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1 Department of Physiology and Pharmacology2 Department of Histology and Embryology, Biological Science Center, Federal University of Pernambuco, Recife, PE, Brazil
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(Received 6 December 2005;
accepted after revision 27 February 2006; first published online 2 March 2006)
Corresponding author A. D. O. Paixão: Departamento de Fisiologia e Farmacologia, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Avenue Prof. Moraes Rego, s/n, Cidade Universitária, 50670-901 Recife, PE, Brazil. Email: adpaixao{at}ufpe.br
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Introduction |
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Other alterations observed in prenatally malnourished rats are reduction in endothelial nitric oxide (NO) production (Franco et al. 2002), increased levels of glucocorticoids (Gardner et al. 1997), increased renin activity (Langley-Evans & Jackson, 1995), increased glomerular angiotensin II binding (Sahajpal & Ashton, 2005) and a high density of sodium transporters in the apical membrane of the thick ascending limb of the loop of Henle (Manning et al. 2002). These mechanisms may result in a positive sodium balance (Manning & Vehaskari, 2001) and some of them, such as the hormonal profile (Langley-Evans et al. 1995) and the high density of sodium transporters, have already been observed in prenatally malnourished juvenile rats (Manning et al. 2002).
High blood pressure is a common precursor of major cardiovascular disease and also of chronic renal failure. In turn, dietary salt is a common factor leading to high blood pressure. A primary deficiency of the kidney to excrete sodium is generally responsible for the effects of dietary salt in causing high blood pressure (de Wardener, 1990a, b) and consequently in cardiovascular disease and chronic renal failure. In genetic hypertension, such as in Dahl salt-sensitive (DS) hypertensive rats and in spontaneously hypertensive rats (SHR), sodium overload leads to a positive sodium balance (Woolfson & de Wardener, 1996). Regarding renal haemodynamics in these hypertensive animals, while SHR develop an increased arteriolar afferent resistance that protects them from hyperfiltration and glomerulosclerosis (Arendshorst & Beierwaltes, 1979), DS rats do not exhibit myogenic autoregulation (Takenaka et al. 1992) and consequently exhibit an increased glomeruloesclerosis index and proteinuria. This indicates that haemodynamic autoregulatory mechanisms may change the course of hypertension sequels in the kidney.
Some of the effects of dietary salt on hypertension are mediated by increased oxidative stress, which increases vascular reactivity and decreases sodium excretion (Lenda et al. 2000; Kitiyakara et al. 2003). Dahl salt-sensitive hypertensive rats submitted to dietary salt overload present an increased oxidative stress (Trolliet et al. 2001; Meng et al. 2002). Even normotensive rats may exhibit a reduced endothelium-dependent dilatation under conditions of high dietary salt (Lenda et al. 2000; Kitiyakara et al. 2003).
In order to investigate whether chronic administration of drinking water containing 1% NaCl changes blood pressure and renal haemodynamics in juvenile Wistar rats subjected to prenatal malnutrition, an evaluation of plasma volume, oxidative stress in the kidney, proteinuria and renal haemodynamics was carried out.
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Methods |
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Female Wistar rats weighing 200–250 g housed at 28°C on a 12 h–12 h light–dark cycle and with free access to tap water and standard pellet chow were randomly assigned to the experimental groups studied. Groups of three females and one male were mated in collective cages and given the control or the experimental diet. Body weight gain was used as a sign of pregnancy. After 10 days of being caged with the male, the female rats that exhibited at least 10 g of body weight gain were housed in individual cages. Female rats that did not exhibit body weight gain during this period were excluded from the study. The control (C, n= 30) group comprised offspring born to dams (n= 11) to whom standard pellet chow was given throughout the mating, pregnancy and lactation periods. The malnourished group comprised offspring of dams (n= 10) which were submitted to a multideficient diet throughout the mating and pregnancy periods (MalN, n= 30). At birth, each litter was culled to eight pups and the male pups were weighed. No dam produced a litter with less than eight pups. No death of dams or pups was observed during the study. At 25 days of age, all male pups were weighed again and weaned onto standard pellet chow ad libitum. Female pups were not included in the experimental protocol because of the known variation of oestrogen plasma levels, according to the day of the oestrous cycle, which directly influences the renal vascular resistance (Evans et al. 1986; Reckelhoff et al. 1998). Furthermore, it has been shown that prenatal malnutrition affects male and female rats differently (Franco et al. 2002). Some rats of the C group, named SC, and part of the MalN group, named SMalN, were weaned onto drinking water containing 1% NaCl. At the age of 70 ± 5 days, some rats of each group, C (n= 9), SC (n= 11), MalN (n= 10) and SMalN (n= 8), were submitted to an evaluation of proteinuria, plasma volume and oxidative stress. The other rats were submitted to an evaluation of renal haemodynamics: C (n= 9), SC (n= 9), MalN (n= 10) and SMalN (n= 8). At the end of each experiment, the anaesthetized animals were killed by exsanguination or by lesion to the diaphragm muscle. All the experimental procedures involving the animals described in this study were approved by the Committee for Ethics in Animal Experimentation of the Federal University of Pernambuco and carried out in accordance with the Committee guidelines.
