Received: 23 March 2021 | Revised: 30 June 2021 | Accepted: 3 July 2021

DOI: 10.1111/vcp.13059

R E FE R E N CE I NTE RVA L S

Complete blood count and biochemistry reference intervals for

healthy adult sheep in the northeastern United States

Elisha A. Frye | Erica L. Behling-­Kelly | Manigandan Lejuene | Julie L. Webb

Department of Population Medicine and

Diagnostic Sciences, Cornell University
College of Veterinary Medicine, Ithaca,
New York, USA
Correspondence
Elisha A. Frye, Animal Health Diagnostic
Center, Cornell University College of
Veterinary Medicine, Ithaca NY, USA.
Email: eab73@cornell.edu
Abstract
Background: Reference intervals (RIs) for routine clinicopathologic data in sheep are
sparse. The authors sought to establish hematologic and biochemical RIs from a var-
ied ovine population to improve data interpretation for small ruminant veterinarians.
Objectives: The goal of this study was to establish ovine CBC and biochemistry ref-
erence intervals by sampling 120 healthy adult sheep, both male and female, from a
variety of breeds, located in the Northeastern United States.
Methods: One hundred and eighteen sheep were included in the CBC RI and 121
sheep were included in the biochemistry panel RI.
Results: RIs for 42 CBC and biochemistry analytes were established in accordance
with the American Society for Veterinary Clinical Pathology and Clinical Laboratory
Standards Institute guidelines.
Conclusions: These RIs are provided to assist small ruminant veterinarians with the
interpretation of CBC and biochemistry panel results in sheep.

KEYWORDS
clinical chemistry, domestic, hematology, ovine, small ruminants

1 | I NTRO D U C TI O N 2 | M ATE R I A L S A N D M E TH O DS

Reference intervals (RIs) for routine clinicopathologic data in
adult domestic sheep are sparse. Veterinarians often interpret
results using RIs listed in textbooks, but the original source of
this data is often unclear.1,2 Alternatively, veterinarians may turn
to peer-­reviewed RIs, but these have often been established in
other countries on breed and/or sex-­specific populations 3,4,5 that
might not be representative of their patients. The New York State
Animal Health Diagnostic Center (AHDC) receives approximately
700 ovine CBC or biochemistry panels per year, representing over
20 breeds and numerous mixed breeds of sheep. This situation is
likely mirrored in other regions, and therefore, the authors sought
to establish hematologic and biochemical RIs from a varied ovine
population to improve services for practitioners providing care for
sheep.
2.1 | Ethics approval
This study, under the umbrella protocol Laboratory test reference in-
tervals, method validation and testing for diagnostic utility of laboratory
assays, was performed under an approved International Animal Care
and Use Committee (IACUC) protocol (18–­29). Signed owner con-
sent was obtained for all sample collections.
2.2 | Animals and sample collection
Sheep from the northeastern United States, including the states of
Maine, New Hampshire, New York, and Pennsylvania, were sampled
to represent the geographic location of typical submissions to the

