Evaluation of plasma fibrinogen concentration as an indicator of physeal or epiphyseal osteomyelitis in foals: 17 cases (2002–2007)

Jennifer M. Newquist Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.

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Gary M. Baxter Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.

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Abstract

Objective—To determine whether high plasma fibrinogen concentration (≥ 900 mg/dL) is a valid indicator of physeal or epiphyseal osteomyelitis in foals.

Design—Retrospective case series.

Animals—17 foals with physeal or epiphyseal osteomyelitis with or without septic arthritis, 17 foals with septic arthritis alone, 20 foals with non–Rhodococcus equi pneumonia, and 22 healthy foals.

Procedures—Medical records were reviewed for information regarding signalment and total WBC count, segmented neutrophil count, and plasma fibrinogen concentration measured when foals were initially evaluated at the hospital. Whether the foals survived to discharge from the hospital was also determined.

Results—Foals with physeal or epiphyseal osteomyelitis had higher plasma fibrinogen concentrations than did foals in the other 3 groups. Sixteen of 17 affected foals had values ≥ 900 mg/dL. The positive predictive and negative predictive values for plasma fibrinogen concentrations between 900 and 1,500 mg/dL as an indicator of osteomyelitis were 84.2% and 98.2%, respectively. Fibrinogen concentrations of 200 to 400 mg/dL and 500 to 800 mg/dL were associated with foals not having physeal osteomyelitis. Having septic arthritis alone or non–R equi pneumonia was significantly associated with a plasma fibrinogen concentration between 500 and 800 mg/dL; however, the positive predictive value of this range as an indicator of those diseases was low. Foals with osteomyelitis had greater total WBC and segmented neutrophil counts than did foals with septic arthritis alone.

Conclusions and Clinical Relevance—A plasma fibrinogen concentration of ≥ 900 mg/dL may be useful as an indicator of physeal or epiphyseal osteomyelitis in foals.

Abstract

Objective—To determine whether high plasma fibrinogen concentration (≥ 900 mg/dL) is a valid indicator of physeal or epiphyseal osteomyelitis in foals.

Design—Retrospective case series.

Animals—17 foals with physeal or epiphyseal osteomyelitis with or without septic arthritis, 17 foals with septic arthritis alone, 20 foals with non–Rhodococcus equi pneumonia, and 22 healthy foals.

Procedures—Medical records were reviewed for information regarding signalment and total WBC count, segmented neutrophil count, and plasma fibrinogen concentration measured when foals were initially evaluated at the hospital. Whether the foals survived to discharge from the hospital was also determined.

Results—Foals with physeal or epiphyseal osteomyelitis had higher plasma fibrinogen concentrations than did foals in the other 3 groups. Sixteen of 17 affected foals had values ≥ 900 mg/dL. The positive predictive and negative predictive values for plasma fibrinogen concentrations between 900 and 1,500 mg/dL as an indicator of osteomyelitis were 84.2% and 98.2%, respectively. Fibrinogen concentrations of 200 to 400 mg/dL and 500 to 800 mg/dL were associated with foals not having physeal osteomyelitis. Having septic arthritis alone or non–R equi pneumonia was significantly associated with a plasma fibrinogen concentration between 500 and 800 mg/dL; however, the positive predictive value of this range as an indicator of those diseases was low. Foals with osteomyelitis had greater total WBC and segmented neutrophil counts than did foals with septic arthritis alone.

Conclusions and Clinical Relevance—A plasma fibrinogen concentration of ≥ 900 mg/dL may be useful as an indicator of physeal or epiphyseal osteomyelitis in foals.

Septicemia and its secondary complications remain a common clinical problem in neonatal foals. In fact, septicemia is reportedly the second most common problem in neonatal foals < 14 days of age, second only to colostral insufficiency.1 The septicemic state may be preceded by omphalitis, pneumonia, enteritis, or other forms of systemic illness. Partial or complete failure of passive transfer of maternal antibodies is the most common predisposing factor.2,3 Results of a retrospective study4 of foals with septic arthritis indicated that 88% (30/34) of foals for which serum IgG concentrations were available had partial or complete failure of passive transfer.

