Beneficial role of amygdalin extracts against animal growth regulator Boldjan induced cardiac toxicity, injury and oxidative stress in male rats

Eman M Hussain; Sura M Alkadhimy; Asmaa M Neamah; Ehab Tousson

doi:10.1093/toxres/tfae042

. 2024 Mar 23;13(2):tfae042. doi: 10.1093/toxres/tfae042

Beneficial role of amygdalin extracts against animal growth regulator Boldjan induced cardiac toxicity, injury and oxidative stress in male rats

Eman M Hussain ¹, Sura M Alkadhimy ², Asmaa M Neamah ³, Ehab Tousson ^4,^✉

PMCID: PMC10960923 PMID: 38529199

Abstract

Millions of individuals have used illicit anabolic-androgenic steroids (AAS), but the long-term cardiovascular associations of these drugs remain incompletely understood. Boldjan is AAS medication which is used in veterinary medicine and by young adults aiming to have a better appearance improving their self-esteem. Therefore; the objective of the current investigation was to examine any potential preventative effects of amygdalin extract against anabolic steroid Boldjan induced cardic toxicity, injury and oxidative stress in male rat. Forty adult male Wistar rats were classified into five groups (Gp1, Control Gp; Gp2, Amygdalin Gp in which rats treated with amygdalin (100 mg/kg body weight/day) daily for 2 weeks; Gp3, Boldjan Gp in which rats treated with Boldjan (10 mg/Kg BW/week) for 4 weeks; Gp4, Boldjan + Amygdalin). Boldjan induced a significant rises in serum lactate dehydrogenase (LDH), creatine kinase (CK) and creatine kinase MB (CK MB), aspartate aminotransferase (AST), total cholesterol (TC), triglycerides (TG), low-density lipoprotein-cholesterol (LDL-C), and very-low-density lipoprotein–cholesterol (VLDL-C), cardiac injury, and malondialdehyde (MDA) levels and a significant depletion in serum high-density lipoprotein-cholesterol (HDL-C), cardiac reduced glutathione (GSH), Superoxide dismutase (SOD) and catalase (Cat) activities as compared to control Gp. In contrast, Amygdalin significantly reversed the Boldjan induced cardiac toxicity in post treated rats Gp (Boldjan + Amygdalin). Amygdalin could be an efficient preventive supplement for mitigating Boldjan induced cardiac toxicity, possibly via controlling oxidative stress events.

Keywords: anabolic-androgenic steroids, Boldjan, amygdalin, cardiac toxicity

Introduction

Millions of individuals have used illicit anabolic-androgenic steroids (AAS), but the long-term cardiovascular associations of these drugs remains incompletely understood. AAS are a group of synthetic molecules derived from testosterone and its related precursors. ^1–3 Due to their ability to increase muscle protein synthesis, AASs are utilized by canine, horse, adolescents and athletes, especially by bodybuilders, both for aesthetic uses and as performance enhancers to increase muscle growth and lean body mass.^4–6 It has been classed as a Schedule III medication and applies to several veterinary products.⁷^,⁸ AAS are widely used illicitly by When used illicitly they can damage health and cause disorders affecting several functions.⁹^,¹⁰

Sudden cardiac death is the most common medical cause of death in athletes.¹¹^,¹² Boldjan is AAS medication which is used in veterinary medicine and by young adults aiming to increase their power, their body mass and weight.¹³ Previous studies have suggested an association between AAS use and cardiovascular disease, with a pathophysiologic link first proposed by early case reports of sudden cardiac death or ischemic stroke among young AAS-using men.²^,³^,¹⁴

Amygdalin or Vitamin B17 (VB17), and formerly called laetrile is one of many nitrilosides which are natural cyanide containing substances highly concentrated in fruit kernels from Rosaceae species such as Prunus armeniaca (apricot), Prunus persica (peach) and Prunus amygdalus varamara.¹⁵^,¹⁶ Amygdalin is consisting of two molecules of glucose, one of them is benzaldehyde which induces an analgesic action, the second is hydrocyanic acid which is an anti-neoplastic compound.¹⁷

