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. Author manuscript; available in PMC: 2022 May 7.
Published in final edited form as: J Biomech. 2021 Mar 15;120:110384. doi: 10.1016/j.jbiomech.2021.110384

Comparison between dry needling and focused ultrasound on the mechanical properties of the rat Achilles tendon: A pilot study

Sujata Khandare a, Molly Smallcomb b, Bailey Klein a, Colby Geary a, Julianna C Simon a,b, Meghan E Vidt a,c
PMCID: PMC8089046  NIHMSID: NIHMS1687330  PMID: 33773298

Abstract

In the U.S., approximately 14 million tendon and ligament injuries are reported each year. Dry needling (DN) is a conservative treatment introduced to alleviate pain and restore function; however, it is invasive and has mixed success. Focused ultrasound (fUS) is a non-invasive technology that directs ultrasound energy into a well-defined focal volume. fUS induces thermal and/or mechanical bioeffects which can be controlled by the choice of ultrasound parameters. fUS could be an alternative to DN for treatment of tendon injuries, but the bioeffects must be established. Thus, the purpose of this pilot study was to compare the effect of DN and fUS on the mechanical properties and cell morphology of 30 ex vivo rat Achilles tendons. Tendons were randomly assigned to sham, DN, or fUS, with 10 tendons per group. Within each group, 5 tendons were evaluated mechanically, and 5 tendons were analyzed histologically. Elastic modulus in the DN (74.05±15.0MPa) group was significantly lower than sham (149.84±59.1MPa; p=0.0094) and fUS (128.84±28.3MPa; p=0.0453) groups. Stiffness in DN (329.05±236.8N/mm; p=0.0034) and fUS (315.26±68.9N/mm; p=0.0027) groups were significantly lower than sham (786.10±238.7N/mm) group. Histologically, localized necrosis was observed in 3 out of 5 tendons exposed to fUS, with surrounding tissue unharmed; no evidence of cellular injury was observed in DN or sham groups. These results suggest that fUS preserves the mechanical properties of tendon better than DN. Further studies are needed to evaluate fUS as an alternative, noninvasive treatment modality for tendon injuries.

Keywords: dry needling, focused ultrasound, tendon, mechanical properties, mechanical testing

Introduction

Tendon, ligament, and joint capsular injuries represent 45% of the 32 million musculoskeletal injuries reported each year in the U.S., with annual costs of ~$254 billion (Praemer A., 1992; BMUS, 2014). Tendinosis is a debilitating condition caused by overuse, and characterized by pain, microtears, and collagen disorganization (Galloway et al. 1992, Riley, 2004; Silva et al., 2011). Common sites of tendinosis include the Achilles tendons, rotator cuff tendons, and patellar tendons (Wilson and Best, 2005). Injured tendons are mechanically weaker, compromising the associated joint biomechanics and increasing the risk for tendon rupture. Tendons are load-bearing structures that must withstand high physiological loads (e.g. up to 1.4x bodyweight at the glenohumeral joint (Westerhoff et al., 2009)). Thus, the mechanical effects of treatment modalities must be considered to ensure that treatments do not diminish mechanical properties while promoting tendon healing.

Tendinosis treatment often begins with immobilization, activity modification, physical therapy, and non-steroidal anti-inflammatory medications (APTA, 2013). Effectiveness of these interventions vary, with some patients showing limited or no alleviation of symptoms (Freedman et al., 2014; Khan and Cook, 2003). Conservative therapies, like dry needling (DN), have been widely used to alleviate pain and restore function (APTA, 2013; Stenhouse et al., 2013). DN involves “peppering” the injured tendon with a thin filiform needle, usually at myofascial trigger points, to create micro-damage (APTA, 2013). Proponents of DN theorize that the micro-damage disrupts pathological tissues, inducing bleeding and release of growth factors that stimulate healing (Hildebrand et al., 1998; Housner et al., 2009; Krey et al., 2015). However, success rates of DN are mixed (Mishra et al., 2014; Rha et al., 2013; Stenhouse et al., 2013), as practitioners vary the location, direction, frequency, and depth of needle insertions, and do not always use real-time ultrasound imaging to provide guidance during needle insertion to target the precise area of injury. Although DN is widely used in the clinic, limited controlled laboratory studies (Riggin et al., 2019) have explored its mechanical effects. Given the widespread acceptance of DN in clinical use and the lack of studies providing scientific assessment of this clinical practice demonstrates a significant literature gap. Therefore, understanding its mechanical effects will help determine whether DN diminishes tendon mechanical properties.