Diets
Malnutrition was induced through a multideficient diet, as previously described (Teodósio et al. 1990; Paixão et al. 2001, 2003, 2005). The ingredients of the multideficient diet (g g–1, expressed as a percentage) comprised beans (18.34), manioc flour (64.81), jerked meat (3.74) and sweet potato (12.76), which were cooked, dehydrated at 60°C and pulverized. All components were mixed with water. Meat fat (0.35%) was then added, and the mixture was shaped into balls that were dehydrated at 60°C for 24 h. The content of its main nutrients was (g g–1, expressed as a percentage): proteins, 8.68; carbohydrates, 80.58; lipids, 1.12; fibre, 7; minerals, 3.96; and sodium chloride, 0.15; for a total of 372 kCal. No vitamin supplement was added. The same nutrients in the standard diet, as indicated by the manufacturer (Purina, Agribands do Brazil, Paulínia, SP, Brazil), were (g g–1, expressed as a percentage): proteins, 23; carbohydrates, 41; lipids, 2.5; fibre, 9; minerals, 8; and sodium chloride, 0.37; for a total of 278 kCal.
Measurement of proteinuria
Urine was collected during a 24 h period in individual metabolic cages. Urinary protein excretion was measured by precipitation with 3% sulphosalicylic acid (Bradley et al. 1979). Turbidity was then determined by measuring the absorbance at a wavelength of 600 nm by means of a spectrophotometer (Spectrophotometer UV-VIS RS 0223, Labomed, Culver City, CA, USA).
Measurement of renal hemodynamics
The rats were anaesthetized with sodium pentobarbitone (Cristália Produtos Químicos Farmacêuticos, Itapira, SP, Brazil; 60 mg kg–1, I.P.) and placed on a temperature-regulated surgical table to maintain rectal temperature at 36.5–37.5°C. Tracheotomy was performed by means of a polyethylene catheter. A catheter was inserted into the left femoral artery for continuous monitoring of mean arterial pressure (MAP) and blood sampling. Initial mean arterial pressure (MAP0) and haematocrit (Hct0) were measured after femoral catheterization (Maddox et al. 1977). Catheters were inserted into both jugular veins, one for intravenous infusion of 10% inulin (Sigma, St Louis, MO, USA; dissolved in 0.9% saline) into the left jugular vein at 1.2 ml h–1, and the other for infusion of isoncotic rat serum into the right jugular vein at 6 ml kg–1 h–1 for 75 min to compensate surgically induced loss of plasma volume (Ichikawa et al. 1978). For the remainder of the experiment, plasma was infused at 1.5 ml kg–1 h–1. A mid-line abdominal incision was made, and a catheter was inserted into the left ureter for collection of urine samples into oil in graduated glass tubes. The left renal artery was carefully dissected to receive a flow probe (1.0 V, Transonic Systems Inc., Ithaca, NY, USA) in order to assess renal blood flow (RBF).
After the surgical procedure was concluded, anaesthesia was supplemented (sodium pentobarbitone, 45 mg kg–1, ip). After a 1 h equilibration period, two 20 min collections of urine were performed to measure urinary flow rate 
and inulin. At the same time MAP, heart rate (HR) and RBF were recorded. Blood samples (60 µl) were collected into a microhaematocrit tube at the beginning and at the end of each 20 min period for measurement of inulin and Hct. Mean arterial pressure and RBF were measured with a flowmeter (106XM, Transonic System Inc.) by means of a transducer (Transpac, Abbott Laboratory, North Chicago, IL, USA) and a flow probe, respectively, and monitored by means of Windaq acquisition (Transonic System Inc.) software on an IBM computer. Mean arterial pressure, RBF and HR recordings were analysed by means of a playback program of the Calc Package in Windaq. Glomerular filtration rate (GFR) was evaluated through inulin clearance. Inulin concentrations in urine and plasma were measured by the anthrone method (Fuhr et al. 1955). Renal plasma flow (RPF), filtration fraction (FF) and renal vascular resistance (RVR) were calculated according to the following equations: RPF = RBF x (1 – Hct); FF = GFR/RPF; and RVR = MAP/RBF. Each renal haemodynamic parameter was corrected in agreement with the corresponding kidney weight (in g).
