ARTÍCULO DE REVISION

Indicators of energy metabolism in llamas (Lama glama) in the prepartum, postpartum and lactation transition period

Indicadores del metabolismo energético en llamas (Lama glama) en el período de transición preparto, posparto y lactancia

Cayo-Rojas, Faustina; Mamani-Linares, Lindón Willy

Cayo-Rojas, Faustina

cayorf31076@gmail.com

Public University of El Alto. Veterinary Medicine and Zootechnics. El Alto, La Paz Bolivia

Mamani-Linares, Lindón Willy

Public University of El Alto. Postgraduate Unit. Agricultural, Livestock and Natural Resources Sciences Area. El Alto, La Paz Bolivia

Journal of the Selva Andina Animal Science

Selva Andina Research Society, Bolivia

ISSN: 2311-3766

ISSN-e: 2311-2581

Periodicity: Bianual

vol. 11, no. 2, 2024

editor.animalscience@sars.org.bo

Received: 01 May 2024

Accepted: 01 September 2024

Published: 01 October 2024

URL: https://portal.amelica.org/ameli/journal/198/19850921985092010/

DOI: https://doi.org/10.36610/j.jsaas.2024.110200065x

Selva Andina Research Society

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Abstract: Energy metabolism indicators allow determining the nutritional and metabolic condition and the energy imbalance that may be the cause of low fertility rates in llamas grazing on native pastures. In llamas, gestation is long, only one calf is born per year and the fertility rate is low. Therefore, measures must be taken to prevent miscarriages and give the offspring the best possible start in life. During the prepartum, postpartum and lactation transition period the decrease in dry matter intake coincides with the increase in nutrient demand due to the onset of lactation, which can lead to a negative energy balance, the enormous metabolic challenges during the transition period are related to the negative energy balance as a result of the mobilization of the body's energy reserves by increasing the concentration of non-esterified fatty acids and beta-hydroxybutyrate in the blood plasma. Camelids have higher blood glucose concentrations, lower plasma ketone body concentrations than domestic ruminants, a weak response to insulin and reduced cellular glucose uptake. The imbalance in metabolic adaptation mechanisms during the transition and lactation period interferes with body homeostasis, also predisposing to the development of ketosis. In addition, early postpartum is associated with a prolonged period of postpartum anestrus, delayed ovulation and poor reproductive outcomes.

Keywords: Negative energy balance, non-esterified fatty acids, beta-hydroxybutyrate, prepartum, postpartum, Lama glama.

Resumen: Los indicadores del metabolismo energético permiten determinar la condición nutricional, metabólica y el desequilibrio energético que puede ser la causa de las bajas tasas de fertilidad en llamas pastoreadas sobre pasturas nativas. En llamas, la gestación es larga, sólo nace una cría por año y la tasa de fertilidad es baja. Por lo tanto, se deben tomar medidas para prevenir abortos espontáneos y ofrecer a las crías el mejor comienzo de vida posible. Durante el período de transición preparto, posparto y lactancia la disminución de la ingesta de materia seca coincide con el aumento de la demanda de nutrientes debido a la llegada de la lactancia, que puede conducir a un balance energético negativo, los enormes desafíos metabólicos durante el periodo de transición están relacionados con el balance energético negativo como resultado de la movilización de las reservas energéticas del cuerpo, al aumentar la concentración de ácidos grasos no esterificados y beta-hidroxibutirato en el plasma sanguíneo. Los camélidos tienen mayores concentraciones de glucosa en sangre, concentraciones más bajas de cuerpos cetónicos plasmáticos que rumiantes domésticos, una débil respuesta a la insulina y reducción de la absorción celular de glucosa. El desequilibrio en los mecanismos de adaptación metabólica durante el período de transición y lactancia interfieren en la homeostasis corporal, también predisponen a la presentación de cetosis. Además, el posparto temprano está relacionado con un período prolongado de anestro posparto, retraso de la ovulación y malos resultados reproductivos.

Palabras clave: Balance energético negativo, ácidos grasos no esterificados, beta-hidroxibutirato, preparto, posparto, Lama glama.

Introduction

South American camelids (SAC) have fulfilled a key role in the culture, economy and food security of Andean countries, and their contribution to the subsistence of low-income farmers is important 1 . Thus, improving breeding systems represents the best strategy to avoid poverty 2 . This is due to the ability of alpacas and llamas to produce fiber and meat under extreme geographic and climatic conditions 3 .