In physiotherapy, diagnostic ultrasound is commonly used as an imaging modality to diagnose tendon injuries and guide treatment. Therapeutic ultrasound at low intensities can induce mild hyperthermia and facilitate increase in tensile strength and collagen alignment in tendons (Enwemeka, 1989; Yeung et al., 2006). Focused ultrasound (fUS) is a non-invasive therapeutic modality that directs ultrasound energy into a well-defined focal volume without damaging surrounding tissues (Bailey et al., 2003; Dubinsky et al., 2008; Maxwell et al., 2012). Choice of ultrasonic parameters and material properties of the tissue at the ultrasound focus directs fUS bioeffects toward thermal ablation from absorption of the acoustic energy or mechanical fractionation from the creation, oscillation, and collapse of cavitation bubbles in a process termed histotripsy (Khokhlova et al., 2014; Maxwell et al., 2012). fUS intervention can be monitored in real-time using magnetic resonance imaging (for heating) or ultrasound imaging (for cavitation bubbles) (Khokhlova et al., 2014). While fUS has been applied clinically to treat uterine fibroids and liver tumors (Khokhlova and Hwang, 2011; Leslie et al., 2012), highly collagenous tissues, like tendons, have posed a challenge to inducing mechanical fractionation (Vlaisavljevich et al., 2011). Muratore et al. (2008) and Yeh et al. (2013) have used high-intensity focused ultrasound to thermally ablate ex vivo bovine Achilles tendons and loosen contractures in ex vivo porcine digital extensor tendons, respectively, but it remains unknown how fUS parameters influence the tendon mechanical properties and the type of bioeffect achieved. If fUS can induce bioeffects similar to DN while facilitating improved collagen alignment as in previous therapeutic ultrasound tendon studies, this could represent a promising non-invasive alternative to DN.

Therefore, the objective of this pilot study was to evaluate and compare the effects of DN and fUS interventions on tendon mechanical properties and cell morphology. Ex vivo rat Achilles tendons were exposed to either DN or fUS before mechanical testing or histological analysis. We hypothesized that fUS-exposed tendons will perform better mechanically than DN-exposed tendons and show detectable histological micro-damage.

Materials and Methods

Study design

Thirty Achilles tendons from 17M/5F Sprague-Dawley rats (age: 6-12 months) were obtained after euthanasia from an unrelated study approved by Penn State Institutional Animal Care and Use Committee. Tendons were randomly divided into 3 groups: sham, DN, and fUS (n=10/group). From each group, 5 tendons were evaluated mechanically, and 5 tendons were analyzed histologically.

Focused Ultrasound (fUS)

fUS was performed in filtered, deionized, and degassed water (~20°C) with a 1.5MHz transducer with f#=0.7 (H-234, Sonic Concepts, Bothell, WA) (Fig. 1A). fUS was monitored in real-time using a Philips/ATL P4-2 transducer (Bothell, WA) and research ultrasound system (Vantage, Verasonics®, Kirkland, WA). Tendon mid-body was exposed to 10ms pulses repeated 60x at 1Hz pulse repetition frequency with peak positive pressure exceeding 80MPa and peak negative pressure exceeding 20MPa. Parameters were chosen based on previous studies (Canney et al., 2010; Khokhlova et al., 2014) in other tissues to emphasize mechanical fractionation rather than thermal ablation.

Figure 1:

Figure 1:

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(A) Focused ultrasound (fUS) experimental arrangement showing the fUS transducer with co-axially aligned imaging probe targeting the rat Achilles tendon; (B) The foot was embedded in epoxy and 4 Verhoeff stain lines were marked on the Achilles tendon; (C) Schematic of the mechanical testing experimental arrangement showing the tendon, which is attached to the foot embedded in epoxy.

Dry needling (DN)

Tendons were submerged in deionized water for 30min to mimic environmental conditions of the fUS group. DN was performed by inserting and quickly removing a fine-gauge (30G) acupuncture needle (0.3 mm diameter, Tai-Chi, Suzhou, Jiangsu, China) from the tendon mid-body 5 times over a period of 12sec.

Sham

Tendons were submerged in deionized water for 30min to mimic the environmental conditions of fUS group without any treatment intervention.

Mechanical testing

The foot, with soft tissue removed, was embedded and allowed to set in epoxy (Loctite, Dusseldorf, Germany). The muscle-tendon segment was submerged in PBS to maintain hydration. Four evenly spaced Verhoeff stain lines were marked perpendicular to the tendon’s long axis (Fig. 1B) for strain analysis. Tendon length was quantified with digital Vernier calipers. Cross-sectional area was quantified using a research ultrasound system (Verasonics® L22-14 transducer) and ImageJ (NIH) software.

