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Effects of Punica granatum L. peel extract supplementation on body weight, cardiac function, and haematological and biochemical parameters in an animal model of metabolic syndrome

Joanna Niewiadomska
Joanna Niewiadomska
, 
Ewa Kumiega
Ewa Kumiega
, 
Michał Płóciennik
Michał Płóciennik
, 
Jacek Gajek
Jacek Gajek
 e 
Agnieszka Noszczyk-Nowak
Agnieszka Noszczyk-Nowak
   | 16 giu 2023
Journal of Veterinary Research's Cover Image
INFORMAZIONI SU QUESTO ARTICOLO
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Pubblicato online: 16 giu 2023
Pagine: 219 - 232
Ricevuto: 13 gen 2023
Accettato: 15 mag 2023
DOI: https://doi.org/10.2478/jvetres-2023-0031
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© 2023 Joanna Niewiadomska et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1.

Violin plots of body weight with regard to individual groups at the final 16th-time point. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means
Violin plots of body weight with regard to individual groups at the final 16th-time point. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means

Fig. 2

The dynamics of body weight increases of individual rats (left side) and of group mean weight increases (right side) during the study period. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 - experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP
The dynamics of body weight increases of individual rats (left side) and of group mean weight increases (right side) during the study period. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 - experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP

Fig. 3

Trajectories of individual rats’ body weight variation and group average variations. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP
Trajectories of individual rats’ body weight variation and group average variations. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP

Fig. 4

Violin plot of the level of acanthocytes by group after eight weeks of pomegranate peel supplementation. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means
Violin plot of the level of acanthocytes by group after eight weeks of pomegranate peel supplementation. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means

Fig. 5

Violin plots of the level of schistocytes by group after eight weeks of pomegranate peel supplementation. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means
Violin plots of the level of schistocytes by group after eight weeks of pomegranate peel supplementation. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means

Fig. 6.

A – Acanthocytes and B – schistocytes found in smears of rat peripheral blood. Abnormal cells are indicated by arrows
A – Acanthocytes and B – schistocytes found in smears of rat peripheral blood. Abnormal cells are indicated by arrows

Fig. 7

Violin plots of fasting blood glucose concentrations by group after eight weeks of pomegranate peel supplementation. fa/fa H2O - control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 - experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 - experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 - experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 - experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means
Violin plots of fasting blood glucose concentrations by group after eight weeks of pomegranate peel supplementation. fa/fa H2O - control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 - experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 - experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 - experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 - experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means

Fig. 8.

Violin plots of lipid profiles by group after eight weeks of pomegranate peel supplementation. A – serum triglyceride concentration; B – serum total cholesterol concentration; C – serum high-density lipoprotein concentration; D – serum low-density lipoprotein concentration. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means
Violin plots of lipid profiles by group after eight weeks of pomegranate peel supplementation. A – serum triglyceride concentration; B – serum total cholesterol concentration; C – serum high-density lipoprotein concentration; D – serum low-density lipoprotein concentration. fa/fa H2O – control group of Zucker diabetic fatty (ZDF) rats with missense mutation in the Lepr leptin receptor gene administered only water; fa/fa 100 – experimental group of ZDF rats with this mutation administered 100 mg/kg body weight (b.w.) pomegranate peel extract (EPP); fa/fa 200 – experimental group of ZDF rats with this mutation administered 200 mg/kg b.w. EPP; fa/+ 100 – experimental group of ZDF rats without this mutation administered 100 mg/kg b.w. EPP; fa/+ 200 – experimental group of ZDF rats without this mutation administered 200 mg/kg b.w. EPP; μ^$${\hat \mu }$$ – predicted value of group means

Mean body weights for individual groups at the final 16th time point

group fa/fa H2O fa/fa 100 fa/fa 200 fa/+ 100 fa/+ 200
n 6 6 6 6 6
Mean 407.14 382.08 392.75 358.97 337.69
Standard deviation 32.68 35.48 36.28 12.90 29.34

Glucose and lipid profile at the beginning of the study (t1) and after eight weeks of pomegranate supplementation (t2)

