Introduction
Downer cow syndrome frequently occurs in the periparturient period and is generally defined as a cow that is recumbent and unable to rise for a variable amount of time (24 to 48 hours).1 Many etiologies can lead to recumbency in dairy cows such as mastitis, metritis, spinal cord compression, musculoskeletal disease and peripheral neuralgia/neuropathy. Metabolic complications associated with muscle weakness leading to recumbency are also common and include hypocalcemia, hypokalemia and hypomagnesemia.2,3 Hypophosphatemia is commonly observed in recumbent cows but its precise causal role in the etiology of downer cow syndrome remains unclear. An association between hypophosphatemia and downer cow syndrome has been previously reported in dairy cows.4 The study showed differences in serum phosphorus concentration between downer cows that positively responded to calcium administration and downer cows that did not respond. However, animals enrolled in the study were not randomly selected and most animals sampled came from downer cows that did not respond to medical treatment, introducing a potential selection bias. Although one study showed that downer cows treated with phosphorus had significantly greater chance to recover than the untreated ones, another revealed that serum phosphorus concentration at the initiation of therapy did not significantly impact the outcome of treatment.5,6 Evidence that hypophosphatemia left untreated in downer cows reduces survival rate is therefore lacking.
Successfully treating low serum phosphorus concentration is difficult. Oral and intravenous administration of dihydrogen phosphate (NaH2PO4) or disodium monohydrogen phosphate (Na2HPO4) would be suitable to treat hypophosphatemia in cows but is not commonly used to the authors’ knowledge.7 A dose of 150 g to 230 g of dihydrogen phosphate (NaH2PO4) per adult cow orally once to twice a day has been previously recommended.8 However, several commercially available products to treat hypophosphatemia often provide a non-biologically active form of phosphorus.7 In Canada, there are no labeled products to treat hypophosphatemia in dairy cows that currently contain a biologically available form of phosphorus.
The purpose of this study was to retrospectively evaluate the association between serum phosphorus concentration upon presentation and the outcome of postpartum cows treated at a large animal hospital. We hypothesized that the outcome of postpartum downer cows would not be affected by serum phosphorus concentration.
Materials and Methods
Medical records of postparturient (0 to 3 weeks postpartum) recumbent dairy cows presented between 1994 and 2016 were reviewed. Information regarding history (age, duration of recumbency before admission), hospitalization (duration of hospitalization, number of flotation therapies, outcome) and blood analysis results upon admission (hematology, biochemistry) including phosphorus concentration was obtained from the database of a previously published study on downer cows.9 Cows were excluded from the study if they were diagnosed with coxofemoral luxation, long bone or vertebral fractures or if relevant data for the analysis were missing. The phosphorus concentration was considered normal when the value was between 3.25 mg/dL and 8.76 mg/dL based on established in-house reference intervals. Blood samples were collected from the coccygeal vein upon arrival or the day following admission, placed into heparin tubes or dry tubes for serum biochemistry panel and processed within 2 hours. Serum inorganic phosphorus concentration was determined using an automated chemistry analyzer (Synchron CX5 and Synchron DX; Beckman Coulter). Methodology for measurement remained the same throughout the duration of the study.