In camelid production, nutrient deficiency and imbalance in metabolic adaptation mechanisms can cause sub-fertility syndrome (less than 50 %). Several authors approve that one of the main obstacles for this species lies in the low fertility rates, both in alpacas and llamas, which usually do not exceed 60 % 4 . And an embryonic mortality rate of 45-56 % has been determined in herds in Peru 5 ⁻ ⁷ .

Early embryonic demise is estimated to be the most common form of reproductive loss in SAC, affecting 10-15 % in the first 60 days of pregnancy. Under these conditions, it can occur up to 60-80 % in the first 90 days of gestation 8 .

Dairy cows at the end of gestation and beginning of lactation have a negative energy balance (NEB), related with a decrease in dry matter (DM) intake and an increase in energy demand 9,10 . In the peripartum period, a marked metabolic change occurs, from a gestational state (low demand) to a lactation state (high demand), associated with a growth in the rate of lipolysis and alterations in insulin action in peripheral tissues ¹¹ .

Dietary insufficiency causes mobilization of adipose reserves, characterized by an increase in non-esterified fatty acids (NEFA) in blood (more than 0.6 mmol L⁻¹) and a slight increase in beta-hydroxybutyrate (BHB) in blood, up to approximately (more than 0.09 to 0.18 mmol L⁻¹) in camelids 12,13 .

NEB is strongly related with the duration of the postpartum an ovulatory period, through the attenuation of luteinizing hormone (LH) and low levels of blood glucose, insulin and insulin-like growth factor 1 (IGF-1), which in set limit the production of estrogens by dominant follicles 14 . Cows with high plasmatic concentrations of NEFA in the transition period postpartum, they have a higher risk of hyperglycemia and insulin resistance (IR) during the period of prepartum and postpartum transition 15 .

There are many reports in the literature on the relationships between NEB and fertility, almost all of them related to beef cattle production systems, dairy farming on pasture, grazing plus supplementation and confined, with feeding totally mixed rations, we did not find in the literature reports that link NEB with indicators of energy metabolism in llamas (total protein, urea or NUS, creatinine, glucose, IR, triacyl-glycerols (TG), cholesterol, NEFA and BHB), under a production system based on native pastures or grazing plus supplementation in the Andean Altiplano.

The nutritional status of the female during the prepartum, postpartum and lactation transition period is very important, nutritional balances or imbalances during these periods can lead to phenotypic and metabolic changes in development of the individual 15,16 . Therefore, the objective of this review was to assemble national and international scientific literature on advances in this knowledge acquired on metabolism indicators energy of llamas, in the prepartum, postpartum and breastfeeding transition period.

Development

Llama production systems are traditional, completely non- specialized and based on extensive grazing in native grasslands, composed mainly of grasses of low nutritional quality 2 . Which it affects the productive performance of camelids, another factor that affects productivity is reproduction. In the pre-partum, delivery and lactogenesis animals undergo a NEB that occurs when the energy needed for metabolism-homeostasis is greater than the energy supplied through nutrient intake ¹⁷ . Dietary insufficiency causes mobilization of adipose reserves, characterized by an increase in NEFA and BHB in camelids blood 13 . Energy imbalance in ruminants can cause a sub-fertility syndrome, low conception rate, increased embryonic mortality and delayed uterine involution ¹⁷ ,18 . All these antecedents indicate that the nutritional status of the female during the pre-partum, post-partum and lactation transition period is quite important 16 .

Pre-birth transition period. The fetal development of domestic camelids shows exponential growth around the seventh month of gestation 19 . Thus, the high nutritional demand for fetal growth coincides with the critical period of the pre-birth transition period of altiplano (August to October), with nutrient deficiency 20 , it is causing an energy imbalance in ruminants ¹⁷ , ¹⁸ .

The dairy cow endures tremendous physiological challenges during the transition period, which is the most critical period 21 , leading to NEB associated with decreased DM intake and increased energy demand 9,10 , impaired immunity, alterations in hormonal activity, nutrient distribution, to help nourish the growing fetus, and support the start of a new lactation ²¹ .

Energy supplementation (with cracked corn kernels) administered three weeks before calving to grazing cows increased milk production and reduced ovarian restart, consistent with improved energy balance, body condition score (BCS), and higher insulin levels during the early postpartum period. supplemental feed may not improve pregnancy rates, an increase in the percentage of calves alive at weaning and weaning weight would improve net returns during the cow-calf phase 22 .

