mao2015 Shoulder skin and muscle hemodynamics during backpack carriage

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Shoulder skin and muscle hemodynamics during backpack carriage

Clifford P. Mao

¹

, Brandon R. Macias

²

, Alan R. Hargens

^*

Department of Orthopaedic Surgery, University of California, San Diego, United States

a r t i c l e i n f o

Article history:

Received 24 September 2014 Accepted 19 April 2015 Available online

Keywords:

Bloodﬂow Oxygenation Pain

a b s t r a c t

The purpose of this study was to quantify the effects of loaded backpacks on shoulder muscle oxygenation, skin bloodflow, and pain. We hypothesized that backpack load carriage is associated with lower shoulder muscle oxygenation and skin microvascular flow. Near-infrared spectroscopy quantified shoulder tissue oxygenation and laser Dopplerflow measured skin microvascularflow. Eight adult volunteers donned a standard backpack without added load, 5 kg load, and 10 kg load for 5 min while standing. An 8 min rest period before each backpack donning condition ensured that all measured parameters returned to baseline. Data were analyzed using a repeated measures ANOVA and significance set at p<0.05. Donning a 10 kg backpack significantly reduced shoulder muscle oxygenation by 22±23%

as compared to the empty backpack control condition (p¼0.023). In addition, a 10 kg backpack load reduced skin microvascularflow by 82±22%, as compared to the empty backpack control condition (p¼0.024). Perceived pain was significantly higher when wearing the 10 kg backpack (level 4 on a 10- maximal pain scale) as compared to the empty backpack (0, 0eno pain) (p<0.05). In conclusion, backpack loads of 10 kg decrease shoulder muscle oxygenation and skin microvascularflow.

1. Introduction

Adults and children use backpacks for recreational and occu- pational purposes to transport items. In the United States, fourth andﬁfth grade students carry a mean backpack loads of 10% and 12% of their body weights, respectively (Forjuoh et al., 2003). In Italy, school children carry backpack loads with a median average load of 9.3 kg or 22% of their body weights (Negrini et al., 1999). In addition, typical backpack loads of Australian school children (age range 8e12 years) are 5.3 kg or 10% of their bodyweight on average (Grimmer and Williams, 2000). In a survey, with over 92% of the children typically carrying backpacks, muscle soreness is the most reported symptom (67.2%) (Pascoe et al., 1997). Speciﬁcally, in this same study 14.7% of children report shoulder pain when donning a backpack (Pascoe et al., 1997). Children carrying (age 6 years) 15e20% bodyweight backpack loads (average load range 3.4e4.6 kg) display muscle fatigue in the upper trapezius after 10 min and in the lower trapezius after 15 min (Hong et al., 2008).

In another study with children, backpack loads weighing 10%e30%

bodyweight signiﬁcantly increase skin contact pressure beneath backpack straps and pain (Macias et al., 2005). In addition, Macias and co-workers observe asymmetric pressure distributions of the right and left shoulder during backpack carriage (10%, 20%, and 30%

bodyweight loads) by school children (Macias et al., 2005). These observed shoulder skin contact pressures during backpack carriage are higher than the pressure thresholds to occlude local tissue bloodﬂow (Macias et al., 2005).

Heavy backpack usage may also affect shoulder health in adult populations. For example, computer models of backpack carriage in adults, using open MRI scans, demonstrate that a 25 kg backpack compresses the tissues beneath backpack straps with an average contact pressures of 10 kPa on the trapezius (Hadid et al., 2012). The magnitude of these compressive forces beneath backpack straps are sufficient to induce nerve damage (Hadid et al., 2012). One study finds that compression from backpack loads displayed increased signs of muscle fatigue in the upper trapezius (Piscione and Gamet, 2006). Recent data byKim et al. (2014), support these computer model predictions, documenting that a 12 kg backpack decreases tactical sensation at thefingers and lowers brachial artery bloodflow.