Statistical methods
Exposure of interest, explanatory variables and outcome—For the present study, the unit of study was the cow and the serum inorganic phosphorus concentration was the exposure of interest (hypophosphatemia: mild > 2.25 to < 3.25 mg/dL, moderate > 1.50 to ≤ 2.25 mg/dL, severe ≤ 1.50 mg/dL, normophosphatemia ≥ 3.25 mg/dL and ≤ 8.76 mg/dL, hyperphosphatemia > 8.76 mg/dL). Among all the information collected (history, hospitalization, and blood analysis results), only important variables involved in the phosphorus homeostasis and potential confounders such as age at admission, year and season of admission (winter, spring, summer, fall) were considered. From clinical examination, heart rate, respiratory rate and temperature at presentation were recorded. Explanatory variables related to history and hospitalization included: date of admission, age on admission (years), days in milk, duration of recumbency before admission (days), duration of hospitalization (days), number of days of flotation therapy, and outcome. Phosphorus supplementation during the hospitalization was not considered as oral or intravenous phosphorus administration is very rarely performed at this large animal hospital. Categories for age on admission and duration of recumbency were established based on a previous study.9 Explanatory variables related to blood analysis results (hematology and serum biochemistry panel) included: phosphorus (mg/dL), creatinine (mg/dL), total carbon dioxide (TCO2; mmol/L), potassium (mmol/L), β-hydroxybutyrate (BHB; umol/L), calcium (mg/dL), PCV (%), fibrinogen (g/L), aminotransferase (AST; U/L), creatine kinase (CK; U/L), leukopenia (< 6,200 leukocytes/μL), neutropenia (< 1,100 neutrophils/μL), presence of toxic neutrophils and left shift (presence of non-segmented neutrophils, myelocytes or meta-myelocytes). Variable categorization was performed using 3 criteria: reference intervals, distribution in the dataset and pathophysiological knowledge. Data distribution and clinical experience were used to categorize the following variables: days in milk, consecutive days of recumbency and age. Muscular enzymes (CK and AST) were categorized based on other studies.9 All variables for which normal values existed (respiratory rate, heart rate, temperature, PCV, white blood cell count, neutrophil count, fibrinogen, urea, creatinine, potassium, calcium, BHB and total carbon dioxide) were categorized as normal (within the reference interval) below the reference interval and/or above the reference interval, except for phosphorus.10 The elevated heart rate cutoff of 100 bpm was used based on previous studies.9,11 Another category (> 120 bpm) was also established based on data distribution and clinical judgement. The outcome was a dichotomous variable (0 = survival, the animal was discharged from the hospital; 1 = non-survival, the animal died or was euthanized).
Descriptive statistics—The mean (and 95% CI) days of hospitalization and flotation therapy, and the survival percentage (and 95% CI) were estimated for the different categories of serum phosphorus concentration (eg, cows with hypophosphatemia [mild, moderate and severe], normophosphatemia and hyperphosphatemia).
Univariable analysis—The association between the outcome and each explanatory variable was assessed using a simple logistic regression. Explanatory variables with an α < 0.2 in the univariable analysis were considered for inclusion in the final multivariable logistic regression model. Collinearity between explanatory variables was identified using simple logistic regression or the χ2 test when assessing categorical variables. For dichotomous variables, collinearity was considered significant if based on the magnitude of the OR (OR > 10) and the P value (P < .05).12 Collinearity between categorical variables was considered significant if the P value of the χ2 test was < .05. If collinearity between 2 explanatory variables was observed, the choice of one variable over the other was performed based on clinical experience. Age at admission, year and season of admission (winter, spring, summer, and fall) were explored as potential confounders by assessing the change in the β-coefficient of the variables of the adjusted model compared to the nonadjusted model. However, they were not retained as a change greater than 20% was not observed.12
