 107: 292-
905 311, 1999.
906 70. Huijing PA. Epimuscular myofascial force transmission: A historical review and
907 implications for new research. J Biomech 42: 9-21, 2009.
908 71. Hunter SK, Ryan DL, Ortega JD, and Enoka RM. Task differences with the same load
909 torque alter the endurance time of submaximal fatiguing contractions in humans. J
910 Neurophysiol 88: 3087-3096, 2002.
911 72. Hyldahl RD, Nelson B, Xin L, Welling T, Groscot L, Hubal MJ, and Parcell AC.
912 Extracellular matrix remodeling and its contribution to protective adaptation
913 following lengthening contractions in human muscle. FASEB J 29: 2894-2904, 2015.
914 73. Jakobsen JR, Mackey AL, Knudsen AB, Koch M, Kjaer M, and Krogsgaard MR.
915 Composition and adaptation of human myotendinous junction and neighboring
916 muscle fibers to heavy resistance training. Scand J Med Sci Sports 27: 1547-1559,
917 2017.
918 74. Joumaa V, Rassier DE, Leonard TR, and Herzog W. The origin of passive force
919 enhancement in skeletal muscle. Am J Physiol 294: C74-78, 2008.
920 75. Kanda K, Sakuma J, Akimoto T, Kawakami Y, and Suzuki K. Detection of titin
921 fragments in urine in response to exercise-induced muscle damage. PLoS One 12:
922 e0181623, 2017.
923 76. Kasemkijwattana C, Menetrey J, Bosch P, Somogyi G, Moreland MS, Fu FH,
924 Buranapanitkit B, Watkins SS, and Huard J. Use of growth factors to improve muscle
925 healing after strain injury. Clin Orthop Relat Res 370: 272-285, 2000.
926 77. Kerr JP, Ward CW, and Bloch RJ. Dysferlin at transverse tubules regulates Ca2+
927 homeostasis in skeletal muscle. Front Physiol 5: 1-5, 2014.
928 78. Kim DH, Lee JH, Yu SM, and An CM. The effect of ankle position on torque and
929 muscle activity of the knee extensor during maximal isometric contraction. J Sport
930 Rehabil Ahead of print, 2019.
931 79. Kjaer M and Heinemeier KM. Eccentric exercise: Acute and chronic effects on
932 healthy and diseased tendons. J Appl Physiol 116: 1435-1438, 2014.
933 80. Koh TJ and Pizza FX. Do inflammatory cells influence skeletal muscle hypertrophy?
934 Front Biosci 1: 60-71, 2009.
935 81. Kongsgaard M, Kovanen V, Aagaard P, Doessing S, Hansen P, Laursen AH, Kaldau
936 NC, Kjaer M, and Magnusson SP. Corticosteroid injections, eccentric decline squat
33
937 training and heavy slow resistance training in patellar tendinopathy. Scand J Med Sci
938 Sports 19: 790-802, 2009.
939 82. Kongsgaard M, Reitelseder S, Pederson TG, Holm L, Aagaard P, Kjaer M, and
940 Magnusson SP. Region specific patellar tendon hypertrophy in humans following
941 resistance training. Acta Physiol Scand 191: 111-121, 2007.
942 83. Kraemer WJ, Duncan ND, and Volek JS. Resistance training and elite athletes:
943 Adaptations and program considerations. J Orthop Sports Phys Ther 28: 110-119,
944 1998.
945 84. Kubo K, Ishigaki T, and Ikebukuro T. Effects of plyometric and isometric training on
946 muscle and tendon stiffness in vivo. Physiol Rep 5: 1-13, 2017.
947 85. Kubo K, Kanehisa H, and Fukunaga T. Effects of different duration isometric
948 contractions on tendon elasticity in human quadriceps muscles. J Physiol 536: 649-
949 655, 2001.
950 86. Kubo K, Morimoto M, Komuro T, Yata H, Tsunoda N, Kanehisa H, and Fukunaga T.
