Postural stress theory.

To the Editor:

I am writing in response to the recent article by Michael J Mueller and Katrina S Maluf titled "Tissue Adaptation to Physical Stress: A Proposed `Physical Stress Theory' to Guide Physical Therapist Practice, Education, and Research" (April 2002). The authors have offered a comprehensive explanation of the proposed "Physical Stress Theory" (PST) and depicted its application to physical therapist practice, education, and research. I commend their efforts and believe that the theory certainly offers "food for thought"; however, I am hesitant to embrace the theory in its totality. I am specifically concerned with 2 tenets presented in the theory.

First, the authors appear to equate increased stress tolerance with tissue hypertrophy. However, hypertrophy is not always a response to stress and is not necessarily a measure of fitness. As the authors note, different levels of exercise may have a beneficial or detrimental effect on tissue remodeling. Furthermore, the beneficial effects of exercise may differ depending on the exercise regimen. The authors remark that "physical stress is a composite value, defined by the magnitude, time, and direction of stress application" (Fundamental Principle H of the PST). Indeed, research indicates that muscle responds differently to the amount and type of activity to which it is subjected. Aerobic exercise (low-magnitude/high-frequency stress) results in increased mitochondrial content and respiratory capacity of muscle fibers, but does not result in hypertrophy. Resistance exercise (high-magnitude/low-frequency stress) results in muscle hypertrophy and higher contractile force (see Booth and Thomason (1) for a complete review). The authors suggest that the role of the physical therapist is to instruct people in an exercise regimen that will "provide an adequate stimulus for hypertrophy of intended tissues." With respect to muscle tissue, the goals of a rehabilitative exercise protocol may not include hypertrophy.

Second, the authors assert that "research has demonstrated that both tendon and ligament respond to exercise-induced stress with increases in cross-sectional area, stiffness, and tensile strength." In the case of tendon, the proposition of a predictable adaptive response is premature. Tendon has been shown to undergo remodeling in response to training; however, compared with muscle, studies of the effects of exercise on tendon are quite limited. Some studies that have examined mechanical changes of tendon in response to exercise suggest that tensile strength and stiffness increase with endurance training. (2-6) Woo and colleagues reported that exercise increased strength and stiffness of digital extensor tendons in swine, (7) but did not affect the digital flexor tendons. (8) Similarly, Tipton et al (9) reported that endurance training increased tensile strength of digital extensor tendons in primates, but did not affect the digital flexor or Achilles tendons. Of special interest in the context of the PST is that Simonsen et al (4) found that a strength training regimen (high force over a few loading cycles) did not stimulate increases in tendon strength. However, low-force endurance training in the form of swimming resulted in stronger tendons. This study suggests that tendons may respond to the total number of muscle contractions that occur during training rather than the absolute tension exerted by the muscle. Thus, exercise programs designed to strengthen muscle may not result in increased tendon strength. Conversely, endurance training regimens, which typically do not result in increased muscle strength, may lead to increases in tendon strength.

Some information exists on structural changes of tendon in response to exercise, but this information is inconsistent. Woo et al (7) and Birch et al (10) reported that digital extensor tendons of swine (Woo et al) and horses (Birch et al) hypertrophied in response to long-term exercise, but that opposing flexor tendons did not hypertrophy. Buchanan and Marsh (2) found that the Achilles tendon of guinea fowl did not hypertrophy in response to long-term training. Thus, it cannot be assumed that increased tendon strength or stiffness is necessarily concomitant with hypertrophy. As yet, a correlation between tendon hypertrophy and increased tensile strength or stiffness has not been established.

Although the PST certainly has merit, I fear that, in the case of muscle tissue, it is overly simplistic and, in the case of tendon, it is based on conjecture rather than solid evidence. Normally, contemporary theories and practices undergo revision as new or overlooked evidence arises. I hope that the authors will consider revising the PST based on the evidence presented.

Cindy Buchanan, PT, PhD
Physical Therapy Department (6RB)
Northeastern University
Boston, MA 02115
([e-mail])

References

(1) Booth FW, Thomason DB. Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev. 1991;71:541-585.

(2) Buchanan CI, Marsh RL. Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J Appl Physiol. 2001;90:164-171.

(3) Kubo K, Kanehisa H, Kawakami Y, Fukunaga T Elastic properties of muscle-tendon complex in long-distance runners. Eur J Appl Physiol. 2000;81:181-187.

(4) Simonsen EB, Klitgaard H, Bojsen-Moller F. The influence of strength training, swim training and ageing on the Achilles tendon and m. soleus of the rat. J Sports Sci. 1995;13:291-295.

(5) Vilarta R, Vidal BC. Anisotropic and biomechanical properties of tendons modified by exercise and denervation: aggregation and macromolecular order in collagen bundles. Matrix. 1989;9:55-61.

(6) Viidik S. The effect of training on the tensile strength of isolated rabbit tendons. Scand J Plast Reconstr Surg. 1967;1:141-147.

(7) Woo SL, Ritter MA, Amiel D, et al. The biomechanical and biochemical properties of swine tendons: long term effects of exercise on the digital extensors. Connect Tissue Res. 1980;7:177-183.

(8) Woo SL, Gomez MA, Amiel D, et al. The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J Biomech Eng. 1981;103: 51-56.

(9) Tipton CM, Matthes RD, Vailas AC, et al. The response of the Galago Senegalensis to physical training. Comp Biochem Physiol. 1979;63-A:29-36.

(10) Birch HL, McLaughlin L, Smith R, et al. Treadmill exercise-induced tendon hypertrophy: assessment of tendons with different mechanical functions. Equine Vet J suppl. 1990;30:222-226.

