Sonographic Measurements of Rectus Femoris Muscle Thickness Strongly Predict Neutropenia in Cancer Patients Receiving Chemotherapy
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Patients
2.2. Data Collection
2.3. Measurement of Skeletal Muscle Area and Definition of Low Skeletal Muscle Mass
2.3.1. CT Measurements
2.3.2. US Measurements
2.4. Definition of Myelotoxicity
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Siddiqui, J.A.; Pothuraju, R.; Jain, M.; Batra, S.K.; Nasser, M.W. Advances in cancer cachexia: Intersection between affected organs, mediators, and pharmacological interventions. Biochim. Biophys. Acta Rev. Cancer 2020, 1873, 188359. [Google Scholar] [CrossRef] [PubMed]
- Wiegert, E.V.M.; de Oliveira, L.C.; Calixto-Lima, L.; Borges, N.A.; Rodrigues, J.; da Mota, E.S.L.M.S.; Peres, W.A.F. Association between low muscle mass and survival in incurable cancer patients: A systematic review. Nutrition 2020, 72, 110695. [Google Scholar] [CrossRef] [PubMed]
- Go, S.I.; Park, M.J.; Song, H.N.; Kang, M.H.; Park, H.J.; Jeon, K.N.; Kim, S.H.; Kim, M.J.; Kang, J.H.; Lee, G.W. Sarcopenia and inflammation are independent predictors of survival in male patients newly diagnosed with small cell lung cancer. Support. Care Cancer 2016, 24, 2075–2084. [Google Scholar] [CrossRef]
- Jung, H.-W.; Kim, J.W.; Kim, J.-Y.; Kim, S.-W.; Yang, H.K.; Lee, J.W.; Lee, K.-W.; Kim, D.-W.; Kang, S.-B.; Kim, K.-I.; et al. Effect of muscle mass on toxicity and survival in patients with colon cancer undergoing adjuvant chemotherapy. Support. Care Cancer 2015, 23, 687–694. [Google Scholar] [CrossRef] [PubMed]
- Barret, M.; Antoun, S.; Dalban, C.; Malka, D.; Mansourbakht, T.; Zaanan, A.; Latko, E.; Taieb, J. Sarcopenia Is Linked to Treatment Toxicity in Patients with Metastatic Colorectal Cancer. Nutr. Cancer 2014, 66, 583–589. [Google Scholar] [CrossRef] [PubMed]
- Prado, C.M.M.; Baracos, V.E.; McCargar, L.J.; Reiman, T.; Mourtzakis, M.; Tonkin, K.; Mackey, J.R.; Koski, S.; Pituskin, E.; Sawyer, M.B. Sarcopenia as a Determinant of Chemotherapy Toxicity and Time to Tumor Progression in Metastatic Breast Cancer Patients Receiving Capecitabine Treatment. Clin. Cancer Res. 2009, 15, 2920–2926. [Google Scholar] [CrossRef] [PubMed]
- Huillard, O.; Mir, O.; Peyromaure, M.; Tlemsani, C.; Giroux, J.; Boudou-Rouquette, P.; Ropert, S.; Delongchamps, N.B.; Zerbib, M.; Goldwasser, F. Sarcopenia and body mass index predict sunitinib-induced early dose-limiting toxicities in renal cancer patients. Br. J. Cancer 2013, 108, 1034–1041. [Google Scholar] [CrossRef] [PubMed]
- Wendrich, A.W.; Swartz, J.E.; Bril, S.I.; Wegner, I.; de Graeff, A.; Smid, E.J.; de Bree, R.; Pothen, A.J. Low skeletal muscle mass is a predictive factor for chemotherapy dose-limiting toxicity in patients with locally advanced head and neck cancer. Oral Oncol. 2017, 71, 26–33. [Google Scholar] [CrossRef]
- Ali, R.; Baracos, V.E.; Sawyer, M.B.; Bianchi, L.; Roberts, S.; Assenat, E.; Mollevi, C.; Senesse, P. Lean body mass as an independent determinant of dose-limiting toxicity and neuropathy in patients with colon cancer treated with FOLFOX regimens. Cancer Med. 2016, 5, 607–616. [Google Scholar] [CrossRef]