Measurement of plasma volume
Plasma volume was measured by means of the Evans Blue (Sigma) dye method as previously described (Farjanel et al. 1997; Roy-Clavel et al. 1999). Briefly, 100 µg of dye in 100 µl saline was injected via the femoral venous catheter. The catheter had previously been filled with saline, and after the dye administration it was flushed with 200 µl saline. After 7.5 min, saline was removed from the arterial catheter and a blood sample was collected into a heparinized syringe. The blood was centrifuged in order to obtain the plasma sample. The dye content of the sample was determined spectrophotometrically at 610 nm (Spectrophotometer UV-VIS RS 0223) and compared to a standard curve designed from known amounts of Evans Blue dye and samples of plasma from donor rats. Plasma volume per 100 g body weight was calculated for statistical analysis.
Measurement of oxidative stress
Oxidative stress was evaluated through TBARS levels according to the method of Buege & Aust (1978). Each kidney was macerated in KCl (1.15%) at a proportion of 10 ml:1 g for 15 min in an ice bath and then transferred to test tubes. Immediately, 2 ml of the reagents, 0.375% thiobarbituric acid (Sigma) and 15% trichloroacetic acid (Vetec Química Fina Ltda., Rio de Janeiro, RJ, Brazil), were added to each millilitre of the kidney homogenate. Duplicate tubes for each reaction were sealed and heated in a water bath at a temperature of 100°C for 15 min. After cooling, the protein precipitate was centrifuged for 10 min; then the supernatant was separated and the absorbance was measured at 535 nm.
Statistical analysis
The results are expressed as means ±S.E.M. The differences between groups were analysed by one-way ANOVA, followed by Student–Newman–Keuls multiple comparison tests. The differences between C and MalN dams were assessed using Student's unpaired t test. The differences were considered significant at P < 0.05.
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Results |
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The dams submitted to multideficient diet presented a lower diet intake (27%, P < 0.01) as well as a lower gain in weight (43%, P < 0.01) when compared to the dams on control diet. However, the reproductive outcome was similar in both groups (Table 1).
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Data on body and kidney weights are presented in Table 2. The birth weight of the MalN group was 39% lower (P < 0.01) than that of the C group. At weaning and at 70 days of age, the body weight of the MalN group was still lower than that of the C group (by 19 and 10%, respectively, P < 0.01). At 70 days of age, the SC group did not show any difference in body weight compared to the C group, while in the SMalN group the body weight was 14% (P < 0.05) higher than that in the MalN group. The value of body weight in the SMalN group was not different from the value observed in the SC group. Kidney weight in the MalN group was 19% (P < 0.05) lower than that in the C group. The values of kidney weight in the SC group were not different from those in the C group. Kidney weight in the SMalN group was, however, 50% (P < 0.05) higher than that in the MalN group, but the same as that in the SC group. The ratio of kidney weight:body weight was the same for MalN and C groups. It was also the same for SC and C groups. However, it was 27% (P < 0.01) higher in the SMalN group than in the MalN group and 30% higher (P < 0.01) in the SMalN group compared with the SC group.
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Plasma volume was 26% (P < 0.05) higher in the MalN group than in the C group. This parameter was the same for the SC and C groups and also for the SMalN and MalN groups (Fig. 1).
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Values of MAP0, not shown in the tables, were higher in the MalN group than in the C group (138 ± 2 versus 105 ± 2 mmHg, P < 0.01, respectively). This parameter was not statistically different for the SC and C groups (122 ± 9 versus 105 ± 2 mmHg, respectively), or for the SMalN and MalN groups (139 ± 2 versus 138 ± 2 mmHg, respectively). However, MAP0 was higher in the SMalN than in the SC group (139 ± 2 versus 122 ± 9 mmHg, respectively, P < 0.05). Values of MAP are shown in Table 3 and, like MAP0, it was higher in the MalN than in the C group (P < 0.05). Mean arterial pressure was the same for the SC and C groups, as well as for the SMalN and MalN groups. However, it was higher in the SMalN than in the SC group (P < 0.05). Heart rate values were similar for all groups studied (Table 3).