Apricot seeds appear several pharmacological properties include antimicrobial anticancer, anti-inflammatory activities and antioxidant.¹⁸^,¹⁹ Oil obtained from kernels of apricots is essentially rich in oleic, linoleic acids and α-, γ-and δ-tocopherols.²⁰^,²¹ Moreover, Apricot kernel proteins might appear a possibility source for the generation of bioactive peptides with angiotensin converting enzyme inhibitory activity.^22–24 Amygdalin has various activities including antitussive, anti-asthmatic, antiatherogenic, anti-cancer, anti-inflammation and anti-ulcer activities.²⁵^,²⁶ The use of Boldjan showed a dramatic increase in the recent years especially by young adults aiming to have a better appearance improving their self-esteem. Therefore; the objective of the current investigation was to examine any potential preventative effects of amygdalin extract against anabolic steroid Boldjan induced cardic toxicity, injury and oxidative stress in male rat.

Materials and methods

Chemical and reagent

Boldjan vial was obtained from Laboratorios Tornel Co., (Holland). Each vial containing oily solution (50 mg/mL vehicle).

Amygdalin was purchased from Amazon for natural oils Company with dose 100 mg/kg body weight.

Animals and experimental design

40 rats (Rattus norvigicus, male albino, weighing 180–190 g, 12–13 weeks old) were delivered from Egyptian NRC. Before the trial began, rats were kept at our Faculty’s animal house for a week. They were kept in conventional circumstances with a standard rodent feed, unlimited access to water, a standard temperature of 25 °C, and a relative humidity of at least 40%. After 2 weeks of acclimatization, rats were assigned to 4 groups (Gps; 10 animals each).

1 ^st Gp: Control Gp; in which rats will not receive any treatment.

2 ^nd Gp: Amygdalin Gp in which animals injected intramuscularly in the hind limb with amygdalin (100 mg/kg body weight/day) daily for 2 weeks.

3 ^rd Gp: Boldjan Gp; in which rats will injected intramuscular with Boldjan (10 mg/Kg BW/week) for 4 weeks.

4 ^th Gp: Treated Boldjan with Amygdalin Gp (Boldjan + Amygdalin); in which rats injected intramuscular injections with Boldjan for 4 weeks and then treated with Amygdalin for another 2 weeks.

At the end of the experimental period, rats from each group were euthanized with anesthetic ether and subjected to a complete necropsy after 10–12 h of fasting. Blood samples were collected from the inferior vena cava of each rat in non-heparinized glass tubes, blood was incubated at room temperature for 10 min and left to clot then centrifuged at 3,000 r.p.m for 10 min and the serum were collected, serum was separated and kept in clean stopper plastic vial at −80 °C until the analysis of serum parameters. Heart were removed, carefully cleaned in cold saline and weighed.²⁷ Half of heart from each group were fixed in 10% neutral buffer formalin for histological and immunohistochemical examinations and the rest were stored in −80 C for the study of oxidative stress parameters.

Clinical chemistry

Cardiac profile parameters

LDH activity and CK levels were estimated according to the method of Moss et al.²⁸ and Zilva and Pannall²⁹ respectively using commercial kit that was supplied by Vitro Scient, Egypt. CK-MB and AST activity in serum were estimated according to the method of Ogunro et al.³⁰ and Anderson et al.³¹ respectively using commercial kit that was supplied by Spinreact, from Spain.

Lipid profile parameters

Serum total cholesterol and triglycerides were determined according to Allain et al.³² and Fossati and Prenciple³³ respectivelly using Kits of, Linear Chemicals, S.L (Spain). Serum HDL-C and LDL-C levels were determined according to Lopes-Virella et al.³⁴ and Friedewald et al.³⁵ using Kits of, Linear Chemicals, S.L (Spain).

Activities of antioxidant enzymes

Heart tissues were weight and homogenized (10% w/v) separately in ice-cold 1.15% KCl- 0.01 mol/L sodium, potassium phosphate buffer (pH 7.4) in a Potter-Elvehjem type homogenizer. The homogenate was centrifuged at 10,000 g for 20 min. at 4 °C, and the resultant supernatant was used for different enzyme assays.