Index fa/fa H2O fa/fa 100 fa/fa 200 fa/+ 100 fa/+ 200
t1 t2 t1 t2 t1 t2 t1 t2 t1 t2
GLU (mmol/L) 17.50 ± 5.90 59.40 ± 11.30 21.40 ± 6.40 63.00 ± 12.80 21.10 ± 8.50 57.80 ± 8.50 7.60 ± 0.60 23.00 ± 3.70 7.70 ± 1.20 22.90 ± 2.80
CHOL (mmol/L) 4.30 ± 0.30 5.10 ± 0.70 4.30 ± 0.20 4.80 ± 0.50 4.10 ± 0.10 5.10 ± 1.00 3.40 ± 0.20 2.20 ± 0.30 3.60 ± 0.10 2.40 ± 0.10
LDL (mmol/L) 2.50 ± 0.10 2.90 ± 0.40 2.40 ± 0.20 3.00 ± 0.40 2.40 ± 0.20 3.20 ± 0.60 1.70 ± 0.10 1.30 ± 0.20 1.80 ± 0.10 1.40 ± 0.10
HDL (mmol/L) 2.20 ± 0.10 2.80 ± 0.20 1.90 ± 0.10 2.80 ± 0.20 1.90 ± 0.20 2.80 ± 0.40 1.20 ± 0.20 1.20 ± 0.20 1.20 ± 0.10 1.10 ± 0.10
TG (mmol/L) 11.50 ± 2.70 5.60 ± 5.60 12.70 ± 3.40 5.70 ± 2.90 12.50 ± 2.80 5.90 ± 1.30 1.30 ± 0.30 1.20 ± 0.60 1.30 ± 0.30 0.90 ± 0.60

Blood cell counts at two time points: at the beginning of the study (t1) and after eight weeks of EPP supplementation (t2)

Index fa/fa H2O fa/fa 100 fa/fa 200 fa/+ 100 fa/+ 200
t1 t2 t1 t2 t1 t2 t1 t2 t1 t2
WBC (K/μL) 10.40 ± 1.63 7.05 ± 1.96 10.50 ± 1.26 6.02 ± 2.33 11.26 ± 2.56 6.40 ± 1.29 8.52 ± 0.86 5.00 ± 1.41 9.38 ± 0.99 3.73 ± 1.25
RBC (G/μL) 7.49 ± 0.21 8.36 ± 0.69 7.63 ± 0.23 8.59 ± 0.44 7.60 ± 0.13 8.19 ± 0.53 7.53 ± 0.64 8.07 ± 0.54 7.69 ± 0.24 7.82 ± 0.63
HGB (g/L) 16.13 ± 0.37 14.53 ± 0.99 16.10 ± 0.37 14.80 ± 0.65 15.90 ± 0.34 14.32 ± 0.73 15.70 ± 0.73 13.88 ± 0.88 16.05 ± 0.42 13.90 ± 0.35
HCT (%) 43.47 ± 1.25 43.23 ± 3.31 39.18 ± 12.49 44.52 ± 2.32 44.12 ± 0.92 42.22 ± 2.66 41.88 ± 3.76 41.86 ± 2.61 42.75 ± 1.48 39.75 ± 3.18
PLT (K/μL) 1,069.33 ± 207.16 748.00 ± 76.58 1033.83 ± 74.09 658.67 ± 67.82 1078.80 ± 76.59 718.20 ± 52.11 905.80 ± 53.27 656.60 ± 244.39 911.67 ± 60.07 738.00 ± 39.33
MCV (fL) 58.00 ± 1.10 51.83 ± 0.75 57.67 ± 0.52 51.83 ± 0.41 58.00 ± 1.00 51.60 ± 0.55 55.60 ± 1.14 51.80 ± 0.84 55.50 ± 0.55 51.00 ± 0.00
MCH (pg) 21.55 ± 0.58 17.43 ± 0.63 21.15 ± 0.22 17.25 ± 0.29 20.88 ± 0.40 17.50 ± 0.42 20.90 ± 1.07 17.18 ± 0.26 20.90 ± 0.19 17.87 ± 1.11
MCHC (g/dL) 37.15 ± 0.69 33.65 ± 1.13 36.50 ± 0.49 33.30 ± 0.62 36.02 ± 0.29 33.92 ± 0.73 37.62 ± 2.00 33.20 ± 0.17 37.58 ± 0.42 35.08 ± 2.23
RET (%) 2.17 ± 0.87 1.85 ± 1.56 2.72 ± 0.31 1.15 ± 0.82 3.60 ± 0.67 0.92 ± 0.33 2.34 ± 0.61 1.12 ± 1.11 1.48 ± 0.69 0.53 ± 0.30
NEU (%) 13.33 ± 6.92 25.50 ± 4.76 19.33 ± 8.04 21.50 ± 4.59 20.40 ± 5.08 33.20 ± 5.72 16.25 ± 7.37 20.75 ± 3.95 12.83 ± 5.53 18.67 ± 4.50
LYM (%) 81.17 ± 5.00 71.50 ± 5.68 76.83 ± 10.26 74.83 ± 6.11 78.40 ± 5.13 61.80 ± 4.76 81.00 ± 8.68 75.75 ± 5.68 84.67 ± 4.63 79.50 ± 4.46
MONO (%) 2.50 ± 3.51 0.83 ± 0.98 1.00 ± 0.89 0.33 ± 0.52 0.20 ± 0.45 2.00 ± 1.58 0.50 ± 1.00 0.25 ± 0.50 1.83 ± 1.33 0.17 ± 0.41
EOS (%) 1.83 ± 0.75 0.67 ± 0.52 1.50 ± 1.38 2.33 ± 2.42 0.60 ± 0.55 1.60 ± 1.34 2.00 ± 1.15 2.50 ± 1.29 0.33 ± 0.52 1.33 ± 1.03