Multivariable analysis—A multivariable logistic regression model was built to explore the association between potential explanatory variables (α < 0.2 in the univariable analysis) and survival. Selection of the explanatory variables included in the final model was performed using a stepwise backward elimination procedure with α values of entry and removal of 0.2 and 0.25 respectively. The exposure of interest (serum phosphorus concentration) was forced in the final multivariable model regardless of the α obtained in the univariable analysis or the stepwise selection. Two-factor interactions between age of the cows, days of recumbency, and all the independent variables of the final model were explored by adding an interaction term between each couple of variables (1 couple at the time). All possible 2-way interactions between clinicopathologic (PCV, AST, creatinine) and heart rate were also explored. Additional interactions between phosphorus and calcium, and phosphorus and creatinine were explored. Interaction terms were retained if P < .05. The goodness-of-fit of the final model was evaluated using the Hosmer-Lemeshow statistic.12
Results
Overall, the study population included a total of 907 recumbent postpartum dairy cows. Of the 1,471 downer cows presented between 1994 and 2016, 476 cows (32.4%) were excluded because they were not in the postpartum period (n = 193) or data concerning days in milk were missing (n = 283). Among the remaining 995 postpartum cows, 69 cows were excluded as they were diagnosed with coxofemoral luxation, long bone or vertebral fractures and 19 cows were excluded due to missing information regarding final diagnosis. Of the remaining cows studied, 19.4% (n = 176) were hypophosphatemic, 78.2% (n = 710) were normophosphatemic, and 2.3% (n = 21) were hyperphosphatemic. Hypophosphatemic cows were categorized by severity. Of the 176 hypophosphatemic cows, hypophosphatemia was classified as mild in 30 cows (3.3%), moderate in 54 cows (6.0%) and severe in 92 cows (10.1%). The distribution of phosphorus concentrations and survival is presented in Supplementary Table S1. A total of 54.5% (n = 96) hypophosphatemic cows were also hypocalcemic (Table 1). Five-hundred forty-one cows (58.4%) survived after hospitalization. No differences were observed between the hypophosphatemic and normophosphatemic groups regarding survival percentage, mean age at admission, mean days of hospitalization, and mean days of flotation therapy (Table 2). A lower survival percentage was observed in hyperphosphatemic cows (n = 21; 33.3%; 95% CI: 13.2 to 53.5) compared to hypophosphatemic (n = 176; 62.5%; 95% CI: 54.5 to 61.8) and normophosphatemic cows (n = 710; 58.2%; 95% CI: 55.4 to 69.7). The distribution of phosphorus and creatinine is presented in Supplementary Table S2.
Distribution of phosphorus and calcium serum concentrations among 907 postpartum downer cows presented between 1994 and 2016.
| Phosphorus (mg/dL) | Calcium (mg/dL) | |||
|---|---|---|---|---|
| < 8.82 | ≥ 8.82 and ≤ 10.82 | > 10.82 | Total | |
| < 3.25 | 96 | 60 | 20 | 176 |
| ≥ 3.25 and ≤ 8.76 | 282 | 335 | 93 | 710 |
| > 8.76 | 8 | 10 | 3 | 21 |
| Total | 386 | 405 | 116 | 907 |
Survival percentage and mean age (years), days of hospitalization and days of flotation therapy for normophosphatemic (≥ 3.25 and ≤ 8.76 mg/dL), hypophosphatemic (< 3.25 mg/dL), and hyperphosphatemic postpartum downer cows (> 8.76 mg/dL).
| Phosphorus (mg/dL) | Variables | ||||
|---|---|---|---|---|---|
| No. of cows | Age, in years | Survival % | Days of hospitalization | Days of flotation | |
| < 3.25 | 176 | 6.0 (5.7–6.3) | 62.5 (55.4–69.7) | 7.9 (7.3–8.6) | 3.0 (2.7–3.4) |
| ≥ 3.25 and ≤ 8.76 | 710 | 5.6 (5.4–5.7) | 58.2 (54.5–61.8) | 8.1 (7.7–8.5) | 3.2 (3.0–3.4) |
| > 8.76 | 21 | 6.5 (5.3–7.8) | 33.3 (13.2–53.5) | 7.1 (4.9–9.3) | 3.1 (2.1–4.1) |
Values reported are mean and 95% CI.