According to Aldubayan et al.³⁶ and Habig et al.³⁷; malondialdehyde (MDA) and reduced glutathione (GSH) activities in tissue homogenate were estimated respectively. Superoxide dismutase (SOD) and catalase (Cat) activities were estimated according to Misra and Fridovich³⁸ and Saggu et al.³⁹ methods respectively.

Histopathological investigation

Heart from different groups were quickly removed, washed in 0.9 saline solutions and fixed in 10% neutral buffered formalin. Fixed specimens were dehydrated in an ascending series of alcohol, cleared in xylene and embedded in molten paraffin (mp. 50–58 °C). Sections of 7 microns thickness were cut using rotary microtome and mounted on clean slides. Sections were stained with Ehrlich’s haematoxylin and counterstained with eosin as a routine method after Tousson.⁴⁰

Statistical analysis

To determine whether the experimental groups had any differences of significance, one-way ANOVA was employed for statistical analysis, with expression of data in the form of mean values ± SE. In the case of biochemical data, statistical significance was established, to be indicated by P < 0.05. The SPSS software (version 21, SPSS^® Inc., USA) was used to conduct every statistical analysis.

Results

Effect of Boldjan and amygdalin on cardiac enzymes

As represented in Table 1 reveaed that; treatments of rats with Boldjan induced a significant elevation in serum LDH, CK, CK MB and AST as compared to control Gp. On the other hand; there was a significant depletion in serum LDH, CK, CK MB and AST in treated rats with Boldjan + Amygdalin as compared to Boldjan Gp.

Table 1.

Variations in serum LDH (U/l), CK (U/l), CK-MB (ng/ml), and AST (U/L) levels in experimental Gps.

	LDH (U/I)	CK (U/I)	CK MB (ng/ml)	AST (U/I)
Control	158.5^a ± 8.5	741.0^a ± 21.5	2.28^a ± 0.11	129.6^a ± 9.9
Amygdalin	143.1^a ± 10.4	725.0^a ± 19.0	1.91^a ± 0.16	111.3^a ± 8.5
*Boldjan*	261.6^b ± 13.0	1191.5^b ± 16.5	4.33^b ± 0.24	240.5^b ± 13.5
Boldjan + Amygdalin	193.6^a^,^b ± 12.57	935.0^a^,^b ± 23.0	3.41^a^,^b ± 0.14	196.0^a^,^b ± 11.3

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Value represents mean ± SE of 10 rats.

^aSignificant difference from Boldjan group at P < 0.05.

^bSignificant difference from the control group at P < 0.05.

Effect of Boldjan and amygdalin on lipid profiles levels

As represented in Table 2 reveaed that; treatments of rats with Boldjan induced a significant elevation in serum total cholestrol, trigelycride, LDL and a significant depletion in serum HDL as compared to control Gp. On the other hand; there was a significant depletion in serum total cholestrol, trigelycride, LDL and a significant elevation HDL in treated rats with Boldjan + Amygdalin as compared to Boldjan Gp.

Table 2.

Variations in serum lipid profiles levels in different Gps.

	Cholesterol (mg/dl)	Triglyceride (mg/dl)	HDL (mg/dl)	LDL (mg/dl)
Control	107.5^a ± 7.9	112.5^a ± 9.5	41.2^a ± 3.33	43.5^a ± 2.19
Amygdalin	98.0^a ± 7.4	96.0^a ± 7.8	43.0^a ± 2.29	35.8^a ± 1.85
*Boldjan*	152.1^b ± 12.5	142.5^b ± 10.4	31.8^b ± 2.06	91.8^a^,^b ± 5.03
Boldjan + Amygdalin	119.9^a^,^b ± 10.5	129.0^a^,^b ± 10.0	37.5^a^,^b ± 2.25	56.7^a^,^b ± 3.41

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Value represents mean ± SE of 10 rats.

^aSignificant difference from Boldjan group at P < 0.05.

^bSignificant difference from the control group at P < 0.05.

Effect of Boldjan and amygdalin on oxidative stress

As represented in Table 3 reveaed that; treatments of rats with Boldjan induced a significant elevation in testicular MDA and a significant depletion in testicular GSH, SOD, catalase as compared to control Gp. On the other hand; there was a significant depletion in testicular MDA and a significant elevation testicular GSH, SOD, catalase in treated rats with Boldjan + Amygdalin as compared to Boldjan Gp.

