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Experimental malnutrition: A systematic review

Marcus Vinicius Henriques Brito

Department of General Surgery, Universidade Estadual do Pará (UEPA), Belém-PA, Brazil

E-mail : wesmiguel@hotmail.com

Mauro de Souza Pantoja

Coordinator of the EMTN (Multidisciplinary Team of Nutritional Therapy, Universidade Estadual do Pará (UEPA), Belém-PA, Brazil

Ana Paula Santos Oliveira Brito

Fellow Master degree, Postgraduate Program in Surgery and Experimental Research, UEPA, Belém-PA, Brazil

Caroline da Silva Alves Palheta

Fellow Master degree, Postgraduate Program in Surgery and Experimental Research, UEPA, Belém-PA, Brazil

Wescley Miguel Pereira da Silva

Graduate student, School of Medicine, Universidade Federal do Pará (UFPA), Belém-PA, Brazil

E-mail : wesmiguel@hotmail.com

William Costa da Silva

Graduate student, School of Medicine, Universidade Estadual do Para(UEPA), Belém-PA, Brazil

DOI: 10.15761/IFNM.1000148

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Abstract

The protein-energy malnutrition (PEM) is an important public health problem. This study aimed to perform a systematic review of articles published in English and Portuguese in the last decade, aimed at research on experimental malnutrition. It was selected studies published from January 2006 to August 2015. The descriptors used were from “modelo de desnutrição” and “model of malnutrition”. The databases consulted were Scielo, PubMed, Lilacs and Cochrane Library. In 17 articles, positive and negative outcomes of malnutrition were searched in different databases. Among these, 8 articles researched the correlation of malnutrition with immune system or gastrointestinal system and 5 articles analyzed the hematopoietic system and the skeletal system. Only 1 paper analyzed the cardiovascular system, 1 analyzed the cutaneous system and 2 the malnutrition itself. Experimental malnutrition articles need to standardize models for malnutrition in more details throughout his writings. Furthermore, it was observed that the studies about malnutrition did not search the relation between surgical stress and malnutrition.

Keywords

 protein malnutrition, protein-energy malnutrition, malnutrition

Introduction

The protein-energy malnutrition (PEM) is a major public health problem that affects millions of people worldwide and can be described as a form of malnutrition where there is inadequate calorie or protein intake. Extreme cases induces in the individual a series of biochemical and organic changes, causing changes in bodily function, and is associated with worsening of the diseases [1].

The PEM has been a statistically significant problem in surgical patients, affecting 22-58% of cases, and is related to higher hospital costs, longer hospitalization, predisposing to a variety of complications, higher incidence of infections and mortality [2]. Clinically, the PEM can be classified into marasmus (deficiency in calorie intake), kwashiorkor (protein malnutrition predominant) or a combination of both, marasmus-kwashiorkor [3].

In this context, laboratory animals have been used increasingly to assess the effects of malnutrition degrees variables in susceptibility to infections and also in the various parameters of the immune response, as well as in several pathologies related to malnutrition [1]. The big advantage of using animal models is to allow highly controlled evaluation of each nutritional parameter, considering that is not possible in the case of human populations.

In this scenario, the present study was to conduct a systematic review of articles published in English and Portuguese in the last decade, aimed at research on experimental malnutrition.

Materials and method

The included studies were about experimental malnutrition, published from January 2006 until August 2015. Keywords used were “modelo de desnutrição” and “model of malnutrition”. Data bases consulted were Scielo, Pubmed, Lilacs and Cochrane Library. It was established the following criteria for inclusion: studies which used extrauterinos animals (post-natal) and articles which were published 10 years ago. As criteria for exclusion: articles with incomplete information and review articles (only original articles were included).

Results

According to elegebility criteria, 17 articles were identified during the study period and are presented in Table 1, and 9 of these ones were published since 2011, showing that the issue is still current. As the place of origin of the articles, 8 of them are from South America, 4 from Europe, 1 from North America and 2 in Asia.