The univariable analysis is presented in Supplementary Table S3. Serum phosphorus concentration, aminotransferase, creatinine, β-hydroxybutyrate, total carbone dioxide, fibrinogen, leukocytes, neutrophils, non-segmented neutrophils, toxic changes on neutrophils, packed cell volume, duration of recumbency, age, heart rate, respiratory rate, and temperature were associated with survival (P < .2) and therefore considered as potential explanatory variables to be included in the final multivariable logistic regression model. Correlated variables included leukopenia and neutropenia (OR = 29; P < .001), non-segmented neutrophils and toxic changes on neutrophils (OR = 26; P < .001), and AST and CK activity (χ2 = 426.6; P < .001). Neutropenia was chosen over leukopenia as it is not affected by lymphocyte count, and AST was chosen over CK as it has been shown to be more useful than CK as a predictive value for nonsurvival in a previous study.9,13
The final multivariable model is presented (Table 3). The variable serum phosphorus concentration was not retained by the stepwise selection. However, it was forced in the final model given the objective of the present study. The odds of nonsurvival between hypophosphatemic (mild: OR = 1.0, 95% CI: 0.6 to 1.8; moderate: OR = 0.5, 95% CI: 0.2 to 1.1; severe: OR = 1.0, 95% CI: 0.4 to 2.4) or hyperphosphatemic (OR = 2.4; 95% CI: 0.7 to 7.6) and normophosphatemic cows were not significantly different, regardless of the severity. Although serum phosphorus concentration was not associated with the outcome in the multivariable model, the remaining explanatory variables (AST, creatinine, total carbone dioxide, age, heart rate, duration of recumbency before admission and PCV) included in the final multivariable logistic regression model were significantly associated with survival. None of the 2-way interactions explored was statistically significant. Specifically, interactions between phosphorus and calcium (P = .30), and phosphorus and creatinine (P = .70) were not observed, therefore the interaction terms were not retained in the final model. The Hosmer-Lemeshow (χ2 = 6.2; 7 degrees of freedom; P = .50) fit statistics suggested a reasonable fit of the model, in which a P value > .05 indicates that the model fits well the data.
Final multivariable logistic regression model for determining the association between hypophosphatemia and survival in 907 postpartum downer cows.
| Variable | Category | ORa | 95% CI | P value |
|---|---|---|---|---|
| Phosphorus (mg/dL) | Normal (≥3.25 to ≤ 8.76) | Reference | — | — |
| Severe hypophosphatemia (≤ 1.50) | 1.0 | 0.4–2.4 | .974 | |
| Moderate hypophosphatemia (> 1.50 to ≤ 2.25) | 0.5 | 0.2–1.1 | .068 | |
| Mild hypophosphatemia (> 2.25 to < 3.25) | 1.0 | 0.6–1.8 | .927 | |
| Hyperphosphatemia (> 8.76) | 2.4 | 0.7–7.6 | .152 | |
| Creatinine (mg/dL)a | Normal (≤ 1.3) | Reference | — | — |
| Hypercreatininemia (> 1.31) | 1.9 | 1.2–3.1 | .011 | |
| AST (U/L)a | Normal (< 500) | Reference | — | — |
| 500 to 999 | 2.3 | 1.6–3.4 | < .001 | |
| ≥ 1,000 | 7.3 | 4.5–11.8 | < .001 | |
| PCV (%) | Normal (≥ 26) | Reference | — | — |
| Anemia (< 26) | 2.8 | 1.0–8.0 | .059 | |
| Heart rate (bpm)a | Normal (60 to 80) | Reference | — | — |
| Bradycardia < 60 | 0.5 | 0.1–3.6 | .525 | |
| Mild tachycardia (> 80 to ≤ 100) | 1.0 | 0.7–1.8 | .696 | |
| Moderate tachycardia (> 100 to ≤ 120) | 1.9 | 1.1–3.1 | .014 | |
| Marked tachycardia (> 120) | 1.9 | 1.0–3.8 | .062 | |
| Days of recumbency | < 24 h | Reference | — | — |
| 24 to < 48 h | 0.8 | 0.4–1.5 | .465 | |
| 2 days | 0.9 | 0.5–1.7 | .765 | |
| 3 days | 1.2 | 0.6–2.4 | .615 | |
| 4 days | 1.4 | 0.6–3.3 | .431 | |
| 5 days | 1.3 | 0.5–3.7 | .622 | |
| 6 days | 1.9 | 0.6–5.7 | .260 | |
| ≥ 7 days | 2.5 | 1.0–6.6 | .057 | |
| Agea | < 3 y | Reference | — | — |
| 3 to < 5 y | 1.1 | 0.6–2.0 | .809 | |
| ≥ 5 y | 1.8 | 1.0–3.2 | .040 | |
| Total carbone dioxide (mmol/L) | Normal (24 to 26) | Reference | — | — |
| Hypocapnia (< 24) | 1.5 | 0.8–2.7 | .205 | |
| Hypercapnia (> 26) | 0.9 | 0.5–1.4 | .514 |
aFor each variable, an OR different from 1 is interpreted as a decrease (< 1) or an increase (> 1) in the odds of non-survival for the cows in each category compared with the cows in the reference category.