© 2022 American Society for Veterinary Clinical Pathology

Vet Clin Pathol. 2022;51:119–125.  wileyonlinelibrary.com/journal/vcp | 119

120 | FRYE et al.
AHDC. The goals were to obtain 120 samples and establish non-
parametric RIs with a 90% confidence interval. Criteria for inclusion
included adult sheep over 6 months of age, a mixture of females,
males, and castrated males, and a representative variety of breeds
and breed crosses commonly found in the region. All sheep had body
conditions scored (BCS) by an experienced small ruminant veteri-
narian using a scoring system from 1 to 5,6 with a BCS of 3, 4, and
5 eligible. A FAMACHA eye color score7 was performed, and only
sheep with a score of 1 or 2 were included. This avoided anemic
sheep presumptively heavily parasitized by the blood-­sucking para-
site Haemonchus contortus.6 Periparturient females, before and after
2 weeks of lambing, were also excluded.
A total of 121 sheep (71 females, 14 males, and 36 castrated
males), with a median age of 2 years (range 7 months to 11 years),
were enrolled. The following purebred sheep breeds were sam-
pled: Bluefaced Leicester (12), Cheviot (1), Colombia (3), Dorper (4),
Dorset (10), Finn (6), Icelandic (3), Katahdin (15), Lincoln (1), Polypay
(16), Shetland (2), and Tunis (10). The remaining sheep were a variety
of crossbreeds, which included the following: Bluefaced Leicester,
Border Leicester, Cheviot, Clun, Colombia, East Friesian, Finn,
Icelandic, Katahdin, Lacaune, Polypay, Romney, Suffolk, and Texel.
Eighty sheep were privately owned by 10 different farmers, 16
were part of a university research flock, and 25 were from a specific
pathogen-­free (SPF) flock for sale for research purposes. All sheep
were fed hay, grain, and minerals; supplementation practices varied
farm to farm, by season and gestation if breeding. Access to pasture
also varied by season and farm owner. The study period occurred
from January 2020 to October 2020, at the convenience of the col-
laborating small ruminant veterinarians as part of routine herd man-
agement and health-­check visits; therefore, samples were collected
during all four seasons in the Northeastern United States. The aver-
age annual temperature in this region ranges from 2°C (36°F) in the
North to 15°C (59°F) in the South, and rainfall varies from 760 to
1520 mm (30 to 60 inches) per year.8 Winters are cold, and blizzards
occur annually.
Each sheep was restrained, and venipuncture of the right or
left jugular vein was performed. Whole blood was collected into ei-
ther a 7 mL Covidien Monoject Vacutainer K3-­EDTA tube or 4 mL
BD Vacutainer K2-­EDTA tube, and a BD Vacutainer serum tube.
Feces were collected into a VWR Specimen Container. Two blood
smears from the EDTA tube were made within an hour of collection.
The serum tube was centrifuged within 4 hours of collection, and
serum was removed from the blood clot and placed in another BD
Vacutainer serum tube. All samples were kept chilled on ice packs
and hand-­delivered to the AHDC or refrigerated until shipment on
ice packs for overnight delivery within 24 hours of sample collection.
2.3 | Laboratory analyses
All samples were analyzed within 24 hours of receipt. The total pro-
tein/total solids analyte of the CBC was determined by refractome-
try of the EDTA-­anticoagulated blood. Hematocrit (Hct), hemoglobin
concentration (Hb), RBC count, mean corpuscular volume (MCV),
mean corpuscular hemoglobin concentration (MCHC), mean cor-
puscular hemoglobin (MCH), red cell distribution width (RDW),
platelet count, mean platelet volume (MPV), and WBC count were
determined on EDTA-­anticoagulated blood using a Siemens Advia
2120i automated hematology analyzer (Siemens Medical Solutions).
The differential WBC count was derived by manually counting 100
cells in Wright-­Giemsa-­stained smears. The biochemical parameters
sodium, potassium, chloride, bicarbonate, anion gap, sodium: potas-
sium (Na/K) ratio, urea nitrogen, creatinine, calcium, phosphorus,
magnesium, total protein, albumin, globulins, albumin: globulin (A/G)
ratio, glucose, aspartate aminotransferase (AST), sorbitol dehydro-
genase (SDH), glutamate dehydrogenase (GLDH), gamma-­glutamyl
transferase (GGT), total bilirubin, direct bilirubin, indirect bilirubin,
creatinine kinase (CK), iron, total iron-­binding capacity (TIBC), and %
iron saturation were measured using a Cobas 501 automated serum
chemistry analyzer (Roche Diagnostics). Basic methodologies for the
Cobas analyzer are listed in Table 1.
Daily QC in the laboratory is performed using statistical con-
trol, a 2SD rule for each measurand, and two commercially available
quality control materials for each analyzer. Upon instrument instal-
lation, extensive instrument performance studies were completed,
and total observed error (1.65 × CV[%] + Bias [%]) was compared
with ASVCP published guidelines for total allowable error to ensure
acceptable analyzer performance. ADVIA summative QC data are
evaluated on a monthly basis to users co-­enrolled in the Streck he-
matology QA program. Cobas generated data are compared with
the group user means provided by Roche on a quarterly basis. The
laboratory also participates in two external QA programs provided
by the Veterinary Laboratory Association and College of American
Pathologists.
Fecal samples for parasite analyses were subjected to the modi-
fied Wisconsin double centrifugation flotation technique using two
different flotation solutions (saturated sugar 1.33 specific gravity
and zinc sulfate 1.18 specific gravity).9 Parasite stages were quan-
tified as eggs, oocysts, or cysts present per gram of feces. Samples
with ≥100 strongyle eggs per gram were further subjected to
Haemonchus egg stain tests (HEGG) to identify Haemonchus contor-
tus eggs. This procedure uses a fluorescent-­t agged peanut agglutinin
that specifically binds to Haemonchus eggs and its hatched larvae.
When viewed under a fluorescent microscope, stained Haemonchus
eggs will fluoresce while other morphologically indistinguishable
strongyle eggs will not.10
2.4 | Statistical analysis
Reference intervals were determined according to the guidelines
of the American Society for Veterinary Clinical Pathology11 and
analyzed using Reference Value Advisor (v.2.1), a set of macroin-
structions for Microsoft Excel.12 Outliers and suspect data were
determined based on Tukey’s method. These values were retained
unless there was convincing preanalytical error, analytical error,
FRYE et al. | 121