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All parameters of renal haemodynamics and proteinuria were the same for the MalN and C groups (Table 3). The renal haemodynamic parameters were also the same for SC and C rats. In contrast, proteinuria was 244% (P < 0.01) higher in the SC compared to the C group. Glomerular filtration rate and FF were higher (87 and 72%, respectively, P < 0.01) in the SMalN group compared to the MalN group. Proteinuria was also higher in the SMalN than in the MalN group (106%, P < 0.01), but was the same for SMalN and SC groups.
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Discussion |
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In this study, prenatal malnutrition was based on the offspring having low birth weights and on the fact that the mothers submitted to the multideficient diet presented a low dietary intake. Thus, besides the deficiency in proteins, lipids, minerals and vitamins, malnutrition was also caloric, although the diet was hypercaloric. It was remarkable that the MalN group did not catch up to the body weight of the C group in juvenile life. However, some malnourished litters of dams on this multideficient diet reached the body weight of the control group in adult life (Paixão et al. 2001, 2005). One explanation for this discrepancy is the variation in the content of sodium chloride in the multideficient diet prepared at different times before use (Paixão et al. 2003). A low sodium intake during perinatal life jeopardizes growth in young rats (Ray et al. 1992; Roy-Clavel et al. 1999; da Silva et al. 2003). The content of sodium chloride in the multideficient diet varied between 0.15 and 0.25%. A low intake of sodium may affect the activity of the renin–angiotensin system in mothers and, consequently, the growth of the offspring (Ray et al. 1992; da Silva et al. 2003), though we cannot confirm that this occurred in the present study. However, at 70 days of age, the SMalN group had higher body and kidney weights than their respective control group. This profile may suggest a positive sodium balance, but no change was observed in plasma volume in either the SMalN group or the SC group compared with their respective control groups. The hypothesis that metabolic disturbances might trigger overweight in rats subjected to prenatal malnutrition should not be discarded (Breier et al. 2001), considering that sodium overload may induce adipocyte hypertrophy and increased plasma leptin in rats prone to obesity (Dobrian et al. 2003) and that prenatally malnourished rats have a high plasma level of leptin (Vickers et al. 2000).
An elevated plasma volume in the MalN group in comparison with the C group suggests that the former animals may develop primary positive sodium balance. This finding corroborates with previous evidence which shows that plasma renin (Manning & Vehaskari, 2001) and glomerular angiotensin II binding (Sahajpal & Ashton, 2005), as well as two sodium transporters, the thick ascending limb Na+–K+–2Cl– and the distal convoluted tubule NaCl cotransporter (Manning et al. 2002), are elevated in rats subjected to protein prenatal malnutrition. The SMalN group did not exhibit an increased plasma volume. Some mechanisms may explain this paradox. It is well known that sodium overload leads to suppression of plasma renin and aldosterone production. However, there is a report showing increased angiotensin production in the kidney during sodium overload (Hollenberg et al. 2003). A high filtration fraction, like that observed in the SMalN group, suggests an increase in angiotensin activity on the afferent arteriole (Alberola et al. 1994; Navar et al. 1996), which is probably responsible for the increased GFR observed in this group. This mechanism probably led to augmented natriuresis to maintain plasma volume and blood pressure. It may be suggested that absence of renal haemodynamic adjustments in the MalN group was responsible for the increased plasma volume. In a previous study, the MalN rats, at 90 days of age, showed increased FF and GFR (Paixão et al. 2001). Like SMalN, the SC group showed neither increased blood pressure nor plasma volume, but on the contrary, the latter group did not show renal haemodynamic alterations. This may suggest that increased interstitial hydrostatic pressure was responsible for natriuresis in the SC group, as previously reported (Chou & Marsh, 1986; Roman, 1988). Other considerations to explain the maintenance of plasma volume and blood pressure in SMalN are the NO production in the kidney and the diet used to induce malnutrition. Drinking water containing 1% NaCl may result in increased kidney NO production to facilitate sodium excretion and enable the maintenance of plasma volume as well as blood pressure (Shultz & Tolins, 1993). Nevertheless, the kidney oxidative stress in the SMalN group was higher than that observed in the SC group. Furthermore, the malnutrition induced by the multideficient diet used in the present study to has different characteristics from malnutrition induced by protein deficiency, which is more frequently used in experimental studies. Besides protein deficiency, the diet in the present study also had a low sodium content that may increase plasma renin activity and reduce angiotensin expression in the kidney of adult rats (da Silva et al. 2003).