Fit of the model: Hosmer-Lemeshow (χ2 = 6.2; 7 degrees of freedom; P = .50)
Discussion
Hypophosphatemia and other electrolyte abnormalities have been associated with muscle weakness, although only few studies specifically have evaluated the contribution of hypophosphatemia to downer cow syndrome.4,14–17 We did not observe an association between serum inorganic phosphorus concentration and survival in our study population which may or may not represent the type of milk fever and down cows seen in the field. Serum phosphorus concentration was also not associated with duration of hospitalization nor increased the number of days of flotation therapy. To our knowledge, this is the largest study assessing serum phosphorus concentration in downer cow syndrome.
In agreement with our findings, 1 study5 analyzing 770 recumbent cows revealed that phosphorus concentration did not have an influence on the recovery rate. A previous study6 assessing prognosis indicators for non-ambulatory cows observed similar findings. Serum phosphorus concentration did not differ significantly between survivors and nonsurvivors. Empirical observations associating hypophosphatemia and downer cow syndrome have been proposed although recumbent cows with low phosphorus concentration do not routinely respond to phosphorus administration.18
It is important to emphasize the association between hypocalcemia and serum phosphorus levels in our study; about 19% of downer cows were hypophosphatemic, of which half were also hypocalcemic. During concomitant hypocalcemia, hypophosphatemia is secondary to an increase in PTH (parathyroid hormone), which promotes renal and salivary phosphorus excretion as well as mobilization of phosphorus from bone. Hypophosphatemia should therefore self-correct following the treatment of hypocalcemia.8 The relationship between calcium and phosphorus was further explored by adding an interaction term between these 2 variables in the final model. The purpose of analyzing the interaction was to investigate whether the association of phosphorus and survival differed depending on the calcium levels (ie, a different association by calcium categories). However, such interaction was not observed in the present study. Of the 80 hypophosphatemic cows that were not hypocalcemic on arrival, a few could have been originally hypocalcemic and treated with calcium prior to admission. This would explain normal serum calcium concentration and not yet normal serum phosphorus concentration. While hypocalcemia is a well-documented cause of recumbency in postpartum dairy cows, the contribution of hypophosphatemia alone in postpartum recumbency remains unclear.
Several other factors prior or during blood sampling can influence the measured value of serum phosphorus concentration. This further complicates the interpretation of abnormal serum phosphorus concentration observed in downer cows. Among external factors, the venipuncture site used to draw blood influences the measured value of serum phosphorus. Serum phosphorus concentration in the jugular vein can be up to 19% lower compared to the coccygeal vein. The fact that jugular veins drain the salivary glands could explain that discrepancy.19 Additionally, intravenous dextrose administration causes a transient hypophosphatemia for up to 1 hour. The resulting insulin peak promotes a phosphorus transfer from the extracellular space to the intracellular space and thus decreases serum phosphatemia.20 In 1 study,21 physical activity such as attempts to stand within 2 to 3 hours prior to blood sampling was associated with a transient hypophosphatemia. While in vitro (preanalytical artifact) and in vivo intravascular hemolysis do not result in increased measured (inorganic) phosphate concentrations,22 inappropriate storage such as lack of refrigeration or cell separation can lead to falsely elevated phosphorus concentrations. To summarize, hypocalcemia is commonly observed in downer cows and jugular vein sampling is frequently used in practice immediately following intravenous treatment. Moreover, dextrose administration before blood sampling is often routinely performed and multiple efforts to stand are frequently attempted by the cow or the farmer before the veterinarian’s visit. Thus, it is difficult to conclude that hypophosphatemia is associated with unresponsive downer cows. Unless the blood sample originated from the coccygeal vein, before dextrose administration and after several hours of rest, the serum phosphorus concentration should be interpreted with caution. If a concomitant hypocalcemia is observed, hypophosphatemia need not be addressed.8,23,24
If hypophosphatemia does need to be addressed rapidly, the treatment must be used off-label as no currently parenteral labeled product provides a form of phosphorus that is bioavailable and effective at increasing the serum phosphorus concentration. Adequate treatment of hypophosphatemia has been previously described.8
The lower survival percentage observed in hyperphosphatemic cows compared to hypophosphatemic and normophosphatemic cows observed in the univariable analysis (Supplementary Table 3) could potentially be explained by renal injury from dehydration, sepsis and/or anti-inflammatory administration causing decreased glomerular filtration rate of phosphorus. Severe skeletal muscle injury or, although rare in ruminants, humoral hypercalcemia of malignancy resulting in decreased PTH levels could also theoretically increase phosphorus concentrations and affect survival.