However, it is unclear if shoulder tissue bloodﬂow is compro- mised during backpack load carriage. Classic studies by Holloway and coworkers demonstrate that forearm skin bloodﬂow decreases 65% with a 10 mmHg of externally applied pressure (Holloway et al.,

*Corresponding author. Tel.:þ1 619 543 6805; fax:þ1 619 543 2540.

E-mail addresses: [email protected] (C.P. Mao), [email protected] (B.R. Macias),[email protected](A.R. Hargens).

1 Tel.:þ1 619 543 3810; fax:þ1 619 543 2540.

2 Tel.:þ1 619 543 4622; fax:þ1 619 543 2540.

Contents lists available atScienceDirect

Applied Ergonomics

j o u rn a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / a p e r g o

http://dx.doi.org/10.1016/j.apergo.2015.04.006

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1976). Therefore, we sought to determine if shoulder skin blood ﬂow and muscle oxygenation are affected while donning a loaded backpack. In addition, we sought to determine if a reduction in hemodynamic parameters are related to perceived pain. We hy- pothesize that increasing backpack load decreases muscle oxygenation and skin bloodﬂow in the shoulder, while causing increased shoulder pain.

2. Materials and methods

This study was approved by the University of California, San Diego Institutional Review Board. All volunteers were verbally informed of the study protocol and risks, volunteers read and signed consent forms prior to testing. Subjects that had any history of musculoskeletal disorders in their upper extremity and back were excluded and not enrolled in the study. Eight subjects (4 men, 4 women, age range: 21e34 years, mean weight ± SD:

64.8±15.2 kg) were tested in the present study. The subjects all wore T-shirts. A Jansport^®backpack (San Leandro, CA; 0.7 kg) was worn continuously throughout the experiment.

Tissue oxygenation and skin bloodﬂow levels were measured noninvasively with near-infrared spectroscopy (NIRS) (Celie et al., 2012; Hampson and Piantadosi, 1988) and with laser Doppler ﬂow (LDF) (Aratow et al., 1991; Hodges and Del Pozzi, 2014;

Watenpaugh et al., 2004), respectively. Speciﬁcally, NIRS was used to measure tissue oxygenation in the forearm in a previous backpack study (Kim et al., 2014). To minimize signal interference the devices were placed on opposite shoulders. The NIRS sensor and the LDF probe were placed over the right and left upper trapezius muscles for all subjects, respectively. The sensor and probe were placed under the backpack strap beneath the T-shirts and against the skin (Fig. 1). Both the sensor and the probe were located proximally transverse to the disc between the ﬁrst and second

thoracic vertebra. Both devices sampled tissue areas where pressures from the backpack straps were applied. Placement of the NIRS sensor (7.5 cm by 3.8 cm; 2 mm thick) and LDF probe (8 mm diameter; 2.2 mm thick) in this orientation provide continuous muscle oxygenation and skin bloodflow monitoring of the upper trapezius. The tissue oxygenation was measured with a NIRS device (INVOS 5100C, Somanetics Corporation, Troy, MI), which used light- emitting diodes (LED) to transmit light at wavelengths of 730 and 810 nm and monitored a penetration depth of about 1e2 cm. The sensor has two detectors spaced 3 cm and 4 cm from the LEDs. The LED photons travel in a parabolic path to the detector (Cui et al., 1991). The NIRS device calculates the difference of the shallow signal from the deep signal to give an oxygenation value deep in the tissue without superficial signal contamination. The NIRS data were reported in units of regional oxygen saturation (rSO2). The LDF device (LASERFLO^®Model BPM 403A, Vasamedics, Inc., Saint Paul, Minnesota) used a 780 nm laser diode and achieved a bloodflow measurement depth of approximately 1 mm. LDF device is a Doppler based technique, measuring Doppler shifts of the back- scattered light due to the moving red blood cells (Nilsson et al., 1980). The LDF data were reported as voltage outputs. We ex- press LDF measures as relative changes in blood flow from a baseline value.