 Year

Tittle

Country

Author(s)

Studied system

Animal

Model

Induction time to malnutrition

Effects

Sex

Number of animals

2006

Preventive strategy for Candida gut translocation during ischemia–reperfusion injury supervening on protein–calorie malnutrition

China

Marotta et al. [15]

Gastrointestinal

Rat Sprague-Dawley

Low protein diet (2,5% casein)

7 days

Significant increase in permeability of the colon malnourished rats. The groups treated with Compound showed partial improvement of this parameter

Uninformed

90

2007

Rapid restoration of colonic goblet cells induced by a hydrolyzed diet containing probiotics in experimental malnutrition

Brazil

Dock -Nascimento,

Gastrointestinal

Rat Wistar

aproteic  (Rhöster)

12 days

Malnutrition decreased the number of goblet cells throughout the colon.

Male

26

Junqueira e Aguilar-Nascimento [12]

2007

Reduction of erythroid progenitors in protein–energy malnutrition

Brazil

Borelli et al. [19]

Hematopoietic

Rat swiss

Low protein diet (20 g/kg - casein)

14 days

Anemia of protein-energy malnutrition was the result of ineffective erythropoiesis.

Male

38

2007

Contribution of polyunsaturated fatty acids to intestinal repair in protein-energy malnutrition

Spain

Nieto et al. [14]

Gastrointestinal

Rat

Low protein diet and hypocaloric (rich in lactose)

14 days

Polyunsaturated fatty acids in the diet can influence the intestinal repair in chronic diarrhea due to protein-energy malnutrition.

Male

80

2007

Restoration by dietary glutamine of reduced tumor necrosis factor production in a low-protein-diet-fed rat model

Japan

Komatsu et al. [10]

Immune

Rat Donryu

Low protein diet (3% casein)

21 days

TNF production by reduction malnourished rat macrophages.

Male

24

2008

Protein-energy malnutrition modifies the production of interleukin-10 in response to Lipopoly saccharide (LPS) in a murine model

Brazil

Fock et al. [6]

Skeletal system e hematopoietic

Rat Swiss Webster

Low protein diet (4% proteína)

14 days

Increased circulating levels of  IL -10 in response to LPS.

Male

84

2009

Protein-energy malnutrition decreases immune response to Leishmania chagasi vaccine in BALB/c mice

Brazil

Malafaia et al.[8]

Immune

Rat Balb/c

Low protein diet and isocaloric (3% casein)

6 weeks

Malnutrition can alter the response to L chagasi vaccine in rats even following nutritional supplementation.

Male and female

40

2010

PTH improves titanium implant fixation more than pamidronate or renutrition in osteopenic rats chronically fed a low protein diet

Switzerland

Dayer et al. [18]

Skeletal system

Rat Sprague-Dawley

Low protein diet and isocaloric (2,5% casein)

6 weeks

Reduction of malnourished rats force and PTH reversed the deleterious effects of malnutrition in mechanical fastening and microarchitecture.

Female

41

2011

Animal model of undernutrition for the evaluation of drug pharmaco kinetics

Spain

Merino-Sanjuán et al. [22]

Malnutrition only

Rat Wistar

Low protein diet and hypocaloric (5% protein)

26 days

The proposed mathematical model allows the body weight of animals to be predicted at a given time taking into account the diet followed in the experimental period.

Male

133

2011

Modelos experimentais de desnutrição e sua influência no trofismo cutâneo

Brazil

Leite et al. [3]

Cutaneous

Rat Wistar

Marasmus (half the standard diet) and Gelatine

60 and 30 days

Dermis thinner , lighter weight and less collagen .

Male

120

2011

Avaliação da gasometria arterial de ratos desnutridos submetidos à anestesia inalatória por éter etílico em vaporizador artesanal

Brazil

Pantoja et al. [20]

Malnutrition only

Rat Wistar

Low protein diet  (“polvilho”)

21 days

The process of malnutrition was effective in reducing weight , serum albumin and bicarbonate.

