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European Journal of Applied Sciences – Vol. 13, No. 1

Publication Date: February 25, 2025

DOI:10.14738/aivp.131.18314.

Tulp, O. L. (2025). Impact of Brown Adipose Tissue Reduction and Overfeeding on Adiposity and Depotspecific Adipose Tissue

Cellularity: Brown Fat Reduction and Adipose Tissue Cellularity. European Journal of Applied Sciences, Vol - 13(1). 397-408.

Services for Science and Education – United Kingdom

Impact of Brown Adipose Tissue Reduction and Overfeeding on

Adiposity and Depotspecific Adipose Tissue Cellularity: Brown

Fat Reduction and Adipose Tissue Cellularity

Orien L Tulp

ORCID: 0000-0001-6904-2573

Colleges of Medicine and Graduate Studies,

University of Science Arts and Technology,

Montserrat, British West Indies, MSR1110

ABSTRACT

Brown adipose tissue contributes to adaptive changes in metabolic energy

expenditure in response to alterations in diet and environmental conditions,

thereby assisting an animal to maintain thermoregulation and energy balance in

various mammalian species including man and animals. Cafeteria overfeeding of

normally lean rats during early postweaning growth typically results in significant

hyperplasia and in an increased capacity non-shivering thermogenesis and energy

expenditure in brown adipose tissue (BAT). The Interscapular BAT depot is readily

surgically accessible and normally represents approximately one third of the total

BAT mass in lean Sprague Dawley (SD) rats. The effects of experimental

overnutrition via offering a Cafeteria feeding regimen (Café) combined with

surgical reduction of the IBAT mass of adipose tissue cellularity and regional fat

deposition was determined in lean SD rats during 8 weeks of postweaning growth

and development to adulthood. Groups (n= 8 rats/group) of male, SD rats were fed

a Purina Chow diet or the Chow diet plus the Café regimen for 52 days from weaning.

An additional group of the Chow+Café regimen were subjected to surgical removal

of their IBAT at 4 weeks of age and continued on the Chow+Café thereafter (Café- IBAT). At 80 days of age, measures of adiposity including anthropometrics and the

mass and adipocyte cellularity in principle abdominal and subcutaneous fat depots

were determined. Body weight (BW) and mid-abdominal girth were ~20% greater

in Café and Café-IBAT, while linear growth was similar in all groups. The mass of all

fat depots was greater in Café fed animals (p=<0.05) and increased further in

subcutaneous depots and total WAT accumulation in the CaféIBAT animals

(p=<0.05). Adipocyte lipid content and cell diameter of Café > controls in all depots

with further increases in abdominal depots with Café-IBAT. Adipocyte number per

WAT depots of Café > Control in all depots, with further increases in the Inguinal SC

depot. Thus, these results are consistent with regional differences in the effects of

Café feeding on postweaning adipose tissue hyperplasia, hypertrophy and depot

mass and which underwent additional depot-specific differentiation in Café-IBAT.

In conclusion, Café resulted in adipocyte hypertrophy in all depots studied, but the

partial reduction of BAT mass in Cafe-IBAT rats resulted in only modest additional

impact on overall adiposity during overfeeding, with the greatest impact in the ING

SC depot, and thereby consistent with potential thermogenic compensation in other

BAT depots to partially minimize the overall impact of the Café overfeeding regimen

on developing adiposity in this strain.

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Keywords: Obesity, Brown Adipose Tissue, Overnutrition, Adipose Cellularity, Adiposity,

Rat.

INTRODUCTION

The magnitude of diet-induced hormonal effects on adipose tissue cellularity and fat accretion

exert differential impacts in subcutaneous vs. abdominal depots.1 The metabolic effects of

brown adipose tissue on the expression of nonshivering thermogenesis (NST) responses to

alterations in diet and environment in rodents are well established, implying a possible role of