The volunteers donned a backpack with three different conditions: empty, 5 kg load, and 10 kg load. To maximize surface contact area of the backpack and prevent load carriage of the backpack on the buttock, then backpack straps were adjusted so the backpacks were all worn with the top of the backpack at shoulder level throughout the experiment, for example, the backpack straps were adjusted to maximize the contact of the backpack with the volunteers' back (Fig. 2). In the beginning of the experiment, subjects donned an empty backpack sitting for 8 min. Sitting positions in the experiments were used solely to allow the volunteers' muscle oxygenation and skin blood flow to return to baseline before continuing on to the next testing condition. Relevant data presented were all collected from the standing positions. Next, subjects stood for 5 min wearing an empty backpack in order to establish baseline values. The subjects rested for 8 min again with an empty backpack kept on to allow muscle oxygenation and skin bloodflow to return to normal. We were not able to immediately check if skin bloodflow and muscle oxygenation values return to baseline, but pilot studies determined that the 8 min resting period was sufficient for these measures to return to baseline. Further- more, test order (either 5 kg or 10 kg condition) after baseline condition were randomized with equal number of subjects. Sub- jects wore either a 5 kg or 10 kg loaded backpack for 5 min followed by an 8 min rest period and repeated. Measurements taken from the last 60 s of the conditions were analyzed. Subjects rated their perceived pain in their shoulder at the end of each measurement using a visual analog scale (0 ¼no pain and 10 ¼worst pain imaginable). All tests were conducted at room temperature (24C).

Statistical analyses were performed using IBM SPSS Statistics (version 21.0, IBM Corp., Armonk, NY). Oxygenation and skin blood flow data were analyzed using repeated-measures ANOVA followed by pairwise comparisons (Least Significant Difference). Perceived pain data was analyzed with Wilcoxon signed rank test. Oxygena- tion and skin blood flow data were presented as means ± SD.

Perceived pain data was presented as medians±SD. Signiﬁcance was set at p<0.05.

3. Results

Increasing backpack load to 5 kg, and then to 10 kg signiﬁcantly decreased trapezius oxygenation (Fig. 3, p<0.01, main effect for load). Mean oxygenation levels after wearing an empty backpack, Fig. 1.The NIRS sensor and the LDF probe were placed over the right and left upper

trapezius muscles, respectively. They were placed under the backpack strap beneath the subjects' T-shirts and proximally transverse to the disc between theﬁrst and second thoracic vertebra for all subjects. LDF probe and NIRS sensor not drawn to scale for graphically clarity.

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5 kg backpack, and 10 kg backpack were 63±9, 57±15, and 50±17 rSO2, respectively. Oxygenation levels while donning the 10 kg backpack were signiﬁcantly lower than oxygenation levels while donning either the 5 kg backpack (p<0.05) or the empty backpack (p¼0.023). Therefore, donning 10 kg backpack for 5 min reduced

mean muscle oxygenation by 22±23%. Mean muscle oxygenation was reduced by 14±15% after donning a backpack with a 10 kg load.

Increasing backpack load by 5 kg, and then 10 kg significantly decreased shoulder skin microvascular flow (Fig. 4, p ¼ 0.02, repeated-measures ANOVA). Skin blood flow after wearing an empty backpack, 5 kg backpack, and 10 kg backpack were 0.60±0.54, 0.28±0.39, and 0.11±0.14 V, respectively. Donning a 10 kg backpack load significantly lowered skin blood flow by 82% ± 22% as compared to the empty backpack condition (p¼0.024). However, skin bloodflow while donning a 5 kg backpack load was not significantly different from the empty backpack control condition.

Perceived pain was signiﬁcantly higher when wearing both the 10 kg (median perceived pain of 4) and 5 kg (median perceived pain of 2) backpack, as compared to the empty backpack (median perceived pain of 0) (Fig. 5, p<0.05).