Male

20

2012

Post-Weaning protein malnutrition increases blood pressure and induces endothelial dysfunctions in rats

Brazil

Belchior et al. [21]

Cardiovascular

Rat Wistar

Low protein diet and hypocaloric ( 9% protein- ration RBD)

3 months

Protein malnutrition after weaning increases blood pressure and induces vascular dysfunction.

Male

20

2012

Modulation of the nuclear factor-kappa B (NF-κB) signalling pathway by glutamine in peritoneal macrophages of a murine model of protein malnutrition

Brazil

Lima et al. [7]

Immune

Rat Balb/c

Low protein diet (2% protein)

21 days

The malnourished animals showed anemia, leukopenia, lower concentration of glutamine in the state of malnutrition .The plasma interferes with the activation of macrophages and higher concentrations of glutamine, in vitro, can negatively affect the NF-κB pathway.

Male

20

2013

An animal model of Kashin-Beck disease induced by a low-nutrition diet and exposure to T-2 toxin

China

Kang et al. [4]

Skeletal system

Rat Sprague-Dawley

Low protein diet, rich in barley(10,2% protein)

4 weeks

Radiographic and histological abnormalities of the tibia.

Male and female

120

2013

Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets

United

Jacobi et al. [13]

Gastrointestinal

Pig

Low protein diet and hypocaloric(half the standard diet)

3 weeks

Lower weight , diarrhea . In infected villi and reduction of lactase activity and increased crypt depth .

Male and female

24

States

2013

Effect of a probiotic fermented milk on the thymus in Balb/c mice under non-severe protein–energy malnutrition

Argentina

Núñez et al. [17]

Immune and hematopoietic

Rat BALB/c

Low protein diet

21 days

Increase of immature thymocytes in malnourished rats and influence of probiotic in the histological and functional recovery of the thymus.

Male and female

35

2013

Protein energy malnutrition decreases immunity and increases susceptibility to influenza infection in mice

England

Taylor et al. [9]

Immune

Rat C57BL/6

Low protein diet and isocaloric  (2% protein)

3 weeks

The malnourished mice exhibited more severe disease following infection with influenza and lower specific antibody response against the virus.

Female

72

Table 1. Articles about experimental malnutrition published from January 2006 until August 2015.

In 17 articles, there was the analysis of different systems in search of positive and negative impacts of malnutrition. It was found 8 articles researching the relationship between malnutrition with the immune system and/or gastrointestinal system, while 5 articles analyzed the hematopoietic system and the skeletal system. Only one paper analyzed the cardiovascular system, one analyzed the cutaneous and 2 studies, just the malnutrition process.

About the experimental animals used, 16 used mice and the pig was used in only one study. The time for induction of the malnutrition was 21 days in 4 studies, while less than 21 days in 5 studies and two weeks or less in 6 studies.

To induction to malnutrition was used the low protein diet mainly, associating this with the low supply of calories in 4 studies. The study by Leite et al., we used 2 methods to get malnutrition, the marasmus method and gelatine method, which is the normal protein diet administration associated with low quality protein. Pantoja et al. used “pouvilho” (a type of biscuit) as a method of induction.

Studies that measured and detected decrease in weight and body growth totaled 7. Serum albumin was kept unchanged only in 1 study. The study of Borelli et al. detected depression of the hematopoietic system, lowering of red blood cells and reticulocytes. Melchior et al. found endothelial dysfunction and high blood pressure in undernourished rats.

Discussion

On the analysis of studies of this review, it can be seen that the experimental malnutrition has become an important area for the better understanding of the pathophysiology of malnutrition. In this regard, several systems have been the subject of research around the world. In China, for example, a study investigated radiographic abnormalities [4]. However, it was the gastrointestinal and immune systems were revealed as the main targets of interest of the scientific community nowadays.

It is noteworthy that the most prevalent cause of immunodeficiency worldwide is severe malnutrition which affects up to 50% of the population in poor countries. The immunological changes resulting from malnutrition can affect both the innate immunity in respect of specific. It has been noted that the availability of components of the complement system and phagocytic function are compromised in malnutrition and this hampers the elimination of pathogens. Both the C3 level, which is the main component opsonic, and the ability of phagocytes to internalize and destroy pathogens, appear reduced in states of desnutrição [5]. Such statements have been exemplified in the studies that correlate immune system with malnutrition, where the main roads studied were the NF-κB and inhibiting macrophages by interleukin 10 [6-10].