BAT on energy balance in mammalian species by dissipating excess caloric intake as heat while

minimizing energy retention in adipose tissues.2,3 Several authors have reported that surgical

reduction of brown adipose tissue resulted in decreases in the capacity for NST in addition to a

greater propensity to develop greater mass and fatness in white adipose tissue depots,

analogous to that which occurs following pharmacologic ablation.4-8 As noted above, the BAT

has also been proposed as a potential buffer to maintain energy balance against excess weight

gain following episodes of excess caloric intake or macronutrient imbalance.9 In addition,

deficits in BAT energy expenditure secondary to multiple physiological factors have been

observed to occur in the obese phenotype of several rodent strains, where they are likely

metabolic contributors to the excess weight gain and early onset adiposity in those animal

species.1013 The current increasing prevalence of obesity and its numerous pathophysiologic

sequelae in Westernized societies represents a serious challenge to the effectiveness,

availability and capacity of treatment resources to manage the disorders linked to the obesity- linked stigmata.14,15 Adipose tissue is now known to contribute a broad range of hormonal

activities, in addition to the roles of insulin, catecholaminergic, thyroidal, and glucocorticoid

regulation.16-20 The nutritional and metabolic factors that contribute to the current epidemic of

obesity and overweight conditions in Western society typically include factors of diet,

environment, and lifestyle, often combined with links to metabolic and genomic

predispositions.18-20 The therapeutic measures to treat the disorders linked to obesity and

overweight conditions typically address one or more of the adaptive or heritable contributors

but often may be only partially effective due to the complex nature of the conditions.

Brown adipose tissue was discovered to occur in humans and other mammalian species several

centuries ago, but its physiologic role in energy metabolism has been discovered only more

recently.2,3,20-22 The morphology and functions of brown adipose tissue differ markedly from

that of white adipose tissue.15,22-25 Both tissue types occupy specific anatomic domains that are

anatomically suited to their physiologic functional role in homeostasis and energy balance.2,3

In white adipose tissue, the primary function is linked to energy storage in the form of

triglycerides in both abdominal and subcutaneous locations. The triglycerides may be formed

via hepatic or dietary origin, and may become deposited in mature adipocytes or preadipocytes

as a single large lipid droplet, surrounded with a thin layer of cytoplasm, a flattened nucleus

located in the cytoplasmic ring, accompanied with the host of cellular organelles common to

somatic cells, and facilitate the processes associated with our basic cellular functions including

cellular metabolism to maintain cellular viability.23 In times of caloric excess, the lipid droplet

may expand to contain up to 1 μg or more of lipid content in response to hormonal and

substrate influences, while in states of caloric deprivation, the lipid droplet may be mobilized

along its outer surfaces to release free fatty acids, thereby contributing to the energy demands

of peripheral tissues.3,23 Adipocytes from white adipocyte tissue may develop from

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URL: http://dx.doi.org/10.14738/aivp.131.18314

preadipocytes via hyperplasia and hypertrophy and once differentiated, remain viable

thereafter. Adipocytes remain responsive to accommodating increases or decreases in energy

intake and thus serve as an energy reserve from the stored triglycerides and fatty acids

throughout adolescence and much of the adult lifespan. Of significant concern, the onset of

overweight and obese conditions is now occurring earlier in the lifespan and remaining longer

than in previous generations. Overweight and obesity now occur more often in children and

adolescents where it can contribute to an earlier onset of the comorbidities commonly

associated with the overweight and obese conditions.14,15

In contrast, the physiological functions and cellular morphology of brown adipose tissue vary

considerably from those of white AT.2,3,22-24 Brown adipocytes are typically smaller, spherical

structures with a round, centrally placed nucleus and abundant specialized mitochondria. The

main physiological function of brown adipose tissue is to contribute to heat generation and

energy expenditure in response to alterations in diet and environment, accomplished via a large

cytoplasmic density of specialized mitochondria.23,25 BAT depots are strategically located in

close proximity to abundant vascular tissues such that the heat generated my circulate to both

central and peripheral tissues. Thus, brown adipose tissue can effectively dissipate the

endogenous heat energy to peripheral tissues to facilitate the regulation of homeostatic body

temperatures.2,3,23-25 Brown adipocytes can mobilize the heat generation process rapidly, via

specialized β-neuroadrenergic membrane-bound receptors and a dedicated

sympathoneurologic presence.3

Because the lipid in brown adipocytes is contained in multiple small locules distributed

throughout the cytoplasm, it provides a greater net metabolizable surface area to lipid content

ratio. Thus, locular surface area is an important consideration that further contributes to the