In the present investigation, as in other studies on prenatal malnutrition (Woodall et al. 1996; Langley-Evans et al. 1999; Woods et al. 2001; Franco et al. 2002), the MalN rats had a higher blood pressure compared to the control rats. Prenatally malnourished rats present oligonephronia (Merlet-Benichou et al. 1994; Langley-Evans et al. 1999) that contributes to hypertension (Mackenzie et al. 1996; Langley-Evans et al. 1999; Woods, et al. 2001). In contrast, salt overload exacerbates hypertension (Trolliet et al. 2001; Meng et al. 2002), in part because it increases oxidative stress (Lenda et al. 2000; Kitiyakara et al. 2003). Probably owing to the aforementioned reasons, however, the SMalN group had the same blood pressure as that of the MalN group.
An important factor contributing to hypertension and proteinuria seems to be endothelial dysfunction, in particular altered vascular reactivity caused by a reduction in NO production or an increment in its utilization for superoxide anion formation (Hayakawa et al. 1997; Dobrian et al. 2003; Zhang et al. 2004). High salt intake may decrease both plasma levels and urinary excretion of nitrates. One possible explanation for this is a reduced availability rather than a decreased production of NO (Fujiwara et al. 2000). The ability of NO to interact quickly with superoxide anion in order to form the potent oxidant peroxynitrite is well documented (Squadrito & Pryor, 1995). In the present study, oxidative stress was elevated in the MalN group. There is evidence of a decreased NO production in aortic rings of prenatally malnourished rats expressed as endothelial dysfunction caused by a reduced superoxide dismutase activity and elevated superoxide radicals (Franco et al. 2002). In agreement with previous findings (Lenda et al. 2000; Kitiyakara et al. 2003), salt overload increased oxidative stress in both MalN and C groups. However, oxidative stress was higher in the SMalN group than in the SC group. Oxidative stress has been implicated in angiotensin II-mediated hypertension. Since the high FF in the SMalN group suggests high angiotensin II activity in the glomerulus and, in addition to the evidence that angiotensin II activity may be increased in the kidney of prenatally malnourished rats (Sahajpal & Ashton, 2005), it may be suggested that differences between SC and SMalN in regard to the levels of TBARS in the kidney may involve angiotensin II. In contrast, leptin, which is increased in prenatally malnourished rats (Vickers et al. 2000), also has a role in increasing oxidative stress (Beltowski et al. 2004, 2005). Although oxidative stress was increased in the MalN group, proteinuria was unaltered. Despite the fact that proteinuria was increased by salt overload, it was the same in both SMalN and SC groups. Unlike the present results, rats exhibiting low birth weight and oligonephronia caused by jeopardized placental blood flow, and additionally submitted to drinking water containing 2% NaCl for 4 weeks, show microalbuminuria accompanied by impairment of renal haemodynamics at 16 weeks of age (Sanders et al. 2005).
Unlike a previous observation in the same experimental model (Paixão et al. 2001), in this study, renal haemodynamics were unchanged. This can be explained if one considers that the animals used in the present study were younger than those previously evaluated. Considering that plasma volume was increased in the MalN group and that the profile of renal haemodynamics was different between the SC and SmalN groups, it may be suggested that impaired tubular sodium reabsorption precedes impaired renal haemodynamics. Juvenile rats submitted to prenatal dexamethasone, which presented low birth weight, did not exhibit renal haemodynamic alterations even when they were treated with dietary protein overload (Martins et al. 2003). The high filtration fraction in the SMalN group suggests an increased hydrostatic pressure in the glomerular capillaries (PGC). High PGC may in turn lead to renal hypertrophy and glomerulosclerosis. In agreement, the SMalN group showed kidney hypertrophy that was not observed in the SC group. However, there is evidence of salt-induced organ hypertrophy, independent from haemodynamic effects (Ahn et al. 2004). Dahl salt-sensitive rats show salt-induced renal fibrosis mediated by increased oxidative stress (Zhang et al. 2004). Furthermore, sodium chloride overload may stimulate TGF-ß to produce kidney and myocardial hypertrophy in normotensive and hypertensive rats (Yu et al. 1998). In prenatally malnourished rats, the production of growth factors is increased, as previously shown (Vickers et al. 2000; Paixão et al. 2005).