- Ansari, E.; Chargi, N.; van Gemert, J.T.M.; van Es, R.J.J.; Dieleman, F.J.; Rosenberg, A.J.W.P.; Van Cann, E.M.; de Bree, R. Low skeletal muscle mass is a strong predictive factor for surgical complications and a prognostic factor in oral cancer patients undergoing mandibular reconstruction with a free fibula flap. Oral Oncol. 2020, 101, 104530. [Google Scholar] [CrossRef]
- Marty, E.; Liu, Y.; Samuel, A.; Or, O.; Lane, J. A review of sarcopenia: Enhancing awareness of an increasingly prevalent disease. Bone 2017, 105, 276–286. [Google Scholar] [CrossRef] [PubMed]
- Kurk, S.; Peeters, P.; Stellato, R.; Dorresteijn, B.; de Jong, P.; Jourdan, M.; Creemers, G.J.; Erdkamp, F.; de Jongh, F.; Kint, P.; et al. Skeletal muscle mass loss and dose-limiting toxicities in metastatic colorectal cancer patients. J. Cachexia Sarcopenia Muscle 2019, 10, 803–813. [Google Scholar] [CrossRef] [PubMed]
- Sjøblom, B.; Benth, J.; Grønberg, B.H.; Baracos, V.E.; Sawyer, M.B.; Fløtten, Ø.; Hjermstad, M.J.; Aass, N.; Jordhøy, M. Drug Dose Per Kilogram Lean Body Mass Predicts Hematologic Toxicity from Carboplatin-Doublet Chemotherapy in Advanced Non-Small-Cell Lung Cancer. Clin. Lung Cancer 2017, 18, e129–e136. [Google Scholar] [CrossRef] [PubMed]
- Willemsen, A.C.H.; Hoeben, A.; Lalisang, R.I.; Van Helvoort, A.; Wesseling, F.W.R.; Hoebers, F.; Baijens, L.W.J.; Schols, A. Disease-induced and treatment-induced alterations in body composition in locally advanced head and neck squamous cell carcinoma. J. Cachexia Sarcopenia Muscle 2020, 11, 145–159. [Google Scholar] [CrossRef] [PubMed]
- de Jong, C.; Chargi, N.; Herder, G.J.M.; van Haarlem, S.W.A.; van der Meer, F.; van Lindert, A.S.R.; Ten Heuvel, A.; Brouwer, J.; de Jong, P.A.; Devriese, L.A.; et al. The association between skeletal muscle measures and chemotherapy-induced toxicity in non-small cell lung cancer patients. J. Cachexia Sarcopenia Muscle 2022, 13, 1554–1564. [Google Scholar] [CrossRef] [PubMed]
- Hilmi, M.; Jouinot, A.; Burns, R.; Pigneur, F.; Mounier, R.; Gondin, J.; Neuzillet, C.; Goldwasser, F. Body composition and sarcopenia: The next-generation of personalized oncology and pharmacology? Pharmacol. Ther. 2019, 196, 135–159. [Google Scholar] [CrossRef] [PubMed]
- Tan, B.H.; Brammer, K.; Randhawa, N.; Welch, N.T.; Parsons, S.L.; James, E.J.; Catton, J.A. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur. J. Surg. Oncol. 2015, 41, 333–338. [Google Scholar] [CrossRef]
- Cruz-Jentoft, A.J.; Baeyens, J.P.; Bauer, J.M.; Boirie, Y.; Cederholm, T.; Landi, F.; Martin, F.C.; Michel, J.-P.; Rolland, Y.; Schneider, S.M.; et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010, 39, 412–423. [Google Scholar] [CrossRef]
- Prado, C.M.; Birdsell, L.A.; Baracos, V.E. The emerging role of computerized tomography in assessing cancer cachexia. Curr. Opin. Support. Palliat. Care 2009, 3, 269–275. [Google Scholar] [CrossRef]
- Shen, W.; Punyanitya, M.; Wang, Z.; Gallagher, D.; St-Onge, M.P.; Albu, J.; Heymsfield, S.B.; Heshka, S. Total body skeletal muscle and adipose tissue volumes: Estimation from a single abdominal cross-sectional image. J. Appl. Physiol. 2004, 97, 2333–2338. [Google Scholar] [CrossRef]
