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Benefits of a 12 week physical activity programme on muscle and bone health in people living with HIV
Journal of Cachexia, Sarcopenia and Muscle ( IF 8.9 ) Pub Date : 2021-10-01 , DOI: 10.1002/jcsm.12824
Matteo Bonato 1, 2 , Laura Galli 3 , Simona Bossolasco 3 , Cecilia Bertocchi 3 , Giuseppe Balconi 3 , Marco Borderi 4 , Pierluigi Viale 4 , Gaspare Pavei 5 , Giampiero Merati 6 , Antonio La Torre 1, 2 , Adriano Lazzarin 3 , Giuseppe Banfi 2, 7 , Paola Cinque 3
Affiliation  

Thanks to the use of combination antiretroviral treatment (cART) people living with HIV (PLWH) have a similar life expectancy to HIV-negative people.1, 2 However, PLWH may be at higher risk to develop chronic diseases associated with persistent immune activation despite virological control.3 Physical activity has been demonstrated because to improve health parameters in PLWH.4 We previously showed in a pilot study that a 12 week protocol consisting of three sessions per week of 60 min brisk walking at 65–75% of maximal heart rate with (strength-walk group) 30 min resistance training or without (walk group), improved physical performance, lipid profile, and inflammatory markers.5

We assessed body composition and bone health in a subset of 25 cART-treated PLWH (Table S1) from this study [19/25 men, median age: 51 (Q1–Q3: 48–56) years; CD4+: 576 (463–701)], with particular attention to the indicators of osteosarcopenia. Percentage of fat mass (FM), fat free mass (FFM) at arms, limbs, and as total body, and bone mineral density (BMD), t-score and z-score at spine (L3/L4), femoral neck, and trochanter were measured by DEXA (Lunar Prodigy, version 8.8, GE, Medical System Madison, WI). The appendicular skeletal muscle mass (ASMMI) index was calculated to assess the presence of sarcopenia (women: ≤5.5 kg/m2; men: ≤7.0 kg/m2).6 The bone t-score was calculated to assess the presence of osteoporosis (−2.5) and osteopenia (−1 to −2.5). Bone remodelling biomarkers were measured in cryopreserved plasma samples by commercially available enzyme-linked immunosorbent assays (R&D Systems Inc, Minneapolis, MN, USA). These included osteoprotegerin (OPG), receptor activator of NF-kappaB ligand (RANKL), c-terminal telopeptide (CTX), and bone alkaline phosphatase (BAP). Samples were analysed in batch at the end of the study and blindly with respect to group assignment. Quantitative variables were expressed as median, first, and third quartiles (Q1–Q3). Per cent changes between baseline (BL) and after 12 week of training W12 within each group were assessed by Wilcoxon signed rank test and between-groups by Mann–Whitney test.

All participants completed the 12 week programme with a median adherence of 64% (Q1–Q3: 59–75%). Among all participants, significant W12 changes in ASMMI from BL were observed in both training groups, and in total, arms and legs FFM in the strength-walk group, with changes from BL significantly larger in the strength-walk than in the walk group for all measurements (Figure 1). According to ASMMI, eight participants (32%; three women and five men) had sarcopenia at baseline [women: 5.5 (5.4–5.5) kg/m2; men: 6.5 (6.4–6.7) kg/m2; age 52 (48–53)]. At Week 12, six of these eight participants normalized ASMMI, including two women [both in the walk group: 6.1 (6.0–6.1) kg/m2] and four men [two of the walk group and two of the strength-walk group: 7.2 (7.1–7.2) kg/m2]. Neither significant W12 changes from BL nor significant change differences between groups were observed for BMD, t-score, z-score at spine, femoral neck, and trochanter. According to the t-score, three participants were diagnosed with osteoporosis at BL (12%) and 20 (80%) with osteopenia. At the end of the training protocol, none of the participants improved the t-score (Table 1). Significant W12 increases from BL were observed in CTX in both training groups. No significant changes were observed of BAP, OPG and RANKL level, and OPG/RANK ratio (Table 1).

