Journal of Clinical LaboratoryAnalysis 5:168-174 (1991)

Diagnostic Value of Lactate Dehydrogenase lsoenzymes in Cerebrospinal Fluid Scott Chatterley, Tsieh Sun, and York Lien Department of Laboratories, North Shore University Hospital-Cornell University Medical College, Manhasset, New York To evaluate the diagnostic value of lactate dehydrogenase (LD) isoenzymes in cerebrospinal fluid (CSF), 93 consecutive CSF specimens were analyzed. These specimens were from patients of four categories: tumors, infections, hemorrhages, and others. It was found that the isoenzyme patterns overlapped among different categories, but they differed within each category and were thus helpful in differentialdiagnosis. For instance, metastatic tumors showed prominent LD-5, whereas a primary brain tumor demonstrated an increase in all fractions. Viral encephalitis revealed an increase in the first three isoenzymes and bacterial meningitis, the last two. In acquired immune deficiency syndrome (AIDS) cases, Key words:

CSF proteins, central nervous system diseases, LD isoenzymes

INTRODUCTION In recent years, the measurement of lactate dehydrogenase (LD) isoenzymes in cerebrospinal fluid (CSF) has been used to detect subclinical leptomeningeal infiltration by carcinoma (1-10). The most consistent finding in this setting is an elevation of the LD isoenzyme-5 (LD-5) and an alteration of the LD-1:LD-5 ratio (5,8,10). Abnormal elevation of LD has also been described in patients with primary malignant brain tumors ( 1 1-18), cerebral infarction (7,12,14,15), infections (7,10,19-25), neonatal hypoxia (26), and acute brain injury (7,12,27). This study covers a broad spectrum of various diseases, with four cases presented to illustrate the LD isoenzyme patterns under some special situations. The findings in some diseases, such as acquired immune deficiency syndrome (AIDS), have not been reported before. Our studies also reveal that elevation of LD-5 in CSF is not necessarily present in cases of metastatic carcinoma to the leptomeninges and brain.

MATERIALS AND METHODS Patients A series of 93 consecutive CSF specimens were analyzed for LD isoenzymes by electrophoresis' The 'pecimens were obtained from patients with metastatic tumor to the brain and leptomeninges (17 cases) as proven by positive CSF cytol0 1991 Wiley-Liss, Inc.

however, LD isoenzyme changes were demonstrated in CSF when only cryptococcal meningitis and not when encephalitis was present. Both subdural and subarachnoid hemorrhages showed elevation of all fractions in our study. Elevation of the first three fractions was usually due to brain tissue damage or hemorrhage, as proven by our isoenzyme study of hemolysate mixed with CSF. The prominence of the last two fractions was related to anaerobic metabolism in the central nervous system or to granulocytic infiltration. In conclusion, LD isoenzyme analysis in CSF is helpful in differential diagnosis of various CNS disorders, although its sensitivity awaits further improvement.

ogy, surgical biopsy, or autopsy, primary brain tumor (four cases), subdural hematoma (two cases), subarachnoid hemorrhage (two cases), bacterial meningitis (15 cases), viral encephalitis (two cases), AIDS (12 cases), and various other disorders (39 cases) (Table I). Twenty specimens from patients who eventually showed no organic disease in the brain and no biochemical abnormalities in CSF were used as controls. LD isoenzyme analysis was also performed on a mixture of hemolysate and normal CSF (1 :9) to determine the effect of hemorrhage in the CSF on the isoenzyme pattern.

LD lsoenzyme Analysis of CSF CSF was obtained by lumbar puncture or via a subcutaneous reservoir attached to a ventricular cannula placed in the lateral cerebral ventricle. CSF analysis included measurement of protein by the Coomassie brilliant blue (CBB)dye binding methods and glucose by the hexokinase methods and bacterial culture and cytologic examination of centrifuged specimens when clinically indicated. With sufficient sample, Received September 18, 1990; accepted December 3, I990 This paper was presented as an abstract at the American Society of Clinical pathologists Meeting In Sari Francisco, March, 1990. Address reprint requests to Dr. T. Sun, Department of Laboratories, North Shore University Hospital-Come11 University Medical College, Manhasset, NY 11030.