- Sergi, G.; Trevisan, C.; Veronese, N.; Lucato, P.; Manzato, E. Imaging of sarcopenia. Eur. J. Radiol. 2016, 85, 1519–1524. [Google Scholar] [CrossRef]
- Ticinesi, A.; Meschi, T.; Narici, M.V.; Lauretani, F.; Maggio, M. Muscle Ultrasound and Sarcopenia in Older Individuals: A Clinical Perspective. J. Am. Med. Dir. Assoc. 2017, 18, 290–300. [Google Scholar] [CrossRef] [PubMed]
- Nijholt, W.; Scafoglieri, A.; Jager-Wittenaar, H.; Hobbelen, J.S.M.; van der Schans, C.P. The reliability and validity of ultrasound to quantify muscles in older adults: A systematic review. J. Cachexia Sarcopenia Muscle 2017, 8, 702–712. [Google Scholar] [CrossRef] [PubMed]
- Strasser, E.M.; Draskovits, T.; Praschak, M.; Quittan, M.; Graf, A. Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age 2013, 35, 2377–2388. [Google Scholar] [CrossRef] [PubMed]
- Abe, T.; Thiebaud, R.S.; Loenneke, J.P.; Young, K.C. Prediction and validation of DXA-derived appendicular lean soft tissue mass by ultrasound in older adults. Age 2015, 37, 114. [Google Scholar] [CrossRef]
- Narici, M.V.; Maffulli, N. Sarcopenia: Characteristics, mechanisms and functional significance. Br. Med. Bull. 2010, 95, 139–159. [Google Scholar] [CrossRef]
- Abe, T.; Thiebaud, R.S.; Loenneke, J.P.; Loftin, M.; Fukunaga, T. Prevalence of site-specific thigh sarcopenia in Japanese men and women. Age 2014, 36, 417–426. [Google Scholar] [CrossRef]
- Abe, T.; Patterson, K.M.; Stover, C.D.; Geddam, D.A.; Tribby, A.C.; Lajza, D.G.; Young, K.C. Site-specific thigh muscle loss as an independent phenomenon for age-related muscle loss in middle-aged and older men and women. Age 2014, 36, 9634. [Google Scholar] [CrossRef]
- Minetto, M.A.; Caresio, C.; Menapace, T.; Hajdarevic, A.; Marchini, A.; Molinari, F.; Maffiuletti, N.A. Ultrasound-Based Detection of Low Muscle Mass for Diagnosis of Sarcopenia in Older Adults. PM&R 2016, 8, 453–462. [Google Scholar] [CrossRef]
- Ata, A.M.; Kara, M.; Kaymak, B.; Gürçay, E.; Çakır, B.; Ünlü, H.; Akıncı, A.; Özçakar, L. Regional and total muscle mass, muscle strength and physical performance: The potential use of ultrasound imaging for sarcopenia. Arch. Gerontol. Geriatr. 2019, 83, 55–60. [Google Scholar] [CrossRef]
- Sanada, K.; Kearns, C.F.; Midorikawa, T.; Abe, T. Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults. Eur. J. Appl. Physiol. 2006, 96, 24–31. [Google Scholar] [CrossRef] [PubMed]
- Abe, T.; Thiebaud, R.S.; Loenneke, J.P.; Ogawa, M.; Mitsukawa, N. Association between forearm muscle thickness and age-related loss of skeletal muscle mass, handgrip and knee extension strength and walking performance in old men and women: A pilot study. Ultrasound Med. Biol. 2014, 40, 2069–2075. [Google Scholar] [CrossRef] [PubMed]
- Kara, M.; Ata, A.M.; Kaymak, B.; Özçakar, L. Sonographic quantification of the forearm muscles in relation with handgrip strength. Clin. Physiol. Funct. Imaging 2018, 38, 1067–1068. [Google Scholar] [CrossRef] [PubMed]
- Common Terminology Criteria for Adverse Events (Ctcae) Version 5. Available online: https://ctep.cancer.gov/protocoldevelopment/electronic_applications/ctc.htm#ctc_50 (accessed on 10 November 2023).