Mass spectrum characteristic and content of phenolic compounds in pomegranate peel extract

Rt (min) MS (M-H)− (m/z) MS/MS (M-H)− (m/z) Name of compounds Polyphenol content
1.67 331 271/169 Galloyl-glucose 2.00 ± 0.03
1.73 781 721/601 Punicalin α/A 3.11 ± 0.06
2.02 1083 611/331/146 HHDP-galloyl-hexoside (punicalagin) 4.20 ± 0.09
2.12 1083 781/622/301 Punicalagin isomer 14.82 ± 1.04
2.33 933 631/450/301 Ellagitannin 4.71 ± 0.40
2.87 1083 781/301 HHDP-gallagyl-hexoside (punicalagin) 93.91 ± 2.05
3.12 1085 907/783/301 Ellagic acid derivative 2.49 ± 0.53
3.69 1083 781/301 HHDP-gallagyl-hexoside (punicalagin) 157.00 ± 2.65
3.89 799 301 Granatin A 4.74 ± 0.32
5.08 783 481/301 Ellagitannin 25.86 ± 1.53
6.20 1085 933/301 Digalloyl-gallagyl-hexoside 10.37 ± 0.65
6.25 783 481/301 Ellagitannin 13.51 ± 0.99
6.38 463 301 Ellagic acid-hexoside 33.63 ± 1.23
6.89 951 907/635/301 Galloyl-HHDP-DHHDP-hex (granatin B) 2.68 ± 0.11
Total (mg/g dry weight) 373.05

Echocardiographic parameters at two time points: at the beginning of the study (t1) and after eight weeks of pomegranate peel supplementation (t2)