TA B L E 1 Basic methodology for biochemical testing performed on the Roche Cobas

Measurand Method

Albumin Bromocresol green dye-­binding

AST NADH oxidation
Electrolytes Indirect ion-­selective potentiometry
Bicarbonate Phosphoenolpyruvate carboxylase based
Bilirubin, total Jendrassik-­Grof based-­Diazo method (diazonium ion)
Bilirubin, direct Jendrassik-­Grof based-­(diazotized sulfanilic acid)
Calcium 5-­nitro-­5′-­methyl-­BAPTA (NM-­BAPTA)
Creatinine kinase Creatine phosphate cleavage
Creatinine Modified Jaffe
GGT L-­gamma-­glutamyl-­3-­c arboxy-­4-­nitroanilde substrate
Glucose Hexokinase
GLDH Alpha-­oxoglutarate substrate
Iron Ferrozinc method
Magnesium Xylidyl blue, diazonium salt
Phosphate Ammonium molybdate
SDH D-­fructose substrate
TIBC Unsaturated Fe binding
Total protein Biuret
Urea nitrogen Urease-­kinetic

Abbreviations: AST, aspartate aminotransferase; GGT, gamma-­glutamyl transferase; GLDH, glutamate dehydrogenase; SDH, sorbitol dehydrogenase;
TIBC, total iron-­binding capacity.

or a pattern inconsistent with health. The distribution of the data
was evaluated by the Anderson-­Darling method, with a P-­value
<0.05, indicating non-­
G aussian distribution. The symmetry of
the data was evaluated using the runs test with a P-­value <0.05
indicating asymmetry. The nonparametric method was used for
analytes with at least 120 results. For analytes with less than 120
results, the parametric method was selected for Gaussian distribu-
tions, and the nonparametric method was selected when data had
a non-­G aussian and asymmetrical distribution (before and after
Box-­C ox transformation). For analytes with at least 120 results,
the 90% confidence intervals (CIs) were calculated using the non-
parametric method. For analytes with fewer than 120 results, the
bootstrap method was used to establish CIs. In any instance where
outliers were removed, the data were re-­analyzed using the meth-
ods above.
3 | R E S U LT S
One hundred nineteen sheep had sufficient feces for analysis. One
hundred seventeen of those sheep had strongyle fecal egg counts
below 1000 eggs/g (light burdens) with a mean of 109 eggs/g. Two
sheep had fecal egg counts greater than 1000 (moderate burdens)
with positive HEGG results of 1300 and 1200 eggs/g.
One hundred twenty-­one chemistry panels and 118 CBCs were
included in the analysis: three CBCs were discarded due to clotting.
Of those 118 CBCs, three had a moderate degree of hemolysis so
the total protein test was not performed. CBC and biochemistry ref-
erence interval data are presented in Tables 2 and 3, respectively.
The majority of suspect and outlier data was retained as the pop-
ulation was well-­defined and general health was well-­established.
One WBC outlier and associated differential were removed because
the lymphocyte result (13 200 cells/μL) suggested an epinephrine
response. A second WBC outlier and associated differential were
removed because the eosinophil and basophil results (4300 and
500 cells/μL, respectively) suggested a parasitic or hypersensitivity
condition. Seventeen platelet count and corresponding MPV outliers
were removed due to marked platelet clumping. Seven CK outliers
were removed because their results were most consistent with re-
straint and/or traumatic venipuncture (>1000 U/L). One sheep had
its total protein, globulin, and A:G ratio results removed because the
globulin outlier (6.0 mg/dL) was suspicious for an inflammatory pro-
cess. Two sheep had their AST, SDH, GLDH, and GGT enzymes re-
moved from the analysis because three of four results were outliers,
suggesting subclinical liver disease.
Reference intervals were not established for GLDH. The data
were non-­Gaussian and nonsymmetrical, both before and after Box-­
Cox transformation, so neither parametric nor robust methods were
considered appropriate. Ninety-­five percent of GLDH results fell
below 60 U/L (see Figure 1), but nonparametric methods generated
an upper reference limit of 134 U/L with a 90% confidence interval
extending from 59 to 207 U/L (112% of the reference interval width).
 122
|