- Huiskamp, L.F.J.; Chargi, N.; Devriese, L.A.; May, A.M.; Huitema, A.D.R.; de Bree, R. The Predictive Value of Low Skeletal Muscle Mass Assessed on Cross-Sectional Imaging for Anti-Cancer Drug Toxicity: A Systematic Review and Meta-Analysis. J. Clin. Med. 2020, 9, 3780. [Google Scholar] [CrossRef] [PubMed]
- Bozzetti, F. Forcing the vicious circle: Sarcopenia increases toxicity, decreases response to chemotherapy and worsens with chemotherapy. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2017, 28, 2107–2118. [Google Scholar] [CrossRef] [PubMed]
- Du Bois, D.; Du Bois, E.F. Clinical Calorimetry: Tenth Paper a Formula to Estimate the Approximate Surface Area If Height and Weight Be Known. Arch. Intern. Med. 1916, XVII, 863–871. [Google Scholar] [CrossRef]
- McLeay, S.C.; Morrish, G.A.; Kirkpatrick, C.M.; Green, B. The relationship between drug clearance and body size: Systematic review and meta-analysis of the literature published from 2000 to 2007. Clin. Pharmacokinet. 2012, 51, 319–330. [Google Scholar] [CrossRef]
- Prado, C.M. Body composition in chemotherapy: The promising role of CT scans. Curr. Opin. Clin. Nutr. Metab. Care 2013, 16, 525–533. [Google Scholar] [CrossRef]
- Prado, C.M.; Lieffers, J.R.; McCargar, L.J.; Reiman, T.; Sawyer, M.B.; Martin, L.; Baracos, V.E. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: A population-based study. Lancet Oncol. 2008, 9, 629–635. [Google Scholar] [CrossRef]
- Abe, T.; Loenneke, J.P.; Thiebaud, R.S.; Ogawa, M.; Mitsukawa, N. Age-related site-specific muscle loss in the thigh and zigzag walking performance in older men and women. Acta Physiol. Hung. 2014, 101, 488–495. [Google Scholar] [CrossRef]
- Borkan, G.A.; Hults, D.E.; Gerzof, S.G.; Robbins, A.H.; Silbert, C.K. Age changes in body composition revealed by computed tomography. J. Gerontol. 1983, 38, 673–677. [Google Scholar] [CrossRef] [PubMed]
- Gallagher, D.; Visser, M.; De Meersman, R.E.; Sepúlveda, D.; Baumgartner, R.N.; Pierson, R.N.; Harris, T.; Heymsfield, S.B. Appendicular skeletal muscle mass: Effects of age, gender, and ethnicity. J. Appl. Physiol. 1997, 83, 229–239. [Google Scholar] [CrossRef] [PubMed]
- Janssen, I.; Heymsfield, S.B.; Wang, Z.M.; Ross, R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J. Appl. Physiol. 2000, 89, 81–88. [Google Scholar] [CrossRef] [PubMed]