The other most studied system was the gastrointestinal which is markedly affected by the effects of PEM. In general, PEM affects the gastrointestinal tract causing atrophy of the gastric and intestinal mucosa. In the stomach causes hyperplasia, ulcerated lesions, decreased hydrochloric acid, weakening of gastric barrier to bacteria. In the intestines, there is a reduction of crypts, villi and intestinal microvilli, size of enterocytes, decreased intestinal transit may generally to constipation, and due to attenuation of the immune system, it is usual to observe infections and diarreia [11-15]. Interestingly, other studies, malnutrition was not significantly contribute to the worsening of the intestinal barrier in rotavirus infection, or to decrease the potency of the vaccine against this pathogen [13,16]. The loss of thymocytes was identified in a study, this loss, as well as changes in the intestinal mucosa, they can be ameliorated by supplementation with probiotic fermented milk [17].

In addition to the immune, and gastrointestinal systems have also been studied bone and hematopoietic system, the main findings loss of bone cells leading to defects like deficient hematopoiesis, lacking blood cells. It has been evidenced histological and radiographic abnormalities in mouse models with Kashin-Beck disease induced malnutrition [4]. Treatment with parathyroid hormone is effective in reversing the deleterious effects of malnutrition long term [18]. In malnutrition, anemia is caused by deficient erythropoiesis as the serum iron and erythropoietin in malnutrition do not change [19].

Although all the selected works have placed on your method data related to diet adopted by the animals, few jobs that have adopted an explicit model of induction to malnutrition, which could easily be replicated by other authors. This was the case of the work of Pantoja et al. [20] and Leite et al. [3], both studies could be considered innovative. At first, it was used as food biscuit flour, “polvilho”, (totally devoid of protein) in Wistar rats diet to check for changes that malnutrition can result in blood gas analysis. Leite et al. used two models to arrive malnutrition: marasmus model which was to halve the mice food portions and the gelatin model, which would correspond to normal protein diet associated with low protein quality [20,3]. In the skin, malnutrition causes loss of collagen with less dermal thickness and negatively influences the tropism cutaneous [3].

As the cardiovascular system, malnutrition induces endothelial dysfunction, an increase of superoxide and nitric oxide in addition to the increased blood pressure [21].

Merino-Sanjuan et al. [22] used the pharmacokinetic study for malnutrition in animal model. Conclusion was the body weight of animals can be predicted at a given time takin in account the diet followed in the experimental period.

It is believed that, as the main characteristics for a model malnutrition, are practicality, the induction time and the adequacy of the animal studied. The evaluated articles, however, can see a significant discrepancy between the induction time in the researched articles, which would justify closer future studies to validate the best induction time for certain species.

Conclusion

It was observed that it is necessary that the experimental malnutrition articles standardize models for induction malnutrition in more detail in the course of his writings, so that other authors may have access to these techniques and can replicate them. In addition, it was noted that the scientific arsenal is lacking in research correlating malnutrition to one of its main causes today: surgical stress.

Acknowledgements

Marcus Vinicius Henriques de Britto and Mauro de Souza Pantoja took part in conception, design and scientific content of the study, critical revision. Ana Paula Santos Oliveira Brito and Carolina Betânia de Jesus Mardock, Caroline da Silva Alves participated in statistical analysis and manuscript preparation. Wescley Miguel Pereira da Silva and William Costa da Silva are responsible for interpretation of data and manuscript preparation in English version.