efficiency of their energy producing functions. The lipid locules are also strategically

distributed throughout the cytoplasmic compartment in proximity to the specialized

mitochondria, thereby creating a larger metabolizable surface area per unit of lipid than occurs

in white adipocytes. The relatively greater metabolizable surface area thereby facilitates a more

rapid mobilization of the contained lipid since lipid mobilization in both tissue types occur

along the outer surface areas of the lipid droplets or locules. Additionally, because the brown

adipocytes contain a centrally located spherical nucleus, surrounded by all essential organelles

required to maintain cellular functions, the ease of morphologic distinction from other

surrounding cells and tissues is readily discerned with or independently of histological staining

or immunoreactive techniques. Brown adipose tissue develops via hyperplasia and limited

hypertrophy prior to adulthood in the rat, while white adipose tissue in most depots may

continue to increase by hyperplasia from preadipocytes and limited hypertrophy throughout

much of the lifespan in rodents.23,24, Once formed, both brown and white adipocytes appear

remain present thereafter and where they may continue to expand in response to caloric status.

Once formed, differentiated adipocytes of either type can remain active as lipid storage depots

virtually indefinitely, to accommodate the energy needs of the organism as needed during both

energy privation and excess. Both tissues normally regulate their lipid stores and metabolic

status via hormonal actions including those inspired by insulin and catecholamines. In contrast,

pharmacologic ablation via inhibition of β-adrenergic functions results in increases in locule

diameter and lipid content in isolated brown adipocytes, consistent with decreased

thermogenic activity.23

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The primary metabolic roles of Insulin, catecholamines, glucocorticoids, and macronutrient

energy intake regulation in addition to numerous other secondary factors via both direct

stimulatory and permissive effects regulation of energy balance in man and animals.15-18 Insulin

functions exhibit both glycemic and lipogenic actions in peripheral tissues via stimulating

glucose uptake, stimulating lipogenesis and lipid uptake of preformed lipids, while impeding

lipid mobilization and ketogenesis from white adipose tissue stores. Thus, insulin is a primary

and highly influential hormone in the peripheral management of energy stores over time.

Catecholamines can bring about the mobilization of glycogen and lipid stores during instances

of duress, including negative energy balance, macronutrient imbalance, and/or food

depravation. While the metabolic effects of insulin actions may persist for hours, the responses

to catecholamine occur rapidly and are initiated via adrenoreceptor actions located on the

plasma membrane. Accordingly, the positive effects of catecholamines on energy balance are

more immediate and give rise to the initiation of the common ‘fight or flight’ response. Plasma

glucose can become significantly elevated within minutes in response to catecholaminergic

stimulation, while in the presence of insulin resistance, plasma glucose and processes of glucose

disposal in peripheral tissues may persist for hours and take longer to recover after the

adrenergic challenge.26

Brown adipocytes have specialized β3-adenoreceptors, in addition to individual

sympathomimetic neural synapses to facilitate highly specialized and virtually instantaneous

responses once activated .3 In white adipose tissue, insulin typically impedes lipoprotein

mobilization, thereby enzymatically limiting the mobilization of free fatty acids and

diglycerides from stored triglycerides.16 Thus, the overall integrated regulation of energy stores

from carbohydrate and lipid sources is a complex and ongoing process, and which may continue

throughout the healthful lifespan of the individual or animal species baring pharmacologic

inactivation.

The presence of brown adipose tissue has been noted in humans for many generations. Among

the earliest observations were those noted during cadaveric dissections some 1500 years ago.21

More recently, histologic evidence in humans has been demonstrated to occur throughout

much of the lifespan.21,22,27 Thus, while the existence of BAT in mammalian species has been

known for many years, the biochemical processes of energy generation in brown adipose tissue

and its presence in adult humans have been established with advances technologic and

diagnostic processes only more recently.2,3,22,23,25 In rodents, the IBAT depot represents

approximately one third of the total BAT mass, and represents the depot that is most

conveniently accessible from a surgical perspective. Thus, the purpose of the present study was

to determine if partial reduction of brown adipose tissue would result in measurable changes

in adiposity and energy storage in a normally lean rat model of following induced hyperphagia

by offering unlimited access to the cafeteria diet approach, typically consisting of multiple

appetizing, energy rich foods common to the Western diet consumed in many developed

countries.5

MATERIAL AND METHODS

Groups of weanling Sprague-Dawley Rats (n = 6-8 rats/group, 40-42 g BW each) were obtained

from Charles River Laboratories, and acclimated to plexiglass shoebox cages in littermate pairs

and fed Purina Chow and house water, as libitum. At 4 weeks of age, two groups were offered a

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of Applied Sciences, Vol - 13(1). 376-396.