This study had some limitations considering its retrospective nature. The population of referred cases could also vary from the ambulatory practitioner’s population and therefore, extrapolation of the data from this study should be performed with caution. Furthermore, treatments administered before blood analysis upon admission were not available. A few blood samples were also taken and submitted for analysis the day following admission if the patient was admitted after opening hours, although treatments were likely administered overnight.
The decision to administer phosphorus for treating downer cow syndrome is often made based on personal experience and preference. When faced with hypophosphatemia as the only abnormal clinicopathologic finding, veterinarians may feel the need to address it without tangible evidence. We therefore caution strongly against assuming that hypophosphatemia plays a primary role when cows are recumbent and unable to stand.
In conclusion, our results suggest that even when untreated, serum phosphorus concentration did not affect the outcome of postpartum downer cows in a hospital setting. Our findings highlight how cautiously serum phosphorus concentration should be interpreted in downer cows.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
Acknowledgments
The authors declare no conflict of interest. No funding was received for this study. The authors declare no off-label use of antimicrobials.
References
- 1.↑
Green AL, Lombard JE, Garber LP, Wagner BA, Hill GW. Factors associated with occurrence and recovery of nonambulatory dairy cows in the United States. J Dairy Sci. 2008;91(6):2275–2283. doi:10.3168/jds.2007-0869
- 2.↑
Correa MT, Erb HN, Scarlett JM. Risk factors for downer cow syndrome. J Dairy Sci. 1993;76(11):3460–3463. doi:10.3168/jds.S0022-0302(93)77685-7
- 3.↑
Peek SF, Divers TJ, Guard C, Rath A, Rebhun WC. Hypokalemia, muscle weakness, and recumbency in dairy cattle. Vet Ther. 2000;1(4):235–244.
- 4.↑
Ménard L, Thompson A. Milk fever and alert downer cows: does hypophosphatemia affect the treatment response? Can Vet J. 2007;48(5):487–491.
- 5.↑
Gelfert CC, Alpers I, Dallmeyer M, et al. Factors affecting the success rate of treatment of recumbent dairy cows suffering from hypocalcaemia. J Vet Med A Physiol Pathol Clin Med. 2007;54(4):191–198. doi:10.1111/j.1439-0442.2007.00940.x
- 6.↑
Burton AJ, Nydam DV, Ollivett TL, Divers TJ. Prognostic indicators for nonambulatory cattle treated by use of a flotation tank system in a referral hospital: 51 cases (1997-2008). J Am Vet Med Assoc. 2009;234(9):1177–1182. doi:10.2460/javma.234.9.1177
- 7.↑
Cohrs I, Grünberg W. Suitability of oral administration of monosodium phosphate, disodium phosphate, and magnesium phosphate for the rapid correction of hypophosphatemia in cattle. J Vet Intern Med. 2018;32(3):1253–1258. doi:10.1111/jvim.15094
- 8.↑
Grünberg W. Treatment of phosphorus balance disorders. Vet Clin North Am Food Anim Pract. 2014;30(2):383–408, vi. doi:10.1016/j.cvfa.2014.03.002
- 9.↑
Puerto-Parada M, Bilodeau MÈ, Francoz D, et al. Survival and prognostic indicators in downer dairy cows presented to a referring hospital: a retrospective study (1318 cases). J Vet Intern Med. 2021;35(5):2534–2543. doi:10.1111/jvim.16249
- 10.↑
Lumsden JH, Mullen K, Rowe R. Hematology and biochemistry reference values for female Holstein cattle. Can J Comp Med. 1980;44(1):24–31.