Postpartum transition period. Apparently, in SAC the dietary restriction could be associated with the physiological and productive state of the animal 23 . It has been described in llamas subjected to chronic nutritional restriction, which had small dominant follicles, corpus luteum, and less progesterone secretion 24 . In addition, dietary changes in cows cause an immediate and rapid stimulation in metabolism ²⁵ . DM intake is the main component of energy balance, which affects fertility in cows 18 .

During the calving season, and without the presence of males, females can remain sexually receptive for periods of up to 36 days, with a brief anestrus of no more than 48 h ²⁶ . When males and females are kept separate, and come together at any time (once a month), both are sexually active throughout the year, and females can give birth in different months 5,26,27 . Thus, to achieve high levels of milk production, in the early postpartum period, their body reserves must be mobilized, which, in turn, are related to energy intake in the dry period (2 months before delivery). Fat reserves are mainly used for lactation and maintenance, and reproductive processes receive a lower priority ¹⁴ , in relationship with another physiological states of maintenance, lactation and growth when available nutritional resources are limited 28 . Therefore, ensuring good nutritional status during this period is an important objective to optimize postpartum in females ²⁹ .

Lactation period. Food availability affects both mother and offspring. The year of birth (dry years vs. rainy years) of the offspring considerably affected live weight (LW) at birth, at weaning, implying that the environment has a marked influence on the development of biomass body weight of the offspring and the pre-and postpartum BCS of llamas over time 30 . In primiparous cows that have a lower BCS during the early postpartum period, cows produce less milk than multiparous cows ³¹ , milk production affects the weaning weight of the offspring.

An important element that increases the survival rate of alpaca offspring is birth weight (higher birth weight, it has lower risk of perinatal complications and less need for bottle feeding). Offspring from mothers who received mineral supplements have higher birth weights 32 . Likewise, weaning weight is higher for calves born to cows that grazed on irrigated pasture in relationship to cows fed with hay after animalbirth 22 . On the other hand, nutritional deficiency associated with breastfeeding is considered the main factor, that is affecting the duration of postpartum anestrus in cattle 33, ³⁴ .

Blood indicators of energy balance. During the transition period (prepartum and postpartum) the decrease in intake, or consumption of DM coincides with the increase in nutrient demand, due to the beginning of lactation, this can lead to a NEB and enormous metabolic challenges, which leads to the mobilization of fat, such incidents would increase the levels of NEFA and BHB in the plasma 35 , as well as alter the blood levels of other indicators: glucose, cholesterol, urea, albumin, aspartate-aminotransferase and glutamate-dehydrogenase 15 .

Metabolites in blood.

Total protein or proteinemia. Wittwer 36 indicates that total protein corresponds to all the proteins present in a serum sample (albumins + globulins). In llamas, the influence of the season (dry or rainy) on serum biochemistry is evident: alanine transaminase, total protein, albumin, increased in summer, while, urea and bilirubin increased in winter 37 .

Llamas develop hypoproteinemia ³⁸ (total proteins: 55.9 g L⁻¹, reference limits: 58-69.3 g L⁻¹) and hypoalbuminemia 39 (albumin: 28.1 g L⁻¹, reference limits: 33.9-40.5 g L⁻¹). According to Tallacagua-Terrazas & Mamani-Tola 40 in the determination of total protein, it was detected that the values are low (43.2 g L⁻¹), in relationship to the data obtained by Copa & Condori 41 , in llamas of baby teeth and two teeth, this it is probably due to the physiological state, because they use more proteins for tissue and body growth.

Non-protein nitrogenous metabolites. Among the non-protein nitrogenous compounds of the body, urea, creatinine, uric acid and ammonia are cited for their clinical interest, the first two being of greatest interest 36 . Likewise, Norambuena et al. ²⁰ ,24 , shown increased NEB and plasma urea concentrations in previous studies carried out in llamas, alpacas and vicuñas. Apparently, camelids use in a greater extent protein as a substrate for energy production and gluconeogenesis, with urea recycling being more efficient 19 .

Blood urea nitrogen (BUN). Urea is a terminal product of protein metabolism, synthesized in the liver from ammonia and the transamination of transport amino acids and those absorbed in the intestine. In ruminants, the formation and use of ammonia in the rumen is of greater importance; it depends on the protein/energy ratio of the diet. In ruminants it is an indicator of the ruminal synchrony of degradable proteins with energy 36 .