- Kara, M.; Kaymak, B.; Frontera, W.; Ata, A.M.; Ricci, V.; Ekiz, T.; Chang, K.V.; Han, D.S.; Michail, X.; Quittan, M.; et al. Diagnosing sarcopenia: Functional perspectives and a new algorithm from the ISarcoPRM. J. Rehabil. Med. 2021, 53, jrm00209. [Google Scholar] [CrossRef] [PubMed]
- Reeves, N.D.; Maganaris, C.N.; Narici, M.V. Ultrasonographic assessment of human skeletal muscle size. Eur. J. Appl. Physiol. 2004, 91, 116–118. [Google Scholar] [CrossRef] [PubMed]
- Aagaard, P.; Suetta, C.; Caserotti, P.; Magnusson, S.P.; Kjaer, M. Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure. Scand. J. Med. Sci. Sports 2010, 20, 49–64. [Google Scholar] [CrossRef] [PubMed]
- Morley, J.E. Hormones and the aging process. J. Am. Geriatr. Soc. 2003, 51, S333–S337. [Google Scholar] [CrossRef]
- Lee, C.G.; Boyko, E.J.; Strotmeyer, E.S.; Lewis, C.E.; Cawthon, P.M.; Hoffman, A.R.; Everson-Rose, S.A.; Barrett-Connor, E.; Orwoll, E.S. Association between insulin resistance and lean mass loss and fat mass gain in older men without diabetes mellitus. J. Am. Geriatr. Soc. 2011, 59, 1217–1224. [Google Scholar] [CrossRef]
- James, D.E.; Jenkins, A.B.; Kraegen, E.W. Heterogeneity of insulin action in individual muscles in vivo: Euglycemic clamp studies in rats. Am. J. Physiol. 1985, 248, E567–E574. [Google Scholar] [CrossRef]
- Clark, B.C. In vivo alterations in skeletal muscle form and function after disuse atrophy. Med. Sci. Sports Exerc. 2009, 41, 1869–1875. [Google Scholar] [CrossRef]
Characteristic | |
---|---|
Age, years | 46.3 ± 14 |
Gender, female | 51 (78.5) |
Diagnosis | |
Breast | 40 (61.5) |
Lymphoma | 17 (26.2) |
Sarcoma | 8 (12.3) |
Comorbidities | |
Hypertension | 7 (10.8) |
Diabetes mellitus | 3 (4.6) |
CAD | 2 (3.1) |
COPD | 1 (1.5) |
Asthma | 3 (4.6) |
Hypothyroidism | 2 (3.1) |
BMI, kg/m2 | 27.4 ± 4.9 |
BSA, m2 | 1.82 ± 0.17 |
Laboratory test | |
Hemoglobin, g/dL | 12.6 ± 1.7 |
MCV, fL | 83.4 ± 6.3 |
RDW, % | 14.1 (13.5–15.5) |
Albumin, g/dL | 4.1 (3.8–4.4) |
CTCAE Grade 3–4 Neutropenia | CTCAE Grade 1–2 Neutropenia | Normal | p | |
---|---|---|---|---|
N | 17 | 21 | 27 | |
Age | 41.9 ± 15.1 | 43.1 ± 12.4 | 51.5 ± 13.4 | 0.037 |
Gender, female | 11 (64.7) | 17 (81.0) | 23 (85.2) | 0.259 |
BMI, kg/m2 | 26.3 ± 4.9 | 25.8 ± 4.3 | 29.5 ± 4.7 | 0.014 |
BSA, m2 | 1.81 ± 0.20 | 1.78 ± 0.18 | 1.87 ± 0.13 | 0.191 |
Adriamycin dosage | 420 (388–490) | 400 (370–495) | 440 (400–480) | 0.319 |
Diagnosis | 0.370 | |||
Breast | 9 (52.9) | 11 (52.4) | 20 (74.1) | |