Index fa/fa H2O fa/fa 100 fa/fa 200 fa/+ 100 fa/+ 200
t1 t2 t1 t2 t1 t2 t1 t2 t1 t2
HR (bpm) 289.00 ± 28.08 234.33 ± 37.03 265.00 ± 21.02 232.25 ± 45.85 245.17 ± 21.34 226.83 ± 32.62 264.60 ± 20.40 230.60 ± 46.55 275.20 ± 11.82 245.80 ± 31.40
LVIDs (mm) 2.52 ± 0.54 2.65 ± 1.03 3.35 ± 1.61 2.65 ± 1.03 3.35 ± 1.23 2.90 ± 1.01 3.36 ± 0.69 2.36 ± 1.19 2.80 ± 0.70 2.28 ± 0.42
LVIDd (mm) 6.48 ± 0.51 6.08 ± 1.15 6.65 ± 0.83 5.82 ± 0.74 6.87 ± 1.25 6.52 ± 0.95 6.08 ± 1.13 5.56 ± 1.39 5.84 ± 0.77 5.68 ± 0.69
LVPWs (mm) 2.93 ± 0.32 3.00 ± 0.39 2.72 ± 0.43 3.00 ± 0.55 2.62 ± 0.39 2.77 ± 0.67 2.68 ± 0.49 3.32 ± 0.72 2.38 ± 0.49 3.18 ± 0.72
LVPWd (mm) 1.80 ± 0.39 1.95 ± 0.42 1.78 ± 0.39 2.22 ± 0.38 1.88 ± 0.28 2.03 ± 0.43 1.98 ± 0.56 1.86 ± 0.19 1.62 ± 0.30 1.94 ± 0.42
IVSs (mm) 3.32 ± 0.38 3.15 ± 0.62 3.10 ± 0.55 3.67 ± 0.71 3.68 ± 0.55 3.22 ± 0.41 3.04 ± 1.10 3.24 ± 0.58 3.30 ± 0.71 3.38 ± 0.36
IVSd (mm) 1.77 ± 0.16 1.77 ± 0.29 1.73 ± 0.13 2.00 ± 0.27 1.92 ± 0.23 1.80 ± 0.43 1.96 ± 0.55 1.62 ± 0.46 1.78 ± 0.19 1.86 ± 0.30
LVEDV (mL) 0.63 ± 0.15 0.55 ± 0.26 0.68 ± 0.22 0.48 ± 0.22 0.80 ± 0.38 0.65 ± 0.26 0.54 ± 0.26 0.44 ± 0.37 0.50 ± 0.16 0.44 ± 0.15
LVESV (mL) 0.05 ± 0.05 0.07 ± 0.05 0.15 ± 0.17 0.05 ± 0.10 0.13 ± 0.12 0.08 ± 0.08 0.10 ± 0.07 0.04 ± 0.09 0.06 ± 0.09 0.02 ± 0.04
SV (mL) 0.60 ± 0.14 0.50 ± 0.24 0.58 ± 0.10 0.40 ± 0.22 0.65 ± 0.31 0.57 ± 0.20 0.44 ± 0.21 0.40 ± 0.28 0.40 ± 0.16 0.38 ± 0.13
CO (L/min) 0.17 ± 0.04 0.12 ± 0.07 0.15 ± 0.02 0.09 ± 0.04 0.16 ± 0.07 0.14 ± 0.06 0.12 ± 0.06 0.09 ± 0.04 0.11 ± 0.04 0.10 ± 0.03
EF (%) 92.85 ± 3.36 89.83 ± 6.38 83.50 ± 14.01 84.12 ± 18.64 85.80 ± 8.92 89.55 ± 5.71 80.68 ± 7.18 90.22 ± 6.40 87.00 ± 7.26 92.64 ± 1.78
FS (%) 61.25 ± 6.78 57.72 ± 12.38 51.52 ± 18.55 53.75 ± 21.09 52.07 ± 12.09 56.62 ± 10.47 44.80 ± 8.12 58.58 ± 13.68 52.18 ± 8.29 59.94 ± 3.22
mFS (%) 25.40 ± 3.67 22.05 ± 3.24 21.50 ± 7.14 18.10 ± 12.31 20.95 ± 4.67 25.25 ± 3.25 18.84 ± 3.43 15.22 ± 3.37 19.92 ± 1.76 19.80 ± 7.22
LAD (mm) 4.22 ± 0.71 3.57 ± 0.47 4.34 ± 1.08 3.82 ± 0.36 4.87 ± 0.53 3.83 ± 0.69 4.30 ± 0.58 4.15 ± 0.42 4.58 ± 0.42 3.76 ± 0.29
AOD (mm) 3.37 ± 0.38 3.23 ± 0.35 3.34 ± 0.73 3.44 ± 0.25 3.85 ± 0.23 3.12 ± 0.51 3.28 ± 0.39 3.65 ± 0.83 3.44 ± 0.22 3.12 ± 0.33
LA/Ao 1.25 ± 0.19 1.10 ± 0.08 1.30 ± 0.11 1.12 ± 0.13 1.26 ± 0.11 1.24 ± 0.17 1.31 ± 0.08 1.17 ± 0.18 1.34 ± 0.18 1.21 ± 0.13
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