URL: http://dx.doi.org/10.14738/aivp.131.18314

highly palatable Cafeteria diet (Café) in addition to the Purina chow regimen. At 4 weeks of age,

one group of the Café diet regimen was subjected to surgical removal of the entire Interscapular

brown adipose tissue depot (Café-IBAT) under pentobarbitalketamine anesthesia as described

elsewhere 5,7-9 and continued on the Café diet regime thereafter. Recovery from the surgery was

uneventful and complete within a few days. Body weights were monitored periodically

throughout the study. After 52 days of the Café regimens animals were sacrificed via cervical

dislocation and measures of biometry including torso length and girth diameter determined

with an anthropometry tape. The epididymal, retroperitoneal, mesenteric, inguinal and dorsal

adipose tissue depots dissected in their entirety, weighed to the nearest mg, and prepared for

measures of adipose tissue cellularity via the osmium fixation methods of Hirsch and Gallian as

performed in our laboratory.24,27,28 Tissue lipid content was determined gravimetrically via the

microchemical method of Dole and Meinertz as conducted in our laboratory.26,30 Measures of

adipocyte diameters were determined with a stage micrometer via light microscopy at 45X

magnification.23 Data were analyzed by ANOVA corrected for multiple comparisons where

indicated and descriptive analysis via standard statistical procedures.31,32 The study was

approved by the Institutional Animal Care and Use Committee.

RESULTS

The measures of biometry after 52 days of the chow or café regimens are depicted in Figure 1

and 2 and show that the Café diet resulted in significantly greater final body weights in both the

Café and the Café-IBAT groups. There were no significant differences in the initial or final body

weight between the Café and Café-IBAT groups however, suggesting that the ablation of IBAT

likely induced only a modest impact on overall parameters of adiposity. Measures of torso

length were similar in all groups, indicative of an adequacy in macro- and micro- nutrient intake

when fed the Café diet. Measures of mid-abdominal girth and girth to torso length ratio were

greater in the Café fed group and were similar in both Café and Café-IBAT groups.

Figure 1: Effects of diet and IBAT removal on initial and final body weight of rats. Data are the

mean ± 1 SEM, N= 8 rats/group.

0

200

400

600

800

1000

INITIAL BW FINAL BW

p = < 0.05

FIGURE 1: BODY WEIGHTS OF RATS

CONTROL CAFÉ CAFÉ-IBAT

p = n.s.

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Figure 2: Effects of diet and IBAT removal on anthropomentric measures. Data are the mean ± 1

SEM, N= 8 rats/group.

Measures of the mass of principle far depots is depicted in Figure 3, and indicated that the mass

of the abdominal (Epididymal (EPI), Retroperitoneal (RP), and Mesenteric (MES), and the

subcutaneous (Dorsal (DOR), and Inguinal (ING)) fat pads were greater in Café fed than control

rats, with further increases in depot mass in the DOR, ING, and total fat pad mass in the Café- IBAT group. The AT cell number of Café > CHOW in subcutaneous (DOR and ING) and abdominal

RP, and unchanged in EPI. Adipocyte diameter and cellular lipid content of Café > CHOW in all

depots. Cell number increased further in DOR, EPI and RP, and the overall differences in cell

diameter corresponded to the measures of cell lipid content. In addition, surgical reduction of

IBAT resulted in further increases in the mass, cell size and cell lipid content particularly in the

ING depot. In the Café diet, IBAT cellularity determinations resulted in greater depot cell

numbers in the dorsal, retroperitoneal and inguinal depots. The café-IBAT group demonstrated

greater cell numbers in the Café-IBAT inguinal depot, while depot cell numbers in the Café-IBAT

retroperitoneal group were also elevated at a level intermediate between the chow and Café

groups.