LD isoenzymes in CSF

169

TABLE 1. Patient Characteristics Clinical diagnosis

Number of cases

Number of cases with abnormal patterns

Metastatic tumor to leptomeningesi brain (clinical suspicion, positive cytology or positive radiology) Primary brain tumor Encephalitis (Viral) Bacterial meningitis AIDS Subdural hematoma Subarachnoid hemorrhage Multiple sclerosis Herniated discispinal stenosis Alcohol withdrawal Other

4 2 15 12 2 2 3 4 14

4 I 2 2 5 2 1 0 2 0 0

Total

93

19

17

18

the specimens were concentrated 10-20-fold by the Minicon concentrator ( - A25) (Amicon Division, WRGraceCo., Danvers, MA). Separation of the LD isoenzymes was performed by electrophoresis on Universal agarose film (Ciba Coming, Palo Alto, CA) at 100 V for 30 min using 0.05 M barbital buffer. The resulting isoenzyme bands were stained with nitroblue tetrazolium chloride (NBT) and quantified by scanning. Total LD was measured in 20 specimens by the spectrophotometric technique (COBAS-BIO).

RESULTS In the 20 control specimens, the total LD ranged from 1.23 to 12.97 U/liter. When the isoenzyme pattern was prominent or abnormal, the total LD was consistently elevated. Therefore, total LD was not quantified in every specimen. The LD isoenzyme patterns in normal controls showed low intensity of LD-1, LD-2, and LD-3 in descending order and negligible quantities of LD-4 and LD-5 (Fig. 1). The normal ranges we used for LD isoenzymes were LD- 1 27.2% -t 1.1%, LD-2 27% 2 0.9%, LD-3 23.8% 2 0.8%, LD-4 17.6% 2 1.5%, and LD-5 2.4% ? 0.8% (8). In CSFmixed with hemolysate, LD- 1, LD-2, and LD-3 became prominent and far exceeded the normal percentages.

Prominent fractions

5 1-5

1-3 4 s Variable 1-5 1-5

LDI:LD5

.1

Normal or slightly 1

t

1 Variable

1

I

-

-

1-3

Traumatic tap (hemolysis)

-

-

-

ognized. One AIDS patient with cytomegalovirus (CMV) retinitis also showed abnormal LD isoenzyme pattern. The remaining six AIDS cases did not show any abnormal pattern regardless of the changes in CSF components.

Hemorrhage In cases of hemorrhage in the central nervous system (CNS), which included two cases of subdural hematoma and two cases of subarachnoid hemorrhage, abnormal patterns were seen in three of the four patients. Both patients with subdural hematoma had a marked increase in all fractions, and one of the two patients with subarachnoid hemorrhage also had an increase in all isoenzyme fractions.

Tumors In the group of tumor patients, only four of the 17 cases of metastatic tumor showed elevation of LD-5 above 9% with a decrease in the LD-l:LD-5 ratio to below 2.5, fulfilling the criteria for metastatic tumors to the leptomeninges and brain established previously (Table 1) (8). One of the four cases of primary brain tumor revealed an increase in all isoenzyme

Infections Two of 25 cases of bacterial meningitis showed significant elevations of LD-4 and LD-5, with a decrease in the LD-1: LD-5 ratio. Two of two patients with viral encephalitis had increased LD-1, LD-2, and LD-3 isoenzymes. In addition, 12 patients with AIDS were studied. Total protein, glucose, leukocyte, and erythrocyte counts in the CSF were examined to determine if the LD isoenzyme distribution was affected by a certain component. Clinical and laboratory data are summarized in Table 2. Of five patients with cryptococcal meningitis, four showed abnormal distribution of LD isoenzymes; however, a common pattern was not rec-

Fig. 1. LD isoenzyme pattern of normal CSF control, showing low intensity of LD-I , LD-2, and LD-3 in descending order and negligible quantities of LD-4 and LD-5.