951 Effects of plyometric and weight training on muscle-tendon complex and jump
952 performance. Med Sci Sports Exerc 39: 1801-1810, 2007.
953 87. Kubo K, Ohgo K, Takeishi R, Yoshinaga K, Tsunoda N, Kanehisa H, and Fukunaga
954 T. Effects of isometric training at different knee angles on the muscle–tendon
955 complex in vivo. Scand J Med Sci Sports 16: 159-167, 2006.
956 88. Kubo K, Yata H, Kanehisa H, and Fukunaga T. Effects of isometric squat training on
957 the tendon stiffness and jump performance. Eur J Appl Physiol 96: 305-314, 2006.
958 89. Kumagi A, Abe T, Brechue WF, Ryushi T, Takano S, and Mizuno M. Sprint
959 performance is related to muscle fascicle length in male 100-m sprinters. J Appl
960 Physiol 88: 811-816, 2000.
961 90. Langberg H, Ellingsgaard H, Madsen T, Jansson J, Magnusson S, Aagaard P, and
962 Kjaer M. Eccentric rehabilitation exercise increases peritendinous type I collagen
963 synthesis in humans with Achilles tendinosis. Scand J Med Sci Sports 17: 61-66,
964 2006.
965 91. Lasevicius T, Ugrinowitsch C, Schoenfeld BJ, Roschel H, Tavares LD, De Souza EO,
966 Laurentino G, and Tricoli V. Effects of different intensities of resistance training with
967 equated volume load on muscle strength and hypertrophy. Eur J Sport Sci 18: 772-
968 780, 2018.
969 92. Lauber B, Lichtwark GA, and Cresswell AG. Reciprocal activation of gastrocnemius
970 and soleus motor units is associated with fascicle length change during knee flexion.
971 Physiol Rep 2: e12044, 2014.
972 93. Lee B and McGill SM. Effect of long-term isometric training on core/torso stiffness. J
973 Strength Cond Res 29: 1515-1526, 2015.
974 94. Lee H-D and Herzog W. Force enhancement following muscle stretch of electrically
975 stimulated and voluntarily activated human adductor pollicis. J Physiol 545: 321-330,
976 2002.
977 95. Leonard TR and Herzog W. Regulation of muscle force in the absence of actin-
978 myosin-based cross-bridge interaction. Am J Physiol 299: C14-C20, 2010.
979 96. Lie SH, Yang RS, Al-Shiakh R, and Lane JM. Collagen in tendon, ligament, and bone
980 healing: A current review. Clin Orthop Relat Res 318: 265-278, 1995.
981 97. Lindh M. Increase of muscle strength from isometric quadriceps exercises at different
982 knee angles. Scand J Rehabil Med 11: 33-36, 1979.
983 98. Loenneke JP, Wilson JM, Marin PJ, Zourdos MC, and Bemben MG. Low intensity
984 blood flow restriction training: A meta-analysis. Eur J Appl Physiol 112: 1849-1859,
985 2012.
34
986 99. Louis J, Billaut F, Vettoretti F, Hausswirth C, and Brisswalter J. Physiological
987 demands of a simulated BMX competition. Int J Sports Med 34: 491-496, 2013.
988 100. Maeo S, Yoshitake Y, Takai Y, Fukunaga T, and Kanehisa H. Neuromuscular
989 adaptations following 12-week maximal voluntary co-contraction training. Eur J Appl
990 Physiol 114: 663-673, 2014.
991 101. Magnusson PS and Kjaer M. The impact of loading, unloading, ageing and injury on
992 the human tendon. J Physiol Ahead of print, 2018.
993 102. Mangine GT, Hoffman JR, Wang R, Gonzalez AM, Townsend JR, Wells AJ, Jajtner
994 AR, Beyer KS, Boone CH, Miramonti AA, LaMonica MB, Fukuda DH, Ratamess
995 NA, and Stout JR. Resistance training intensity and volume affect changes in rate of
996 force development in resistance-trained men. Eur J Appl Physiol 116: 2367-2374,
997 2016.