The plasma concentration of urea in camelids is 3.2-12.8 mmol L⁻¹ in llamas, 3.9-10.2 mmol L⁻¹ in alpacas. Urea decrease levels are infrequent, although it can occur in association with serious liver diseases or protein malnutrition ⁴² .

In llamas, high concentrations of plasma urea were observed when they consumed foods with low gross protein content (6.2 %), it reveals different metabolic adaptations of proteins and/or nitrogen, something not observed in true ruminants such as sheep and goats. These characteristics may contribute to explaining the lower metabolic rates in llamas compared to real ruminant 43 . Tallacagua-Terrazas & Mamani-Tola ⁴⁰ informed urea values of 90 mg dL⁻¹ in llamas, these parameters are high for the species ⁴⁴ .

The BUN is directly influenced by the amount of crude protein (CP) in the diet ⁴⁵ ,46 , another important aspect is also the energy content of the feed 47 . In alpacas, ranges of 13.53-20.54 mg dL⁻¹ and values from 11.61 to 20.18 mg dL⁻¹ in sheep were reported. It was concluded that, although there is a direct relationship between BUN and the levels of CP in the diet in both species (alpacas and sheep), the rates of increase are different between them 45 . Tallacagua-Terrazas & Mamani-Tola ⁴⁰ informed BUN levels of 42.03 mg dL⁻¹ for llamas, these values are similar for alpacas, Dixon et al. 48 showed values of 44 mg dL⁻¹ in alpacas (reference interval 13 to 28 mg dL⁻¹), these values are high in llamas and alpacas in relationship to sheep and cattle. It should be considered that the nutritional needs for maintenance of adult animals are lower than for animal in growth stage ⁴⁹ , and, therefore, urea recycling of an adult animal will be lower than in growing animals, thus increasing BUN levels. In this case, recycled urea can be an important source of nitrogen to sustain microbial fermentation and, therefore, guarantee efficient digestion and the utilization of low protein content feeds 50 .

The mean plasma urea nitrogen (BUN) concentration for all animals in the first week of postpartum was significantly higher than the mean for the other three weeks. Moreover, decrease in temperature, that occurred with a change from summer to autumn, it appeared to coincide with an increase in BUN levels ⁵¹ .

Creatinine. Metabolite generated in the muscles from phosphocreatine as a source of energy. Its production in each individual is constant and it is eliminated by the kidney through glomerular filtration without tubular reabsorption, so it is a measure of the degree of glomerular filtration. Indicator of renal function 36 . The plasma concentration of creatinine in mammals is 15 to 150 μmol L⁻¹, in camelids as llamas, it is 79.5-247. 5 μmol L⁻¹ and 54-177 μmol L⁻¹ in alpacas ⁴² . In young growing animals, the plasma concentration is encountered highest values 40 .

Other cases of azotemia in SAC were described following acute renal failure because of poisoning Chamorro et al. 52 Dixon et al. 48 , reported creatinine increase of 176.8 μmol L⁻¹ (reference interval, 80-150 μmol L⁻¹) in alpaca calves. Clinical chemistry in alpacas revealed increased creatinine, urea, calcium and potassium. These results are similar to those described by Jankovsky et al. ⁵³ . In addition, kidney changes were escorted by azotemia, hyperphosphatemia and also hypocalcemia 54 Biochemical parameters did not report changes in serum creatinine 44 with an overall mean serum creatinine level of 92 μmol L⁻¹ in llamas grazed on native pastures 24 . While creatinine concentration in all categories of llamas was higher than in alpacas 39 .

Carbohydrates. Wittwer 36 arguments that carbohydrates or glucides are the main energy source of animal cellula. Most frequent alterations in carbohydrate metabolism in cattle are ketosis type I (hypoglycemia or hyperketonemia), II (diabetic or hyperinsulinic) and dietary (butyric or dietary).

Glucose or glycemia. Camelids have higher blood glucose concentrations than domestic ruminants, and they have a weak insulin response and slow cellular uptake of glucose. Feed-restricted camelids have reduced glucose clearance, and sick camelids may be even more glucose intolerant. While ruminants with fatty liver and ketosis have concurrent hypoglycemia, camelids often have hyperglycemia 55 . Therefore, glucose administration must be carefully controlled in anorexic camelids.