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TABLE 2. LD Isoenzyme Patterns of HIV-Positive Patients Patient 1

2 3 4 5 6

7 8 9 10 11

12

Clinical diagnosis RiO meningitis Cryptococcal meningitis Cryptococcal meningitis HIV Encephalopathy Cryptococcal meningitis Severe headache, fever, chills HIV Encephalopathy, seizures RiO myelopathy lethargy Lymphoma (abdominal), cranial neuropathy Cryptococcal meningitis HIV encephalopathy, CMV retinitis Cryptococcal meningitis

Age (years)

Sex

Total protein

36 50 27 29 37

M M M F M

39 68 70 41 13

-

25

M

32 38

(mgW

Glucose (mg/dl)

80 42

WBC (X

RBC

103imm3) ( X 103imm3)

LD Isoenzyme Pattern

3 0

53 48

3 0 26 144 0

0 0 0

Normal 1-3 t 3,4 Normal Normal

56

51

0

102

Normal

M M

53 45

54 43

0

4 0

Normal Normal

34 31

M M

25 62

44 50

2 0

Normal

0

29 34

F

41 304

49 I29

0 3

0 4

t 1-3.5

M

1 1

t

ti T

1-5

fractions, whereas the other three cases showed no prominent isoenzyme bands.

of LD-4 and LD-5 (Fig. 2). LD-l:LD-5 ratio was 0.13, and LD-5 was 34.5% of the total LD isoenzymes.

Others

Case 2

The CSF of three patients with multiple sclerosis was also examined. All three showed an abnormal gamma globulin content and oligoclonal banding by protein electrophoresis; LD isoenzymes appeared normal in all cases. Two cases of herniated lumbar disc showed an increase in fractions 1, 2, and 3, probably the result of traumatic tap (hemolysis). The remaining cases showed no abnormal LD isoenzyme pattern. Among 93 patient specimens, 12 cases showed detectable LD-5, which included four cases of metastatic carcinoma (two breast, two lung), one case of primary brain tumor (grade IV astrocytoma), two cases of bacterial meningitis, two cases of AIDS, two subdural hematoma cases, and one subarachnoid hemorrhage case (Table 1). LD-1:LD-5 ratios less than 2.5 were seen in all the above cases. On the other hand, 13 cases of metastatic tumor did not show a significant increase of LD-5. The following are four cases to illustrate the changes of the LD isoenzyme pattern in CSF under different situations.

A 78-year-old male presented with a history of having fallen at home. He developed weakness of his right side and became confused. Computed tomography (CT) scan revealed a large subdural hematoma, with a shift of the midline structures to the right. Lumbar puncture was performed and showed xanthochromia. The CSF contained erythrocytes 13.6 x 103/mm3,leukocytes 1,620/mm3 with 96% polymorphonuclear leukocytes, glucose 16 mg/dl(O.89 mmol/liter), and total protein of 4.7 g/dl(47 @liter). The patient underwent emergency evacuation of the hematoma, subsequently improved, and was discharged with no evidence of hemiparesis. The LD isoenzyme pattern showed a marked increase in all LD fractions, with fractions 3, 4, and 5 being the most prominent (Fig. 3). The LD-I:LD-5 ratio was 0.33, with the LD-5 fraction being 55% of the total LD isoenzymes.

Case 1 A 67-year-old female with insulin-dependent diabetes mellitus presented to the emergency room with fever, chills, diaphoresis, and low back pain, which radiated down both legs. Lumbar puncture was performed and revealed turbid fluid. The CSF contained erythrocytes 10,000/mm3, leukocytes 5,3000/mm3 with 45% polymorphonuclear leukocytes, glucose 101 mg/dl(5.60 mmol/liter), and total protein 1.22 gldl (12.2 g/liter). Bacterial cultures were positive for Staphylococcus aureus. The patient was treated with 6 weeks of vancomycin and rifampin and subsequently recovered. The LD isoenzyme pattern showed a significant elevation

Fig. 2. Case 1 . LD isoenzyme pattern in bacterial meningitis, showing a significant increase in LD-4 and LD-5.

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tumor showed an infiltrating lobular carcinoma with focal signet-ring cell features and infiltration of the overlying skin. The patient was subsequently treated with adriamycin, 5-fluorouracil, and intrathecal methotrexate. CSF was obtained on admission, showing a total protein of 0.37 g d d l (3.7 @liter), glucose 114 mg/dl(6.33 mmol/liter), and a few erythrocytes and leukocytes. Cytologic examination of the CSF was positive for malignant cells. The LD isoenzyme pattern revealed an increase in LD-5, with a 1 5 ratio of 2.0 (Fig. 5 ) . Fig. 3. Case 2. LD isoenzyme pattern in subdural hematoma, showing an increase in all fractions with a large increase in fraction 5.