TA B L E 2 Hematology reference intervals established from 118 sheep using an ADVIA 2120 and manual differential

LRL of URL of
Measurand Units n Mean SD Median Min Max P-­value* Dist Method RI RI CI of LRL CI of URL

Hematocrit L/L 118 36 4.3 36 22 47 0.063 G P 27 44 26–­29 43–­46

RBC 1012/L 118 11.8 1.4 11.4 6.3 14.6 0.003 NG NP 8.1 13.8 6.3–­8.7 13.2–­14.6
Hemoglobin g/L 118 126 15 127 74 163 0.469 G P 95 156 91–­99 152–­160
MCV fL 118 32 2.8 32 26 38 0.001 NG NP 27 37 26–­28 36–­38
MCHC g/L 118 350 13 350 300 380 <0.001 NG NP 320 370 300–­330 370–­380
MCH pg 118 11 0.9 11 9 13 <0.001 NG NP 9 13 9–­10 12–­13
RDW % 118 16.9 1.4 16.8 14.4 21.4 0.168 G P 14 19.6 13.7–­14.4 19.3–­20.0
WBC 109/L 116 7.3 1.8 7.1 4.1 12.2 0.008 NG NP 4.5 11.8 4.1–­4.9 10.5–­12.2
Neutrophil 109/L 116 2.6 1.3 2.1 0.7 7.1 <0.001 NG NP 1.0 6.1 0.7–­1.1 5.5–­7.1
Lymphocyte 109/L 116 3.9 1.6 3.6 1.3 9.1 <0.001 NG NP 1.5 8.3 1.3–­2.1 6.9–­9.1
9
Monocyte 10 /L 116 0.1 0.1 0.1 0 0.5 <0.001 NG NP 0 0.4 0–­0 0.4–­0.5
Eosinophil 109/L 116 0.7 0.7 0.4 0 4.6 <0.001 NG NP 0 2.3 0–­0 2.0–­4.6
Basophil 109/L 116 0 0.1 0 0 0.2 <0.001 NG NP 0 0.2 0–­0 0.2–­0.2
Platelet 109/L 101 400 167 365 141 1133 0.001 NG NP 152 736 141–­193 708–­1133
MPV fL 101 8.3 2.6 7.9 4.3 18.6 <0.001 NG NP 4.8 15.7 4.3–­5.3 12.2–­18.6
TP g/L 114 73 6 72 59 87 6.7 G P 61 85 59–­62 84–­87

Abbreviations: CI, 90% confidence interval; Dist, Distribution; G, Gaussian; LRL, lower reference limit; MCH, mean cell hemoglobin; MCHC, mean corpuscular hemoglobin concentration; MCV, mean cell
volume; MPV, mean platelet volume; NG, non-­Gaussian; NP, nonparametric; P, parametric; RBC, red blood cell; RDW, red blood cell distribution width; RI, reference interval; TP, total protein; URL, upper
reference limit; WBC, white blood cell.
*Anderson-­Darling, <0.05 indicates non-­Gaussian distribution.
FRYE et al.
TA B L E 3 Biochemistry reference intervals established from 121 sheep using a Cobas 501

LRL of URL of
FRYE et al.