Table 3.

Changes in serum cardiac malondialdehyde (MDA), reduced glutathione (GSH), catalase (CAT), and superoxide dismutase (SOD) activities in different groups.

	MDA (nmol/g tissue)	GSH (mmol/g tissue)	Catalase (mmol/min/g/tissue)	SOD (U/g tissue)
Control	22.3^a ± 1.35	0.44^a ± 0.02	55.0^a ± 3.6	0.66^a ± 0.03
Amygdalin	20.5^a ± 1.24	0.51^a ± 0.04	59.5^a ± 3.8	0.72^a ± 0.05
*Boldjan*	49.5^b ± 2.75	0.23^b ± 0.04	24.9^b ± 1.8	0.40^b ± 0.01
Boldjan + Amygdalin	36.5^a^,^b ± 2.15	0.35^a^,^b ± 0.05	40.5^a^,^b ± 3.5	0.61^a ± 0.05

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Value represents mean ± SE of 10 rats.

^aSignificant difference from Boldjan group at P < 0.05.

^bSignificant difference from the control group at P < 0.05.

Effect of Boldjan and amygdalin on cardiac tissues

Heart sections in control and Amygdalin Gps revealed a normal myofibrillar structure with striations (Fig. 1A and B). Heart sections in treated rat with Boldjan revealed severe myocardial hypertrophy, necrosis, mild fibrosis, moderate focal haemorrhage and moderate leukocyte infiltration (Fig. 1C). Heart sections in Boldjan + Amygdalin revealed a moderate myocardial hypertrophy, and mild leukocyte infiltration (Fig. 1D).

Discussion

Athletes can use injectable AASs to directly increase and develop muscle mass.²^,⁴¹ In addition, women utilise it in numerous cosmetics to plump up their lips, cheeks, buttocks, and breasts.¹³ Furthermore, eating meat from animals that have received AAS treatment may have an indirect impact on people. Boldjan is a new AAS drug is utilised by young individuals who want to gain weight, physical mass, and power as well as by veterinarians. Anabolic effects of AAS include first stimulating cell proliferation and second improving male traits through androgenic effects.¹¹^,¹² These effects are different but overlap. The anabolic effects of AAS promote cellular protein synthesis, which leads to tissue accumulation, particularly in muscles. Through the androgen receptor, AAS affect myocytes, causing left ventricular hypertrophy and dilatation as well as impaired contraction and relaxation.⁶ Current investigation was to examine the potential effects of amygdalin extract against Boldjan induced cardic toxicity, injury and oxidative stress in male rat.

Our results revealed that; Boldjan injection in rats induced a significant elevation in LDH, CK, CK MB and AST levels indicate muscles damage. Serum CK-MB levels are being used in the diagnosis of cardiovascular system disorders.^42–44 Similar findings were reported by Patanè et al.⁷; Albaz et al.⁸ who reported that; testosterone and nandrolone application on adolescent rabbits induced elevations in serum CK-MB level. Similarly, Lok et al.⁴⁵ who find an increase CK-MB is observed in with the male rats after testosterone injection while, Tasgin et al.⁴⁶ reported that; no increase has been observed in CKMB levels with female rats. Our results agree with Tousson et al.⁶ who find that; treatments of rats with boldenone undecylenate induced elevation in serum AST, LDH and CK. Similarly, Riezzo et al.⁴⁷ who reported that; AAS induced elevation in LDH in experimental mice/rats models. Current results revealed that; a significant depletion in serum LDH, CK, CK MB and AST in treated rats with Boldjan + Amygdalin as compared to Boldjan Gp. Our results agree with Elmalla et al.¹⁹ who reported that; vitamin B17 have have myocardial protection activity against Ehrlich tumor development in female mice. Also; Tousson et al.²¹ and Said et al.⁴⁸ who find that; amygdalin (vitamin B17) induced depletion for the elevation of AST in EAC. This finding was inagreement with our results, since post treated rats with Amygdalin (vitamin B17) showed significant decrease in serum LDH, CK, CK MB and AST.