Case 3 A 36-year-old female with metastatic breast carcinoma was admitted to the hospital for work-up of lumbar back pain. The patient’s past medical history was significant for a left modified radical mastectomy for infiltrating ductal carcinoma. Axillary lymph nodes were negative for metastatic carcinoma, and estrogen/progesterone receptors were also negative. She developed local recurrence 1 year later and was treated with radiotherapy and chemotherapy. The patient did well for 3 years, but subsequently developed metastatic disease to the brain and lung. Lumbar puncture was performed and revealed glucose 35 mg/dl(36 mmol/liter) and total protein 4.54 mg/dl (4,540 g/liter). Suspicious cells were seen on cytologic examination of the CSF. Myelogram and CT scans of the spinal cord revealed evidence of cord compression. The patient received radiation therapy to the spine and eight to ten courses of intrathecal methotrexate. She progressively deteriorated and suffered respiratory arrest. At autopsy, metastatic tumor was found in multiple viscera, including lungs, liver, and adrenals bilaterally. Additional secondary tumor was identified in sections of the cerebral cortex, cerebellum, and spinal cord. The leptomeninges showed extensive infiltration with involvement of the cauda equina and surrounding multiple spinal nerve roots. Microscopically the tumor was a poorly differentiated carcinoma (Fig. 4a), considered to be a second primary arising in the lung. The LD isoenzyme pattern showed prominence of LD-1, LD-2, and LD-3, with fractions 4 and 5 being only faintly detectable (Fig. 4b). The LD-1:LD-5 ratio was 2.4. LD-5 constituted 11% of the total LD isoenzymes.

Case 4 A 59-year-old female presented with progressive weakness in both lower extremities over a 1 month period. The patient also felt numbness of her toes bilaterally. Magnetic resonance imaging (MRI) revealed severe spinal stenosis, with a ventral defect. Bone scan showed diffuse blastic and lytic lesions. Chest examination demonstrated a 4 cm mass in the left breast, with cervical and axillary adenopathy. Excision of the

DISCUSSION Previous studies have shown that the determination of CSF LD and its isoenzyme distribution can be helpful in the diagnosis of various CNS diseases (5,7). Abnormal LD isoenzyme patterns can be seen in CNS infections, most notably an increase in fractions 1 and 2 in viral infections and an increase in LD-4 and LD-5 in bacterial meningitis (7,19,20, 22,25). Beaty and Oppenheimer ( 14)demonstrated increased LD activity in the CSF in 24 of 25 patients with bacterial meningitis and found a predominance of fractions 4 and 5. The bacterial species involved in meningitis including Hemophilus influenza, Escherichia coli, Klebsiellu pneumoniae, and Neisseria meningitidis, as encountered in an investigation by Nelson et al. (22), did not cause any difference in the LD isoenzyme pattern. In bacterial meningitis, the increased LD-5 is believed to result from local granulocytic infiltration (7,10,20-22,25). Extracts of granulocytes have shown a similar pattern (1 9). Cases of tuberculous meningitis have shown elevations of fractions 3 , 4 , and 5 , of which LD-3 was most predominant (20,2 1,25). The increased LD-3 was considered to be originated from lymphocytes in contact with the CSF (20). Our study demonstrated positive findings in only two of 15 cases of meningitis, suggesting that abnormal LD isoenzyme patterns appear only in heavy infections and a low sensitivity of this test for the diagnosis of meningitis. In viral encephalitis, the increase in LD-1 and LD-2 has been attributed to the presence of lymphocytes as the most probable source; however, brain tissue has also been implicated as a source for these fractions (19). It is interesting to note in our study that human immunodeficiency virus (HIV) encephalitis alone did not cause any change in the LD isoenzyme pattern in CSF. When complicated by cryptococcal meningitis, multiple LD isoenzymes became prominent, but a consistent pattern did not emerge from this study. A case of HIV encephalitis complicated with CMV retinitis showed marked increase in LD- 1 , -2, -3, and -5. However, the CSF findings did not indicate meningitis. The absence of leukocytes in the CSF suggests that the LD-5 may arise directly from the brain tissue. To our knowledge, studies of LD isoenzymes in the CSF of AIDS patients have not been undertaken. When neurologic symptoms appear in these patients, an altered LD isoenzyme pattern may indicate superimposed infection in the CNS.

