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Clin Infect Dis. Author manuscript; available in PMC 2009 July 27.

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Published in final edited form as:
Clin Infect Dis. 2009 March 15; 48(6): 816–821. doi:10.1086/597096.

Lumbar Puncture in HIV-Infected Patients with Syphilis and No
Neurologic Symptoms
Khalil G. Ghanem, Richard D. Moore, Anne M. Rompalo, Emily J. Erbelding, Jonathan M.
Zenilman, and Kelly A. Gebo
Johns Hopkins University School of Medicine, Baltimore, Maryland

Abstract

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Background—The decision to perform lumbar puncture in patients with asymptomatic human
immunodeficiency virus (HIV) infection and syphilis is controversial. The Centers for Disease
Control and Prevention recommend certain criteria that warrant lumbar puncture. Here, we assess
the performance of these criteria for detecting asymptomatic neurosyphilis (ANS).
Methods—Eligible subjects consisted of all patients with concurrent HIV infection and syphilis in
a prospective clinical cohort who had no neurologic symptoms at the time of lumbar puncture. We
retrospectively applied different stratification criteria to calculate the performance of lumbar
puncture in detecting ANS: (1) lumbar puncture in patients with late latent syphilis or syphilis of an
unknown duration, regardless of the CD4 cell count or rapid plasma reagin titer; (2) lumbar puncture
if the CD4 cell count was ≤350 cells/mL and/or the rapid plasma reagin titer was ≥1:32, regardless
of the syphilis stage; and (3) lumbar puncture in the context of serologic nonresponse to syphilis
therapy.
Results—Two hundred two of 231 patients with syphilis did not have neurologic symptoms.
Immediate lumbar puncture was performed for 46 patients, and 10 cases (22%) of ANS were detected.
With use of the first criterion, 2 (14%) of 10 cases of ANS in patients with early-stage syphilis would
have been missed (sensitivity, 80% [95% confidence interval {CI}, 44%–97%]; specificity, 76%
[95% CI, 60%–89%]). Criterion 2 would not have missed any cases of ANS (sensitivity, 100% [95%
CI, 70%–100%]; specificity, 87% [95% CI, 72%–96%]) but would have required that a lumbar
puncture be performed for 88% of patients. Performance of lumbar puncture performed in 13 cases
based on serologic nonresponse to syphilis therapy yielded 4 cases (31%) of ANS.

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Conclusions—In patients with concurrent HIV infection and syphilis, the use of criteria based on
rapid plasma reagin titer and CD4 cell count, instead of stage-based criteria, improved the ability to
identify ANS.
In the era before penicillin, patients who received a diagnosis of syphilis—even those without
neurologic symptoms—underwent routine lumbar puncture (LP) and examinations of CSF
specimens during evaluations for neurosyphilis [1]. Patients with asymptomatic neurosyphilis
(ANS) were more likely to develop long-term neurologic sequelae [2,3] than were those with
normal CSF. After World War 2, the rates of neurologic complications of syphilis decreased
significantly, despite the use of penicillin formulations that did not achieve treponemicidal

© 2009 by the Infectious Diseases Society of America. All rights reserved.
Reprints or correspondence: Dr. Khalil G. Ghanem, Johns Hopkins University, Bayview Medical Center, Div. of Infectious Diseases,
4940 Eastern Ave., B3N, Baltimore, MD, 21224 (E-mail: kghanem@jhmi.edu).
Presented in part: Joint Conference of the British Association for Sexual Health and HIV/ American Sexually Transmitted Diseases
Association, Brooklyn, New York, May 2008 (abstract E-06).
Potential conflicts of interest. All authors: no conflicts.

. but those studies included both patients with and patients without neurologic symptoms [12. Patients were screened with the nontreponemal RPR test as part of routine clinical care. led to the abandonment of routine LP in patients without neurologic symptoms. longitudinal clinical cohort. we excluded patients who had neurologic symptoms at the time of the Clin Infect Dis. Asymptomatic neurosyphilis Patients in the cohort who received a diagnosis of and were treated for syphilis during the period 1990–2006 were eligible for the study.16]. the “Sexually Transmitted Diseases Treatment Guidelines. Collected clinical data include all clinical. As HIV infection evolves into a treatable chronic disease.13]. coupled with the rapid serologic response of the nontreponemal titers after penicillin treatment [5. All charts for patients with a syphilis diagnosis were reviewed. There is no disagreement that patients with concurrent syphilis and HIV infection who present with neurologic symptoms should undergo immediate LP to rule out neurosyphilis. and/or a reactive CSF Venereal Diseases Research Laboratory [VDRL] test result) [14]. a number of case reports of neurosyphilis in patients with HIV infection [7–10] prompted the need to revisit the issue of LP for such patients. NIH-PA Author Manuscript Previous studies involving HIV-infected patients found an increased risk of neurosyphilis in patients with CD4 cell counts ≤350 cells/mL and rapid plasma reagin (RPR) titers ≥1:32. Author manuscript. and laboratory parameters. all patients are offered the opportunity to join the Johns Hopkins HIV Clinical Cohort. MD) provides HIV continuity care to >4000 patients. Page 2 NIH-PA Author Manuscript levels in the CSF [4]. available in PMC 2009 July 27. In the 1980s. reactive specimens were confirmed using the fluorescence treponemal antibody absorption test. reactive syphilis serologic test results. and/or protein level. therapeutic. 2006” of the Centers for Disease Control and Prevention (CDC) recommend LP for all HIV-infected patients who present with late. latent syphilis or syphilis of unknown duration and for all patients with evidence of serologic failure after receipt of syphilis therapy [11]. For this latter group. The 2006 guidelines acknowledge that some experts also recommend adherence to RPR titer– and CD4 cell count– based criteria but that the likelihood that neurosyphilis would be detected with the latter criteria was unknown [11]. Maintenance of the database and use of its contents for analysis of patient outcomes are approved by the Institutional Review Board of the Johns Hopkins University School of Medicine. Criteria for the diagnosis of ANS included lack of neurologic signs and symptoms. >10 cells/µL. Syphilis diagnoses were made by clinicians on the basis of CDC criteria [17]. Our goal was to compare the sensitivity and specificity of different risk stratification criteria for the diagnosis of ANS among HIV-1–infected patients who were enrolled in a large. without an alternative diagnosis. METHODS Population and data abstraction NIH-PA Author Manuscript The Johns Hopkins Moore Clinic (Baltimore.Ghanem et al. A detailed description of this dynamic cohort has been presented elsewhere [15]. Because this was a study of ANS. There is controversy about the need for LP among patients with concurrent syphilis and HIV infection who do not have neurologic symptoms. > 50 mg/dL. We recently reported that HIV-infected patients with syphilis and neurologic symptoms are more likely to have higher RPR titers and lower CD4 cell counts [14]. clinicians need consensus guidelines to help manage syphilis and to evaluate for ANS in this population. These observations. Characteristics of these patients are presented elsewhere [14. At enrollment.6]. and the presence of ≥1 abnormal finding during examination of CSF specimens (WBC count.

The 2 main reasons were an Clin Infect Dis. 0–14 days) after syphilis diagnosis. We also evaluated the yield of detecting ANS for delayed LP performed in response to inadequate serologic response to syphilis therapy. Of the 202 cases. available in PMC 2009 July 27. Patients who underwent LP for reasons other than evaluation of syphilis were excluded from the study. Characteristics of these patients and their clinical courses are presented elsewhere [14. with respect to syphilis diagnosis and treatment. 10 (21%) were found to be ANS. We used standard definitions to calculate the sensitivity (true-positive results divided by the sum of true-positive and false-negative results) and specificity (true-negative results divided by the sum of true-negative and false-positive results) measures. For abstraction of the records. 100–360 days) after diagnosis and treatment of syphilis. 27 cases of symptomatic neurosyphilis and 2 cases of other neurologic conditions that caused symptoms (cryptococcal meningitis and progressive multifocal leukoencephalopathy) were excluded. and 14 cases (23%) of ANS were detected. was used to conduct analyses. Of these 48 cases. Review of the medical records revealed that the LP was performed because of underlying HIV infection in patients with newly diagnosed syphilis (78%).Ghanem et al. Page 3 NIH-PA Author Manuscript LP. The first is based on the CDC criterion that LP should be performed for all infected patients with concurrent syphilis and HIV infection who have the late latent stage of syphilis or syphilis of unknown duration. Of these 231 episodes.1 (Stata Corp. The proportional hazard assumption with robust variance estimation was tested using scaled Schoenfeld residuals against log of time. and 57% involved elevated protein levels). The demographic and clinical characteristics of patients with these cases. Author manuscript. respectively. and all 3 abnormalities were noted in 8% of cases. The remaining 13 of 61 patients who continued to be neurologically asymptomatic underwent LP a median of 287 days (interquartile range. version 10. 43% involved isolated pleocytosis. Collected follow-up data included RPR titers. irrespective of syphilis stage. protein level in 58%. .16]. 2 abnormalities were noted in 42% of cases. The remaining 202 did not have neurologic signs or symptoms at the time of syphilis evaluation. We evaluated the impact of LP on the risk for subsequent re-treatment of syphilis by using time-to-event statistical models. follow-up LP. a total of 180 HIV-infected patients received diagnosis of 231 episodes of syphilis. Stata software. irrespective of CD4 cell count or RPR titer [11]. and data on CD4 cell counts at or near (≤90 days) the times of LP and RPR titer determination. The diagnosis of ANS was based on pleocytosis in 46% of cases. and need for syphilis re-treatment. stratified by LP status.05 were considered to represent statistical significance. Only 1 abnormality was noted in 50% of cases (of those. RESULTS NIH-PA Author Manuscript During the period 1990–2006. the timing of the LP. Statistical analysis NIH-PA Author Manuscript We compared independent means and proportions using the Wilcoxon signed rank test and the χ2 test. We used the Andersen-Gill method to adjust for the repeated measures [18]. are summarized in table 1. An inadequate serologic response was defined as the lack of a ≥4-fold decrease in the RPR titer ≥12 months after receipt of appropriate therapy for syphilis or a ≥4-fold increase in the RPR titer ≥30 days after receipt of syphilis therapy [11]. and a positive CSF VDRL result in 50%. The second criterion consists of performing LP for all patients with concurrent syphilis and HIV infection who have a CD4 cell count ≤350 cells/mL and/or a RPR titer ≥1:32. and pregnancy (4%). respectively. concern about a high initial RPR titer documented by the health care provider (18%). LP was performed for 48 (79%) of 61 cases a median of 1 day (interquartile range. P values <.). We compared paired means and proportions using Student’s paired t test and McNemar’s test. LP was performed for 61 (30%). we included the reasons for performing the LP. We retrospectively applied 2 sets of criteria for performing immediate LP.

In our population. Additional research is warranted that weighs risks of neurologic sequelae. 43 (90%) had one or both. In our study. where it is feasible to schedule an LP. the provider had not documented whether LP was even considered. 4 (31%) were found to be ANS. 0. NIH-PA Author Manuscript Of the 48 patients who underwent immediate LP. One alternative to LP is treating coinfected patients with a therapeutic regimen that adequately penetrates the CNS [19. A recent study that included both patients with symptomatic neurosyphilis and patients with asymptomatic neurosyphilis found that use of the RPR-based criterion (RPR titer. The application of the CD4 cell count– or RPR-based criterion was more sensitive. . Compared with the stage-based criterion. 1. 37 (77%) had a pretreatment RPR titer ≥1:32. 3 cases of ANS would have been missed. P = .4). but no cases of ANS would have been missed. 1 case of ANS would have been missed. 95% CI. Two cases of ANS (or ANS occurring in 18% of cases of early syphilis) would have been missed. making outpatient therapy difficult in many settings. Clin Infect Dis. NIH-PA Author Manuscript The decision to perform LP was not associated with the likelihood of short-term syphilis retreatment. Page 4 increasing RPR titer ≥30 days after therapy (48%) or a lack of a ≥4-fold decrease in the RPR titer in response to therapy (52%).20]. 38% of patients who were neurologically asymptomatic and did not undergo LP were ultimately retreated for syphilis. and 37 (77%) had late-latent or an unknown duration of syphilis. application of the CD4 cell count/RPR criteria would have meant that 88% of cases underwent LP. which only included asymptomatic patients. Of the 13 of 61 cases that remained asymptomatic for which delayed LP was performed because of a lack of serologic titer response after therapy for syphilis. the application of either criterion would have led to performance of LP for 70%–90% of syphilis cases. LP. DISCUSSION The currently recommended CDC syphilis stage–based criterion may be inadequate if the goal is to identify ANS. Intravenous and intramuscular formulations of penicillin readily achieve that goal. it may be difficult to convince an asymptomatic patient that an LP will contribute to an improved outcome. Figure 1 summarizes the retrospective application of the late-latent stage–based criterion to the entire cohort.3. LP is not without complications. ≥1:32) without the CD4 cell count criterion also led to no missed cases of ANS [13]. 30 (63%) had a CD4 cell count ≤350 cells/ mL.3. In our clinical setting. available in PMC 2009 July 27. if an RPR titer ≥1: 32 had been used as the sole criterion. If a CD4 cell count ≤350 cells/mL had been used as the sole criterion. Author manuscript. compared with 36% of those who did undergo LP (unadjusted hazard ratio.7−2. application of the CD4 cell count/RPR criterion would lead to performance of ∼20% more LPs. 68% of the cases were late-latent stage at the time of syphilis diagnosis and would have required an LP. because it did not miss any cases of ANS. such as sexually transmitted diseases clinics where syphilis is commonly diagnosed. And lastly. On the remaining charts. After a median of 4 years of follow-up. use of the RPR titer cutoff without the CD4 cell count criterion would have led to decreased sensitivity and 1 missed case of ANS in a patient with early syphilis who presented with an RPR titer of 1:16 and CD4 cell count of 167 cells/ mL. A review of the clinic notes (72 charts) in cases in which LP was not performed revealed that patients refused the procedure in 38% of cases. In addition. NIH-PA Author Manuscript LP requires additional resources and training and may be difficult to perform in many outpatient settings. Overall. to minimize the potential for long-term sequelae.Ghanem et al. it was performed in less than one-third of cases. but these agents require daily injections over several weeks. As shown in figure 2.

Of the 4 patients (31%) who subsequently received a diagnosis of ANS. Moreover. Studies conducted in the early part of the 20th century suggested that CSF abnormalities in asymptomatic patients who had either early or late latent syphilis resulted in symptomatic neurosyphilis up to twice as frequently as in those with normal CSF parameters [2. At the time of syphilis diagnosis. . 9 (69%) of 13 patients had late latent syphilis. However. the rates of symptomatic neurosyphilis decreased [4]. The neurologic sequelae of syphilis can be devastating [14]. only 2 (50%) had late latent syphilis. NIH-PA Author Manuscript This study has several limitations. we reviewed the medical charts of all patients to determine the reasons for LP.25] suggest that application of RPR/CD4 cell count–based criteria improve the ability to identify ANS. HIV infection may cause CSF abnormalities [21]. There are no standard criteria for the diagnosis of neurosyphilis. the clinical significance of ANS in the antibiotic era is unclear. We have no way of ascertaining—even indirectly—whether performance of an LP at the time of syphilis diagnosis in these patients would have demonstrated CNS involvement earlier. Our data and those of others [13. There were a relatively small number of LPs performed. with frequent reports of symptomatic neurosyphilis in patients who had been adequately treated for early or late latent syphilis [7–10]. and we may have missed LPs if they had been performed elsewhere. Trying to minimize the number of LPs performed without compromising patient care is helpful. Acknowledgments We thank the staff and patients of the Johns Hopkins HIV Clinical Cohort. and to this end. >30% of patients were found to have ANS. although all would have satisfied the CD4 cell count/RPR criterion. the criteria to perform LP were applied retrospectively. the findings are likely to be generalizable to other populations. However. especially among patients who have or are at risk of acquiring HIV infection [22–24]. selective criteria for performing LP have been advanced.Ghanem et al. even as the rates of LP decreased. The re-treatment rates may have been associated with either treatment failure or reinfection. In the pre-HIV penicillin era. we did not have reliable histories to distinguish one from the other. First. The ability to determine whether the early LP management strategy has an impact on decreasing long-term morbidity in these patients would have required a much longer followup period.3]. Thus. Finally. Only 50% of our cases had positive CSF VDRL results. available in PMC 2009 July 27. but they are often necessary. In our study. suggesting that penicillin therapy for early. and 12 patients (92%) had a CD4 cell count ≤350 cells/mL and/or an RPR titer ≥1:32. NIH-PA Author Manuscript Our patient population consisted mostly of African American patients with fairly heterogeneous risk factors for syphilis and HIV infection. No CSF fluorescence treponemal antibody absorption tests were performed. Author manuscript. and difficult to perform in many settings where patients are diagnosed with syphilis. NIH-PA Author Manuscript The current CDC recommendation that LP be performed for patients with concurrent HIV infection and syphilis whose RPR titers either do not respond appropriately to therapy or whose titers increase after therapy [11] may be the decision rule that identifies the highest number of cases of ANS.and late-latent syphilis (in addition to receipt of antibiotics with treponemicidal activity for other indications) may be adequate to prevent late neurologic sequelae in patients with ANS. The rates of syphilis continue to increase. time consuming. LPs are invasive. things changed in the HIV era. Clin Infect Dis. To try and minimize bias. we did use criteria that are accepted and that would have led to administration of therapy for neurosyphilis in routine clinical practice. Page 5 and therapy against close serologic follow-up of the HIV-infected patient with ANS in the HAART era.

et al. Gebo KA. The profile of neurosyphilis in Denmark: a clinical and serological study of all patients in Denmark with neurosyphilis disclosed in the years 1971–1979 incl. [PubMed: 16888612] 12. Sex Transm Dis 1977. Gebo KA. The classification.G. available in PMC 2009 July 27. and R. HIV and syphilis: when to perform a lumbar puncture. Treatment of seropositive primary syphilis: an evaluation of 196 patients. Bolan G.47:258–265. Moore JE.96:1–14. Lukehart SA. Berman SM. Musher DM. Sex Transm Dis 1977.A. Al-Egaily SS. Maxwell CL. Erbelding EJ. 2.316:1587–1589.G. [PubMed: 2122225] 18. Page 6 Financial support. Berry CD. 1985–1992. National Institutes of Health (K23-HD047395 to K. Alteration in the natural history of neurosyphilis by concurrent infection with the human immunodeficiency virus.47:1–68. penicillin. Dunlop EM. and AIDS.G. J Infect Dis 1998. AIDS 2008. K24-DA00432. Syphilis. Weinstock HS. Zenilman JM. Flood JM. et al. Bayne L. JAMA 1930. [PubMed: 4575351] 20. [PubMed: 929349] 6.M.34:141–144. Gill RD. Andersen PK.). Wharton M. by Wassermann reaction (CWRM) in the cerebrospinal fluid. Guthe T. Simon RP.D. NIH-PA Author Manuscript References NIH-PA Author Manuscript NIH-PA Author Manuscript 1. National Institute of Drug Abuse (K23-DA00523. The prognosis of early and late asymptomatic neurosyphilis. Zenilman JM. Poll B.). Sex Transm Dis 2007.Ghanem et al. [PubMed: 9586651] 16. Houang ET. Pedersen NS. Willcox RR.39(RR13):1–43.G. Erbelding EJ. Guroy ME. Morse DL. Ghanem KG. Acta Derm Venereol Suppl (Stockh) 1981. MMWR Recomm Rep 1990. 4. Antiretroviral therapy is associated with reduced serologic failure rates for syphilis among HIV-infected patients. N Engl J Med 1987. N Engl J Med 1939. San Francisco.17:S38–S41. Collier AC. [PubMed: 18532887] 17. Hopkins HH.A. [PubMed: 929350] 7. Clin Infect Dis 2008.241:2538–2540. [PubMed: 2037785] 10.22:1145–1151.). neurosyphilis.). Asymptomatic neurosyphilis VI. Author manuscript. [PubMed: 18525260] 15. Buehler JW.33:231–246. [PubMed: 3587291] 9. National Institute of Aging (R01AG026250 to K. Jorgensen BB. [PubMed: 14745693] 13. De Wit S. Studies in asymptomatic neurosyphilis II. Neurosyphilis during the AIDS epidemic. [PubMed: 374763] Clin Infect Dis. Marra CM. Libois A. MMWR Recomm Rep 2006.189:369–376. Penicillin in the treatment of syphilis: the experience of three decades. Case definitions for public health surveillance. Fiumara NJ. J Infect Dis 2004. Sexually transmitted diseases treatment guidelines. Ann Stat 1982. Ghanem KG. Johns DR. Understanding the clinical and economic outcomes of HIV therapy: the Johns Hopkins HIV Clinical Practice cohort. 19. J Infect Dis 1991. and prognosis of early asymptomatic neurosyphilis. Bull World Health Organ 1972. [PubMed: 16865051] 14. Centers for Disease Control and Prevention.55(RR11):1–94.95:1637–1641. Vogt RL. Ross Clinician Scientist Award (to K. Neurologic relapse after benzathine penicillin therapy for secondary syphilis in a patient with HIV infection. [PubMed: 9534965] 11. Treatment of secondary syphilis: an evaluation of 204 patients. Moore RD. Rompalo AM. J Acquir Immune Defic Syndr Hum Retrovirol 1998. and RO1-DA-11602 to K.G. Neurosyphilis in a clinical cohort of HIV-1-infected patients. Smith SL. [PubMed: 3587290] 8. Moore RD. Moore JE. Chorba TL.163:1201–1206. Hooton TM. Neurosyphilis and its treatment. Penicillin levels in blood and CSF achieved by treatment of syphilis.A.10:1100–1120. 2006. Idsoe O. Perdrup A. Cerebrospinal fluid abnormalities in patients with syphilis: association with clinical and laboratory features.177:931–940. Tierney M. . and JHU Richard S.4:92–95.316:1569–1572.4:96–99. Felsenstein D. N Engl J Med 1987.221:817–819. 3. JAMA 1979. Rompalo AM. Merritt HH. Workowski KA. Cox’s regression model for counting processes: a large sample study. Fiumara NJ. Bulletin of the Johns Hopkins Hospital 1922. treatment. Moore RD. [PubMed: 6953720] 5.

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asymptomatic neurosyphilis. UD. Page 8 NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 1.Ghanem et al. LL. late-latent stage of syphilis. Retrospective application of the first risk stratification criterion. which was based on current Centers for Disease Control and Prevention (CDC) recommendations for performance of lumbar puncture (LP) at the time of syphilis diagnosis in all late latent and unknown duration stages of syphilis. . Author manuscript. NIH-PA Author Manuscript Clin Infect Dis. available in PMC 2009 July 27. unknown duration of syphilis. ANS.

NIH-PA Author Manuscript Clin Infect Dis. . asymptomatic neurosyphilis. Page 9 NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 2. available in PMC 2009 July 27. which was based on performance of a lumbar puncture (LP) in patients with a CD4 cell count ≤350 cells/mL and/ or a rapid plasma reagin (RPR) titer ≥1:32.Ghanem et al. Author manuscript. Retrospective application of the second risk stratification criterion. ANS.

available in PMC 2009 July 27.1 (22–61) African American 120 (85) 45 (94) 12 (92) White 16 (11) 3 (6) 1 (8) MSM 43 (31) 14 (29) 5 (38) Heterosexual 62 (44) 23 (48) 6 (46) Injection drug user 48 (34) 22 (46) 5 (38) Syphilis stage Early 50 (35) 11 (23) 4 (31) LL or UD 91 (65) 37 (77) 9 (69) 128 (16–256) 256 (32–1024) 128 (32–512) 55 (39) 25 (52) 8 (62) 330 (132–501) 264 (130–396) 206 (140–345) 55 (39) 30 (63) 10 (77) 16.824) 4276 (348–73. unless otherwise indicated.Ghanem et al. LL. RPR.034 (316–100. Author manuscript. MSM. . UD. stratified by lumbar puncture (LP) status.452) 86 (61) 31 (65) 8 (62) Characteristic Female sex Age. unknown duration. late latent.6 (23–68) 37. median (IQR) Previous history of syphilis NIH-PA Author Manuscript CD4 cell count.726) 3567 (178–63. men who have sex with men. mean years (range) Race Risk group for HIV infection RPR titer. (%) of patients. Page 10 Table 1 Demographic and clinical characteristics of patients included in the analyses. Data are no. interquartile range. median copies/mL (IQR) Use of HAART in previous 6 months NOTE. IQR. NIH-PA Author Manuscript Clin Infect Dis. rapid plasma reagin. NIH-PA Author Manuscript No LP (n = 141) Immediate LP (n = 48) Delayed LP (n = 13) 51 (36) 16 (33) 3 (23) 38. cells/mL Median (IQR) ≤350 cells/mL HIV RNA level.8 (24–55) 38.