Septic arthritis and osteomyelitis are often sequels to septicemia in foals.2,4,5 In some circumstances, the inciting systemic illness may not be clinically apparent.2,5 Septic arthritis or osteomyelitis may be classified according to the location of the lesions, with S-type involving the synovium or joint, E-type involving the epiphysis, and P-type involving the physis.2 Septic arthritis (S-type) is most common, but a combination of types may develop in the same foal. For example, results of 1 study4 indicated that 33% of 78 foals with septic arthritis also had osteomyelitis.

As with septicemia, septic arthritis and physeal or epiphyseal osteomyelitis are important problems in foals because they often result in a guarded prognosis, increase the degree of illness and risk of death, and can result in a decrease in quality of athletic performance. In a retrospective study6 that included 66 foals with septic arthritis, only 45% survived to discharge from the hospital and 52% had associated osteomyelitis. In another study7 involving Thoroughbred foals with septic arthritis, investigators found that only 48.3% of foals successfully treated for septic arthritis subsequently started at least 1 race, compared with 66.2% of foals without septic arthritis from the same dam. Results from a third study4 indicated that 26% of 78 foals affected with septic arthritis developed degenerative joint disease.

The diagnosis of septic arthritis in foals is often straightforward because most foals develop joint effusion that is easily palpable and lameness. Arthrocentesis typically reveals a high WBC count and high total protein concentration in the synovial fluid, which are findings suggestive of infection.5 However, bacteriologic culture of synovial fluid samples from joints with suspected infection yields positive results for only 64% of samples, even though infection likely exists.8

Physeal osteomyelitis with or without joint involvement is much more challenging to diagnose in foals. The acute onset of lameness associated with osteomyelitis in foals can be misinterpreted by owners as a traumatic injury not requiring aggressive treatment. No joint effusion or limb swelling may be palpable because the infection is confined to the physis, and radiographic changes may not be apparent at the time of initial evaluation but often develop 1 to 2 weeks later.8 A screening test to identify foals with physeal or epiphyseal osteomyelitis in the early stage of the disease or to indicate whether foals with septic arthritis may also have osteomyelitis would be a helpful diagnostic tool.

In our experience, foals with physeal or epiphyseal osteomyelitis have a marked increase in plasma fibrinogen concentration. Fibrinogen, an indicator of nonspecific inflammation in horses, is an acutephase protein produced by hepatocytes in response to proinflammatory mediators released early in the innate immune response.9 For veterinary clinicians, the ability to use plasma fibrinogen concentration to detect physeal or epiphyseal osteomyelitis in foals would help determine the prognosis of foals suspected of having the disease and whether more aggressive treatment or diagnostics may be necessary. However, to our knowledge, no studies have been conducted to evaluate high plasma fibrinogen concentration as a specific indicator of physeal or epiphyseal osteomyelitis in foals. The purpose of the study reported here was to evaluate whether high plasma fibrinogen concentration (≥ 900 mg/dL) is a valid indicator of physeal or epiphyseal osteomyelitis in foals. Our hypothesis was that the fibrinogen concentration would be significantly higher in foals with physeal or epiphyseal osteomyelitis than in healthy foals and foals with other infectious conditions.

Materials and Methods

Case selection—The medical records of foals < 4 months of age that were treated at the Colorado State University Veterinary Teaching Hospital from January 1, 2000, to August 15, 2007, were examined. Selected foals were categorized into 1 of 4 groups. Group 1 consisted of foals with physeal or epiphyseal osteomyelitis, with or without septic arthritis, that had been diagnosed radiographically via identification of bone demineralization within the epiphysis or physis that was consistent with infection. Group 2 consisted of foals with septic arthritis that had been diagnosed via cytologic evaluation of synovial fluid (ie, high total protein concentration and high WBC count, with neutrophils as the predominant cell type) and had no radiographic abnormalities within the affected joint or joints throughout the arthritic state. Group 3 included foals with non–Rhodococcus equi pneumonia that was confirmed via lack of characteristic radiographic changes associated with R equi pneumonia, isolation of other pathogens (mostly streptococci) from transtracheal wash samples, or both. Group 4 consisted of healthy foals that were admitted to the hospital for surgical correction of angular limb deformities.

Medical records review—Data collected from the medical records included age, sex, and breed of foal as well as discharge status (discharged or euthanatized). Total WBC and neutrophil counts and plasma fibrinogen concentration were measured in blood samples obtained when horses were initially evaluated at the hospital, and these data were also collected. At that time, plasma fibrinogen concentrations of all foals were determined by means of the heat precipitation method.10,11 Blood samples were collected via jugular venipuncture into tubes containing EDTA, plasma was harvested, and plasma total protein concentration was measured with a refractometer.a Plasma samples were subsequently heated to 56°C in a hot water bath or dry heater block for 3 to 10 minutes and recentrifuged, and plasma total protein concentrations were remeasured. The difference in these plasma concentrations was considered the fibrinogen concentration (mg/dL). Total WBC counts were determined by use of an automated hematologic system,b and cell differentials were estimated using results from 100 manual cell counts. Only foals for which all of the aforementioned information was available were included in the study.

Statistical analysis—For statistical purposes, data regarding plasma fibrinogen concentrations were classified into 3 categories: 200 to 400 mg/dL, 500 to 800 mg/dL, and ≥ 900 mg/dL. To evaluate the probabilities of each of the 4 groups of foals having a positive test result for each category (ie, a fibrinogen concentration that was included in the category range), PPVs and 95% CIs were calculated. To evaluate the probabilities of each of the 4 groups of foals having a negative test result for each category (ie, a fibrinogen concentration that was not included in the category range), NPVs and 95% CIs were calculated.

For statistical analysis, foal age was classified into 2 categories (≤ 60 days and > 60 days). Discharge status was classified as either euthanatized or discharged from the hospital. Associations of fibrinogen category with foal group, breed, sex, age, and discharge status were evaluated by use of the Pearson χ2 test. A Fisher exact test was used when any cell in the 2 × 2 contingency table contained ≤ 5 observations. Nonparametric ANOVA (Wilcoxon) analysis was performed to evaluate associations between the mean age score of the 4 groups. Data were then stratified by age to evaluate associations between foal group and fibrinogen category by use of the Mantel-Haenszel χ2 test. Associations between WBC and segmented neutrophil counts and fibrinogen category were evaluated via linear regression analysis with a generalized estimating equation method.c Survival to discharge was compared among foals in various fibrinogen categories by means of logistic regression analysis.c Statistical softwared was used for all analyses. Results were considered significant at values of P < 0.05.

Results

Seventy-six foals were included in the study. There were 17 foals each in groups 1 (physeal or epiphyseal osteomyelitis, with or without septic arthritis) and 2 (septic arthritis alone), 20 foals in group 3 (non–R equi pneumonia), and 22 foals in group 4 (healthy). All foals were between 1 and 119 days of age (mean, 42.9 days; median, 34 days). Characteristics of groups of foals were statistically summarized (Table 1). There were 35 fillies, 40 colts, and 1 castrated male. Breeds included Quarter Horse (n = 42), American Paint (9), Thoroughbred (6), Morgan (3), Warmblood breeds (3), Appaloosa (2), Arabian (2), and 1 each of various other breeds. Distributions of breeds and sexes did not differ significantly among the 4 groups. Results of ANOVA indicated that the foals in groups 1 and 2 were significantly (P < 0.001) younger than those in groups 3 and 4. However, the Mantel-Hansel analysis in which the variable age was controlled for revealed that the overall association between foal group and plasma fibrinogen category was significant (P < 0.001) and the associations between each age group and plasma fibrinogen category were significant (foals ≤ 60 days old, P < 0.001; foals > 60 days old, P < 0.001).

Table 1—

Age and hematologic characteristics of foals with physeal or epiphyseal osteomyelitis, with or without septic arthritis (group 1); foals with septic arthritis without osteomyelitis (group 2); foals with non–Rhodococcus equi pneumonia (group 3); and healthy foals (group 4) admitted to a veterinary teaching hospital.

GroupNo. of foalsSurvival (%)Age (d)Plasma fibrinogen concentration (mg/dL)WBC count (× 103 cells/μL)Segmented neutrophil count (× 103 cells/μL)
MeanSDMedianMedianRangeMeanSDRangeMeanSDRange
11735a32.1a27.421a1,100a700–1,50018.16a5.1610.1–29.614.78a5.197.5–27.8
21759a17.53a27.77a700b200–1,00010.19b,c5.522.2–22.28.09b,c5.261.2–21.1
32090b63.8b33.061b600b300–80014.86b5.705.5–28.511.06b4.763.2–20.0
422100c52.0b25.645b350c200–5009.55c2.475.1–15.06.37c2.012.7–10.0

Survival represents the proportion of foals that survived to discharge from the hospital.

Values within the same column with different superscript letters are significantly (P < 0.05) different.

Having osteomyelitis was significantly (P < 0.001) associated with a plasma fibrinogen concentration of ≥ 900 mg/dL (Table 2). The PPV and NPV of detecting a plasma fibrinogen concentration of ≥ 900 mg/dL in a foal with osteomyelitis were 84.21% and 98.25%, respectively. Plasma fibrinogen concentrations in the ranges of 200 to 400 mg/dL and 500 to 800 mg/dL were associated with foals not having osteomyelitis (P < 0.001 and P = 0.01, respectively). Plasma fibrinogen concentrations in the range of 500 to 800 mg/dL were significantly associated with foals having septic arthritis alone (P = 0.03) or pneumonia (P < 0.001). However, the PPV of this range for identifying foals with septic arthritis alone was poor (15.8%). Being healthy was significantly associated with a fibrinogen concentration in the range of 200 to 400 mg/dL (reference range, 100 to 400 mg/dL). The PPV and NPV of this range for identifying healthy foals were 63.6% and 97.7%, respectively.

Table 2—

Positive predictive values and NPVs of fibrinogen concentration range as an indicator of osteomyelitis (group 1), septic arthritis (group 2), non–R equi pneumonia (group 3), or health (group 4) in foals evaluated at a veterinary teaching hospital.

GroupNo. of foalsFibrinogen concentration (mg/dL)PPVNPVP value
Estimate (%)95% CIEstimate (%)95% CI
10200–4000060.4744.45–74.63< 0.001
1500–8004.170.22–23.1269.2354.74–80.880.01
16900–1,50084.2159.51–95.8398.2589.37–99.91< 0.001*
25200–40015.155.72–32.6772.0956.10–84.170.19
9500–80037.519.55–59.2484.6271.37–92.660.03
3900–1,50015.794.17–40.4975.4461.96–85.470.54
37200–40021.219.63–39.469.7753.70–82.330.38
13500–80054.1733.24–3.8386.5473.60–93.97< 0.001
0900–1,5000064.9151.06–76.760.003
421200–40063.6445.14–79.0497.6786.20–99.88< 0.001
1500–8004.170.22–23.1259.6245.13–72.690.001
0900–1,5000061.4047.56–73.710.001

Reported P value indicates the significance of association between fibrinogen concentration range and group.

Fisher exact P value.

Foals with osteomyelitis also had a higher total WBC count than did foals with septic arthritis alone (P < 0.001) or pneumonia (P = 0.03; Table 1). Those with osteomyelitis and those with pneumonia also had a higher WBC count than did healthy foals (P < 0.001 for both comparisons), but the WBC count did not differ between healthy foals and those with septic arthritis alone (P = 0.68). Foals with osteomyelitis also had a significantly greater segmented neutrophil count than did foals with septic arthritis alone (P < 0.001) or pneumonia (P = 0.008), but the segmented neutrophil counts did not differ between healthy foals and those with septic arthritis alone (P = 0.23).

Of the 76 foals included in the study, 20 (26%) were euthanatized and 56 (74%) were discharged from the hospital. Eleven of the 17 foals with osteomyelitis, 7 of the 17 foals with septic arthritis alone, and 2 of the 20 foals with pneumonia were euthanatized; none of the 22 healthy foals were euthanatized. There was no significant (P = 0.17) difference in distributions of foals that survived to discharge between groups 1 and 2 (OR, 2.6; 95% CI, 0.53 to 13.45). In general, foals with osteomyelitis were 2.6 times as likely to be euthanatized as foals with septic arthritis alone (95% CI, 0.53 to 13.45; P = 0.17) and 16.5 times as likely to be euthanatized as foals with pneumonia (95% CI, 2.3 to 151.3; P < 0.001).

Discussion

Traditionally, radiographs and results of synovial fluid analysis are heavily relied upon to aid in the diagnosis of septic arthritis and associated osteomyelitis in horses.2,5,8 However, radiography is a somewhat insensitive means of detecting osteomyelitis in foals, and the disease can be misdiagnosed in the early stages. A screening test to help identify foals with physeal or epiphyseal osteomyelitis may be helpful when determining whether additional diagnostic tests or treatments are indicated. According to the results of the present study, secondary physeal or epiphyseal osteomyelitis should be suspected in foals with septic arthritis that have a plasma fibrinogen concentration ≥ 900 mg/dL. In addition, any lame foal with a fibrinogen concentration ≥ 900 mg/dL should be closely evaluated for physeal or epiphyseal osteomyelitis, even when no limb or joint swelling is evident. Evaluation of plasma fibrinogen concentration is fast, inexpensive, requires only 1 blood sample, and should be performed in all foals with musculoskeletal abnormalities to help rule out the possibility of physeal or epiphyseal osteomyelitis.

The primary exception to using an increase in fibrinogen concentration as an indicator of physeal or epiphyseal osteomyelitis is in foals with R equi pneumonia. Hyperfibrinogenemia is the most consistent laboratory finding in foals with R equi pneumonia.12 In a study13 of foals with confirmed R equi pneumonia, mean plasma fibrinogen concentrations were reportedly 756 ± 236 μg/dL and 863 ± 227 μg/dL in foals that did and did not survive to discharge from the hospital, respectively.13 This characteristic increase in plasma fibrinogen concentration would make measurement of fibrinogen a less reliable test to help diagnose physeal or epiphyseal osteomyelitis in foals suspected of having R equi pneumonia. However, rhodococcal pneumonia is easily diagnosed by characteristic radiographic changes in the lung fields, including alveolar patterns of regional consolidation and signs of abscess formation. Foals affected with R equi pneumonia typically have signs of tachypnea, increased respiratory effort, and fever, which are not typical of foals affected with osteomyelitis alone but are common in foals with pneumonia.12 Because of the ease by which foals with R equi pneumonia could be distinguished from foals with other types of pneumonia, we believed exclusion of these foals from our study would be minimally detrimental to assessing the usefulness of high plasma fibrinogen concentration as an indicator of physeal or epiphyseal osteomyelitis.

Foals with multisystemic disease were also excluded from the present study because septic foals may have multiple body systems affected, with pneumonia and enteritis as the most common sequelae. In a study3 of septic foals, 50% had respiratory disease whereas 38% had enteritis. In the present study, foals with non–R equi pneumonia were the only foals with systemic illness evaluated. Foals with concurrent enteritis or enteritis alone were not evaluated, and exclusion of such foals may have affected the specificity of plasma fibrinogen concentration as an indicator of osteomyelitis.

In neonatal foals, hemostatic indices are variable. Data from a 1995 study14 in which hemostatic indices in healthy foals were evaluated indicated that the mean plasma fibrinogen concentration was significantly lower in foals at 24 hours of age than in older foals and adult horses; however, by 1 week of age, the plasma fibrinogen concentration was statistically equivalent to that of mature horses. A significant difference between the mean ages of foals in the 4 groups was detected in the present study; however, an analysis in which the variable age was controlled for revealed that the overall association between foal group and plasma fibrinogen category was significant. The difference in age among the groups was not unexpected because one would expect that foals with pneumonia and those undergoing surgery for angular limb deformities would be older than foals with septic arthritis or physeal or epiphyseal osteomyelitis.

Foals with osteomyelitis or pneumonia had significantly higher WBC and segmented neutrophil counts than did healthy foals, and having osteomyelitis was significantly associated with higher WBC and segmented neutrophil counts, compared with values in foals with septic arthritis alone or pneumonia. Leukocytosis and neutrophilia are nonspecific indicators of inflammation that may develop with infection or inflammation in any part of the body, and like high plasma fibrinogen concentration, these characteristics suggested the presence of osteomyelitis in affected foals. However, the degree of increase in neutrophil count does not necessarily correlate with the degree of inflammation or infection because it depends upon the balance between production of neutrophils by bone marrow and distribution of neutrophils within tissues.9 Many foals with septic arthritis and concurrent septicemia are actually neutropenic. In a study4 of foals with septic arthritis, 6 of 42 (14%) foals were neutropenic, 21 (50%) were neutrophilic, and 15 (36%) had segmented neutrophil counts within the reference range. The variability in WBC and segmented neutrophil counts in foals with septic arthritis was not evident in the foals with osteomyelitis in our study, and this lack of variability may explain the significant increase in WBC and segmented neutrophil counts in the foals with osteomyelitis. Alternatively, the significant increase in WBC and segmented neutrophil counts may have reflected a more severe infection associated with osteomyelitis, compared with the infection associated with septic arthritis alone.

The percentage of foals with septic arthritis alone that survived to discharge from the hospital in the present study (59%) was similar to percentages in other reports (eg, 62%6 and 57%15). High proportions of surviving foals (78%4 and 84.1%7) were reported for 2 studies, and these high values were attributed to early recognition and treatment of septic arthritis. In a study16 of foals with septic osteomyelitis, 80.6% of affected foals survived to discharge from the hospital and 44.4% went on to official race starts. Those proportions are all higher than the proportion of foals with osteomyelitis that survived to discharge in the present study (35%). The lower proportion in our study might have been attributable to the severity and location of the infection, the existence of other concurrent illnesses, or the financial constraints of owners. Most foal owners in the present study originated from small farm operations that did not have established protocols for foal management.

The results of the study reported here supported the use of high plasma fibrinogen concentration as a predictor of physeal or epiphyseal osteomyelitis in foals. Specifically, when the concentrations are ≥ 900 mg/dL, osteomyelitis should be suspected in neonatal foals. Plasma fibrinogen concentrations within the range of 500 to 800 mg/dL were associated with septic arthritis alone or systemic infection (pneumonia) but should not be used as a definitive diagnostic test because of the low PPVs associated with this range in those foal groups.

ABBREVIATIONS

CI

Confidence interval

NPV

Negative predictive value

OR

Odds ratio

PPV

Positive predictive value

a.

Reichert TS Meter, Fisher Scientific, Pittsburgh, Pa.

b.

Advia 120 Hematology System, Siemens Corp, New York, NY.

c.

PROC GENMOD, SAS, version 9.1, SAS Institute Inc, Cary, NC.

d.

SAS, version 9.1, SAS Institute Inc, Cary, NC.

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