TY - JOUR
AU - Stander, M. A.
AB - ABSTRACT Eight Döhne Merino rams were used to quantify apparent absorption, distribution to tissues, and excretion of dietary melamine in sheep. Two batches of concentrate pellets were made; one (CON) contained corn gluten meal with no detectable melamine and the other (MEL) contained corn gluten meal that was previously found to be highly contaminated with melamine at 15,117 mg/kg. The MEL pellets contained 1,149 mg/kg of melamine. During a 10-d adaptation period, all the animals received a forage-based diet supplemented with 600 g/d of the CON pellets. This was followed by an 8-d collection period during which 6 of the animals received MEL pellets and 2 received CON pellets. Melamine intake of sheep that received MEL pellets was 0.69 g/d. Blood samples were taken before first ingestion of MEL pellets on d 1 and again on d 3, 6, and 8 of the collection period for melamine and serum creatinine analyses. Feces and urine were collected quantitatively over the 8 d for proximate and melamine analyses. All the animals were slaughtered at the end of the trial, and samples of the LM, liver, kidneys, and abdominal fat were taken for melamine analysis. Data of the 2 sheep that received CON pellets for the duration of the trial confirmed that no melamine was detected in any of the samples, and no statistical analyses were performed on these data. The apparent digestibility or efficiency of absorption of ingested melamine was 76.7%. Melamine was detected in the urine, blood, muscle (LM), and fat tissue of all the sheep that received MEL pellets. Serum melamine concentrations reached 5.4 mg/kg on d 8 of the collection period, and the meat (LM) contained 9.6 mg/kg of melamine. Calculations on the partitioning of ingested melamine suggested that urine is the major excretion route accounting for 53.2%, whereas feces accounted for 23.3% of ingested melamine. Approximately 3.5% of the ingested melamine was detected in muscle. It was concluded that ingested melamine is highly absorbable from the small intestine and that a pathway exists for the distribution of dietary melamine to meat. INTRODUCTION The industrial chemical melamine (C3H6N6), or 1,3,5-triazine-2,4,6-triamine, contains 670 g/kg of N on a molecular-weight basis (Merck, 2001). Melamine can artificially increase the apparent protein content of feedstuffs because CP is calculated from the N content (AOAC, 2000). In 2008, 6 Chinese babies died and 296,000 fell ill after drinking melamine-tainted infant formula (Allaboutfeed, 2009). Melamine, added to adulterated gluten meal that was manufactured in China and exported worldwide, was also the cause of numerous pet deaths around the world in 2007 (World Health Organization, 2008b). Literature on melamine in animal diets is limited. MacKenzie (1966) reported BW loss and mortalities when melamine was fed to sheep, and according to Clark (1966), an intake of >10 g/d per sheep resulted in urinary calculi crystalluria and consequent death. In the latter study, it was found that 7 g/d fed to sheep with an average BW of 35 kg showed no ill effects. Newton and Utley (1978) reported that melamine was not an efficient N source for ruminants, although an intake of 45 g/d by steers could be regarded as safe. Cruywagen et al. (2009) confirmed for the first time that a pathway exists for the absorption of melamine from feed and its eventual appearance in milk and that approximately 2% of ingested melamine was excreted in milk. Andersen et al. (2008) and Reimschuessel et al. (2008) have shown that melamine, when added to feed in a pure form, occurs in the meat of fish and pigs, but no literature could be found on the quantification of melamine partitioning into various routes of excretion or deposition. A study was done at the Stellenbosch University to test the hypothesis that dietary melamine would be absorbed by sheep and distributed to the meat and organs. A further aim was to determine the apparent digestibility of melamine in sheep and to quantify the distribution to meat and organs and its excretion via urine and feces. MATERIALS AND METHODS The trial protocol was approved