998 103. Mass DP, Tuel RJ, Labarbera M, and Greenwold DP. Effects of constant mechanical
999 tension on the healing of rabbit flexor tendons. Clin Orthop Relat Res 296: 301-306,
1000 1993.
1001 104. Mass H and Sandercock TG. Force transmission between synergistic skeletal muscles
1002 through connective tissue linkages. J Biomed Biotechnol 2010: 9, 2010.
1003 105. McHugh M, Connolly DAJ, Eston RG, and Gleim GW. Exercise-induced muscle
1004 damage and the potential mechanisms for the repeated bout effect. Sports Med 27:
1005 157-170, 1999.
1006 106. McMahon GE, Morse CI, Burden A, Winwood K, and Onambele GL. Impact of range
1007 of motion during ecologically valid resistance training protocols on muscle size,
1008 subcutaneous fat, and strength. J Strength Cond Res 28: 245-255, 2014.
1009 107. McNeil CJ, Allen MD, Olympico E, Shoemaker JK, and Rice CL. Blood flow and
1010 muscle oxygenation during low, moderate, and maximal sustained isometric
1011 contractions. Am J Physiol 309: R475-R481, 2015.
1012 108. Mitchell CJ, Churchward-Venne TA, Parise G, Bellamy L, Baker SK, Smith K,
1013 Atherton PJ, and Phillips SM. Acute post-exercise myofibrillar protein synthesis is
1014 not correlated with resistance training-induced muscle hypertrophy in young men.
1015 PLoS One 9: e89431, 2014.
1016 109. Moore DR, Phillips SM, Babraj JA, Smith K, and Rennie MJ. Myofibrillar and
1017 collagen protein synthesis in human skeletal muscle in young men after maximal
1018 shortening and lengthening contractions. Am J Physiol 288: E1153-E1159, 2005.
1019 110. Moore DR, Young M, and Phillips SM. Similar increases in muscle size and strength
1020 in young men after training with maximal shortening or lengthening contractions
1021 when matched for total work. Eur J Appl Physiol 112: 1587-1592, 2012.
1022 111. Moritani T, Sherman WM, Shibata M, Matsumoto T, and Shinohara M. Oxygen
1023 availability and motor unit activity in humans. Eur J Appl Physiol Occup Physiol 64:
1024 552-556, 1986.
1025 112. Morrison N. QI: The Russian training secret. Testosterone Nation, 2016.
1026 113. Nalbandian M and Takeda M. Lactate as a signaling molecule that regulates exercise-
1027 induced adaptations. Biology 5: E38, 2016.
1028 114. Nigg BM and Herzog W. Biomechanics of the Musculo-skeletal System. Wiley, 2007.
1029 115. Noorkoiv M, Nosaka K, and Blazevich AJ. Neuromuscular adaptations associated
1030 with knee joint angle-specific force change. Med Sci Sports Exerc 46: 1525-1537,
1031 2014.
1032 116. Noorkoiv M, Nosaka K, and Blazevich AJ. Effects of isometric quadriceps strength
1033 training at different muscle lengths on dynamic torque production. J Sports Sci 33:
1034 1952-1961, 2015.
35
1035 117. Nuzzo JL, Finn HT, and Herbert RD. Causal mediation analysis could resolve
1036 whether training-induced increases in muscle strength and mediated by muscle
1037 hypertrophy. Sports Med Ahead of print, 2019.
1038 118. Oranchuk DJ, Nelson AR, Storey AG, and Cronin JB. Variability of regional
1039 quadriceps architecture in trained men assessed by B-Mode and extended field
1040 ultrasonography. Int J Sports Physiol Perform Ahead of print, 2019.
1041 119. Oranchuk DJ, Robinson TL, Switaj ZJ, and Drinkwater EJ. Comparison of the hang
1042 high-pull and loaded jump squat for the development of vertical jump and isometric
1043 force-time characteristics. J Strength Cond Res 33: 17-24, 2019.
1044 120. Oranchuk DJ, Storey AG, Nelson AR, and Cronin JB. Isometric training and long-
1045 term adaptations; effects of muscle length, intensity and intent: A systematic review.