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Figure 1
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Changes of body composition parameters in people living with HIV following a 12 week physical activity protocol of walk or strength-walk exercise. Data were assessed by Mann–Whitney test (differences between-groups) and Wilcoxon signed rank test (changes between BL and W16 within-groups, below graphs). Level of significance was set at 0.05. Box plots show median and interquartile ranges, and whiskers extend to the highest and lowest observations. ASMMI, appendicular skeletal muscle mass index, BL, baseline; W12, week 12.
Table 1. Bone mineral density, t-score, z-score results, and bone remodelling biomarkers results
Walk (n = 15) Strength-walk (n = 10)
BL W12 P BL W12 P
Spine
BMD (g/cm2) 61.5 (56.8–64.8) 62.4 (57.5–65.0) 0.135 62.2 (53.9–64.2) 62.3 (54.5–64.6) 0.109
t-score −1.2 (−1.6 to –0.8) −1.1 (−1.5 to –0.7) 0.173 −1.4 (−1.9 to –1.2) −1.3 (1.8 to –0.9) 0.141
z-score −1.0 (−1.4 to –0.7) −0.8 (−1.5 to –0.2) 0.113 −1.4 (−1.8 to –0.8) −1.2 (−2.0 to –0.7) 0.137
Femoral neck
BMD (g/cm2) 4.3 (3.7–5.1) 4.0 (4.8–5.4) 0.107 5.2 (4.3–5.9) 5.2 (4.3–5.9) 0.711
t-score −1.6 (−1.9 to –0.4) −1.5 (−1.8 to –0.3) 0.201 −0.9 (−1.0 to –0.5) −0.8 (−1.1 to –0.4) 0.468
z-score −1.1 (−1.6 to –0.2) −0.9 (−1.3 to –0.3) 0.147 −1.3 (−1.5 to –0.8) −1.1 (−1.5 to –0.2) 0.297
Trocanther
BMD (g/cm2) 8.3 (6.7–9.7) 8.6 (6.8–9.8) 0.229 9.7 (8.7–10.3) 9.4 (8.7–10.6) 0.642
t-score −1.5 (−2–2 to –0.2) −1.5 (−2.1 to –0.1) 0.108 −0.6 (−1.2 to –0.1) −0.7 (−1.2 to –0.2) 0.394
z-score −0.9 (−1.5 to –0.1) −1.0 (−1.7 to –0.1) 0.688 −0.4 (−0.9 to –0.1) −0.8 (−1.3 to –0.2) 0.203
Bone remodelling biomarkers
OPG (pg/mL) 1393 (1244–2418) 1617 (1253–2240) 0.107 1324 (957–1658) 1243 (1123–1516) 0.769
RANKL (pg/mL) 4.92 (3.23–7.78) 4.96 (2.62–7.78) 0.497 4.96 (2.62–5.88) 4.36 (2.91–6.57) 0.921
OPG/RANKL 325 (231–492) 354 (195–433) 0.978 228 (173–310) 212 (169–306) 0.193
CTX (pg/mL) 0.54 (0.32–0.84) 0.76 (0.57–0.92) 0.034 0.61 (0.36–0.67) 0.76 (0.46–0.87) 0.005
BAP (ng/mL) 8.44 (5.42–9.71) 7.10 (5.29–9.02) 0.124 8.63 (5.87–11.67) 6.83 (6.12–10.09) 0.185
  • BAP, bone alkaline phosphatase; BL, baseline; BMD, bone mineral density; CTX, c-terninal telopeptide; OPG, osteoprotegerin; RANKL, receptor activator of NF-kappaB ligand; W12, week 12.
  • Values are expressed as median (Q1–Q3). Data were assessed by Wilcoxon signed rank test (changes between BL and W12 within groups and by BMD).

The main finding of this study was a significant increase in muscle mass in PLWH including patients with sarcopenia. This is relevant because sarcopenia is an emerging health issue in HIV infection,7, 8 where both ageing and persistent immune activation may contribute to its development, in addition to other potential factors, like cART, risk behaviours, for example, smoking or use of drugs, and other co-morbidities.9 Although moderate aerobic activity alone was also associated in this study with increased appendicular muscle mass, the benefit of concurrent and resistance training was significantly superior, confirming that resistance exercise is relevant to counteract sarcopenia in PLWH.10, 11 We did not observe improvements of DEXA bone parameters following the 12 week moderate-intensity exercise protocol. It is possible that this exercise intervention was too short to increase bone mineralization, relative to the length of a bone remodelling cycle.12, 13 On the other hand, we observed a significant increase of CTX plasma level in both training groups, with neither change of the classical bone formation marker BAP nor of the plasma OPG/RANKL concentration ratio as additional index of bone resorption. The increase of CTX plasma levels following exercise may thus represent a feedback stimulus for the reparative activity of the bone-remodelling unit.14

Our study has some limitations. First, we did not include a non-exercise control group. Second, the low sample size did not allow drawing firm conclusions on the efficacy of the two training protocols on the studied parameters. Finally, this was a relatively short-duration study.

In conclusions, PLWH following a physical activity protocol based on the combination of resistance and moderate aerobic training is likely to improve to improve total and appendicular muscle mass. Our study provides information to design larger interventional controlled studies to assess the efficacy of exercise protocols in increasing muscle mass and potentially reducing sarcopenia in PLWH.