Following sham, DN, or fUS intervention, the proximal end of the tendon was held in a custom-designed clamp lined with sandpaper and mounted on an MTS-858 Mini Bionix mechanical testing system (MTS Systems Corp., Eden Prairie, MN) (Fig. 1C). This study used an established mechanical testing protocol reported previously (Huang et al., 2004; Riggin et al., 2019). Briefly, tendons were preloaded to 0.08N, followed by 10 cycles of preconditioning from 0.1N-0.5N, then allowed to rest for 300sec. Stress-relaxation test was performed where tendons were subjected to 5% strain at 2.5mm/sec followed by a 600sec hold to allow the tendon to reach equilibrium force. Load-to-failure in axial tension was performed at a constant rate of 0.015mm/sec. The experiment was recorded using a Canon Rebel T6 camera at 30 frames/sec. Percent relaxation was calculated as percent change from peak stress to equilibrium stress from the stress-relaxation test. Strain was calculated by measuring change in distance between Verhoeff stain lines during the load-to-failure test using ImageJ software. Stiffness and elastic modulus were calculated as the slope of load-displacement curve and stress-strain curve, respectively.

Histology

The ex vivo tendon samples were evaluated using cell morphology after DN and fUS exposure to determine the kind of tissue damage generated. Tendons were fixed in 10% neutral buffered formalin for 10 days and processed using standard paraffin wax techniques (Leica TP 1020, Leica Biosystems, Nussloch, Germany). Tendons were serially sectioned using a microtome (Shandon Finesse, Thermo Fisher Scientific, Waltham, MA, USA) with a 7-10 μm thickness and ~200 μm depth between slides before staining with Hematoxylin and Eosin (H&E) for analysis of cellular morphological changes, or alpha-nicotinamide adenine dinucleotide diaphorase (α-NADH-d) for analysis of enzymatic activity where the lack of stain indicates lack of cell viability .

Statistical analysis

Shapiro–Wilk tests were performed to evaluate for normal distribution in the percent relaxation, stiffness, and elastic modulus in all the three treatment groups. Parametric statistical test was performed using one-way ANOVA in SAS software (SAS Institute, Inc., Cary, NC, v9.4). Group means of percent relaxation, stiffness, and elastic modulus across intervention groups were compared, with p<0.05 considered significant.

Results

There was no significant difference in percent relaxation of tendons exposed to DN (16.07±12.7%; p=0.1981) or fUS (8.42±5.8%; p=0.9617) when compared to sham (8.69±5.2%) (Fig. 2A). Elastic modulus of tendons exposed to DN (74.05±15.0MPa) was significantly lower than both fUS (128.84±28.3MPa; p=0.0453) and sham (149.84±59.1MPa; p=0.0094) groups. No difference was observed in elastic moduli between fUS and sham groups (p=0.4088) (Fig. 2B). Stiffness of tendons exposed to DN (329.05±236.8N/mm) and fUS (315.26±68.9N/mm) were not statistically different (p=0.9142), but were both significantly lower than sham (786.10±238.7N/mm; p=0.0034 and p=0.0027, respectively) (Fig. 2C).

Figure 2:

Figure 2:

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(A) Percent relaxation, (B) elastic modulus, and (C) stiffness of rat Achilles tendons exposed to sham, dry needling (DN), and focused ultrasound (fUS).

No histological evidence of injury was observed in DN or sham groups (Fig. 3A, 3B). Three of 5 tendons in the fUS group showed focal necrosis (Fig. 3C); the other 2 tendons showed no injury. Analysis of enzymatic activity using NADH stained cells showed localized cell death at the ultrasound target, which was confirmed by lack of stain uptake (Fig. 3D).

Figure 3:

Figure 3:

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Representative H&E histology images of (A) sham, (B) dry needling (DN), and (C) focused ultrasound (fUS) treatments, with ellipse indicating fUS target area. (D) NADH histology image showing cell death at the fUS target, as indicated by the lack of stain uptake in the fUS target area (ellipse).

Discussion

This pilot study examined and compared effects of DN and fUS on ex vivo tendon mechanical properties and cell morphology. Results suggest that DN and fUS interventions caused a decrease in mechanical properties, with elastic modulus and percent relaxation of fUS-exposed tendons being similar to sham. Focal necrosis was observed histologically in 3 out of 5 tendons exposed to fUS with no injury observed in DN or sham groups.