1046 Scand J Med Sci Sports 29: 484-503, 2019.
1047 121. Paddon-Jones D, Leveritt M, Lonergan A, and Abernethy P. Adaptation to chronic
1048 eccentric exercise in humans: The influence of contraction velocity. Eur J Appl
1049 Physiol 85: 466-471, 2001.
1050 122. Pascoe MA, Holmes MR, Stuart DG, and Enoka RM. Discharge characteristics of
1051 motor units during long-duration contractions. Exp Physiol 99: 1387-1398, 2014.
1052 123. Pierce JR, Clark BC, Ploutz-Snyder LL, and Kanaley JA. Growth hormone and
1053 muscle function responses to skeletal muscle ischemia. J Appl Physiol 101: 1588-
1054 1595, 2006.
1055 124. Power GA, Rice CL, and Vandervoort AA. Increased residual force enhancement in
1056 older adults is associated with a maintenance of eccentric strength. PLoS One 7, 2012.
1057 125. Powers K, Schappacher-Tilp G, Jinha A, Leonard T, Nishikawa K, and Herzog W.
1058 Titan force in enhanced in actively stretched skeletal muscle. J Exp Biol 214: 3629-
1059 3636, 2014.
1060 126. Purslow PP. Muscle fascia and force transmission. J Bodyw Mov Ther 14: 411-417,
1061 2010.
1062 127. Reeves ND, Narici MV, and Maganaris CN. Strength training alters the viscoelastic
1063 properties of tendons in elderly humans. Muscle Nerve 28: 74-81, 2003.
1064 128. Rio E, Kidgell D, Purdam C, Gaida J, Moseley GL, Pearce AJ, and Cook J. Isometric
1065 exercise induces analgesia and reduces inhibition in patellar tendinopathy. Br J Sports
1066 Med 49: 1277-1283, 2015.
1067 129. Rio E, Purdam C, Gurdwood M, and Cook J. Isometric exercise to reduce pain in
1068 patellar tendinopathy in-season: Is it effective "on the road?". Clin J Sport Med, 2017.
1069 130. Rio E, van Ark M, Docking S, Moseley GL, Kidgell D, Gaida JE, van den Akker-
1070 Scheek I, Zwerver J, and Cook J. Isometric contractions are more analgesic than
1071 isotonic contractions for patellar tendon pain: An in-season randomized clinical trial.
1072 Clin J Sport Med 27: 253-259, 2017.
1073 131. Roberts TJ. Contribution of elastic tissues to the mechanics and energetics of muscle
1074 function during movement. J Exp Biol 219: 266-275, 2016.
1075 132. Rudroff T, Barry BK, Stone AL, Barry CJ, and Enoka RM. Accessory muscle activity
1076 contributes to the variation in time to task failure for different arm postures and loads.
1077 J Appl Physiol 102: 1000-1006, 2007.
1078 133. Rudroff T, Justice JN, Holmes MR, Matthews SD, and Enoka RM. Muscle activity
1079 and time to task failure differ with load compliance and target force for elbow flexor
1080 muscles. J Appl Physiol 110: 125-136, 2011.
1081 134. Rudroff T, Kalliokoski KK, Block DE, Gould JR, Klingensmith WC, and Enoka RM.
1082 PET/CT imaging of age- and task-associated differences in muscle activity during
1083 fatiguing contractions. J Appl Physiol 114: 1211-1219, 2013.
36
1084 135. Saito A and Akima H. Knee joint angle affects EMG–force relationship in the vastus
1085 intermedius muscle. J Electromyogr Kinesiol 23: 1406-1412, 2013.
1086 136. Schaefer LV and Bittmann FN. Are there two forms of isometric muscle action?
1087 Results of the experimental study support a distinction between a holding and a
1088 pushing isometric muscle function. BMC Sports Sci Med Rehabil 9: 1-13, 2017.
1089 137. Schoenfeld BJ. The mechanisms of muscle hypertrophy and their application to
1090 resistance training. J Strength Cond Res 24: 2857-2872, 2010.