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Fig. 4. Case 3 . a: Autopsy section of spinal nerve root, showing extensive infiltration of the leptomeninges by poorly differentiated carcinoma cells. Hematoxylin and eosin (H&E). X 200. b: LD isoenzyme pattern in metastatic lung carcinoma, showing prominence of LD- 1, LD-2, and LD-3, with fraction 5 constituting only 1 I % of the total LD isoenzymes.

Fig. 5. Case 4. LD isoenzyme pattern in metastatic breast carcinoma, showing an increase in LD-5.

In cases of subdural hematoma and subarachnoid hemorrhage, all fractions appear markedly elevated, with fractions 3, 4, and 5 being the most prominent. Hemolysis typically results in an increase in fractions 1, 2, and 3 and does not appear to contribute to the increase in fractions 4 and 5 as demonstrated in our hemolysate study as well as in a previous report (26). Granulocytes present in the blood or anaerobic metabolism due to local circulatory disturbance may contribute to the elevation of these fractions. In the absence of infection or hemorrhage, an increase in LD-5 above 9% and a decrease in the LD-l/LD-5 ratio below 2.5 suggest the presence Of lePtomeningea1 tumor (4). Ten of 1 I patients with metastatic tumor to the leptomen-

LD lsoenzymes in CSF

inges studied by Sherwin et al. (8) showed an abnormal distribution of LD isoenzymes, and Fleisher et al. ( 2 ) also demonstrated a consistent increase in LD-5 in patients with metastases from lung and breast carcinoma as well as malignant melanoma metastases. Fleisher et al. (2) also studied the effects of storage at 3°C for up to 1 week and found that it does not alter the total LD activity, but LD-5 activity was markedly decreased. Patients with leukemic infiltration of the CNS have also shown a “shift” in the LD isoenzyme pattern to the cathodic fractions (LD-3, LD-4, and occasionally LD-5) ( 2 2 ) .The increased LD-5 is considered to be secondary to a transfer from aerobic to anaerobic metabolic processes by the malignant cells (I-4,6-8,13). In our only LD-positive case of primary brain tumor, the pattern showed elevation of all fractions and an elevation of LD-5 to greater than lo%, which has been equated with brain tumors of high grade (1). A glioblastoma multiforme grade IV was demonstrated at autopsy. Our studies confirm the findings in previous reports about the LD isoenzyme patterns in leptomeningeal metastatic tumors, bacterial meningitis, and viral encephalitis. However, the 13 cases of leptomeningeal metastatic tumors with negative LD isoenzyme patterns in our study clearly document that even extensive leptomeningeal metastasis (as seen in our case 3) may, under certain circumstances, show questionable or nondiagnostic elevation of LD-5. Thus the absence of LD-5 in CSF cannot rule out metastatic tumor. The influencing factor in these cases is presently unclear, but it may be related to local tissue blocking of the release of LD-5 to the CSF. It appears that the major source of these enzymes is the tumors themselves in contact with the CSF (1 1). The destruction of nervous tissue by tumor with the release of intracellular enzymes may be another source (1 1). The presence of LD-5 in cases of meningitis, hematoma, and primary brain tumor, on the other hand, underscores the importance of excluding infections, hemorrhages, and primary tumors before the diagnosis of metastatic tumor is made. The changes in LD isoenzymes are considered to be independent of serum LD concentrations when the blood-brain barrier is intact. With altered blood-brain barrier permeability, such as in bacterial meningitis, there is an increased movement of enzymes into the CSF. However, previous reports have shown conflicting results regarding their influence on CSF LD patterns (19). In conclusion, the LD isoenzyme patterns in CSF do help in differential diagnosis between closely related disorders, such as encephalitis and meningitis, as well as metastatic tumors and primary brain tumors. However, the isoenzyme pattern alone is not diagnostic and is not sensitive enough for early detection of brain lesions. We want to emphasize particularly the nonspecificity of LD-5 in the diagnosis of metastatic brain tumors; previous studies seemed to overemphasize the reliability of this correlation (2,3).

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Diagnostic value of lactate dehydrogenase isoenzymes in cerebrospinal fluid.

To evaluate the diagnostic value of lactate dehydrogenase (LD) isoenzymes in cerebrospinal fluid (CSF), 93 consecutive CSF specimens were analyzed. Th...
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