- 11.↑
Labonté J, Dubuc J, Roy JP, Buczinski S. Prognostic value of cardiac troponin I and L-lactate in blood of dairy cows affected by downer cow syndrome. J Vet Intern Med. 2018;32(1):484–490. doi:10.1111/jvim.14874
- 12.↑
Dohoo IR, Martin W, Stryhn HE. Veterinary Epidemiologic Research. VER Inc; 2003. Accessed June 30, 2022. https://www.islandscholar.ca/islandora/object/ir:ir-batch6-2657
- 13.↑
Shpigel NY, Avidar Y, Bogin E. Value of measurements of the serum activities of creatine phosphokinase, aspartate aminotransferase and lactate dehydrogenase for predicting whether recumbent dairy cows will recover. Vet Rec. 2003;152(25):773–776. doi:10.1136/vr.152.25.773
- 14.↑
Forrester SD, Moreland KJ. Hypophosphatemia. Causes and clinical consequences. J Vet Intern Med. 1989;3(3):149–159. doi:10.1111/j.1939-1676.1989.tb03091.x
- 15.
Wächter S, Cohrs I, Golbeck L, Wilkens MR, Grünberg W. Effects of restricted dietary phosphorus supply to dry cows on periparturient calcium status. J Dairy Sci. 2022;105(1):748–760. doi:10.3168/jds.2021-20726
- 16.
Grünberg W, Scherpenisse P, Dobbelaar P, Idink MJ, Wijnberg ID. The effect of transient, moderate dietary phosphorus deprivation on phosphorus metabolism, muscle content of different phosphorus-containing compounds, and muscle function in dairy cows. J Dairy Sci. 2015;98(8):5385–5400. doi:10.3168/jds.2015-9357
- 17.↑
Grünberg W, Scherpenisse P, Cohrs I, et al. Phosphorus content of muscle tissue and muscle function in dairy cows fed a phosphorus-deficient diet during the transition period. J Dairy Sci. 2019;102(5):4072–4093. doi:10.3168/jds.2018-15727
- 18.↑
Grünberg W. Phosphorus homeostasis in dairy cattle: some answers, more questions. In: Proceedings of the 17th Annual Tri-State Dairy Nutrition Conference; 2008:29–35.
- 19.↑
Parker BJ, Blowey RW. A comparison of blood from the jugular vein and coccygeal artery and vein of cows. Vet Rec. 1974;95(1):14–18. doi:10.1136/vr.95.1.14
- 20.↑
Grünberg W, Morin DE, Drackley JK, Constable PD. Effect of rapid intravenous administration of 50% dextrose solution on phosphorus homeostasis in postparturient dairy cows. J Vet Intern Med. 2006;20(6):1471–1478. doi:10.1892/0891-6640(2006)20[1471:eoriao]2.0.co;2
- 21.↑
Palmer LS, Cunningham WS, Eckles CH. Normal variations in the inorganic phosphorus of the blood of dairy cattle*. J Dairy Sci. 1930;13(3):174–195. doi:10.3168/jds.S0022-0302(30)93517-5
- 22.↑
Jacobs RM, Lumsden JH, Grift E. Effects of bilirubinemia, hemolysis, and lipemia on clinical chemistry analytes in bovine, canine, equine, and feline sera. Can Vet J. 1992;33(9):605–608.
- 23.↑
Cheng YH, Goff JP, Horst RL. Restoring normal blood phosphorus concentrations in hypophosphatemic cattle with sodium phosphate. Vet Med (USA). 1998;93(4):383–385, 388.
- 24.↑
Goff JP. Treatment of calcium, phosphorus, and magnesium balance disorders. Vet Clin North Am Food Anim Pract. 1999;15(3):619–639, viii. doi:10.1016/s0749-0720(15)30167-5