1091 138. Schoenfeld BJ. Does exercise-induced muscle damage play a role in skeletal muscle
1092 hypertrophy? J Strength Cond Res 26: 1441-1453, 2012.
1093 139. Schoenfeld BJ, Grgic J, Ogborn D, and Krieger JW. Strength and hypertrophy
1094 adaptations between low- versus high-load resistance training: A systematic review
1095 and meta-analysis. J Strength Cond Res 31: 3508-3523, 2017.
1096 140. Schott J, McCully K, and Rutherford OM. The role of metabolites in strength training:
1097 Short versus long isometric contractions. Eur J Appl Physiol Occup Physiol 71: 337-
1098 341, 1995.
1099 141. Scott BR, Peiffer JJ, and Goods PSR. The Effects of Supplementary Low-Load Blood
1100 Flow Restriction Training on Morphological and Performance-Based Adaptations in
1101 Team Sport Athletes. J Strength Cond Res 31: 2147-2154, 2017.
1102 142. Seedman J. Eccentric Isometrics: The ultimate way to strength train. Advanced
1103 Human Performance.
1104 143. Seiberl W, Power GA, and Hahn D. Residual force enhancement in humans: Current
1105 evidence and unresolved issues. J Electromyogr Kinesiol 25: 571-580, 2015.
1106 144. Seiberl W, Power GA, Herzog W, and Hahn D. The stretch-shortening cycle (SSC)
1107 revisited: Residual force enhancement contributes to increased performance during
1108 fast SSCs of human m. adductor pollicis. Physiol Rep 3: e12401, 2015.
1109 145. Shalabi N, Cornachione A, de Souza Leite F, Vengallatore S, and Rassier DE.
1110 Residual force enhancement is regulated by titin in skeletal and cardiac myofibrils. J
1111 Physiol 595: 2085-2098, 2017.
1112 146. Shepstone TN, Tang JE, Dallaire S, Schuenke MD, Staron RS, and Phillips SM.
1113 Short-term high- vs. low-velocity isokinetic lengthening training results in greater
1114 hypertrophy of the elbow flexors in young men. J Appl Physiol 98: 1768-1776, 2005.
1115 147. Shim J and Garner B. Residual force enhancement during voluntary contractions of
1116 knee extensors and flexors at short and long muscle lengths. J Biomech 45: 913-918,
1117 2012.
1118 148. Simpson CL, Kim BDH, Bourcet MR, Jones GR, and Jakobi JM. Stretch training
1119 induces unequal adaptation in muscle fascicles and thickness in medial and lateral
1120 gastrocnemii. Scand J Med Sci Sports 27: 1597-1604, 2017.
1121 149. Sorensen JR, Skousen C, Holland A, Williams K, and Hyldahl RD. Acute
1122 extracellular matrix, inflammatory and MAPK response to lengthening contractions in
1123 elderly human skeletal muscle. Exp Gerontol Ahead of print, 2018.
1124 150. Spurway NC. Hiking physiology and the "quasi-isometric" concept. J Sports Sci 25:
1125 1081-1093, 2007.
1126 151. Storey A and Smith HK. Unique aspects of competitive weightlifting: Performance,
1127 training and physiology. Sports Med 42: 769-790, 2012.
1128 152. Stoter IK, MachIntosh BR, Fletcher JR, Pootz S, Zijdewing I, and Hettinga FJ. Pacing
1129 strategy, muscle fatigue, and technique in 1500-m speed-skating and cycling time
1130 trials. Int J Sports Physiol Perform 11: 337-343, 2016.
1131 153. Suchomel TJ, Nimphius S, Bellon CR, and Stone MH. The importance of muscular
1132 strength: Training considerations. Sports Med 48: 765-785, 2018.