Our results revealed that; Boldjan injection in rats induced a significant elevation in cholesterol, triglycride, LDL and a significant depletion in HDL leading to increased risk for atherosclerotic heart disease and myocardial hypertrophy. Our results agreed with those reported by Frati et al.⁴⁹ who reported that; AAS induced cardiac toxicity and elvation in cholesterol, triglycride, LDL. Our results agreed with those reported by EL-Ghareib and Ashry⁵⁰ who find that the total lipids and cholesterol levels significantly increased in calves treated with Boldenone undecylentae. Similarly, Urhausen et al.⁵¹ who find that HDL-cholesterol was distinctly lower in athletes used anabolic-androgenic steroids. Also; Achar et al.⁵² showed that anabolic-androgenic steroids abusers had significantly higher LDL and lower HDL levels than non-abusers. These results were consistent with those reported by Sader et al.⁵³ who find that; a significant decreased in HDL cholesterol levels in treated rabbits with the anabolic steroid nandrolone. Our results are not agreement with Tousson et al.⁶ who reported that, Boldenone induced no changes in serum triglyceride in rats. Current results revealed that; a significant depletion in serum cholesterol, triglycride, LDL and a significant elevation in HDL levels in treated rats with Boldjan + Amygdalin as compared to Boldjan Gp regarding the effect of Amygdalin on lipid profile. Several studies were performed to evaluate the pharmacological and therapeutic benefits of vitamin B17 in treating different conditions like diabetes, dyslipidemia, indigestion and flatulence, inflammation, aging and cancer with variable results and mechanisms Our results are agreement with El-Masry et al.²³ who find that; vitamin B17 induced a depletion in serum cholesterol, triglycride, LDL and a significant elevation in HDL levels in EST. Also agree with Lv et al.⁵⁴ who reported that; Amygdalin ameliorates the progression of atherosclerosis in LDL receptor-deficient mice.

Our results revealed that; Boldjan injection in rats induced changes in oxidative stress biomarker levels and antioxidant defense systems in rat cardiac muscles. Current results revealed that, a significant elevation in cardiac MDA and a significant depletion in GSH, catalase, and SOD as compared to control. Our results are in agreement with Tousson et al.¹ who reported that; AAS Boldenone induced oxidative stress in rabbit liver and kidney tissues. Our results agree with Surai⁵⁵ reported that silymarin is a potent antioxidant inhibiting the lipid peroxidation and prevents the reduction of glutathione enhancing the activity of antioxidants enzymes. Our results agree with Frankenfeld et al.⁵⁶ who showed a decrease in the activity of catalase enzyme after AAS (nandrolone decanoate) intake. Current results revealed the treatments with Amygdalin (Boldjan + Amygdalin) revealed depletion in cardiac MDA and elevation in GSH, catalase, and SOD as compared to Boldjan Gp. Oxidative stress arises when the production of reactive oxygen species overwhelms the intrinsic anti-oxidant defences.^57–59 Our results agree with El-Masry et al.²² who reported that; vitamin B17 improved changes in oxidative stress, DNA damage, apoptosis and proliferation in EAC mice. Also; agree with Elmalla et al.¹⁹ who studied the effect of vitamin B17 on cardiomyopathy against Ehrlich tumor development in female mice.

Current results revealed that; Boldjan injection in rats induced a severe myocardial hypertrophy, degeneration and may be rupture of the cardiac muscle and moderate leukocyte infiltration. Also, these results coincide with Hassan et al.⁵⁷ who reported that; AAS sustaining induces severe ischemic necrosis and degeneration of the cardiac muscle fibers in male albino rats. Our results are in agreement with Abdelhafez⁶⁰ who showed highly degenerated muscle fibers with areas of hemorrhage and widened endomysium. Also, Elgendy et al.⁶¹ reported hypertrophy and degeneration of both cardiac and skeletal muscles and explained this by its effect on the androgen receptors that are widely distributed in different types of muscles. Schmidt and Schmieder⁶² who reported that; a dministration of Boldenone induce various histologic cardiac lesions in young male rats including marked myocardial hypertrophy, necrosis, marked interstitial fibrosis misshapen nuclei, moderate focal hemorrhage, moderate leukocyte infiltration and an increase in PCNA expressions. Our results are in agreement with Tousson et al.⁶ who reported that the Boldenone induced muscle hypertrophy and fibrosis in cardiac muscles in male rabbits. Also; our results are in agreement with McCarthy et al.⁶³ who reported that the anabolic steroid-induced muscle hypertrophy in skeletal and cardiac muscles in humans. The development of new drug carrier designs for particular applications could advance significantly via natural polymeric-based nanomaterials.⁶⁴^,⁶⁵ Current results are in agreement with Elmalla et al.¹⁹ who studied the effect of vitamin B17 on cardiomyopathy against Ehrlich tumor development in female mice. The obtained results in agreement with Nofal et al.⁶⁶ and Abdel-Daim⁶⁷ who reported that although the human body continuously produces free radicals, it possesses several defense system, which are constitutes of enzymes and radical scavengers such as superoxide dismutase, catalase and glutathione peroxidase while non-enzymatic category contains vitamin C, E, A, β-caretenoids, uric acid and ubiquinone. These are called “first line antioxidant defense system” but are not completely efficient because almost all components of living bodies, tissues and cells undergo free radical destruction.