4. Discussion

The present data support our hypothesis that increasing backpack load decreases muscle oxygenation and skin bloodflow in shoulders of adults. Tissue oxygenation and skin microvascular flow decreased significantly when donning a 10 kg backpack, which represents an 11e23% bodyweight load. Moreover, the present data demonstrate that reductions of skin microvascular flow and oxygenation are accompanied by greater perceived shoulder pain.

Compression of the shoulder by the backpack strap decreased skin microvascularflow. We did not measure deep tissue microvascular flow beneath the backpack strap due to the limited penetration of laser light. However, it is possible that compression of tissue beneath the backpack strap is transmitted to deeper tissues. The present study did not directly measure skin contact pressure. However, donning a 10 kg backpack load decreases skin blood flow by 82% as compared to the 65% decrease in skin microvascularflow with 10 mmHg of externally applied pressure (Holloway et al., 1976).Macias et al. (2005)report that the peak skin contact pressure beneath backpack straps at 10% (mean load of 6.2 kg) bodyweight in children are 36e67 mmHg, and at 20%

bodyweight (mean load of 12.4 kg) are 70e110 mmHg. When

Fig. 3.A 10 kg but not a 5 kg backpack significantly lowers muscle oxygenation in the upper trapezius. Data displayed as means±SD. Significant repeated-measures ANOVA main effect for load, p<0.01.yOxygenation is significantly lower while wearing a 10 kg backpack than oxygenation compared to wearing an empty backpack, p¼0.023.zOxygenation is significantly lower while wearing a 10 kg backpack than oxygenation while wearing a 5 kg backpack, p<0.05. Mean oxygenation decreased by 22%±23% and 14%±15% from empty backpack condition to 10 kg load condition and from 5 kg load condition to 10 kg load condition, respectively.

Fig. 2.Backpacks were worn high on the back throughout the experiment. The backpack straps were worn securely by all subjects throughout the experiment.

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inflated, tourniquet cuffs transmit compression from the skin surface to the femur (approximately 5e10 cm deep) (Crenshaw et al., 1988; Hargens et al., 1989). Therefore, it may be possible that high backpack loads diminish microvascularflows to tissues deeper than regions monitored in the present study. The lower tissue oxygenation observed when donning a 10 kg backpack load sug- gests decreased microcirculatory bloodflow and ischemia to un- derlying shoulder tissues (Hampson and Piantadosi, 1988).

Therefore, this ischemia may produce higher levels of perceived pain with heavier backpack loads.

Hadid and co-workers demonstrated that the magnitude of the compressive forces beneath backpack (25 kg) straps are sufficient to induce nerve damage (Hadid et al., 2012). Kim and coworkers document that a 12 kg backpack decreases tactical sensation at the fingers and lower brachial artery blood flow in only 10 min of backpack donning (Kim et al., 2014). Our presentfindings quantify the magnitude of change in oxygenation and skin microvascular flow from donning a 10 kg backpack, thus providing us a better idea

of the extent of the physiological effects of carrying heavy backpacks. While the long-term effects of carrying heavy backpacks are still unknown, given the results of this study and previous research, backpack loads should be minimized to reduce compression of tissues beneath backpack straps and to avoid pain.

Some limitations in this study should be considered. This study employed backpack donning duration of less than 10 min. The duration of backpack carriage was minimized to enable subjects to don heavy loads and to complete each study of all subjects.

Approximately 61% of students from 4th to 12th grade typically don a backpack to and from school for more than 20 min a day (Talbott et al., 2009). The testing duration used in the present study is less than the typical length of backpack use. However, our measures of bloodﬂow and oxygenation were stable during the last minute of each condition. It is possible that longer carriage duration may decrease tissue oxygenation and increase perceived pain further.

Therefore, the observed decrements in tissue oxygenation occurred after a relatively short duration and may be even greater during Fig. 4.Heavier loads produced lower skin microvascularﬂow in the upper trapezius. Data are means±SD. *Signiﬁcant repeated-measures ANOVA main effect for load, p¼0.02.

ySkin bloodflow while donning the 10 kg backpack was significantly 82%±22% lower than skin bloodflow while donning the empty backpack, p¼0.024.