by the Animal Ethics Committee of Stellenbosch University. Animals and Treatments Eight Döhne Merino rams, 12 mo of age and weighing 59.5 ± 6.5 kg, were used in the trial. They were housed individually in 1.5 × 0.9 m pens with slatted wooden floors in a well-ventilated barn. Each sheep had free access to a feed trough and fresh water via a ball-valve-controlled drinking bowl. Housing and care was performed according to current ethical norms (SANS, 2008), and the animals did not experience any discomfort at any stage of the trial. Two batches of concentrate pellets were made (Table 1); one contained local corn gluten meal with no detectable melamine (control treatment; CON), whereas the other contained corn gluten meal of Chinese origin that was previously found to be adulterated and contained melamine at 15,117 mg/kg (melamine treatment; MEL). The adulterated corn gluten meal had a CP content of 674 g/kg (DM base), and previous microscopic analysis revealed that it consisted of wheat starch, wheat bran, corn bran, corn gluten feed, corn gluten meal, urea, melamine, and colorants (Cruywagen and Reyers, 2009). Concentrate pellets for ruminants in South Africa would usually not contain more than 70 g/kg of corn gluten meal. In an attempt to ensure that we had the best chance of detecting significant concentrations of melamine in the meat and to calculate accurate deposition and excretion values, it was decided to include the maximum amount of corn gluten meal in the concentrate pellets, 69 g/kg. The same batch of pellets was used in a dairy cow trial (Cruywagen et al., 2009), but 3 random samples were collected from a 50-kg lot that was specific for the current study. Samples were pooled and analyzed for melamine as described below. The average melamine content of the MEL pellets was 1,149 mg/kg. Table 1. Composition of the concentrate pellets fed during the melamine trial Item  Amount, g/kg of DM  Physical composition      Ground corn  516   Soybean meal, 47% CP  213   Cottonseed meal, 40% CP  67   Corn gluten meal, 60% CP1  69   Fish meal  25   Molasses syrup  50   Molasses meal  40   Limestone  10   Salt  5   Monocalcium phosphate  3   Premix2  2  Chemical composition      CP (CON)3  251   CP (MEL)3  261   aNDF4  176   Ether extract  31   Ash (CON)3  58   Ash (MEL)3  68  Item  Amount, g/kg of DM  Physical composition      Ground corn  516   Soybean meal, 47% CP  213   Cottonseed meal, 40% CP  67   Corn gluten meal, 60% CP1  69   Fish meal  25   Molasses syrup  50   Molasses meal  40   Limestone  10   Salt  5   Monocalcium phosphate  3   Premix2  2  Chemical composition      CP (CON)3  251   CP (MEL)3  261   aNDF4  176   Ether extract  31   Ash (CON)3  58   Ash (MEL)3  68  1The melamine treatment (MEL) contained corn gluten meal from China that had 15,117 mg/kg of melamine, whereas the control treatment (CON) contained locally produced corn gluten meal that had no detectable concentrations of melamine. 2Trace mineral premix supplied by Advit Animal Nutrition SA (Pty.) Ltd., Kempton Park, South Africa. 3The CP and ash contents of the diets differed due to the nature of the Chinese gluten meal. 4aNDF = ash-corrected NDF. View Large Table 1. Composition of the concentrate pellets fed during the melamine trial Item  Amount, g/kg of DM  Physical composition      Ground corn  516   Soybean meal, 47% CP  213   Cottonseed meal, 40% CP  67   Corn gluten meal, 60% CP1  69   Fish meal  25   Molasses syrup  50   Molasses meal  40   Limestone  10   Salt  5   Monocalcium phosphate  3   Premix2  2  Chemical composition      CP (CON)3  251   CP (MEL)3  261   aNDF4  176   Ether extract  31   Ash (CON)3  58   Ash (MEL)3  68  Item  Amount, g/kg of DM  Physical composition      Ground corn  516   Soybean meal, 47% CP  213   Cottonseed meal, 40% CP  67   Corn gluten meal, 60% CP1  69   Fish meal  25   Molasses syrup  50   Molasses meal  40   Limestone  10   Salt  5   Monocalcium phosphate  3   Premix2  2  Chemical composition      CP (CON)3  251   CP (MEL)3  261   aNDF4  176   Ether extract  31   Ash (CON)3  58   Ash (MEL)3  68  1The melamine treatment (MEL) contained corn gluten meal from China that had 15,117 mg/kg of melamine, whereas the control treatment (CON) contained locally produced corn gluten meal that had no detectable concentrations of melamine. 