中文翻译:

为期 12 周的体育锻炼计划对 HIV 感染者肌肉和骨骼健康的益处

由于使用联合抗逆转录病毒治疗 (cART),艾滋病毒感染者 (PLWH) 的预期寿命与艾滋病毒阴性者相似。1, 2然而,尽管进行了病毒学控制,PLWH 可能更容易患上与持续免疫激活相关的慢性疾病。3身体活动已被证明是因为可以改善 PLWH 的健康参数。4我们之前在一项试点研究中表明,为期 12 周的方案包括每周 3 次 60 分钟的快走,以最大心率的 65-75% 进行(力量步行组)30 分钟阻力训练或不进行(步行组) ,改善身体机能、血脂和炎症标志物。5

我们评估了本研究中 25 名接受 cART 治疗的 PLWH 的身体成分和骨骼健康(S1)[19/25 男性,中位年龄:51(Q1-Q3:48-56)岁;CD4 + : 576 (463–701)],特别注意骨肌减少症的指标。手臂、四肢和全身的脂肪量 (FM)、无脂肪量 (FFM) 以及脊柱 (L3/L4)、股骨颈的骨矿物质密度 (BMD)、 t分数和z分数的百分比,和转子通过 DEXA(Lunar Prodigy,8.8 版,GE,Medical System Madison,WI)测量。计算附肢骨骼肌质量 (ASMMI) 指数以评估是否存在肌肉减少症(女性:≤5.5 kg/m 2;男性:≤7.0 kg/m 2)。6骨头计算t分数以评估骨质疏松症 (-2.5) 和骨质减少 (-1 至 -2.5) 的存在。通过市售的酶联免疫吸附测定法(R&D Systems Inc,Minneapolis,MN,USA)在冷冻保存的血浆样品中测量骨重塑生物标志物。这些包括骨保护素 (OPG)、NF-kappaB 配体的受体激活剂 (RANKL)、c 末端端肽 (CTX) 和骨碱性磷酸酶 (BAP)。在研究结束时对样品进行分批分析,并在分组分配方面进行盲目分析。定量变量表示为中位数、第一和第三四分位数(Q1-Q3)。通过 Wilcoxon 符号秩检验和 Mann-Whitney 检验评估每组内基线 (BL) 和训练 12 周后 W12 之间的百分比变化。

所有参与者都完成了为期 12 周的计划,中位依从率为 64%(第一季度至第三季度:59-75%)。在所有参与者中,在两个训练组中都观察到 BL 的 ASMMI 的 W12 显着变化,并且在力量步行组中,总体而言,手臂和腿部 FFM 的变化在力量步行组中从 BL 的变化明显大于步行组。所有测量值(1)。根据 ASMMI,8 名参与者(32%;3 名女性和 5 名男性)在基线时患有肌肉减少症 [女性:5.5 (5.4–5.5) kg/m 2;男性:6.5 (6.4–6.7) kg/m 2;52 岁(48-53 岁)]。在第 12 周,这 8 名参与者中有 6 名使 ASMMI 正常化,其中包括两名女性 [均在步行组:6.1 (6.0–6.1) kg/m 2] 和四名男子 [步行组中的两名和力量步行组中的两名:7.2 (7.1–7.2) kg/m 2 ]。在脊柱、股骨颈和大转子处的 BMD、 t评分、z评分均未观察到与 BL 相比的 W12 显着变化和组间显着变化差异。根据t分数,3 名参与者在 BL (12%) 被诊断出患有骨质疏松症,20 名 (80%) 被诊断出患有骨质减少症。在培训协议结束时,没有一个参与者提高了t分数(1)。在两个训练组的 CTX 中观察到 BL 的 W12 显着增加。BAP、OPG 和 RANKL 水平以及 OPG/RANK 比值均未观察到显着变化(1)。