37
1133 154. Suter E and Herzog W. Extent of muscle inhibition as a function of knee angle. J
1134 Electromyogr Kinesiol 7: 123-130, 1997.
1135 155. Tabary JC, Tabary C, Tardieu C, Tardieu G, and Goldspink G. Physiological and
1136 structural changes in the cat's soleus muscle due to immobilization at different lengths
1137 by plaster casts. J Physiol 224: 231-244, 1972.
1138 156. Takagi R, Ogasawara R, Tsutaki A, Nakazato K, and Ishii N. Regional adaptation of
1139 collagen in skeletal muscle to repeated bouts of strenuous eccentric exercise. Pflügers
1140 Archiv 468: 1565-1572, 2016.
1141 157. Takarada Y, Nakamura Y, Aruga S, Onda T, Miyazaki S, and Ishii N. Rapid increase
1142 in plasma growth hormone after low-intensity resistance exercise with vascular
1143 occlusion. J Appl Physiol 88: 61-65, 2000.
1144 158. Takarada Y, Takazawa H, Sato Y, Takebayaski S, Tanaka Y, and Ishii N. Effects of
1145 resistance exercise combined with moderate vascular occlusion on muscular function
1146 in humans. J Appl Physiol 88: 2097-2106, 2000.
1147 159. Tanimoto M, Kawano H, Gando Y, Sanada K, Yamamoto K, Ishii N, Tabata I, and
1148 Miyachi M. Low-intensity resistance training with slow movement and tonic force
1149 generation increases basal limb blood flow. Clin Physiol Funct Imaging 29: 128-135,
1150 2009.
1151 160. Thepaut-Mathieu C, Van Hoecke J, and Maton B. Myoelectrical and mechanical
1152 changes linked to length specificity during isometric training. J Appl Physiol 64:
1153 1500-1505, 1988.
1154 161. Topp R, Woolley S, Hornyak J, Khuder S, and Kahaleh B. The effect of dynamic
1155 versus isometric resistance training on pain and functioning among adults with
1156 osteoarthritis of the knee. Arch Phys Med Rehabil 83: 1187-1195, 2002.
1157 162. Tracy BL, Byrnes WC, and Enoka RM. Strength training reduces force fluctuations
1158 during anisometric contractions of the quadriceps femoris in old adults. J Appl
1159 Physiol 96: 1530-1540, 2004.
1160 163. Trezise J, Collier N, and Blazevich AJ. Anatomical and neuromuscular variables
1161 strongly predict maximum knee extension torque in healthy men. Eur J Appl Physiol
1162 116: 1159-1177, 2016.
1163 164. Ullrich B, Kleinöder H, and Brüggemann G-P. Influence of length-restricted strength
1164 training on athlete's power-load curves of knee extensors and flexors. J Strength Cond
1165 Res 24: 668-678, 2010.
1166 165. Ullrich B, Kleinoder H, and Bruggemann GP. Moment-angle relations after specific
1167 exercise. Int J Sports Med 30: 293-301, 2009.
1168 166. Van Gheluwe B, Huybrechts P, and Deporte E. Electromyographic evaluation of arm
1169 and torso muscles for different postures in windsurfing. Int J Sport Biomech 4: 156-
1170 165, 1988.
1171 167. Van Hooren B and Bosch F. Is there really an eccentric action of the hamstrings
1172 during the swing phase of high-speed running? part I: A critical review of the
1173 literature. J Sports Sci 35: 2313-2321, 2017.
1174 168. Van Hooren B and Bosch F. Is there really an eccentric action of the hamstrings
1175 during the swing phase of high-speed running? part II: Implications for exercise. J
1176 Sports Sci 35: 2322-2333, 2017.
1177 169. Verkhoshansky Y and Siff MC. Supertraining. Rome, Italy: Ultimate Athlete
1178 Concepts, 2009.
1179 170. Watanabe Y, Madarame H, Ogasawara R, Nakazato K, and Ishii N. Effect of very
1180 low-intensity resistance training with slow movement on muscle size and strength in
1181 healthy older adults. Clin Physiol Funct Imaging 34: 463-470, 2014.