0

5

10

15

20

25

30

35

TORSO, cm. GIRTH, cm GIRTH/TORSO x10

p = n .s.

FIGURE 2: BIOMETRY OF RATS

CONTROL CAFÉ CAFÉ-IBAT

*

*

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of Applied Sciences, Vol - 13(1). 376-396.

URL: http://dx.doi.org/10.14738/aivp.131.18314

Figure 3: Effects of diet and IBAT removal on adipose tissue mass. Data are the mean ± 1 SEM,

N= 8 rats/group. Abdominal represent the arithmetic sum of the epididymal, mesenteric and

retroperitoneal depots, and subcutaneous represents the sum of the Dorsal and inguinal

depots. The SUM represents the arithmetic sum of the abdominal and subcutaneous depots,

and the Adiposity represents the sum of the fat pad mass divided by the final body weights of

the rats.

Figure 4: Effects of diet and IBAT removal on adipocyte diameter. Data are the mean ± 1 SEM,

N= 8 rats/group. Abdominal cell diameters represent the arithmetic sum of the epididymal,

mesenteric and retroperitoneal depots, and subcutaneous cell diameters represent the sum of

the mean of the dorsal and inguinal adipocytes. The mean cell diameter represents the

arithmetic mean of the abdominal and subcutaneous depots.

0

50

100

150

200

ABDOMINAL WAT, g SUBCUTANEOUS

WAT, g

SUM WAT ADIPOSITY

p = < 0.05 (Control vs Cafe;)

FIGURE 3: EFFECT OF CAFE' AND IBAT ON ADIPOSITY

CONTROL CAFÉ CAFÉ-IBAT

0

20

40

60

80

100

120

CELL DIA, SQ CELL DIA, ABD MEAN CELL DIA

p = trend (Control vs. Cafe')

FIGURE 4: MEAN ADIPOCYTE DIAMETER

CONTROL CAFÉ CAFÉ-IBAT

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Figure 5: Effects of diet and IBAT removal on adipocyte lipid content. Data are the mean ± 1

SEM, N= 8 rats/group. Abdominal cell lipid content represents the mean of the epididymal,

mesenteric and retroperitoneal depots, and subcutaneous cell lipid content represents the

mean of the dorsal and inguinal adipocytes. The mean cell lipid content represents the

arithmetic mean of the abdominal and subcutaneous depots.

Figure 6: Effects of diet and IBAT removal on adipocyte number. Data are the mean ± 1 SEM, N=

8 rats/group. Abdominal cell lipid content represents the mean cell number/depot of the

epididymal, mesenteric and retroperitoneal depots (right panel), and subcutaneous cell

number (Left panel) represents the mean of the dorsal and inguinal adipocytes. The mean cell

number in the far-right panel represents the arithmetic mean of the cell number in the

abdominal and subcutaneous depots.

0

0.2

0.4

0.6

0.8

1

1.2

CELL LIPID, SQ, ug CELL LIPID, ABD, ug MEAN LIPID, ug

p = < 0.05 (Control vs Cafe')

FIGURE 5: MEAN CELL LIPID CONTENT

CONTROL CAFÉ CAFÉ-IBAT

0

20

40

60

80

100

120

SQ CELL NR ABD CELL NR SUM SQ+ABD

p = < 0.05 (Control vs Cafe')

FIGURE 6: EFFECT OF DIET AND IBAT ON ADIPOCYTE CELLULARITY

CONTROL CAFÉ CAFÉ-IBAT

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of Applied Sciences, Vol - 13(1). 376-396.

URL: http://dx.doi.org/10.14738/aivp.131.18314

DISCUSSION

The presence of brown adipose tissue in hibernating and other animals had previously been

reported for many years, but its relationship to energy balance and diet-induced adaptive

thermogenesis in mammalian species and humans remained unknown or controversial for

many years. 2,3 In the 20th Century, Sims et al were among the first in recent history to describe

the phenomena of ‘luxus consumption’ in humans, which they had observed in human

volunteers in the Vermont Study of Obesity.33 In that study, healthy, normal weight and

predominantly sedentary volunteers consumed up to 10,000 excess calories/day without

becoming obese, and most subjects quickly lost the modest extra weight they had gained upon

return to normal energy intakes and without significant changes in daily physical activity.32