Conclusion

Boldjan injection induced cardiac toxicity and post treatment of Boldjan with amygdalin improved cadaic functions and structure; there fore amygdalin could be an efficient preventive supplement for cardiac toxicity, possibly via controlling oxidative stress events.

Contributor Information

Eman M Hussain, Department of Biology, Collage of Science, Al-Qadisiyah University, Iraq.

Sura M Alkadhimy, Department of Hotel Studies, College of Tourism Sciences, University of Karbala, Iraq.

Asmaa M Neamah, Department of Environment, College of Science, Al-Qadisiyah University, Iraq.

Ehab Tousson, Department of Zoology, Faculty of Science, Tanta University, Egypt.

Author contributions

Ehab Tousson proposed the idea and the experimental design, analyzed the data, approved the final draft, reviewed drafts of the paper and, approved the final draft. Eman M. Hussain and Sura M. Alkadhimy, performed the experiments, contributed reagents/materials/analysis tools, analyzed the data, and wrote the original manuscript. Asmaa M. Neamah analyzed the data, contributed reagents/materials/analysis tools, collected data and reviewed drafts of the paper.

Funding

No fund.

Conflict of interest statement: The authors declare no competing interests.

Data availability

All the data and material were available. The data of this article are included within the article and its additional files.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All the data and material were available. The data of this article are included within the article and its additional files.

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PERMALINK

Beneficial role of amygdalin extracts against animal growth regulator Boldjan induced cardiac toxicity, injury and oxidative stress in male rats

Eman M Hussain

Sura M Alkadhimy

Asmaa M Neamah

Ehab Tousson

Abstract

Introduction

Materials and methods

Chemical and reagent

Animals and experimental design

Clinical chemistry

Cardiac profile parameters

Lipid profile parameters

Activities of antioxidant enzymes

Histopathological investigation

Statistical analysis

Results

Effect of Boldjan and amygdalin on cardiac enzymes

Table 1.

Effect of Boldjan and amygdalin on lipid profiles levels

Table 2.

Effect of Boldjan and amygdalin on oxidative stress

Table 3.

Effect of Boldjan and amygdalin on cardiac tissues

Fig. 1.

Discussion

Conclusion

Contributor Information

Author contributions

Funding

Data availability

References

Associated Data

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Beneficial role of amygdalin extracts against animal growth regulator Boldjan induced cardiac toxicity, injury and oxidative stress in male rats

Eman M Hussain

Sura M Alkadhimy

Asmaa M Neamah

Ehab Tousson

Abstract

Introduction

Materials and methods

Chemical and reagent

Animals and experimental design

Clinical chemistry

Cardiac profile parameters

Lipid profile parameters

Activities of antioxidant enzymes

Histopathological investigation

Statistical analysis

Results

Effect of Boldjan and amygdalin on cardiac enzymes

Table 1.

Effect of Boldjan and amygdalin on lipid profiles levels

Table 2.

Effect of Boldjan and amygdalin on oxidative stress

Table 3.

Effect of Boldjan and amygdalin on cardiac tissues

Fig. 1.

Discussion

Conclusion

Contributor Information

Author contributions

Funding

Data availability

References

Associated Data

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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