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 important¹. Thus, improving breeding systems represents the best strategy to avoid poverty². This is due to the ability of alpacas and llamas to produce fiber and meat under extreme geographic and climatic conditions³.

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 gestation⁸.

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 tissues¹¹.

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 follicles¹⁴. 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 transition¹⁵.

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 quality². 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 intake¹⁷. Dietary insufficiency causes mobilization of adipose reserves, characterized by an increase in NEFA and BHB in camelids blood¹³. 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 important¹⁶.

Pre-birth transition period. The fetal development of domestic camelids shows exponential growth around the seventh month of gestation¹⁹. 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 deficiency²⁰, 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 period²¹, 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 lactation²¹.

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 phase²².

Postpartum transition period. Apparently, in SAC the dietary restriction could be associated with the physiological and productive state of the animal²³. It has been described in llamas subjected to chronic nutritional restriction, which had small dominant follicles, corpus luteum, and less progesterone secretion²⁴. In addition, dietary changes in cows cause an immediate and rapid stimulation in metabolism²⁵. DM intake is the main component of energy balance, which affects fertility in cows¹⁸.

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 h²⁶. 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 priority¹⁴, in relationship with another physiological states of maintenance, lactation and growth when available nutritional resources are limited²⁸. Therefore, ensuring good nutritional status during this period is an important objective to optimize postpartum in females²⁹.

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 time³⁰. In primiparous cows that have a lower BCS during the early postpartum period, cows produce less milk than multiparous cows³¹, 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 weights³². Likewise, weaning weight is higher for calves born to cows that grazed on irrigated pasture in relationship to cows fed with hay after animalbirth²². 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 plasma³⁵, as well as alter the blood levels of other indicators: glucose, cholesterol, urea, albumin, aspartate-aminotransferase and glutamate-dehydrogenase¹⁵.

Metabolites in blood.

Total protein or proteinemia. Wittwer³⁶ 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 winter³⁷.

Llamas develop hypoproteinemia³⁸ (total proteins: 55.9 g L^-1, reference limits: 58-69.3 g L^-1) and hypoalbuminemia³⁹ (albumin: 28.1 g L^-1, reference limits: 33.9-40.5 g L^-1). According to Tallacagua-Terrazas & Mamani-Tola⁴⁰ 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 & Condori⁴¹, 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 interest³⁶. 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 efficient¹⁹.

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 energy³⁶.

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 malnutrition⁴².

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 ruminant⁴³. Tallacagua-Terrazas & Mamani-Tola⁴⁰ informed urea values of 90 mg dL^-1 in llamas, these parameters are high for the species⁴⁴.

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 feed⁴⁷. 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 them⁴⁵. Tallacagua-Terrazas & Mamani-Tola⁴⁰ 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 stage⁴⁹, 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 feeds⁵⁰.

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 levels⁵¹.

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 function³⁶. 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 alpacas⁴². In young growing animals, the plasma concentration is encountered highest values⁴⁰.

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 hypocalcemia⁵⁴ Biochemical parameters did not report changes in serum creatinine⁴⁴ with an overall mean serum creatinine level of 92 μmol L^-1 in llamas grazed on native pastures²⁴. While creatinine concentration in all categories of llamas was higher than in alpacas³⁹.

Carbohydrates. Wittwer³⁶ 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 hyperglycemia⁵⁵. 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 alpacas⁴².

Fowler & Bravo⁵⁶ 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 carbohydrates⁵⁷. 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 insulin⁵⁹. In dairy cows, periparturient ketosis can be categorized by hyperglycemia and hyperinsulinemia, probably due to IR⁶⁰, and it is classified as type II ketosis due to its similarities with type I diabetes mellitus⁶¹. 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 lipolysis¹¹.

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, respectively⁶¹. 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 ketosis³⁶.

Lipids and ketone bodies. According to Wittwer³⁶ 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 metabolism³⁶.

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 alpacas⁴². 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 supplied⁴³. 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 fertility⁶³.

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 ruminants³⁶.

Prepartum cows had inferior cholesterol concentrations (±27 %) than lactating cows, in relationship with low DM intake in primiparous cows³⁶. backwards³¹, 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 nutrition⁶².

Plasma cholesterol concentration in camelids is 0.34-2.3 mmol L^-1 in llamas and 0.24-2.15 mmol L^-1 in alpacas³⁹. 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 period³⁶.

Plasmatic NEFA concentration in mammals oscillates between 0.1 and 0.5 mmol L^-1, It is being higher after prolonged fasting³⁶. They are raised in cases of hepatic lipolysis⁴². 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 success³¹.

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 llamas⁴³.

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 NEB⁴⁰. Camelids have lower concentrations of plasmatic ketone bodies than domestic ruminants³⁹. 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 fermentation⁴³.

In alpacas, NEFA values of (0.24 mmol L^-1) are exposed⁴². 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 diet⁶⁸, 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 camelids⁶⁹. 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 die⁷⁰.

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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