Author Response:

Dr Buchanan writes to voice 2 concerns with principles that we presented in the "Physical Stress Theory." (1) Both of these concerns seem to be related to how the theory predicts tissue adaptation to relative increases in physical stress levels.

First, Dr Buchanan is concerned that we "appear to equate increased stress tolerance with tissue hypertrophy." Fundamental Principle E states, however, that "[p]hysical stress levels that exceed the maintenance range (ie, overload) result in increased tolerance of tissues to subsequent stresses." (1) (p387) We were careful to explain that "[h]ypertrophy is one [emphasis added] common mechanism by which tissues become more tolerant of subsequent physical stresses." (1) (p387) We consistently used hypertrophy (ie, increased cross-sectional area) as an example of tissue adaptation to increased stress (see Tab. 1 and Figs. 1-3 in the article,) but we explained that "[o]ther examples of adaptations that may increase tissue stress tolerance include hormonal changes, altered cell membrane excitability, and changes in the material properties of tissues." (1) (p387) We stated, "In general, biological tissues adapt to increased levels of stress by increasing cross-sectional area, density, or volume." (1) (p387) Clearly, some biological tissues adapt to certain types of increased physical stresses without a traditional hypertrophy of tissue. Although muscle fibers do not increase cross-sectional area in response to aerobic exercise (low-magnitude/high-frequency stress), they do increase in density or volume of other structures such as mitochondria and capillaries. (2) Adaptations are specific to the type of stress applied and result in a modified tissue that is more tolerant of these specific subsequent stresses (Fundamental Principle E). (1)

Dr Buchanan's second concern is that "In the case of tendon, the proposition of a predictable adaptive response is premature." The Physical Stress Theory (PST) predicts that tendon will become more tolerant of subsequent physical stresses after increased stresses and less tolerant of subsequent stresses if exposed to lower than typical stresses. However, the theory does not predict quantitative thresholds for this change. In our literature review, we cited a number of studies that demonstrate that "tendon and ligament respond to exercise-induced stress with increases in cross-sectional area, stiffness, and tensile strength," (3-6) and several of these studies are also cited by Dr Buchanan. Dr Buchanan's own research (7) indicates that the Achilles tendon of guinea fowl show increased tendon stiffness in response to long-term exercise. Furthermore, Buchanan and Marsh "hypothesize that increases in tendon stiffness observed after endurance training may not be associated with a requirement for increased strength, but rather might represent a mechanism to resist tendon damage due to mechanical fatigue." (7) These results and the subsequent hypothesis described by Dr Buchanan are perfectly consistent with what we would predict using the PST.

Dr Buchanan correctly points out that some studies have shown aerobic exercise-induced changes in the extensor tendons of swine (8) and primates, (4) but not in the flexor tendons. We suggest that the PST offers a useful interpretation of these mixed results and provides direction for future research. Based on Fundamental Principles D and E of the PST, (1) we hypothesize that the exercise stimulus used in these studies was insufficient to meet the threshold of physical stress required for adaptive changes in flexor tendons. Experiments could be devised to increase the magnitude or the time (duration, repetition, or rate) (1) (p388) of stresses experienced by the flexor tendons. As Woo et al (8) indicated, the relationship between a change in the mechanical properties of a tendon to changing stress and strain duration may best be represented by a highly nonlinear curve. A relatively small decrease in stress through immobilization may result in a rapid degradation of material properties, whereas a relatively large stress (via exercise) may be required to enhance the material properties of some biological soft tissues such as tendon (see Fig. 11 in Woo et al (8)). Conversely, Woo et al (8) speculated that perhaps the digital flexor tendon cannot adapt to physical stresses because it is constrained by, and must glide within, its sheath. This speculation is inconsistent with what we would predict from the PST. If future experiments indicate that greater levels of physical stress fail to produce a beneficial adaptive response in flexor tendons, then the PST would need to be modified. We are aware of no new evidence, however, to discount the basic premises outlined in the theory.

We appreciate the opportunity to clarify certain portions of the PST. Rather than seeing a conflict between the experimental results of the adaptive response of muscle or tendon to increased stress and the response predicted by the theory, however, we see how the theory can be used to help interpret research results and guide subsequent studies. We believe the PST can provide a general framework to guide these specific research studies to help identify thresholds of adaptation.

Michael J Mueller, PT, PhD
Associate Professor

Katrina S Maluf PT, MSPT
Graduate Student
Program in Physical Therapy
Washington University School of Medicine
St Louis, MO 63108

References

(1) Mueller MJ, Maluf KS. Tissue adaptation to physical stress: a proposed "physical stress theory" to guide physical therapist practice, education, and research. Phys Ther. 2002;82:383-403.

(2) Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol. 1984;56:831-838.

(3) Cabaud HE, Chatty A, Gildengorin V, Feltman RJ. Exercise effects on the strength of the rat anterior cruciate ligament. Am J Sports Med. 1980;8:79-86.

(4) Tipton CM, Matthes RD, Vailas AC, et al. The response of the Galago Senegalensis to physical training. Comp Biochem Physiol. 1979;63A:29-36.

(5) Woo SL, Gomez MA, Sites TJ, et al. The biomechanical and morphological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J Bone Joint Surg Am. 1987;69:1200-1211.

(6) Woo SL, Ritter MA, Amiel D, et al. The biomechanical and biochemical properties of swine tendons: long term effects of exercise on the digital extensors. Connect Tissue Res. 1980;7:177-183.

(7) Buchanan CI, Marsh RL. Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J Appl Physiol. 2001;90:164-171.

(8) Woo SL, Gomez MA, Woo YK, Akeson WH. Mechanical properties of tendons and ligaments, II: the relationships of immobilization and exercise on tissue remodeling. Biorheology. 1982;19:397-408.