References

  1. Katona P, Katona-Apte J (2008) The interaction between nutrition and infection. Clin Infect Dis 46: 1582-1588. [Crossref]
  2. Isidro MF, Lima DS (2012) Protein-calorie adequacy of enteral nutrition therapy in surgical patients. Rev Assoc Med Bras 58: 580-586. [Crossref]
  3. Leite SN, Jordão Júnior AA, Andrade TA, Masson Ddos S, Frade MA (2011) Experimental models of malnutrition and its effect on skin trophism. An Bras Dermatol 86: 681-688. [Crossref]
  4. Kang P, Yao Y, Yang J, Shen B, Zhou Z, et al. (2013) An animal model of Kashin-Beck disease induced by a low-nutrition diet and exposure to T-2 toxin. Osteoarthritis Cartilage 21: 1108-1115. [Crossref]
  5. França T (2009) Efeito da desnutrição protéico-calórica experimental na resposta imune e na susceptibilidade á infecção por Staphylococcus aureus [Mestre]. Universidade Estadual Paulista, Instituto de Biociências de Botucatu.
  6. Fock RA, Vinolo MA, Crisma AR, Nakajima K, Rogero MM, et al. (2008) Protein-energy malnutrition modifies the production of interleukin-10 in response to lipopolysaccharide (LPS) in a murine model. J Nutr Sci Vitaminol (Tokyo) 54: 371-377. [Crossref]
  7. da Silva Lima F, Rogero M, Ramos M, Borelli P, Fock R (2012) Modulation of the nuclear factor-kappa B (NF-κB) signalling pathway by glutamine in peritoneal macrophages of a murine model of protein malnutrition. European Journal of Nutrition. 52: 1343-1351.
  8. Malafaia G, Serafim T, Silva M, Pedrosa M, Rezende S (2009) Protein-energy malnutrition decreases immune response to Leishmania chagasi vaccine in BALB/c mice. Parasite Immunology 31: 41-49.
  9. Taylor A, Cao W, Vora K, Cruz J, Shieh W, et al. (2012) Protein Energy Malnutrition Decreases Immunity and Increases Susceptibility to Influenza Infection in Mice. Journal of Infectious Diseases. 207: 501-510.
  10. Komatsu W, Mawatari K, Miura Y, Yagasaki K (2007) Restoration by Dietary Glutamine of Reduced Tumor Necrosis Factor Production in a Low-Protein-Diet-Fed Rat Model. Bioscience, Biotechnology and Biochemistry. 71: 352-357.
  11. Molina G, Pelissari F, Feirhmann A (2013) Consequências da desnutrição protéica para o trato gastrointestinal.
  12. Dock-Nascimento D, Junqueira K, Aguilar-Nascimento J (2007) Rapid restoration of colonic goblet cells induced by a hydrolyzed diet containing probiotics in experimental malnutrition. Acta Cirurgica Brasileira. 22.
  13. Jacobi SK, Moeser AJ, Blikslager AT, Rhoads JM, Corl BA, et al. (2013) Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets. World J Gastroenterol 19: 5094-5102. [Crossref]
  14. Nieto N, Mesa MD, López-Pedrosa JM, Torres MI, Ríos A, et al. (2007) Contribution of polyunsaturated fatty acids to intestinal repair in protein-energy malnutrition. Dig Dis Sci 52: 1485-1496. [Crossref]
  15. Marotta F, Barreto R, Kawakita S, Minelli E, Pavasuthipaisit K, et al. (2006) Preventive strategy for Candida gut translocation during ischemia–reperfusion injury supervening on protein–calorie malnutrition. Chinese Journal of Digestive Diseases. 7: 33-38.
  16. Maier E, Weage K, Guedes M, Denson L, McNeal M, et al. (2013) Protein-energy malnutrition alters IgA responses to rotavirus vaccination and infection but does not impair vaccine efficacy in mice. Vaccine. 32: 48-53.
  17. Núñez I, Galdeano C, Carmuega E, Weill R, de Moreno de Le, et al. (2013) Effect of a probiotic fermented milk on the thymus in Balb/c mice under non-severe protein–energy malnutrition. British Journal of Nutrition. 110: 500-508.
  18. Dayer R, Brennan T, Rizzoli R, Ammann P (2009) PTH improves titanium implant fixation more than pamidronate or renutrition in osteopenic rats chronically fed a low protein diet. Osteoporosis International. 21: 957-967.
  19. Borelli P, Blatt S, Pereira J, de Maurino BB, Tsujita M, et al. (2007) Reduction of erythroid progenitors in protein-energy malnutrition. Br J Nutr 97: 307-314. [Crossref]
  20. Pantoja M, Portela Neto A, Cunha I, Moreira R (2011) Avaliação da gasometria arterial de ratos desnutridos submetidos à anestesia inalatória por éter etílico em vaporizador artesanal. Rev para med. 25.
  21. de Belchior A, Angeli J, de O. Faria T, Siman F, Silveira E, et al. (2012) Post-Weaning Protein Malnutrition Increases Blood Pressure and Induces Endothelial Dysfunctions in Rats. PLoS ONE. 7: e34876.
  22. Merino-Sanjuán M, Catalán-Latorre A, Nácher A, Miralles-Arnau S, Jiménez-Torres NV (2011) Animal model of undernutrition for the evaluation of drug pharmacokinetics. Nutr Hosp 26: 1296-1304. [Crossref]