Measurand Units n Mean SD Median Min Max P-­value* Dist Method RI RI CI of LRL CI of URL

Sodium mmol/L 121 148 2.6 147 142 154 0.002 NG NP 143 154 142–­144 152–­154
Potassium mmol/L 121 5.0 0.5 4.9 4.0 6.7 0.007 NG NP 4.1 6.0 4.0–­4.2 5.7–­6.7
Chloride mmol/L 121 105 2.5 105 99 111 0.004 NG NP 100 109 99–­101 109–­111
Bicarbonate mmol/L 121 24.3 2.4 24 18 31 0.008 NG NP 20 29 18–­21 29–­31
Anion gap mmol/L 121 23.7 3.3 24 16 36 <0.001 NG NP 17.1 32 16–­19 29–­36
Na/K ratio 121 30.1 2.9 30 22 37 0.04 NG NP 24.1 36 22–­26 35–­37
Urea nitrogen mmol/L 121 7.1 2.3 7.1 2.5 12.5 0.206 G NP 2.5 11.8 2.5–­3.8 10.4–­12.5
Creatinine μmol/L 121 70.7 17.7 70.7 44.2 97.4 <0.001 NG NP 44.2 97.2 44.2–­4 4.2 88.4–­97.2
Calcium mmol/L 121 2.6 0.2 2.6 1.8 2.9 <0.001 NG NP 2.0 2.9 1.8–­2.3 2.9–­2.9
Phosphorus mmol/L 121 1.9 0.5 1.9 0.9 3.1 0.1 G NP 1.1 3.1 0.9–­1.2 2.7–­3.13
Magnesium mmol/L 121 0.9 0.1 0.9 0.7 1.2 0.00 NG NP 0.7 1.0 0.7–­10.7 1.0–­1.2
Total protein g/L 120 71 6.0 70 59 86 0.266 G NP 60 82 59–­61 80–­86
Albumin g/L 121 37 4.0 38 25 45 0.02 NG NP 29 43 25–­31 43–­45
Globulin g/L 120 33 7.0 33 22 51 0.005 NG NP 22 50 22–­23 45–­51
A/G ratio 120 1.2 0.3 1.1 0.5 1.9 <0.001 NG NP 0.7 1.8 0.5–­0.7 1.7–­1.9
Glucose mmol/L 121 3.8 0.6 3.7 2.2 6.3 0.01 NG NP 2.7 5.3 2.2–­2.9 5.1–­6.3
AST U/L 119 124 32.3 123 69 242 0.017 NG NP 71 206 69–­78 190–­242
SDH U/L 119 24.6 17.7 20 7 109 <0.001 NG NP 7 80 7–­9 72–­109
GLDH U/L 119 20.7 15.9 15 0 207 N/A N/A N/A N/A N/A N/A N/A
GGT U/L 119 48.2 15.6 48 0 97 0.001 NG NP 20 86 0–­28 77–­97
Bilirubin μmol/L 121 1.7 0.09 0 0 3.42 <0.000 NG NP 0 1.7 0–­0 1.7–­3.4
Indirect μmol/L 121 1.7 0.09 0 0 3.42 <0.000 NG NP 0 1.7 0–­0 1.7–­3.4
bilirubin
Direct bilirubin μmol/L 121 0 0 0 0 0 N/A N/A N/A 0 0 0–­0 0–­0
CK U/L 114 216 181.4 162 69 958 <0.001 NG NP 74 931 69–­8 4 666–­958
Iron μmol/L 121 29.4 8.5 29.2 7.9 61.9 0.0 NG NP 16.3 53.0 7.9–­18.6 43.5–­61.6
TIBC μmol/L 121 64.2 10.9 65.3 26.1 91.5 0.06 G NP 43.3 88.1 26.1–­47.3 82.0–­91.47
% Saturation % 121 46 12.2 45 11 92 <0.001 NG NP 25 82 11–­29 64–­92