Glycemia in mammals fluctuates between 2.14 to 7 mmol L⁻¹, being lower in ruminants, (2.5-4.1 mmol L⁻¹) 36 . Plasma glucose concentration is 4.3 to 9.9 mmol L⁻¹ in llamas and 5.1 to 9.1 mmol L-1 in alpacas ⁴² .

Fowler & Bravo ⁵⁶ described that normal concentrations range from 4.3 to 9.9 mmol L⁻¹. This range is twice that of cattle and sheep (2.5 and 3.9 mmol L⁻¹) at several stages of gestation. The higher blood glucose concentrations compared to other ruminants may be due to IR or the inability of camelids to switch their metabolism from fat to carbohydrates ⁵⁷ . According to Burton et al. 58 glucose concentrations ranged from 6.6 to 12.7 mmol L⁻¹ for mothers, with the highest concentration occurring at the time of parturition. However, it is not possible to determine whether the glucose peak occurred before parturition or peaked on the day of parturition.

Insulin resistance (IR). It is known by a state of reduced sensitivity of target cells to respond to physiological concentrations of insulin ⁵⁹ . In dairy cows, periparturient ketosis can be categorized by hyperglycemia and hyperinsulinemia, probably due to IR 60 , and it is classified as type II ketosis due to its similarities with type I diabetes mellitus ⁶¹ . Barboza et al. 15 informed prepartum hyperglycemia (>4.1 mmol L⁻¹) in cattle, that were the main risk factors for IR in the transition period. Studies have proposed that IR is a homeostatic adaptation of the dairy cow to prioritize the mammary gland and promote gluconeogenesis and lipolysis ¹¹ .

The imbalance in the metabolic adaptation mechanisms during the transition period and early lactation interferes body homeostasis, and also it predisposes to the presentation of ketosis. Ketosis is classified into type I and II, due to a shortage of precursors or a blockage in the gluconeogenic capacity to meet energy demand, respectively ⁶¹ . Type I ketosis happens between the third and sixth week of lactation, because of the high energy demand, accompanied by hypoglycemia, hypoinsulinemia and high circulating concentrations of ketone bodies. On the other hand, type II ketosis occurs around calving due to NEB and the mobilization of adipose tissue, obese cows are the most susceptible due to the greater depression in DM consumption in the peripartum period. Acetonemia or subclinical ketosis happens in cows with BHB values > 1.2 mmol L⁻¹; cows with clinical ketosis present BHB values > 3.0 mmol L⁻¹ in all animals with type II ketosis 36 .

Lipids and ketone bodies. According to Wittwer ³⁶ lipids found in plasma are cholesterol and triacylglycerols (triglycerides), which form part of lipoproteins, in addition to NEFAs and ketone bodies (acetone, acetoacetate and BHB).

Triacylglycerol or triacylglycerolemia. This is a constituent of adipose tissue formed by glycerol bound to three fatty acids and as such is the main source of energy for the body. It is an indicator of suspected primary and secondary alterations in lipid metabolism 36 .

The plasma concentration of TG in camelids is 0-0.27 mmol L⁻¹ in llamas and 0.12-0.51 mmol L⁻¹ in alpacas 42 . On the other hand, McKenzie et al. ³⁸ reported a plasma concentration of TG of 0.53 mmol L⁻¹ in llamas and alpacas, with a reference range of 0.09 to 0.63 mmol L⁻¹.

Plasma TG concentrations (mmol L⁻¹) are generally of similar magnitude in llamas, sheep and goats, and they are not affected by the diet supplied 43 . Husakova et al. ⁶² reported higher concentrations of TG, cholesterol, vitamins and some minerals in alpacas in the group of animals that received supplementation in the winter feed.

Pregnant and non-pregnant alpacas have similar plasma TG concentrations (0.3 vs. 0.4 mmol L⁻¹) with a general range of (0.1-0.5 mmol L⁻¹) 23 . The high liver TG, in turn, these are associated with an increase in the interval - first ovulation (open days) and reduced fertility 63 .

Cholesterol or cholesterolemia. It can be of external or internal origin, the latter is predominating in herbivores, mostly synthesized by the liver, and in adipose tissue in ruminants, from acetyl-CoA, which is then esterified. It is found in animals as a component of the cell membrane and precursor of steroid hormones. Cholesterol is an indicator of supposed primary or secondary alterations in lipid metabolism. Cholesterolemia in mammals fluctuates between 1.5 and 6.5 mmol L⁻¹, It is being higher after food intake and in older animals. Hypocholesterolemia and hypoadrenocorticism are appreciated in diets with scarse energy or fiber in ruminants 36 .