Editorial Information

Editor-in-Chief

Renee Dufault
Food Ingredient and Health Research Institute

Article Type

Review Article

Publication history

Received date: April 10, 2016
Accepted date: April 29, 2016
Published date: May 03, 2016

Copyright

©2016 Brito MVH. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation

Brito MVH, Pantoja M, Brito APSO, Palheta CSA, da Silva WMP, et al., (2016) Experimental malnutrition: A systematic review. Integr Food Nutr Metab 3: doi: 10.15761/IFNM.1000148

Corresponding author

Wescley Miguel Pereira da Silva

Graduate student, School of Medicine, Universidade Federal do Para (UFPA), Belem-PA, Brazil.

E-mail : wesmiguel@hotmail.com

 Year

Tittle

Country

Author(s)

Studied system

Animal

Model

Induction time to malnutrition

Effects

Sex

Number of animals

2006

Preventive strategy for Candida gut translocation during ischemia–reperfusion injury supervening on protein–calorie malnutrition

China

Marotta et al. [15]

Gastrointestinal

Rat Sprague-Dawley

Low protein diet (2,5% casein)

7 days

Significant increase in permeability of the colon malnourished rats. The groups treated with Compound showed partial improvement of this parameter

Uninformed

90

2007

Rapid restoration of colonic goblet cells induced by a hydrolyzed diet containing probiotics in experimental malnutrition

Brazil

Dock -Nascimento,

Gastrointestinal

Rat Wistar

aproteic  (Rhöster)

12 days

Malnutrition decreased the number of goblet cells throughout the colon.

Male

26

Junqueira e Aguilar-Nascimento [12]

2007

Reduction of erythroid progenitors in protein–energy malnutrition

Brazil

Borelli et al. [19]

Hematopoietic

Rat swiss

Low protein diet (20 g/kg - casein)

14 days

Anemia of protein-energy malnutrition was the result of ineffective erythropoiesis.

Male

38

2007

Contribution of polyunsaturated fatty acids to intestinal repair in protein-energy malnutrition

Spain

Nieto et al. [14]

Gastrointestinal

Rat

Low protein diet and hypocaloric (rich in lactose)

14 days

Polyunsaturated fatty acids in the diet can influence the intestinal repair in chronic diarrhea due to protein-energy malnutrition.

Male

80

2007

Restoration by dietary glutamine of reduced tumor necrosis factor production in a low-protein-diet-fed rat model

Japan

Komatsu et al. [10]

Immune

Rat Donryu

Low protein diet (3% casein)

21 days

TNF production by reduction malnourished rat macrophages.

Male

24

2008

Protein-energy malnutrition modifies the production of interleukin-10 in response to Lipopoly saccharide (LPS) in a murine model

Brazil

Fock et al. [6]

Skeletal system e hematopoietic

Rat Swiss Webster

Low protein diet (4% proteína)

14 days

Increased circulating levels of  IL -10 in response to LPS.