38
1182 171. Watanabe Y, Tanimoto M, Oba N, Kiyoshi S, Muyachi M, and Ishii N. Effect of
1183 resistance training using bodyweight in the elderly: Comparison of resistance exercise
1184 movement between slow and normal speed movement. Geriatr Gerontol Int 15: 1270-
1185 1277, 2015.
1186 172. Watanabe Y, Tanimoto M, Ohgane A, Sanada K, Miyachi M, and Ishii N. Increased
1187 muscle size and strength from slow-movement, low-intensity resistance exercise and
1188 tonic force generation. J Aging Phys Act 21: 71-84, 2013.
1189 173. Yamauchi J and Koyama K. Relation between the ankle joint angle and the maximum
1190 isometric force of the toe flexor muscles. J Biomech Ahead of print, 2019.
1191 174. Yoo W-G. Effects of the slow speed-targeting squat exercise on the vastus medialis
1192 oblique/vastus lateralis muscle ratio. J Phys Ther Sci 27: 2861-2862, 2015.
1193 175. Zbidi S, Zinoubi B, Hammouda O, Vandewalle H, Serrau V, and Driss T. Co-
1194 contraction training, muscle explosive force and associated electromyography
1195 activity. J Sports Med Phys Fitness 57: 725-733, 2017.
1196
1197
1198
1199
1200
1201
1202
1203
1204
1205
1206
1207
1208
1209
39
1210 Figure 1. The three-component model of force transmission
1211
1212 Figure 2. The three-component model of force transmission in muscle contracting at short
1214
1215 Figure 3. Initial quasi-isometric hold and final position following a maximal eccentric
1217
1218 Figure 4. Initial quasi-isometric hold and final position following a maximal eccentric
1220
1222
1223
1224
1225
1226
1227
1228
40
1229 Table 1. The theoretical potential of dynamic, eccentric, isometric and eccentric quasi-isometric resistance training to benefit musculotendinous morphology and performance
Training outcome Training method Contractile element Series elastic component Parallel elastic component
Dynamic ++++ + +
Eccentric +++++ ++ ++
Morphology
Isometric ++ ++ +
EQI ++++ ++ ++
Dynamic ++++ + +
Eccentric ++ +++ ++
Endurance
Isometric +++ ++ +
EQI +++++ ++ ++
Dynamic +++ + +
EQI +++ ++ ++
Dynamic +++++ + +
Eccentric ++++ ++ ++
Power
Isometric ++ ++ +
EQI + + ++
1230 Ranked on a scale from + (low potential) to +++++ (high potential). Adapted from Suchomel et al., 2018. EQI = eccentric quasi-isometric.
1231
41
1232 Table 2. Hypothetical resistance training program for an athlete recovering from patellar tendonitis
Phase 1: Pain and load management
Day 1 Day 2
Exercise Sets x Reps Intensity Tempo ROM Exercise Sets x Reps Intensity Tempo ROM
Isometric Wall-squat 4 x 30-60s BW N/A 30-60º Isometric knee extension 4 x 30-60s 70% MVIC N/A 30-60º
Mini-band hip-thrust 3 x 15-20 BW 2-1-2-1 Full 1-leg DB Romanian deadlift 3 x 10-12 Moderate 3-0-1-0 Full
Clam shells 3 x 10-15 Band 2-1-2-1 Full Mini-band side shuffle 3 x 10-15 Band 1-0-1-0 0-30º
EQI knee extension 2 x 60-90s 50-60% 1RM N/A Pain free EQI knee extension 2 x 60-90s 50-60% 1RM N/A Pain free
Each phase = 2-3 weeks. Tempo = eccentric-pause-concentric-pause. Reps = repetitions. ROM = range of motion. BW = body-weight. N/A = not applicable. MVIC = maximal voluntary
isometric contraction. EQI = eccentric quasi-isometric. s = seconds. 1RM = one repetition maximum. DB = dumbbell. ECC = eccentric. BB = barbell.
1233
1234
1235
1236
1237
42
1238
1239
1240
1241
43
1242 44
1243
1244
1245
1246
1247
45
1248
1249
46
1250
47