Prepartum cows had inferior cholesterol concentrations (±27 %) than lactating cows, in relationship with low DM intake in primiparous cows ³⁶ . backwards ³¹ , cholesterol concentration increased during the early postpartum period in both primiparous and multiparous categories, although multiparous cows had higher cholesterol around day 60 after early postpartum than primiparous cows, calves had considerably higher cholesterol than the older group, it can be explained by the fact that most of the sampled calves had breast milk as the main part of their nutrition 62 .

Plasma cholesterol concentration in camelids is 0.34-2.3 mmol L⁻¹ in llamas and 0.24-2.15 mmol L⁻¹ in alpacas 39 . Pregnant and non-pregnant alpacas have similar plasma cholesterol concentration (1 vs. 0.9 mmol L⁻¹) ²³ .

Non-esterified fatty acids (NEFA). These are long-chain free fatty acids (>12 C), that usually derive from the degradation of TG in adipose tissue, liver and mammary gland. These are conveyed in the plasma, for having as their final destination their β-oxidation, or the neosynthesis of TG. The degree of fat mobilization, mainly in ruminants are an indicator of an energy deficiency. The most frequently described condition that presents an increase of NEFA in the plasma is the increase in its mobilization in response to a negative energy balance. Its greatest clinical use is in ruminants in order to evaluate the nutritional balance of cows in the transition period 36 .

Plasmatic NEFA concentration in mammals oscillates between 0.1 and 0.5 mmol L⁻¹, It is being higher after prolonged fasting 36 . They are raised in cases of hepatic lipolysis 42 . Strieder Barboza et al. ¹⁵ report NEFA values >0.40 mmol L⁻¹ in dairy cows, because of to excessive lipomobilization.

The plasmatic concentration of NEFA in camelids is (<0.6 mmol L⁻¹) ⁴² , with a range of (0.1- 0.7 mmol L⁻¹) 62 . Similarly, Norambuena et al. 20,24 indicated that BEN increased plasmatic NEFA concentrations in previous studies conducted on llamas, alpacas, and vicuñas. Biochemical analysis of llama and alpaca plasma exposed raised NEFA concentrations (0.30 mEq L⁻¹) ³⁴ . Norambuena et al. 20 moreover stated an increase in NEFA blood (more than 0.6 mmol L⁻¹) in camelids. The values described in this study were lower than those cited above. Likewise, Putman et al. ⁶⁴ cited that NEFA levels appear to be high after two days of drying off or after finishing lactation. Pregnant and non-pregnant alpacas have comparable NEFA concentrations (0.6 vs. 0.8 m-mol L⁻¹), it is indicating that the energy metabolic state does not explain the differences found in their reproductive success 31 .

NEFA levels gradually decline over time (days postpartum) ⁶⁵ , it is accompanied by a reduction in the mobilization of reserve tissues. Also, Alforma et al. ⁶⁶ indicated that NEFA levels diminished as the postpartum period progressed in cows. No rise in postpartum of NEFA were observed in llamas ⁴³ .

Ketone bodies or ketonemia. These are three intermediate products of energy metabolism, it is produced by β-oxidation of fatty acids in hepatocytes when acetyl-CoA is transformed into BHB, acetoacetate and acetone. The quantity of BHB and acetoacetate in the hepatocyte is the same. It is mainly used in ruminants as an indicator of energy deficiency. The unit for BHB 1 mg dL⁻¹ x 0.096 = 1 mmol L⁻¹, it is present in cases of mobilization of fat reserves compared to a NEB 40 . Camelids have lower concentrations of plasmatic ketone bodies than domestic ruminants 39 . BHB concentrations in llamas seem to reflect hepatic ketogenesis, and therefore, an altered metabolic state of the animal, unlike true ruminants, where BHB is greatly influenced by foregut fermentation ⁴³ .