Lower elastic modulus and stiffness of tendons exposed to DN suggests that tendons have reduced mechanical properties compared to sham. These results are consistent with Riggin et al. (2019) who observed reduced stiffness and elastic modulus of tendons 1-week and 6-weeks post-DN intervention on healthy rat tendons. However, in our study, no histological evidence of micro-damage was observed in the DN group, although attempts were made to scale the tendon-to-needle gauge size ratio and dosage of DN from humans to rats. Further work in healthy tendons involving different DN dosages is needed to validate presence of micro-damage and better understand whether DN causes permanent changes in tendon mechanical properties.

Focused ultrasound has the potential to overcome some limitations of DN while retaining its key features. Specifically, fUS is used under ultrasound guidance, has controllable targeting, and, importantly, has the potential to non-invasively create controllable micro-damage in tendons from the initiation of cavitation bubble cloud. The elastic modulus of tendons exposed to fUS was similar to that of sham, although stiffness was significantly lower than sham. Importantly, parameters used in the current fUS intervention resulted in thermal denaturation rather than mechanical fractionation in 3 out of 5 tendons. No injury was observed in the other 2 tendons, likely due to interference between acoustic waves and experimental fixtures.

Previous studies have explored the use of high-intensity focused ultrasound using different ultrasound parameter sets on tissues with varying mechanical properties. Vlaisavljevich et al., 2011 demonstrated that the threshold to initiate a cavitation bubble cloud induced by histotripsy increases with increasing mechanical strength of the target tissue. Initiation threshold in dense collagenous tissues, like tendons (24.37 ± 0.82 MPa) and cartilage (27.52 ± 0.33 MPa), was higher than that in fat (14.27 ± 2.92 MPa) or muscle (18.49 ± 0.87 MPa) tissue. Yeh et al., 2013 describes the use of pulsed high-intensity focused ultrasound on ex vivo porcine ligaments and tendons to loosen contractures in the tissue. Their study reported exponential decrease in tissue tensile stiffness with increase in insonation duration, however, the mechanical testing protocol and ultrasound parameter set used in this study were different from our study. Specifically, we used higher peak pressures and a different pulsing scheme (lower duty factor, higher pulse duration, lower pulse repetition frequency) in our pursuit of achieving mechanical disruption. Our study builds on prior work and demonstrates promise in guiding the development of fUS parameter sets to produce localized mechanical damage via cavitation bubble clouds, while minimizing the potential for thermal bioeffect.

The ultrasound parameters used in our study were chosen to emphasize mechanical fractionation from acoustic cavitation to induce localized micro-damage, which is anticipated to be similar, but more localized, than what occurs with DN. Although histology results from both H&E and NADH stain images suggest the occurrence of localized injury, the injury was thermal rather than mechanical. Ongoing work includes studying various combinations of ultrasound parameters and identifying the specific combination causing mechanical fractionation rather than thermal denaturation. Previous studies (Enwemeka, 1989; Yeung et al., 2006) show that application of lower intensities of therapeutic ultrasound on tendon induces mild hyperthermia and facilitates increases in tensile strength and collagen alignment. Muratore et al. (2008) also showed the ability of fUS to ablate ex vivo bovine Achilles tendons at lower intensities than used in this study. An ongoing challenge for the field, and simultaneous thrust of our ongoing work, is to use fUS to create micro-damage in tendons without inducing negative effects to the surrounding tissue.

Despite this pilot study’s small sample size (n=5/group), outcomes show differences in mechanical properties of tendons exposed to DN and fUS, motivating continued work with larger sample sizes. This pilot study provides a foundation for future work involving in vivo animal models of tendinosis. This study was performed on ex vivo rat Achilles tendons and no biological mechanisms or collagen alignments were investigated that could help elucidate mechanisms underpinning observed changes in mechanical properties. Recorded mechanical properties exhibited a high amount of variability, especially in the DN group. We surmise that these variations may be due to uneven sex distribution of rats in sham (1F, 4M), DN (5M), and fUS (3F, 2M) groups. However, these results are consistent with a previous study (Pardes et al., 2016) exploring effects of sex on tendon mechanical properties.

In this pilot study, evaluation of mechanical properties of ex vivo rat Achilles tendons after DN or fUS intervention suggests that mechanical properties are preserved after fUS intervention compared to DN. Ongoing work includes extending these results to larger samples sizes. Additional studies are needed to better understand the mechanical effects of DN and fUS intervention and evaluate fUS’s effects in in vivo animal models to clarify whether this intervention may be an alternative, non-invasive treatment for tendon injuries.

Acknowledgements

Dr. Yak-Nam Wang for tendon histology advice. Funding from the National Institutes of Health – National Institute of Biomedical Imaging and Bioengineering (R21EB027886); NSF Graduate Research Fellowship (Smallcomb; Grant#DGE1255832); Penn State College of Engineering Multidisciplinary Seed Grant.

Footnotes

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