Fig. 5.Shoulder pain while donning a loaded backpack. Data displayed as median±SD. *Perceived pain was signiﬁcantly higher when wearing both the 10 kg and 5 kg backpack, as compared to the empty backpack, p<0.05.

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extended donning durations. In addition, placement of the probe beneath the shoulder strap may have altered the strap-to-skin interface. However, to minimize this confounding variable probe thickness was less than 2.2 mm. Moreover, the subjects did not report pain associated with probe placement during the study.

Skin contact pressures on the right shoulder were 40 mmHg higher than the left shoulder when donning a loaded backpack (Macias et al., 2005). In the present study, a 10 kg backpack load resulted in a 22% decrease in tissue oxygenation on the right shoulder and 82% decrease in skin bloodﬂow on the left shoulder.

The backpack straps were adjusted to distribute the load equally among the left and right shoulders. However, if the skin contact pressure was higher on the right shoulder than the left, we would anticipate that the skin microvascularﬂow decrease on the right shoulder to be greater than the 82% decrease observed on the left shoulder. The backpack utilized in the present study consisted of two shoulder straps (5.5 cm width). Alternate backpack designs, for example those utilizing hip-belts can reduce shoulder strap compressive forces by 29% (Mackie et al., 2005). Therefore, backpack designs that reduce skin contact pressures may minimize reductions to skin microvascularﬂow and shoulder oxygenation.

Future studies should focus on the effects of heavy backpack loads on populations such as school children and soldiers (Rodriguez-Soto et al., 2013). In surveying students in grades 4e12, 99.9% use backpacks (Talbott et al., 2009). Therefore, it is important to document if 10% bodyweight backpack loads affect tissue blood flow and oxygenation in this younger population. In conclusion, backpack loads of 10 kg decrease shoulder muscle oxygenation and skin microvascularflow significantly. In addition, greater perceived shoulder pain is reported in association with lower muscle oxygenation and skin microvascular flow. Therefore, minimizing backpack loads and using backpacks that distribute skin contact pressures more widely may help minimize shoulder pain.

Disclosure of potential conﬂict of interest There is no conﬂict of interest in this study.

Acknowledgments

The authors thank Brittany Lim for her assistance during the early stages of this study with the early designs of the experiment.

The authors also thank Robert Healey for backpack illustrations.

The authors also thank Drs. Sae Hoon Kim and Jamila Siamwala for their assistance and helpful discussion of the experimental results.

This work is supported by the National Space Biomedical Research Institute through NCC 9-58 (to BRM). This study was funded by NASA grant # NNX10AM18G (to ARH).

References

Aratow, M., Hargens, A.R., Meyer, J.U., Arnaud, S.B., 1991. Postural responses of head and foot cutaneous microvascularﬂow and their sensitivity to bed rest. Aviat.

Space Environ. Med. 62, 246e251.

Celie, B., Boone, J., Van Coster, R., Bourgois, J., 2012. Reliability of near infrared spectroscopy (NIRS) for measuring forearm oxygenation during incremental handgrip exercise. Eur. J. Appl. Physiol. 112, 2369e2374.

Crenshaw, A.G., Hargens, A.R., Gershuni, D.H., Rydevik, B., 1988. Wide tourniquet cuffs more effective at lower inﬂation pressures. Acta Orthop. 59, 447e451.

Cui, W., Kumar, C., Chance, B., 1991. Experimental study of migration depth for the photons measured at sample surface. Time-Resolv. Spectrosc. Imaging Tissues 1431, 181e191.

Forjuoh, S.N., Lane, B.L., Schuchmann, J.A., 2003. Percentage of body weight carried by students in their school backpacks. Am. J. Phys. Med. Rehabil. 82, 261e266.

Association of Academic Physiatrists.

Grimmer, K., Williams, M., 2000. Gender-age environmental associates of adoles- cent low back pain. Appl. Ergon. 31, 343e360.