In alpacas, NEFA values of (0.24 mmol L⁻¹) are exposed 42 . Norambuena et al. 20,24 report that NEFA increased plasmatic BHB concentrations in llamas, alpacas and vicuñas. Norambuena et al. 23 , also it reported a slight increase in BHB (up from 0.1 to 0.19 mmol L⁻¹) in camelids, the values reported in this study were lower than those cited above. Biochemical analysis of llama and alpaca plasma revealed elevations of plasma BHB levels (1.17 mg dL⁻¹) ³⁸ . The increase in BHB, although, it is not as closely correlated with CC as reported by Reist et al. ⁶⁷ , it could also be a reflection of low energy in the post-partum diet ⁶⁸ , BHB levels remained higher for longer after parturition, probably due to a different composition of the diet or a lower amount of DM intake. According to Norambuena et al. 20 BHB values were higher than expected under nutritional energy balance, indicating a lipolytic and ketogenic metabolic response, respectively, in domestic camelids.

Negative energy balance, ketosis and their risk factors. Feed intake offers the essential energy for reproduction in camelids ⁶⁹ . According to Norambuena et al. ²³ , energy restriction levels in feed have different consequences such as: low energy restriction (30 %) of maintenance energy requirements for 28 days in llamas did not affect LW, BCS and metabolic parameters that may indicate NEB. However, moderate energy restriction at 40 % for 21 days in alpacas affected BCS, LW and corpus luteum diameter.

Primary ketosis or pregnancy toxemia occurs in ruminants due to NEB, this is causing lipid mobilization, fatty liver and ketosis. However, camelids are slightly different in their digestive and metabolic systems: glycemia is higher and ketones are lower in relationship to true ruminants. It is an infrequent trait in camelids compared to small ruminants. In contrast, severely debilitated females, abortion or parturition induction should be considered to alleviate the syndrome. Insufficient energy intake during or at the end of pregnancy is often responsible for increased body fat mobilization, fatty liver, and ketonemia. It is indirect evidence of a lipid disorder, and affected camelids occasionally can die 70 .

Conclusion

Based on the available technical-scientific information, it can be concluded that: If during the transition period prepartum, postpartum and lactation, maintenance requirements are not fulfilled, this can lead to NEB and enormous metabolic challenges, it lead to fat mobilization, such incidences produce changes of indicator levels of energy metabolism in llamas like: total protein, urea or BUN, glucose, TG, cholesterol, NEFA and BHB.

SAC suffer from BEN during the dry season, it can increase plasma concentrations of NEFA, BHB and NUS have been reported in previous studies in llamas, alpacas and vicuñas. Elevated BUN values were reported in llamas and alpacas. This may cause abortions and contribute to low fertility rates in the herds. Furthermore, BHB concentrations in llamas seem to reflect hepatic ketogenesis and, therefore, metabolic alteration of the animal.

Plasma glucose levels were similar between llama and alpaca species. Studies have proposed that IR is a homeostatic adaptation to prioritize the mammary gland and promote gluconeogenesis and lipolysis.

Plasmatic TG concentrations are commonly comparable in order of magnitude in llamas, sheep, and goats and are not affected by diet. Hypocholesterolemia is appreciated in diets with low energy or fiber intake in ruminants.

This review agrees to indicate that more researches are needed to evaluate NEB (NEFA, BHB) in pregnant llamas in different seasons of the year and transition periods (prepartum and postpartum) to improve reproductive performance and maximize productivity in South American camelid production systems.

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Notes

Source of financing: The study was funded with own resources of the authors.

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Conflicts of interest: The manuscript was elaborated and reviewed by the authors, who declare that there is no conflict of interest that could risk the validity of the results presented.

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Acknowledgments: The authors thank to Área Ciencias Agrícolas, Pecuarias y RRNN de la UPEA, La Paz, Estado Plurinacional de Bolivia for the support provided during the development of the research work.

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Ethical considerations: The research fulfilled with the ethical standards of the information process.

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Authors' contribution to the article: The authors realize information gathering and bibliographic compilation, as well as the review and writing of the final review.

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Research limitations: The authors indicate that there were no limitations in this review.

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Article ID: 139/JSAAS/2024

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Editor's Note: Journal of the Selva Andina Animal Science (JSAAS). All statements expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, editors, and reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Author notes

* Contact address: Public University of El Alto. Veterinary Medicine and Zootechnics. Between Sucre Avenue A and Juan Pablo II Avenue s/n Zona Villa Esperanza. Phone: +591-2844177 - 2845787. Cell phone: +591 73095766 El Alto, La Paz, Plurinational State of Bolivia.

Faustina Cayo Rojas E-mail address: cayorf31076@gmail.com

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