2Trace mineral premix supplied by Advit Animal Nutrition SA (Pty.) Ltd., Kempton Park, South Africa. 3The CP and ash contents of the diets differed due to the nature of the Chinese gluten meal. 4aNDF = ash-corrected NDF. View Large During a 10-d adaptation period, all the sheep received a forage-based diet [50:50 alfalfa hay and wheat straw (wt/wt)], offered at 90% of ad libitum intake and supplemented with 600 g/d of the CON pellets. This was followed by an 8 d collection period when 6 of the animals received the MEL pellets and 2 continued to receive the CON pellets. All the sheep consumed all their pellets daily; thus the total daily melamine intake could be calculated to be 0.689 g/sheep. This is substantially less than the 7 g/d previously shown to be nontoxic by Clark (1966). Blood was collected from the jugular vein before first ingestion of melamine on d 1 and again on d 3, 6, and 8 of the collection period for melamine and serum creatinine analyses. Vacuette serum tubes (VGRG455092R 9 mL Red Serum, supplied by Lasec, Cape Town, South Africa) were used for blood collection. After collection, tubes were placed on ice and transported to the laboratory, where they were centrifuged at 1,500 × g for 10 min at 4°C. Serum was subsequently pipetted off and transferred to microcentrifuge tubes for analysis. Feces and urine were collected quantitatively over the 8-d period for proximate and melamine analyses. All the sheep were slaughtered at the end of the trial and samples of the LM (100 g), liver (100 g), kidneys (complete left kidney), and abdominal fat (100 g) were collected for melamine analysis. Tissue samples were freeze-dried, whereas fecal samples were dried at 60°C for 48 h before analysis. Urine samples were stored at −20°C until analyzed. Chemical Analyses For melamine analysis, an adapted method of Shai et al. (2008) was used. The following sample preparation methods were used before solid phase extraction (SPE). Dried feed, fecal, and tissue samples were ground through a 1-mm screen. The ground samples (1 g) were extracted with 50% acetonitrile, 0.1% formic acid (10 mL) under sonication for 2 h in an ultrasonic bath (Branson 2210, Branson Ultrasonics Corporation, Danbury, CT). The extracts (3 mL) were then loaded on the SPE cartridges (Phenomenex Strata SCX; 55 µm, 70 A, 500 mg/3 mL, supplied by Separations, Randburg, South Africa). As the contaminated pellets contained increased concentrations of melamine, extracts from these were diluted 100 fold, and only 0.5 mL of the diluted extract was filtered through the cartridge along with an internal standard (0.1 mL of 0.5 mg/L of 13C315N3 melamine, Cambridge Isotope Laboratories Inc., Andover, MA). For urine analysis, samples (0.5 mL) were loaded onto the SPE cartridges along with 0.1 mL of the internal standard. Serum samples were prepared by the addition of acetonitrile (0.75 mL) and 0.1 mL of the internal standard to the sample, followed by centrifugation at 4,500 × g for 10 min at 20°C. The supernatant was injected directly into the liquid chromatograph triple quadruple mass spectrophotometer (LC-MS/MS) without undergoing SPE. Cation exchange SPE cartridges were conditioned with 6 mL of methanol, followed by 6 mL of water. The effluents of sample extracts (0.5 or 3 mL depending on the matrix) were loaded onto the cartridges together with 100 µL of the internal standard. Thus, 0.05 µg of labeled melamine was loaded onto each cartridge. The internal standard was used to correct for incomplete extraction that might occur. The cartridges were washed with 0.1 N HCl (6 mL) followed by methanol (6 mL), aspirated under vacuum for 1 min, and the melamine was eluted into a clean tube using 6 mL of ammonium hydroxide:methanol:dichloromethane (1:5:5). The extracts were dried under a stream of N2 and resuspended in 1 mL of acetonitrile (50%). Samples were analyzed by LC-MS/MS on a Waters API Quattro Micro triple quadruple mass spectrometer coupled to a Waters 2690 HPLC (Waters