Hadid, A., Epstein, Y., Shabshin, N., Gefen, A., 2012. Modeling mechanical strains and stresses in soft tissues of the shoulder during load carriage based on load- bearing open MRI. J. Appl. Physiol. 112, 597e606.

Hampson, N.B., Piantadosi, C.A., 1988. Near infrared monitoring of human skeletal muscle oxygenation during forearm ischemia. J. Appl. Physiol. 64, 2449e2457.

Hargens, A.R., Akeson, W.H., Mubarak, S.J., Owen, C.A., Gershuni, D.H., Garﬁn, S.R., Lieber, R.L., Danzig, L.A., Botte, M.J., Gelberman, R.H., 1989. Tissueﬂuid pressures: from basic research tools to clinical applications. J. Orthop. Res. 7, 902e909.

Hodges, G.J., Del Pozzi, A.T., 2014. Noninvasive examination of endothelial, sym- pathetic, and myogenic contributions to regional differences in the human cutaneous microcirculation. Microvasc. Res. 93, 87e91.

Holloway, G.A., Daly, C.H., Kennedy, D., Chimoskey, J., 1976. Effects of external pressure loading on human skin bloodﬂow measured by 133Xe clearance.

J. Appl. Physiol. 40, 597e600.

Hong, Y., Li, J.X., Fong, D.T., 2008. Effect of prolonged walking with backpack loads on trunk muscle activity and fatigue in children. J. Electromyogr. Kinesiol.: Off. J.

Int. Soc. Electrophysiol. Kinesiol. 18, 990e996.

Kim, S.H., Neuschwander, T.B., Macias, B.R., Bachman Jr., L., Hargens, A.R., 2014.

Upper extremity hemodynamics and sensation with backpack loads. Appl.

Ergon. 45, 608e612.

Macias, B.R., Murthy, G., Chambers, H., Hargens, A.R., 2005. High contact pressure beneath backpack straps of children contributes to pain. Arch. Pediatr. Adolesc.

Med. 159, 1186e1187.

Mackie, H.W., Stevenson, J.M., Reid, S.A., Legg, S.J., 2005. The effect of simulated school load carriage conﬁgurations on shoulder strap tension forces and shoulder interface pressure. Appl. Ergon. 36, 199e206.

Negrini, S., Carabalona, R., Sibilla, P., 1999. Backpack as a daily load for school- children. Lancet 354, 1974.

Nilsson, G.E., Tenland, T., Oberg, P.A., 1980. Evaluation of a laser dopplerﬂow- meter for measurement of tissue bloodﬂow. IEEE Trans. Bio-Med. Eng. 27, 597e604.

Pascoe, D.D., Pascoe, D.E., Wang, Y.T., Shim, D.M., Kim, C.K., 1997. Inﬂuence of carrying book bags on gait cycle and posture of youths. Ergonomics 40, 631e641.

Piscione, J., Gamet, D., 2006. Effect of mechanical compression due to load carrying on shoulder muscle fatigue during sustained isometric arm abduction: an electromyographic study. Eur. J. Appl. Physiol. 97, 573e581.

Rodriguez-Soto, A.E., Jaworski, R., Jensen, A., Niederberger, B., Hargens, A.R., Frank, L.R., Kelly, K.R., Ward, S.R., 2013. Effect of load carriage on lumbar spine kinematics. Spine 38, E783eE791.

Talbott, N.R., Bhattacharya, A., Davis, K.G., Shukla, R., Levin, L., 2009. School backpacks: it's more than just a weight problem. Work: J. Prev. Assess. Rehabil. 34, 481e494.

Watenpaugh, D.E., Breit, G.A., Buckley, T.M., Ballard, R.E., Murthy, G., Hargens, A.R., 2004. Human cutaneous vascular responses to whole-body tilting, Gz centri- fugation, and LBNP. J. Appl. Physiol. (1985) 96, 2153e2160.