Rothwell and Stock later demonstrated the apparent presence of brown fat activity in humans

following adrenergic activation, thereby further linking the thermogenic response to dietary

and environmental factors.22 While the presence of brown adipose tissue in hibernating

animals and in humans had been known, the biochemical mechanisms implicated and the

physiologic contributions have now been elucidated by Himms-Hagen and others.2,3 The

thermogenic mechanism was found to revolve around specialized mitochondria in BAT that are

capable of generating heat from the hydrolysis of high energy phosphate bonds from ATP, a

process sometimes referred to as ‘uncoupled’ oxidative phosphorylation.2,3 The process results

in the generation of ~ 7 kcal/mole of high energy phosphate bonds as heat and typically occurs

without being linked to biosynthetic processes.3The effects of pharmacologic inhibition of BAT

thermogenesis via β-blockade resulted in microscopic enlargement of the lipid locule diameters

indicative of decreased thermogenic activity.23 Attempts to document excess weight gain and

greater adiposity following surgical removal of IBAT have yielded variable results.5-7, 9,10,24

In conclusion, the results of this study indicate that café- induced overfeeding resulted in depot

specific increases in adiposity including increases in body weight, abdominal circumference,

and in adipose tissue cellularity in abdominal and subcutaneous depots. The results obtained

herein are qualitatively similar to those that have been reported by other authors. 6,7,9,10,14,24,35-

37 In the present study, the increases in adipose tissue cellularity occurred by a combination of

hyperplasia and hypertrophy of adipocytes that were expressed differently in different depots.

In the epididymal depot, adipocyte hyperplasia is likely complete by puberty, and increased in

depot mass beyond puberty occur via limited hypertrophy. Epididymal cell diameters and cell

lipid content exhibited only a modest trend toward greater lipid content following the Café diet

in either Café group or Café-IBAT were without additional effect. Likewise, adipocyte number

in the dorsal, retroperitoneal and inguinal depots increased significantly when fed the café diet,

but the cell number in the Café-IBAT group was greater only in the Inguinal depot. The reasons

for the differential effects of overfeeding on differential depot specific alterations in adipose

tissue cellularity are unclear but may be secondary to depot specific differences in insulin

sensitivity, lipogenic actions, and chronological differences in lipid accretion in the different

depots. Effects on linear growth were not observed, suggesting that the Café diet as offered in

combination with their chow regimen likely provided adequate nutrition to accommodate lean

tissue growth and development. In contrast, the differences in adiposity correlated more with

net energy intake, including refined carbohydrates and processed food items of less nutritional

value. While measures of adipocyte number in the IBAT were not measured in the present

study, parallel studies in both rats and mice reported an approximate 3-fold increase in IBAT

mass and cellularity after an analogous 52-day or shorter feeding regimen.7,8,24,29,34-37

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SUMMARY AND CONCLUSIONS

The results of this study showed that feeding a Café diet supplement to normally lean rat during

the postweaning growth period resulted in depot-specific increases in mass and cellularity

characteristics in lean, Sprague-Dawley rats. Partial surgical reduction of BAT mass by

removing the Interscapular depot in its entirety resulted in modest additional depot-specific

increases in adiposity, but the net increases were not proportionate to the proportion of BAT

removed. Whether other BAT depots may have compensated by additional increases in

cellularity or thermogenic functions remain unclear, however in an earlier study, resting and

norepinephrine simulated thermogenic responses were only modestly decreased following a

similar surgical reduction of IBAT.5,6 Thus, overfeeding via the Café regimen in a strain of

normally lean rats is an effective method to bring about modest physiological changes in

adiposity and adipose tissue cellularity in white adipose tissue depots via differential depot- specific effects on adipocyte hyperplasia and hypertrophy.

ACKNOWLEDGEMENTS

The author thanks the University of Science Arts and Technology, Montserrat for the

Institutional resources to complete this study.

Application of AI (Artificial Intelligence) Disclaimer

Author hereby declares that NO generative AI technologies such as Large Language Models

(ChatGPT, COPILOT, etc) and text-to-image generators have been used during the writing or

editing of this manuscript.

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