Corporation, Milford, MA). The limit of detection of the method was 0.005 mg/kg for feed, fecal, and tissue samples and 0.001 mg/kg for urine and serum samples. Statistical Analyses Because no melamine was detected in any of the samples taken from the 2 control sheep, they were not included in the statistical analyses. For the 6 animals that received the MEL pellets, SE values were determined for melamine concentrations within the various tissue samples, as well as for apparent digestibility. Because there was only 1 melamine treatment, the SE values were determined to indicate the degree of variation that occurred. To compare the various organs in terms of melamine concentrations, a 1-way ANOVA was done, followed by a Bonferroni multi-comparison procedure. For serum and urine melamine concentrations, as well as for serum creatinine concentrations, samples were collected over time and data were subjected to repeated measures ANOVA. All data were analyzed using SAS (SAS Inst. Inc., Cary, NC) with the GLM procedure for ANOVA and the MIXED MODELS procedure for repeated measures ANOVA, respectively. Significance was declared at P < 0.05. RESULTS AND DISCUSSION Muscle and kidney had similar melamine concentrations on a DM basis and were approximately 3 times greater than that of liver, whereas the melamine concentration in the abdominal fat was approximately 200-fold less than the average of muscle and kidney concentrations (Table 2). This is contradictory to results by Lü et al. (2009a) who found melamine concentrations in the breast and liver of chickens to be similar, but much less than in the kidney. It should be kept in mind, however, that the distribution kinetics of melamine to tissues may differ between poultry and ruminants. In the Lü et al. (2009a) study, broilers received a diet containing 1,000 mg/kg of melamine for 42 d and after 28 d they reported melamine concentrations (DM basis) of 8.0, 9.7, and 29.5 mg/kg in breast, liver, and kidney, respectively. At 42 d they found that the melamine concentrations had decreased to 3.7, 2.7, and 9.2 mg/kg in the same respective tissues. These authors speculated that the broilers developed an improved capacity to clear melamine from body tissues with advancing age. In our study, the melamine concentration of the MEL pellets was 1,149 mg/kg, which was quite similar to that of Lü et al. (2009a). However, melamine concentrations in the different tissues were much greater in our study than in that of Lü et al. (2009a), and the sheep in the current study received the melamine-contaminated diet for only 7 d. Table 2. Melamine concentration (mg/kg of wet and dry tissue) in different tissues of sheep that ingested 700 mg/d of melamine Item  Muscle  Liver  Kidney  Fat  SEM  P-value  Wet basis  9.63a  4.00b  9.63a  0.20c  0.752  <0.001  Dry basis  36.5a  13.4b  41.2a  0.19c  2.897  <0.001  Item  Muscle  Liver  Kidney  Fat  SEM  P-value  Wet basis  9.63a  4.00b  9.63a  0.20c  0.752  <0.001  Dry basis  36.5a  13.4b  41.2a  0.19c  2.897  <0.001  a–cMeans within rows with different superscripts differed significantly (P < 0.001). View Large Table 2. Melamine concentration (mg/kg of wet and dry tissue) in different tissues of sheep that ingested 700 mg/d of melamine Item  Muscle  Liver  Kidney  Fat  SEM  P-value  Wet basis  9.63a  4.00b  9.63a  0.20c  0.752  <0.001  Dry basis  36.5a  13.4b  41.2a  0.19c  2.897  <0.001  Item  Muscle  Liver  Kidney  Fat  SEM  P-value  Wet basis  9.63a  4.00b  9.63a  0.20c  0.752  <0.001  Dry basis  36.5a  13.4b  41.2a  0.19c  2.897  <0.001  a–cMeans within rows with different superscripts differed significantly (P < 0.001). View Large The apparent digestibility of dietary melamine was 76.7% (Table 3). Because the calculation of apparent digestibility was based on the difference between ingested and melamine excreted in the feces, this value would include melamine degraded in the rumen. No documented results could be found on the degradability of melamine in the rumen, but based on increased rumen NH3 concentrations observed by Newton and Utley (1978) who supplemented steers with melamine, it was hypothesized that melamine might be