Abbreviations: A/G Ratio, albumin/globulin ratio; AST, aspartate aminotransferase; CI, 90% confidence interval; CK, creatine kinase; Dist, Distribution; G, Gaussian; GGT, gamma-­glutamyl transferase;
GLDH, glutamate dehydrogenase; LRL, lower reference limit; N/A, not applicable; Na/K Ratio, sodium/potassium ratio; NG, non-­Gaussian; NP, nonparametric; RI, reference interval; SDH, sorbitol
dehydrogenase; TIBC, total iron-­binding capacity; URL, upper reference limit.
*Anderson-­Darling, <0.05 indicates non-­Gaussian distribution.
|
123
124 | FRYE et al.
F I G U R E 1 Box plot of GLDH results (U/(L) showing a significant
right tail skew of accepted data (gray circles), suspect data (orange
Xs), and outlier data (red asterisks)
4 | DISCUSSION
Haemonchus contortus infection is a common problem in sheep, and
moderate to marked parasite burdens often produce anemia. By per-
forming both a FAMACHA score and a fecal egg count with HEGG,
a higher parasite burden of blood-­sucking H. contortus adults were
accounted for, even if they were intermittently shedding eggs. No
sheep were excluded from the study based on fecal results. Two ani-
mals did not have sufficient feces for flotation, but their hematocrits
were both 39%, higher than the mean hematocrit, indicating a lack
of clinically significant Haemonchus contortus parasite burdens. Of
the 119 fecal samples analyzed, only two sheep had moderate total
parasite burdens (strongyle egg counts greater than 1000). These
sheep had positive HEGG results of 1300 and 1200 eggs/g, consid-
ered a light burden of H. contortus,13 and hematocrits of 31% and
29%, neither of which was identified as an outlier during reference
interval determination.
Samples for this study were collected from multiple sexes and
breeds of sheep kept under various housing and feeding conditions
across several US States throughout an entire calendar year. This
variety was specifically sought to generate RIs representative of the
varied population and sampling conditions encountered by most small
ruminant veterinarians. No attempt was made to partition the data.
This lack of partitioning may have produced wider RIs than could oth-
erwise be obtained, but the goal was to obtain RIs that would apply to
a variety of adult sheep. In addition, partitioning would have reduced
sample size and confidence in any RIs generated.
Besides the platelet and CK errors noted above (both common
preanalytical errors), very few outliers were identified, and statis-
tically acceptable RIs were obtained for most analytes. However,
GLDH had a wider range of results with a significant right-­t ail skew.
A nonparametric reference interval generated from these data did
not represent 95% of the population and had an upper limit CI wider
than the reference interval itself. Parametric and robust methods,
using raw and transformed data, were also unacceptable. Additional
outlier removal was considered but could not be justified based on
clinical, hematologic, or biochemical findings. Satisfactory reference
intervals could not be produced from these data, so the GLDH re-
sults have been reported as basic statistics only.
GLDH is an uncommon analyte so typically not included in pub-
lished reference interval studies of sheep. Only two other ovine
GLDH RIs were found, and their ranges, 0–­20 and 0–­25 U/L, are
noticeably different from those of our study. 2,14 The methodology
associated with the first RI is uncertain, while the instrumentation
associated with the second is the same as our laboratory. The sig-
nificance of our GLDH results is uncertain, and its variability could
be a common finding amongst healthy sheep. There was no obvious
correlation with patient age, sex, pregnancy status, BCS, or farm
of origin. Subclinical hepatocellular injury or lipidosis is a possible
explanation, but most outliers were isolated findings in apparently
healthy sheep, and there was no pattern of abnormalities to further
suggest liver disease. Preanalytical or analytical error is also a possi-
ble explanation. No significant errors or interferences are known for
GLDH measurements that would produce these increases in healthy
sheep, but stability and dilution studies have not been performed in
this species.
These RIs are provided to assist small ruminant veterinarians
with the interpretation of sheep CBC and biochemistry panel re-
sults. Additional GLDH results from healthy sheep, including stabil-
ity studies, might be warranted to determine the significance of the
outlier results.
AC K N OW L E D G M E N T S
The authors thank Dr. Mary Smith, Cornell University College
of Veterinary Medicine, Dr. Meghan Flanagan, Annabessacook
Veterinary Clinic, Dr. Christina Watts, Starland Veterinary Services,
Dr. Kathy Baxendell, Groton City Animal Hospital, Dr. Julie Hurley,
New England Ovis, Dr. Jean Feldman, and Dr. Scott Blond for their
sample collection.
ORCID
Elisha A. Frye https://orcid.org/0000-0002-7784-6771
Erica L. Behling-­Kelly https://orcid.org/0000-0001-9189-4238
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How to cite this article: Frye EA, Behling-­Kelly EL, Lejuene M
& Webb JL. Complete blood count and biochemistry
reference intervals for healthy adult sheep in the
northeastern United States. Vet Clin Pathol. 2022;51:119–
125. doi: 10.1111/vcp.13059