A percutaneous needle biopsy technique for sampling the supraclavicular brown adipose tissue depot of humans

M Chondronikola, P Annamalai, T Chao, C Porter, M K Saraf, F Cesani, L S Sidossis, M Chondronikola, P Annamalai, T Chao, C Porter, M K Saraf, F Cesani, L S Sidossis

Abstract

Brown adipose tissue (BAT) has been proposed as a potential target tissue against obesity and its related metabolic complications. Although the molecular and functional characteristics of BAT have been intensively studied in rodents, only a few studies have used human BAT specimens due to the difficulty of sampling human BAT deposits. We established a novel positron emission tomography and computed tomography-guided Bergström needle biopsy technique to acquire human BAT specimens from the supraclavicular area in human subjects. Forty-three biopsies were performed on 23 participants. The procedure was tolerated well by the majority of participants. No major complications were noted. Numbness (9.6%) and hematoma (2.3%) were the two minor complications noted, which fully resolved. Thus, the proposed biopsy technique can be considered safe with only minimal risk of adverse events. Adoption of the proposed method is expected to increase the sampling of the supraclavicular BAT depot for research purposes so as to augment the scientific knowledge of the biology of human BAT.

Conflict of interest statement

Conflict of interest: None

Figures

Figure 1. Biopsy procedure
Figure 1. Biopsy procedure
(a) 2-deoxy-2-[18F]fluoro-D-glucose (18F-FDG)- Positron Emission Tomography/Computed Tomography image from a study participant. The intense orange color corresponds to metabolically active brown adipose tissue. (b) The study participant lying on the table of the computed tomography (CT) procedure room. (c) CT scout image corresponding to the supraclavicular area after the insertion of the injection needle to ensure its placement. (d) Tubing attached to the 6 mm Bergstrom needle and BD syringe to generate suction. (e) The study physician (P.A.) during the biopsy procedure. For Figures 1a and b informed consent to publish was obtained from the study participant.
Figure 2. Molecular and functional data supporting…
Figure 2. Molecular and functional data supporting the sampling of supraclavicular BAT deposit using the PET/CT guided needle biopsy method
(a–b) Uncoupling protein 1 (UCP1) staining (20x) in a abdominal subcutaneous (a) and supraclavicular adipose (b) tissue sample, demonstrating typical characteristic of brown adipose tissue (i.e. intense UCP1 staining and multi-locular cells) in supraclavicular adipose tissue. (c–d) Stages of mitochondrial respiration in an abdominal subcutaneous (c) and supraclavicular adipose (d) tissue sample, indicating a higher uncoupled respiration rate compared to the abdominal adipose tissue in basal conditions and upon the addition of oxidative substrates. GDP: Guanosine diphosphate, CCCP: Carbonyl cyanide m-chlorophenyl hydrazine.

References

    1. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360(15):1518–25.
    1. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360(15):1500–8.
    1. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. American journal of physiology Endocrinology and metabolism. 2007;293(2):E444–52.
    1. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360(15):1509–17.
    1. Sidossis L, Kajimura S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015;125(2):478–86.
    1. Cypess AM, White AP, Vernochet C, Schulz TJ, Xue R, Sass CA, et al. Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat Med. 2013;19(5):635–9.
    1. Sharp LZ, Shinoda K, Ohno H, Scheel DW, Tomoda E, Ruiz L, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PloS one. 2012;7(11):e49452.
    1. Lee P, Greenfield JR, Ho KK, Fulham MJ. A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. American journal of physiology Endocrinology and metabolism. 2010;299(4):E601–6.
    1. Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell metabolism. 2011;14(2):272–9.
    1. Chondronikola M, Volpi E, Borsheim E, Porter C, Annamalai P, Enerback S, et al. Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes. 2014;63(12):4089–99.
    1. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150(2):366–76.
    1. Hu HH, Tovar JP, Pavlova Z, Smith ML, Gilsanz V. Unequivocal identification of brown adipose tissue in a human infant. J Magn Reson Imaging. 2012;35(4):938–42.
    1. Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, et al. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab. 2011;96(8):2450–5.
    1. Lidell ME, Betz MJ, Dahlqvist Leinhard O, Heglind M, Elander L, Slawik M, et al. Evidence for two types of brown adipose tissue in humans. Nat Med. 2013;19(5):631–4.
    1. Shinoda K, Luijten IH, Hasegawa Y, Hong H, Sonne SB, Kim M, et al. Genetic and functional characterization of clonally derived adult human brown adipocytes. Nat Med. 2015
    1. Tarnopolsky MA, Pearce E, Smith K, Lach B. Suction-modified Bergstrom muscle biopsy technique: experience with 13,500 procedures. Muscle Nerve. 2011;43(5):717–25.
    1. Gupta S, Wallace MJ, Cardella JF, Kundu S, Miller DL, Rose SC. Quality improvement guidelines for percutaneous needle biopsy. J Vasc Interv Radiol. 2010;21(7):969–75.
    1. Porter C, Reidy PT, Bhattarai N, Sidossis LS, Rasmussen BB. Resistance Exercise Training Alters Mitochondrial Function in Human Skeletal Muscle. Med Sci Sports Exerc. 2014
    1. Cox RA, Mlcak RP, Chinkes DL, Jacob S, Enkhbaatar P, Jaso J, et al. Upper airway mucus deposition in lung tissue of burn trauma victims. Shock. 2008;29(3):356–61.
    1. Nicholls DG. Hamster brown-adipose-tissue mitochondria. The control of respiration and the proton electrochemical potential gradient by possible physiological effectors of the proton conductance of the inner membrane. Eur J Biochem. 1974;49(3):573–83.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj