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Erythrocyte sedimentation rate at diagnosis in culture positive cases of active tuberculosis.

Byline: Muhammad Yousuf, Salih Bin Salih, Sameera Al-Johani and Adel Alothman

ABSTRACT

Objective: To evluate the Erythocyte Sedimentation Rate (ESR) at the time of diagnosis in culture positive cases of different types of active tuberculosis (TB).

Methodology: In this retrospective descriptive study conducted at King Abdulaziz Medical City, Riyadh, Saudi Arabia, ESR was done by a modified Westergren method using a rapid test. Cases of active TB (defined as a case of TB up to two weeks from the start of anti-tuberculous treatment), were evaluated for ESR at the time of diagnosis.

Results: Of 246 cases of culture positive TB, ESR results during active phase were available in 195 (79.3%) patients. Number (%) of patients with pulmonary, extra-pulmonary and disseminated TB were 69 (35%), 78 (40%) and 49 (25%) respectively. Two (1%) of these patients were HIV positive. ESR was elevated in 169 (87%) and was normal in 26 (13%) patients. Mean ESR in all patients was 67.6 mm/hr with no statistical difference between patients with different TB types. ESR between 1-30, 31-60, 61-90, 91-120 and 121-150 mm/hr represented 19%, 23%, 23%, 19% and 6% of the cases respectively, whereas 44 (22.6%) of the patients had ESR more than 100 mm/hr. Conclusion: In HIV negative patients with suggestive features of TB but without any other underlying disease affecting the ESR, the baseline ESR may be a valuable diagnostic test to suspect TB in resource poor countries.

KEY WORDS: ESR, Diagnosis, Active Tuberculosis.

INTRODUCTION

About two billion people in the world i.e. one in every third person, is infected with Mycobacterium tuberculosis.1 Ninety-five percent of all cases and 99% of deaths due to tuberculosis (TB) occur in the developing countries, with the greatest burden in Sub-Saharan Africa, and South-East Asia.2 The problem of TB in these parts of the world is compounded by the fact that resources to combat TB in these countries are very scarce.

According to 2002 estimates, per head expenditure in developing countries is about 2-3% of the amount spent on health care in the developed countries.3 Erythrocyte Sedimentation Rate (ESR) is an inexpensive, easily available investigation paticulary in resource poor countries, where TB is common. In clinical practice, ESR is commonly done as a non-specific test for a wide range of pathological

How to cite this article: Yousuf M, Salih SB, Al-Johani S, Alothman A. Erythrocyte sedimentation rate at diagnosis in culture positive cases of active tuberculosis. Pak J Med Sci 2012;28(1):87-90

INTRODUCTION

About two billion people in the world i.e. one in every third person, is infected with Mycobacterium tuberculosis.1 Ninety-five percent of all cases and 99% of deaths due to tuberculosis (TB) occur in the developing countries, with the greatest burden in Sub-Saharan Africa, and South-East Asia.2 The problem of TB in these parts of the world is compounded by the fact that resources to combat TB in these countries are very scarce.

According to 2002 estimates, per head expenditure in developing countries is about 2-3% of the amount spent on health care in the developed countries.3 Erythrocyte Sedimentation Rate (ESR) is an inexpensive, easily available investigation paticulary in resource poor countries, where TB is common. In clinical practice, ESR is commonly done as a non-specific test for a wide range of pathological conditions such as acute and chronic infections, systemic inflammatory and neoplastic diseases.4 In a study to evaluate the causes of extremely elevated ESR defined as equal to or more than 100 millimeter per hour (mm/hr). We found TB to be one of the 10 main causes.5 Although there are few studies that have investgated the ESR in patients with TB,6-9 such studies were either small or had the diagnosis not entirely confirmed by cultures. There is no recent study to evaluate ESR in culture positive cases of different types of TB.

METHODOLOGY

This retrospective descriptive study was conducted in King Abdulaziz Medical City (KAMC), a tertiary care teaching center in Riyadh, Saudi Arabia. The study was approved by the institutional research and ethical committee. The medical record numbers of all cases of culture positive TB cases diagnosed during the four years period of January 2005 to December 2008 were retrieved and used to review ESR done during the active disease (defined as up to two weeks after the start of antituberculous treatment) in these cases.

The ESR at KAMC was performed by a rapid modified Westergren method on whole blood samples obtained through standard venipuncture techniques in 4 mls BD vacutainer tubes (BD, Plymouth, UK) or vacuette tubes (Greiner Bio-one, Kremsmunster, Austria) with dior tri-postassium EDTA. The test was performed using an automated TEST1

THL Analyser (Alifax, Padova, Italy). This automated ESR analyser measures the capacity of the red cells to aggregate photometrically over a very short period of time and translates the results into traditional units as mm/hr. Our hospital laboratory has a normal reference range of 0-15 mm/hr for males and 0-20 mm/hr for females.

The diagnosis of TB was made by culture of body secretions or tissue cultures of specimens from the involved areas. All specimens underwent digestion and decontamination using sodium hydroxide. From the sediment obtained, smears and cultures were prepared. Smears were stained using Auramine-Rhudamine stain (Becton, Dickinson, BD Bioscience(r)) as screening test. All positive smears were confirmed by acid-fast staining (Ziehl-Neelsen stain, ZN) (Becton, Dickinson, BD Bioscience(r)). Three parallel systems of isolation and detection were used: The mycobacteria growth indicator tube (MGiT) (Becton, Dickinson, BD Bioscience(r)), the solid medium method - Lowenstein-Jensen culture Watin Biolife(r)) and Polymerase Chain Reaction (Becton, Dickinson, BD Bioscience.(r))

Depending on the site/s involved, TB was classified as pulmonary or extra-pulmonary as per WHO guidelines2 and disseminated if the patient had miliary TB or involvement of two or more organ systems. ESR was arbitrarily graded as less than 30, 30-60, 61-90, 91-120 and 121-150 mm/hr and also in to 2 categories of less than 100 and 100 mm/hr or more with partial modification as described in other studies.7,10

The data noted included demographic information about age, gender, date of TB diagnosis based on culture report, date of ESR test with its value date of commencement of antituberculous treatment and HIV status along with any co-morbid conditions. Plasma albumin and hemoglobin levels, when available, were also retrieved in these cases during the active phase of TB. The information was copied on a pre-designed standardized data capture Microsoft Excel spread sheet. The data was subsequently computed on a PC by using Microsoft excel on Windows 2000 professional. SPSS software (release 17.0, SPSS Inc., Chicago, U.S.) was used for all statistical analyses. The difference of ESR levels between the three TB groups was examined using ANOVA test. All tests were two-tailed. P-value less than 0.05 was considered as significant.

RESULTS

During the study period, of 246 non-duplicate cases of culture positive TB, the ESR was available during the active disease in 195 (79.3%) patients. Of these, 114 (58.5%) were males while 81 (41.5%) were females. Six of these patients were non-Saudi, while 189 were Saudi. All patients except two were HIV negative. Out of all cases of TB, pulmonary, extrapulmonary and disseminated TB represented 68

Table-I: Mean, standard deviation (SD) and median ESR (mm/hr) in patients with different types of TB.

Type of tuberculosis (TB)###Number (%)###Mean ESR###SD###Median ESR

Pulmonary TB###68 (35%)###71.77###36.026###73

Extra-pulmonary TB###78 (40%)###65.57###35.027###59

Disseminated TB###49 (25%)###65.51###35.309###69

Total###195 (100%)###67.62###34.656###70

SD= Standard deviation, ESR= Erythrocyte sedimentation rate

(35%), 78 (40%) and 49 (25%) cases respectively. ESR was elevated in 169 (87%) and normal in 26 (13%) of these patients. Mean ESR in all patients was 67.6 mm/hr with no statistically significant difference between pulmonary, extra-pulmonary and disseminated TB with p=0.50 (Table-I). Mean plasma albumin and hemoglobin levels were available in 178 and 192 of all study patients and were 37.6 G/L and 121.1 G/L respectively. ESR in different types of TB according to gender is shown in Fig.1. Forty four (22.6%) patients had ESR 100 mm/hr or more while 151 (77.4%) had ESR less than 100 mm/hr. ESR below 100 or 100 mm/hr or more in patients with different types of TB is shown in Fig.2, Only two (1%) of our patients were HIV positive. Both had disseminated TB, one was Saudi and other was non-Saudi with ESR of 80 and 76 mm /hr respectively.

DISCUSSION

In this study of predominantly non-HIV culture positive cases of active TB, we found that ESR was elevated in 87% and normal in 13% of the patients. In 77% of cases the ESR was less than 100 mm/hr. Most of our patients had extrapulmonary TB mainly because in these cases the diagnosis needed further investigations including biopsy and culture of the tissues, for which the patients were referred from other hospitals to our center. In a study of 24 patients with tuberculous spondylitis (Pott's Disease) diagnosed on the basis of a positive smear of sputum or biopsy tissue for AFB or a suggestive granuloma on histopathologic examination of the biopsy, ESR was less than 30, 31-60, 61-90 and 60-100 mm/hr in 35.7%, 28.6%, 35.7% cases with none having ESR more than 100 mm/hr.6

This compares to an ESR of 20-40 and greater than 40 mm/hr in 21.4 % and 73.2% cases in a study of 69 cases of tuberculous spondylitis with diagnosis based on clinical, radiologic, histopathologic and AFB smear or culture at our center in Riyadh, Saudi Arabia.7

A previous Saudi study of 50 patients with sputum smear positive cases of pulmonary TB evaluated hematological abnormalities and detected mean ESR of 70.13 and 73.65 with a range of 1-140 and 6-113 mm/hr in male and female patients respectively,8 however, no details about number of patients having ESR in normal, above normal or above 100 was described. In a study of 68 children up to 14 years with TB from Qatar,9 where the diagnosis of TB was based on culture or response of the patients to antitubeculous treatment, 33% of the children had normal ESR with only 4 (5.9%) children having ESR greater than 100 mm/hr. The HIV status of these patients was also not defined.

Another study from South Africa,10 looked at the ESR in patients with active TB (88% cases had pulmonary TB with HIV positive in 83% of patients). ESR was raised in all these patients with 76% of the patients having ESR greater than 100 mm/hr. ESR greater than 100 mm/hr was more common in HIV positive cases. However, there was no detail about the methodology of diagnosis of TB and definition of pulmonary or extra-pulmonary TB. The results of this study were in sharp contrast to a small study of 34 HIV-positive patients with pulmonary TB from India,11 where the mean and median values of ESR, respectively, were 38.5 mm/hr and 30.0 mm/hr among patients with HIV infection (n=34) compared to 102 and 108 mm/hr among those without HIV infection. This study also did not define the methodology used to diagnose TB.

As ESR may be raised in patients with HIV infection,12 another small South African study evaluated raised ESR (median 98, range 51-140 mm/hr) in children with advanced HIV infection and suspicion of pulmonary TB,13 Pulmonary TB was not proven in any of these children indicating that in patients with HIV infection, raised ESR does not indicate TB. Therefore, these studies indicate that in patients with HIV infection, raised ESR does not help in the diagnosis of TB. To resolve the issue whether ESR is valuable in diagnosis of TB in HIV positive cases, a prospective study of ESR in HIV positive patients with and without TB needs to be carried out. However, in patients without HIV infection as in our study, raised ESR in the presence of suggestive features of TB should lead to further investigations to rule in or rule out the diagnosis of TB. Low normal plasma albumin and low blood hemoglobin as seen in our study are part of the acute phase reaction and anemia of chronic disorder.14

These changes are common in most of chronic inflammations including TB.

The strengths of our study were relatively larger sample size, diagnosis based on culture, classification of TB into pulmonary, extrapulmonary and disseminated with stratification of ESR in to different levels including below and above 100 mm/hr. Except for lymph node TB, diagnosing extra-pulmonary TB is often difficult and challenging, because it often needs availability of sophisticated diagnostic techniques which are not available in settings where TB is common. A sizable number of patients in our study were patients with extra-pulmonary TB, mainly because this hospital is a tertiary care center with referral of suspected TB cases from other hospitals where facilities for tissue diagnosis or TB cultures are not available. However, our study data was collected retrospectively which might not be able to control the potential confounders affecting the ESR values.

The differences in the results of these studies may also be due to the other factors which affect the values of ESR including nutritional status, hemoglobin and albumin level or other associated infections or conditions which may independently raise the ESR and whether the TB is primary, relapse or recurrent infection.

In HIV negative patients with suggestive features of TB but without any other underlying disease affecting the ESR, the baseline ESR may be a valuable diagnostic test to suspect TB in resource poor countries.

ACKNOWLEDGEMENT

We gratefully acknowledge the help of Dr Aiman El-Saed Ramadan, Biostatistician, infection prevention and control department, King Abdulaziz Medical City, and Assistant Professor of Epidemiology and Biostatistics, College of Public Health and Health Informatics, King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia, for his technical help in statistical analysis and graphics.

REFERENCES

1. Dye C, Scheele S, Dolin P, Pathania V , Raviglione MC. Global burden of tuberculosis: Estimated incidence, prevalence, and mortality by country. JAMA 1999;282:677-686.

2. World Health Organization (2006 a). Global tuberculosis control: Surveillance, planning and financing. Geneva, Switzerland: WHO; 2006. Publication WHO/ HTM/ TB/2006.362.

3. World Bank. World development indicators.Washington, DC; World Bank, 2002.

4. Brigden ML. Clinical utility of erythrocyte sedimentation rate. Am Fam Physician 1999;60:1443-1450.

5. Yousuf M, Akhter J, Al-Khairy K, Al-Saadan MA, Bin-Salih S. Extremely elevated erythrocyte sedimentation rate: etiology at a tertiary care center in Saudi Arabia. Saudi Med J 2010;31:1227-1231.

6. Mirsaeidi SM, Tabarsi P, Amiri MV. Clinical and radiological presentation of adult tuberculous spondylitis. Tanaffos 2003;2:59-65.

7. Alothman A, Memish ZA, Awada A, Al Mahmood S, Al Sadoon A, Rahman MM, et al. Tuberculous spondylitis: analysis of 69 cases from Saudi Arabia. Spine 2001;26:E565-E570.

8. Al-Omar IA, Al-Ashban RM, Shah AH. Hematological abnormalities in Saudis suffering from pulmonary tuberculosis and their response to treatment. Res J Pharmacol 2009;3:78-85.

9. Al-Marri MRHA, Kirkpatrick MB. Erythrocyte sedimentation rate in childhood tuberculosis: is it still worthwhile? Int J Tubrc Lung Dis 2000;4:237-9.

10. Ukpe IS, Southern L. Erythrocyte sedimentation rate values in active tuberculosis with and without HIV co-infection. S Afr Med J 2006;96:427-428.

11. Sarkar K, Baraily S, Dasgupta S. Erythrocyte sedimentation rate may be an indicator for screening of tuberculosis patients for underlying HIV infection, particularly in resource-poor settings: An experience from India. J Health Popul Nutr 2004;22:220-221.

12. Ndakotsu MA, Salawu L, Durosinmi MA. Relation between erythrocyte sedimentation rate, clinical and immune status in HIV-infected patients. Niger J Med 2009;18:208-210.

13. Kunneke M, Maynier S, Kruger M. A higher ESR is not an indication of pulmonary tuberculosis in children with advanced HIV-infection. Int Conf AIDS. 2000; 13 (Abstract)

14. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999;340(6):448-454.

Muhammad Yousuf, Salih Bin Salih, Sameera Al-Johani and Adel Alothman

1 Muhammad Yousuf, FRCP (I), FRCP (Edin), FACP, Department of Medicine, 2. Salih Bin Salih, MD, FACP, Department of Medicine, 3. Sameera Al-Johani, FRCPC, Department of Laboratory Medicine and Pathology, 4. Adel Alothman, MB, FRCPC, FACP, Department of Medicine, 1-4: King Abdulaziz Medical City, King Saud Bin Abdulaziz University of Health Sciences, Riyadh, Saudi Arabia., Correspondence: Muhammad Yousuf, Consultant, Division of Internal Medicine, Department of Medicine, Mail Code: 1443, PO Box 22490, King Abdulaziz Medical City, Riyadh 11426, Saudi Arabia., E-mail: drmyousuf@hotmail.com, Received for Publication: April 5, 2011, Revision Received: November 10, 2011, Revision Accepted: November 25, 2011
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Publication:Pakistan Journal of Medical Sciences
Article Type:Report
Geographic Code:7SAUD
Date:Mar 31, 2012
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