Male

84

2009

Protein-energy malnutrition decreases immune response to Leishmania chagasi vaccine in BALB/c mice

Brazil

Malafaia et al.[8]

Immune

Rat Balb/c

Low protein diet and isocaloric (3% casein)

6 weeks

Malnutrition can alter the response to L chagasi vaccine in rats even following nutritional supplementation.

Male and female

40

2010

PTH improves titanium implant fixation more than pamidronate or renutrition in osteopenic rats chronically fed a low protein diet

Switzerland

Dayer et al. [18]

Skeletal system

Rat Sprague-Dawley

Low protein diet and isocaloric (2,5% casein)

6 weeks

Reduction of malnourished rats force and PTH reversed the deleterious effects of malnutrition in mechanical fastening and microarchitecture.

Female

41

2011

Animal model of undernutrition for the evaluation of drug pharmaco kinetics

Spain

Merino-Sanjuán et al. [22]

Malnutrition only

Rat Wistar

Low protein diet and hypocaloric (5% protein)

26 days

The proposed mathematical model allows the body weight of animals to be predicted at a given time taking into account the diet followed in the experimental period.

Male

133

2011

Modelos experimentais de desnutrição e sua influência no trofismo cutâneo

Brazil

Leite et al. [3]

Cutaneous

Rat Wistar

Marasmus (half the standard diet) and Gelatine

60 and 30 days

Dermis thinner , lighter weight and less collagen .

Male

120

2011

Avaliação da gasometria arterial de ratos desnutridos submetidos à anestesia inalatória por éter etílico em vaporizador artesanal

Brazil

Pantoja et al. [20]

Malnutrition only

Rat Wistar

Low protein diet  (“polvilho”)

21 days

The process of malnutrition was effective in reducing weight , serum albumin and bicarbonate.

Male

20

2012

Post-Weaning protein malnutrition increases blood pressure and induces endothelial dysfunctions in rats

Brazil

Belchior et al. [21]

Cardiovascular

Rat Wistar

Low protein diet and hypocaloric ( 9% protein- ration RBD)

3 months

Protein malnutrition after weaning increases blood pressure and induces vascular dysfunction.

Male

20

2012

Modulation of the nuclear factor-kappa B (NF-κB) signalling pathway by glutamine in peritoneal macrophages of a murine model of protein malnutrition

Brazil

Lima et al. [7]

Immune

Rat Balb/c

Low protein diet (2% protein)

21 days

The malnourished animals showed anemia, leukopenia, lower concentration of glutamine in the state of malnutrition .The plasma interferes with the activation of macrophages and higher concentrations of glutamine, in vitro, can negatively affect the NF-κB pathway.

Male

20

2013

An animal model of Kashin-Beck disease induced by a low-nutrition diet and exposure to T-2 toxin

China

Kang et al. [4]

Skeletal system

Rat Sprague-Dawley

Low protein diet, rich in barley(10,2% protein)

4 weeks

Radiographic and histological abnormalities of the tibia.

Male and female

120

2013

Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets

United

Jacobi et al. [13]

Gastrointestinal

Pig

Low protein diet and hypocaloric(half the standard diet)

3 weeks

Lower weight , diarrhea . In infected villi and reduction of lactase activity and increased crypt depth .

Male and female

24

States

2013

Effect of a probiotic fermented milk on the thymus in Balb/c mice under non-severe protein–energy malnutrition

Argentina

Núñez et al. [17]

Immune and hematopoietic

Rat BALB/c

Low protein diet

21 days

Increase of immature thymocytes in malnourished rats and influence of probiotic in the histological and functional recovery of the thymus.

Male and female

35

2013

Protein energy malnutrition decreases immunity and increases susceptibility to influenza infection in mice

England

Taylor et al. [9]

Immune

Rat C57BL/6

Low protein diet and isocaloric  (2% protein)

3 weeks

The malnourished mice exhibited more severe disease following infection with influenza and lower specific antibody response against the virus.

Female

72

Table 1. Articles about experimental malnutrition published from January 2006 until August 2015.