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图1
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HIV 感染者在 12 周的步行或力量步行运动方案后身体成分参数的变化。通过 Mann-Whitney 检验(组间差异)和 Wilcoxon 符号秩检验(组内 BL 和 W16 之间的变化,下图)评估数据。显着性水平设定为 0.05。箱线图显示中位数和四分位数范围,胡须延伸到最高和最低观测值。ASMMI,附肢骨骼肌质量指数,BL,基线;W12,第 12 周。
表 1.骨矿物质密度、t分数、z分数结果和骨重塑生物标志物结果
步行(n  = 15) 力量行走(n  = 10)
提单 W12 提单 W12
脊柱
骨密度 (g/cm 2 ) 61.5 (56.8–64.8) 62.4 (57.5–65.0) 0.135 62.2 (53.9–64.2) 62.3 (54.5–64.6) 0.109
t分数 -1.2(-1.6 至 –0.8) -1.1(-1.5 到 –0.7) 0.173 -1.4(-1.9 到 –1.2) −1.3(1.8 到 –0.9) 0.141
z分数 -1.0(-1.4 到 –0.7) -0.8(-1.5 到 –0.2) 0.113 -1.4(-1.8 到 –0.8) -1.2(-2.0 到 –0.7) 0.137
股骨颈
骨密度 (g/cm 2 ) 4.3 (3.7–5.1) 4.0 (4.8–5.4) 0.107 5.2 (4.3–5.9) 5.2 (4.3–5.9) 0.711
t分数 -1.6(-1.9 到 –0.4) -1.5(-1.8 到 –0.3) 0.201 -0.9(-1.0 到 –0.5) -0.8(-1.1 至 –0.4) 0.468
z分数 -1.1(-1.6 至 –0.2) -0.9(-1.3 至 –0.3) 0.147 -1.3(-1.5 到 –0.8) -1.1(-1.5 到 –0.2) 0.297
棘轮
骨密度 (g/cm 2 ) 8.3 (6.7–9.7) 8.6 (6.8–9.8) 0.229 9.7 (8.7–10.3) 9.4 (8.7–10.6) 0.642
t分数 -1.5(-2–2 至 –0.2) -1.5(-2.1 到 –0.1) 0.108 -0.6(-1.2 到 –0.1) -0.7(-1.2 到 –0.2) 0.394
z分数 -0.9(-1.5 到 –0.1) -1.0(-1.7 到 –0.1) 0.688 -0.4(-0.9 至 –0.1) -0.8(-1.3 到 –0.2) 0.203
骨重塑生物标志物
OPG (皮克/毫升) 1393 (1244–2418) 1617 (1253–2240) 0.107 1324 (957–1658) 1243 (1123–1516) 0.769
RANKL (皮克/毫升) 4.92 (3.23–7.78) 4.96 (2.62–7.78) 0.497 4.96 (2.62–5.88) 4.36 (2.91–6.57) 0.921
OPG/RANKL 325 (231–492) 354 (195–433) 0.978 228 (173–310) 212 (169–306) 0.193
CTX (皮克/毫升) 0.54 (0.32–0.84) 0.76 (0.57–0.92) 0.034 0.61 (0.36–0.67) 0.76 (0.46–0.87) 0.005
BAP (纳克/毫升) 8.44 (5.42–9.71) 7.10 (5.29–9.02) 0.124 8.63 (5.87–11.67) 6.83 (6.12–10.09) 0.185
  • BAP,骨碱性磷酸酶;BL,基线;BMD,骨矿物质密度;CTX,c-末端端肽;OPG,骨保护素;RANKL,NF-kappaB配体的受体激活剂;W12,第 12 周。
  • 值表示为中位数(Q1-Q3)。通过 Wilcoxon 符号秩检验(组内 BL 和 W12 之间的变化和 BMD)评估数据。

这项研究的主要发现是包括肌肉减少症患者在内的 PLWH 的肌肉质量显着增加。这是相关的,因为肌肉减少症是 HIV 感染中一个新出现的健康问题,7, 8除了其他潜在因素(如 cART、风险行为,例如吸烟或使用药物和其他并发症。9尽管在这项研究中,仅适度的有氧运动也与增加的四肢肌肉质量相关,但同时进行和阻力训练的益处显着优越,这证实了阻力运动与抵抗 PLWH 的肌肉减少症有关。10, 11在 12 周中等强度运动方案后,我们没有观察到 DEXA 骨骼参数的改善。相对于骨重塑周期的长度,这种运动干预可能太短而无法增加骨矿化。12, 13另一方面,我们观察到两个训练组的 CTX 血浆水平显着增加,经典骨形成标志物 BAP 和血浆 OPG/RANKL 浓度比都没有变化作为骨吸收的附加指标。因此,运动后 CTX 血浆水平的增加可能代表了对骨重塑单元修复活动的反馈刺激。14

我们的研究有一些限制。首先,我们没有包括非运动对照组。其次,低样本量无法就两种训练方案对所研究参数的有效性得出确切结论。最后,这是一项相对较短的研究。

总之,PLWH 遵循基于阻力和适度有氧训练相结合的身体活动方案可能会改善总肌肉和附肢肌肉质量。我们的研究为设计更大规模的介入对照研究提供了信息,以评估运动方案在增加肌肉质量和潜在减少 PLWH 肌肉减少症方面的功效。

更新日期:2021-10-01
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