Making an analogy with genetic hypertensive models, DS rats and SHR, the renal haemodynamic profile of prenatally malnourished rats submitted to sodium overload seems closest to that of DS rats, in which precocious changes in the renal haemodynamics may lead to precocious morphological changes in the kidney (Takenaka et al. 1992), while SHR show renal autoregulatory mechanisms that protect them from precocious glomerulosclerosis (Arendshorst & Beierwaltes, 1979).
In summary, sodium overload did not exacerbate the hypertension in juvenile prenatally malnourished rats, but induced renal haemodynamic alterations that are compatible with the development of renal disease.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Alberola AM, Salazar FJ, Nakamura T & Granger JP (1994). Interaction between angiotensin II and nitric oxide in control of renal hemodynamics in conscious dogs. Am J Physiol 267, R1472–R1478.
Almeida JR & Mandarim-de-Lacerda CA (2005). Maternal gestational protein-calorie restriction decreases the number of glomeruli and causes glomerular hypertrophy in adult hypertensive rats. Am J Obstet Gynecol 192, 945–951.[CrossRef][Medline]
Arendshorst WJ & Beierwaltes WH (1979). Renal and nephron hemodynamics in spontaneously hypertensive rats. Am J Physiol 236, F246–F251.
Beltowski J, Wojcicka G, Jamroz-Wisniewska A, Borkowska E & Marciniak A (2005). Antioxidant treatment normalizes nitric oxide production, renal sodium handling and blood pressure in experimental hyperleptinemia. Life Sci 77, 1855–1868.[Medline]
Beltowski J, Wojcicka G, Marciniak A & Jamroz A (2004). Oxidative stress, nitric oxide production, and renal sodium handling in leptin-induced hypertension. Life Sci 74, 2987–3000.[CrossRef][Medline]
Bradley M, Schumann GB & Ward PCJ (1979). Examination of urine. In Clinical Diagnosis and Management by Laboratory Methods, 16th edn, ed. Henry JB, pp. 559–634. W. B. Saunders, Philadelphia.
Breier BH, Vickers MH, Ikenasio BA, Chan KY & Wong WP (2001). Fetal programming of appetite and obesity. Mol Cell Endocrinol 185, 73–79.[CrossRef][Medline]
Buege JA & Aust SD (1978). Microsomal lipid peroxidation. Meth Enzymol 52, 302–310.[Medline]
Chou CL & Marsh DJ (1986). Role of proximal convoluted tubule in pressure diuresis in the rat. Am J Physiol 251, F283–F289.
da Silva AA, de Noronha IL, de Oliveira IB, Malheiros DM & Heimann JC (2003). Renin angiotensin system function and blood pressure in adult rats after perinatal salt overload. Nutr Metab Cardiovasc Dis 13, 133–139.[CrossRef][Medline]
de Wardener HE (1990a). The primary role of the kidney and salt intake in the aetiology of essential hypertension: Part I. Clin Sci 79, 193–200.[Medline]
de Wardener HE (1990b). The primary role of the kidney and salt intake in the aetiology of essential hypertension: Part II. Clin Sci 79, 289–297.[Medline]
Dobrian
AD, Schriver
SD, Lynch
T
&
Prewitt
RL (2003). Effect of salt on hypertension and oxidative stress in a rat model of diet-induced obesity. Am J Physiol Renal Physiol
285, F619–F628.
Evans JK, Naish PF & Aber GM (1986). Oestrogen-induced changes in renal haemodynamics in the rat: influence of plasma and intrarenal renin. Clin Sci 71, 613–619.[Medline]
Farjanel J, Denis C, Chatard JC, Geyssant A (1997). An accurate method of plasma volume measurement by direct analysis of Evans blue spectra in plasma without dye extraction: origins of albumin-space variations during maximal exercise. Eur J Appl Physiol Occup Physiol 75, 75–82.[Medline]
Franco
MCP, Arruda
RMMP, Dantas
APV, Kawamoto
EM, Fortes
ZB, Scavone
C, Carvalho
MHC, Tostes
RCA
&
Nigro
D (2002). Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc Res
56, 145–153.