hydrolyzed in the rumen to some extent. Table 3. Apparent digestibility and partitioning of melamine in sheep that ingested 700 mg/d of melamine Item  % ± SE of ingested melamine  Apparent digestibility  76.3 ± 4.3  Excreted via feces  23.7 ± 4.3  Excreted via urine  54.1 ± 2.8  Distributed to muscle (LM)  3.6 ± 0.5  Item  % ± SE of ingested melamine  Apparent digestibility  76.3 ± 4.3  Excreted via feces  23.7 ± 4.3  Excreted via urine  54.1 ± 2.8  Distributed to muscle (LM)  3.6 ± 0.5  View Large Table 3. Apparent digestibility and partitioning of melamine in sheep that ingested 700 mg/d of melamine Item  % ± SE of ingested melamine  Apparent digestibility  76.3 ± 4.3  Excreted via feces  23.7 ± 4.3  Excreted via urine  54.1 ± 2.8  Distributed to muscle (LM)  3.6 ± 0.5  Item  % ± SE of ingested melamine  Apparent digestibility  76.3 ± 4.3  Excreted via feces  23.7 ± 4.3  Excreted via urine  54.1 ± 2.8  Distributed to muscle (LM)  3.6 ± 0.5  View Large Most of the melamine ingested over the 8-d period was excreted in urine (54.1%), whereas 23.7% was excreted via the feces (Table 3). Although no studies could be found to compare the partitioning of melamine between urine and feces, it is well known that absorbed melamine is excreted via urine (Mast et al., 1983; Wu et al., 2010). The efficiency of melamine uptake by the meat (LM in this case) was calculated by expressing the grams of melamine retained in the muscle as a fraction of the amount ingested. A complicating factor would be the melamine clearance rate from various tissues. According to Lv et al. (2010), once melamine was withdrawn from the diet of lambs, it took 6 d to reach concentrations that were less than 0.01 mg/kg, whereas Lü et al. (2009b) reported the depletion time to be 7 d in ducks. In dairy cows, Cruywagen et al. (2009) found that milk melamine concentrations reached undetectable concentrations 6 d after melamine withdrawal from the diet. In the current trial, lambs received the MEL diet for 7 d. It was thus decided to base calculations of melamine uptake efficiency on the total amount of melamine ingested over the 7 d. In the current study, the only muscle that was sampled was the LM. The values for melamine deposition in the muscle were thus calculated based on the assumption that 1) melamine would be deposited at the same efficiency in all the muscles, and 2) that muscle composed 67.3% of the carcass weight in Merino sheep (Greeff, 1992). The deposition efficiency was then calculated as the total amount of melamine retained in the muscle as a fraction of the total melamine intake during the 7 d that the sheep received the MEL pellets, assuming a depletion time of 7 d. Approximately 3.6% of the ingested melamine was deposited in the meat. On the same basis, Cruywagen et al. (2009) found that the transmission efficiency of melamine from feed to milk was 2.1%. Blood and urine were sampled for the first time 2 d after the sheep received the MEL pellets, and by then melamine appeared in significant concentrations in both serum and urine (Figure 1). Serum melamine concentrations increased significantly from d 3 to 8. As expected, melamine concentrations were much greater in urine than in serum because urine is the major excretion route of melamine. Both serum and urine concentrations of melamine increased over time. Figure 1. View largeDownload slide a) The effect of dietary melamine on serum melamine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). b) The effect of dietary melamine on urine melamine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). Figure 1. View largeDownload slide a) The effect of dietary melamine on serum melamine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). b) The effect of dietary melamine on urine melamine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). In humans and primates, melamine reacts with uric acid to form melamine-urate crystals in the kidney (Cruywagen and Reyers, 2009). In most other animals (with low serum uric acid concentrations), melamine alone is not very toxic, and according to the report of an expert meeting of the World Health Organization (2008a), when