Lymphoma | 5 (29.4) | 8 (38.1) | 4 (14.8) | |
Sarcoma | 3 (17.6) | 2 (9.5) | 3 (11.1) | |
US-MT | ||||
Anterior arm | 25.4 ± 5.7 | 24.3 ± 4.1 | 27.3 ± 4.8 | 0.104 |
RA | 9.6 ± 2.0 | 9.5 ± 1.9 | 9.9 ± 1.4 | 0.613 |
RF | 17.6 ± 3.4 | 20.0 ± 3.7 | 21.8 ± 3.6 | 0.002 |
VI | 15.7 ± 4.1 | 16.6 ± 2.9 | 19.5 ± 3.4 | 0.001 |
VL | 21.4 ± 2.9 | 22.7 ± 4.0 | 24.7 ± 3.1 | 0.017 |
Gastrocnemius | 17.8 ± 1.9 | 18.6 ± 1.8 | 19.5 ± 1.6 | 0.020 |
FL | 33.7 ± 6.1 | 34.2 ± 3.6 | 33.9 ± 3.5 | 0.975 |
PA (°) | 29.3 ± 4.9 | 33.3 ± 4.9 | 31.9 ± 3.8 | 0.088 |
CT-L3 (CSA) | ||||
Paravertebral | 44.9 ± 10.1 | 43.3 ± 8.0 | 47.9 ± 7.9 | 0.165 |
Psoas major | 18.6 ± 8.3 | 17.7 ± 5.6 | 18.9 ± 7.7 | 0.902 |
Total | 126.9 ± 29.0 | 124.6 ± 27.5 | 134.7 ± 28.5 | 0.278 |
CTCAE Grade 3–4 Neutropenia | p | |
---|---|---|
Females | 0.005 | |
Low RF (n = 14) | 7 (50.0) | |
Normal RF (n = 37) | 4 (10.8) | |
Males | 0.063 | |
Low RF MT (n = 5) | 4 (80.0) | |
Normal RF (n = 9) | 2 (22.2) |
OR | CI | p | |
---|---|---|---|
Age | 0.977 | 0.926–1.031 | 0.395 |
Gender, male * | 2.830 | 0.641–12.501 | 0.170 |
BMI | 1.029 | 0.885–1.197 | 0.711 |
Low RF MT | 9.210 | 2.401–35.326 | 0.001 |
OR | CI | p | |
---|---|---|---|
Age | 0.978 | 0.897–1.065 | 0.606 |
BMI | 1.023 | 0.851–1.230 | 0.810 |
Low RF MT | 6.629 | 1.283–34.238 | 0.024 |
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Share and Cite
Güner, G.; Özçakar, L.; Baytar, Y.; Onur, M.R.; Demir, M.; Aktaş, B.Y.; Aktepe, O.H.; Güven, D.C.; Taban, H.; Yıldırım, H.Ç.; et al. Sonographic Measurements of Rectus Femoris Muscle Thickness Strongly Predict Neutropenia in Cancer Patients Receiving Chemotherapy. Cancers 2024, 16, 1061. https://doi.org/10.3390/cancers16051061
Güner G, Özçakar L, Baytar Y, Onur MR, Demir M, Aktaş BY, Aktepe OH, Güven DC, Taban H, Yıldırım HÇ, et al. Sonographic Measurements of Rectus Femoris Muscle Thickness Strongly Predict Neutropenia in Cancer Patients Receiving Chemotherapy. Cancers. 2024; 16(5):1061. https://doi.org/10.3390/cancers16051061
Chicago/Turabian StyleGüner, Gürkan, Levent Özçakar, Yusuf Baytar, Mehmet Ruhi Onur, Metin Demir, Burak Yasin Aktaş, Oktay Halit Aktepe, Deniz Can Güven, Hakan Taban, Hasan Çağrı Yıldırım, and et al. 2024. "Sonographic Measurements of Rectus Femoris Muscle Thickness Strongly Predict Neutropenia in Cancer Patients Receiving Chemotherapy" Cancers 16, no. 5: 1061. https://doi.org/10.3390/cancers16051061