Fuhr J, Kaczmarczyk J & Kruttgen CD (1955). Eine einfache colorimetrische Method zur Inulinbestimmung fur Nierenclearanceunter-suchungen bei Stoffwechselgesunden und Diabetikern. Klin Wochenschr 33, 729–730.[CrossRef][Medline]
Fujiwara
N, Osanai
T, Kamada
T, Katoh
T, Takahashi
K
&
Okumura
K (2000). Study on the relationship between plasma nitrite and nitrate level and salt sensitivity in human hypertension: modulation of nitric oxide synthesis by salt intake. Circulation
101, 856–861.
Gardner
DS, Jackson
AA
&
Langley-Evans
SC (1997). Maintenance of maternal diet-induced hypertension in the rat is dependent on glucocorticoids. Hypertension
30, 1525–1530.
Hayakawa
H, Coffee
K
&
Raij
L (1997). Endothelial dysfunction and cardiorenal injury in experimental salt-sensitive hypertension: effects of antihypertensive therapy. Circulation
96, 2407–2413.
Hollenberg NK, Price DA, Fisher NDL, Lansang MC, Perkins B, Gordon MS, Williams GH & Laffel LMB (2003). Glomerular hemodynamics and the renin-angiotensin system in patients with type 1 diabetes mellitus. Kidney Int 63, 172–178.[Medline]
Hoy WE, Rees M, Kile E, Mathews JD & Wang Z (1999). A new dimension to the Barker hypothesis: low birthweight and susceptibility to renal disease. Kidney Int 56, 1072–1077.[CrossRef][Medline]
Ichikawa I, Maddox DA, Cogan MC & Brenner BM (1978). Dynamics of glomerular ultrafiltration in euvolemic Munich-Wistar rats. Renal Physiol 1, 121–131.
Kitiyakara
C, Chabrashvili
T, Chen
Y, Blau
J, Karber
A, Aslam
S, Welch
WJ
&
Wilcox
CS (2003). Salt intake, oxidative stress, and renal expression of NADPH oxidase and superoxide dismutase. J Am Soc Nephrol
14, 2775–2782.
Langley-Evans SC & Jackson AA (1995). Captopril normalises systolic blood pressure in rats with hypertension induced by fetal exposure to maternal low protein diets. Comp Biochem Physiol A Physiol 110, 223–228.[Medline]
Langley-Evans SC, Welham SJ & Jackson AA (1999). Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64, 965–974.[CrossRef][Medline]
Lenda
DM, Sauls
BA
&
Boegehold
MA (2000). Reactive oxygen species may contribute to reduced endothelium-dependent dilation in rats fed high salt. Am J Physiol Heart Circ Physiol
279, H7–H14.
Mackenzie HS, Lawler EV & Brenner BM (1996). Congenital oligonephropathy: The fetal flaw in essential hypertension? Kidney Int Suppl 55, S30–S34.[Medline]
Maddox DA, Price DC & Rector FC Jr (1977). Effects of surgery on plasma volume and salt and water excretion in rats. Am J Physiol 233, F600–F606.
Manning
J, Beutler
K, Knepper
MA
&
Vehaskari
VM (2002). Upregulation of renal BSC1 and TSC in prenatally programmed hypertension. Am J Physiol Renal Physiol
283, F202–F206.
Manning J & Vehaskari VM (2001). Low birth weight associated adult hypertension in the rat. Pediatr Nephrol 16, 417–422.[CrossRef][Medline]
Martins JP, Monteiro JC & Paixao ADO (2003). Renal function in adult rats subjected to prenatal dexamethasone. Clin Exp Pharmacol Physiol 30, 32–37.[CrossRef][Medline]
Meng
S, Roberts
LJ
II, Cason
GW, Curry
TS
&
Manning
RD
Jr (2002). Superoxide dismutase and oxidative stress in Dahl salt-sensitive and -resistant rats. Am J Physiol Regul Integr Comp Physiol
283, R732–R738.
Merlet-Benichou C, Gilbert T, Muffatjoly M, Lelievre Pegorier M & Leroy B (1994). Intrauterine growth-retardation leads to a permanent nephron deficit in the rat. Pediatr Nephrol 8, 175–180.[CrossRef][Medline]
Navar
LG, Inscho
EW, Majid
SA, Imig
JD, Harrison-Bernard
LM
&
Mitchell
KD (1996). Paracrine regulation of the renal microcirculation. Physiol Rev
76, 425–536.