either melamine or cyanuric acid is ingested by animals, it is rapidly absorbed and excreted directly in urine. However, when both melamine and cyanuric acid are present in feed, they can react on a 1:1 basis to form spoke-like melamine cyanurate crystals from aqueous solutions. These crystals may result in renal damage and have been implicated as a causative toxicity agent in the Chinese protein export contamination and the 2007 pet food recall (He et al., 2008). Serum creatinine concentrations were thus determined in the current study (Figure 2) because increased concentrations could be an indication of renal damage due to impaired glomerular filtration rate (Rees, 2004). Little information is available on the effect of dietary melamine on serum creatinine concentrations in ruminants. In the classic work of Clark (1966), it was reported that a single oral dose of 100 g of melamine to sheep, as well as daily doses of 25 to 50 g over a period of 7 to 9 d, were lethal and increased BUN and serum creatinine concentrations significantly. Clark (1966) also reported that when sheep were dosed with 10 g of melamine/d, serum creatinine concentration increased sharply, with terminal levels of 230 to 407 µmol/L. Puschner et al. (2007), who did an assessment of melamine and cyanuric acid toxicity, reported that cats dosed with a mixture of melamine and cyanuric acid (32 to 181 mg/kg of each compound) for 2 d manifested increased serum creatinine concentrations. According to Reimschuessel et al. (2008), 1 pig that ate a chocolate pudding snack containing melamine and cyanuric acid, both included at 400 mg/kg, had a serum creatinine concentration of 866 µmol/L (reference range 44 to 177 µmol/L). In another study, Nilubol et al. (2009) reported increased serum creatinine concentrations in pigs that presented with melamine- and cyanuric acid-associated renal failure. Figure 2. View largeDownload slide The effect of dietary melamine on serum creatinine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). Black box: melamine treatment, n = 6; gray box: values of 2 control sheep are provided as baseline reference only. Figure 2. View largeDownload slide The effect of dietary melamine on serum creatinine concentration of sheep. The melamine concentration of the diet was 1,149 mg/kg, and sheep ingested 700 mg/d of melamine. Bars in the chart that contain different letters (a, b) differed (P < 0.05). Black box: melamine treatment, n = 6; gray box: values of 2 control sheep are provided as baseline reference only. Because the current trial was initially planned to measure melamine concentrations in blood, tissue, and excreta, and to calculate transmission efficiencies, only 2 CON sheep were maintained after the adaptation period for the sole purpose of confirming that no melamine was detected in sheep fed the CON diet. The serum creatinine concentrations of the 2 CON sheep were, however, also determined (before and during the trial) and are indicated in Figure 2, merely as a basic reference. Although serum creatinine concentrations increased after 3 d, the increase was of no biological significance because based on the discussions above, it is clear that all the creatinine values observed in our study were within the normal reference range. On each of the sampling days, serum samples were analyzed within 24 h; thus analyses were not done simultaneously on all the samples collected during the trial. The SE for each analysis day was quite small, and it could thus be possible that the greater creatinine concentrations observed from d 3 was an artifact of the analysis. This speculation is supported by the fact that the serum creatinine concentrations of the 2 control sheep also appeared to be greater from d 3. 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TI - Quantification of melamine absorption, distribution to tissues, and excretion by sheep
JO - Journal of Animal Science
DO - 10.2527/jas.2010-3531
DA - 2011-07-01
UR - https://www.deepdyve.com/lp/oxford-university-press/quantification-of-melamine-absorption-distribution-to-tissues-and-Y60GAeu8H7
SP - 2164
EP - 2169
VL - 89
IS - 7
DP - DeepDyve
ER -