Paixão ADO, Alessio ML, Martins JP, Leger CL, Monnier L & Pares-Herbute N (2005). Regional Brazilian diet-induced pre-natal malnutrition in rats is correlated with the proliferation of cultured vascular smooth muscle cells. Nutr Metab Cardiovasc Dis 15, 302–309.[Medline]
Paixão ADO, Maciel CR, Teles MBB & Figueiredo-Silva J (2001). Regional Brazilian diet-induced low birth weight is correlated with changes in renal hemodynamics and glomerular morphometry in adult age. Biol Neonate 80, 239–246.[CrossRef][Medline]
Paixão ADO, Nunes FA, Monteiro JC & Maciel CR (2003). Low sodium chloride content in a multideficient diet induces renal vasodilatation in rats. Nutr Res 23, 85–89.[CrossRef]
Ray PE, Schambelan M, Hintz R, Ruley EJ, Harreh J & Holliday MA (1992). Plasma renin activity as a marker for growth failure due to sodium deficiency in young rats. Pediatr Nephrol 6, 523–526.[Medline]
Reckelhoff JF, Hennington BS, Moore AG, Blanchard EJ & Cameron J (1998). Gender differences in the renal nitric oxide (NO) system: dissociation between expression of endothelial NO synthase and renal hemodynamic response to NO synthase inhibition. Am J Hypertens 11, 97–104.[CrossRef][Medline]
Roman
RJ (1988). Pressure-diuresis in volume-expanded rats. Tubular reabsorption in superficial and deep nephrons. Hypertension
12, 177–183.
Roy-Clavel E, Picard S, St-Louis J & Brochu M (1999). Induction of intrauterine growth restriction with a low sodium diet fed to pregnant rats. Am J Obstet Gynecol 180, 608–613.[CrossRef][Medline]
Sahajpal
V
&
Ashton
N (2005). Increased glomerular angiotensin II binding in rats exposed to a maternal low protein diet in utero. J Physiol
563, 193–201.
Sanders
MW, Fazzi
GE, Janssen
GM, Blanco
CE
&
De Mey
JG (2005). High sodium intake increases blood pressure and alters renal function in intrauterine growth-retarded rats. Hypertension
46, 71–75.
Shultz PJ & Tolins JP (1993). Adaptation to increased dietary salt intake in the rat. Role of endogenous nitric oxide. J Clin Invest 91, 642–650.[Medline]
Squadrito GL & Pryor WA (1995). The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem Biol Interact 96, 203–206.[CrossRef][Medline]
Takenaka
T, Forster
H, De Micheli
A
&
Epstein
M (1992). Impaired myogenic responsiveness of renal microvessels in Dahl salt-sensitive rats. Circ Res
71, 471–480.
Teodósio NR, Lago ES, Romano SAM & Guedes RCA (1990). A regional basic diet from Northeast Brazil as a dietary model of experimental malnutrition. Arch Latinoamer Nutr XL 4, 533–547.
Trolliet MR, Rudd MA & Loscalzo J (2001). Oxidative stress and renal dysfunction in saltsensitive hypertension. Kidney Blood Press Res 24, 116–123.[CrossRef][Medline]
Vickers
MH, Breier
BH, Cutfield
WS, Hofman
PL
&
Gluckman
PD (2000). Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab
279, E83–E87.
Woodall SM, Johnston BM, Breier BH & Gluckman PD (1996). Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res 40, 438–443.[Medline]
Woods LL, Ingelfinger JR, Nyengaard JR & Rasch R (2001). Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 49, 460–467.[Medline]
Woods LL, Weeks DA & Rasch R (2004). Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65, 1339–1348.[CrossRef][Medline]
Woolfson RG & de Wardener HE (1996). Primary renal abnormalities in hereditary hypertension. Kidney Int 50, 717–731.[Medline]
Yu
HCM, Burrell
LM, Black
MJ, Wu
LL, Dilley
RJ, Cooper
ME
&
Johnston
CI (1998). Salt induces myocardial and renal fibrosis in normotensive and hypertensive rats. Circulation
98, 2621–2628.
Zhang JJ, Bledsoe G, Kato K, Chao L & Chao J (2004). Tissue kallikrein attenuates salt-induced renal fibrosis by inhibition of oxidative stress. Kidney Int 66, 722–732.[CrossRef][Medline]
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P < 0.05 versus MalN and 
P < 0.05 versus SC (one-way ANOVA followed by Student–Newman–Keuls test).