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Joint Infectious Diseases Conference: Venkata G. Meka October 17, 2001 Case Presentation: CC: “Rash all over” HPI: Patient was a 36 year-old white male HIV + (CD4 19, viral load 450K as of July 10, 2001). Approximately 2 weeks prior to presentation, he was exposed to 2 toddlers who had not had their vaccinations and subsequently developed measles. Then, 7 days ago, he developed coryza and cough. Then, 5 days ago, he developed a maculopapular rash that began on his chest and then moved to his face, back, and extremities. The rash eventually became pruritic, blanching, and then confluent. It subsequently moved into his palms and soles. He also experienced fever and intermittent headaches. He denied photophobia or nuchal rigidity. Review of systems was otherwise unremarkable. In terms of vaccinations, he remembered getting a killed measles vaccine as a child. PMH: 1. HIV: diagnosed in 1987 history of PCP pneumonia in 1992, requiring intubation and ICU stay followed at the Fenway Clinic 2. Asthma 3. No surgical history Allergies: Penicillin (angioedema) Medications: 1. Bactrim DS 1 tablet orally once daily 2. Diflucan 100 mg tablet orally once daily 3. No HAART therapy (to start new regimen soon, has been off meds since December 2000) Social History: Homosexual, lives with his partner Denies tobacco, illicit drug use Alcohol socially (occasional beer or glass of wine at parties) Physical Exam: Vitals 99.6 106 133/85 20 97% (RA) Gen resting comfortably HEENT no scleral icterus, no sinal tenderness, no conjunctivitis anterior cervical lymphadenopathy bilaterally posterior pharynx without erythema, exudates, or Koplik’s spots Heart regular rate and rhythm; no murmurs, rubs, or gallops Lungs clear to auscultation bilaterally Abdomen soft, nontender, nondistended, bowel sounds present no masses or organomegaly Extremities no edema blanching rash confluent on face and trunk morbilliform on extremities and involving palms, soles Labs: none drawn at this point Imaging: none done at this point Background: Given this presentation, our differential included a drug reaction to Bactrim, atypical measles, or classic measles. He had already taken his Bactrim that day, but we held any subsequent doses. Given the history of receiving the killed vaccine, this could have been atypical measles. This is a syndrome described in people that were administered the killed measles vaccine and then years later were exposed to wild measles virus. In the setting of undetectable or very low measles antibody titer, these patients developed unusual manifestations of measles followed by the appearance of extremely high measles antibody titers. The symptoms included a prodrome of fever and pain for 1-2 days and then the appearance of a rash. Differing from classic measles, the rash began peripherally and could be urticarial, maculopapular, hemorrhagic, and/or vesicular. Patients also had edema of the extremities, interstitial pulmonary infiltrates, hepatitis, and occasionally a pleural effusion. The syndrome had a prolonged course and could be fatal. Of note, no measles virus has been isolated from these patients, and they do not appear to transmit measles to others. (1,2,3) In regards to the possibility of classic measles, there are three questions that will be addressed. First, how does HIV infection affect immunity to measles? Second, how does measles infection present in HIV-infected individuals? Third, should HIV-infected individuals be vaccinated for measles? How does HIV infection affect immunity to measles? : In 1990, the CDC reported 27,786 cases of measles; and although this new epidemic mainly affected children, 15%-20% of those cases were in adults. Also, the associated case fatality rate of 3.2 deaths per 1,000 cases reported was the highest rate reported in 30 years. (4) Then in 1991, Glaser et al. conducted a study of the prevalence of measles antibodies among HIV-infected New York State prison inmates. (5) Fifty-one HIVinfected inmates consented to measles antibody testing. Fifty of the inmates had a history of intravenous drug use. CD4 counts ranged from greater than 500 cells/mm3 (13 of 51), 200-500 cells/mm3 (16 of 51), and less than 200 cells/mm3 (22 of 51). Six of 51 (11.8%) were seronegative for measles. This included 3 born after January 1, 1957 and 3 born before 1957. None of the inmates could readily provide proof of vaccination. Does the presence of HIV infection identify a group that is at high risk for measles infection, as measured by a lack of serum antibody to measles? Also, does HIVrelated immunodeficiency over time lead to a loss of measles antibody and thereby, leave the HIV-infected individual vulnerable to measles infection? (6) Brunell et al. looked at the measles antibody response in HIV-infected babies, children, and adults. They hypothesized that severe measles occurs in immunized as well as nonimmunized HIV-infected individuals and suggested that both immunologic memory and the initial response to measles may be impaired by HIV infection. That the initial response is affected was supported by the finding that post-measles immunization titers of HIV-infected babies were significantly lower (p=0.01) than those of normal babies. Poor immunologic memory was evidenced in HIV-infected children by lower titers than in normal children (p<0.001) and by a continuing decline in measles antibody that was not arrested by reimmunization. Impaired memory appeared to be associated with defective avidity maturation. HIV-infected babies and infants or children had a significantly lower avidity index (AI) than age-matched normal children (p<0.01). AI increases during the first few months after infection and has been used to differentiate recent from remote infections. HIV-infected adults, who were infected with HIV after exposure to measles, did not have AI values significantly different from normal adults (p=0.18) but had significantly greater values than did HIV-infected babies and children (p<0.01). They concluded from this that the adult immune response to measles was less affected. (7) Several studies subsequently looked at the prevalence of measles antibody in HIV-infected adults. (8,9,10,11) Zolopa et al. conducted a retrospective cohort study involving 172 HIV-negative and 299 HIV-positive homosexual men. They found no relationship between changes in the CD4 cell count and measles antibody level. Sha et al. looked at 105 asymptomatic HIV-seropositive adults and screened them for measles antibody. They found that neither the presence nor the level of antibody were predictable from patient age, history of measles or immunization, CD4 count, percentage of CD4 cells, or CD4:CD8 ratio. Kemper et al. looked at the seroprevalence of measles antibody in 619 HIV-infected adults and evaluated risk factors for lack of antibody and presumed susceptibility to measles. Neither minority status, stage of HIV infection, CD4 cell count, nor a history of opportunistic infection was found to be related the presence/absence of antibody. Finally, Wallace et al. conducted a prospective survey of 210 HIV-infected adults and found that 95% of the adults had demonstrable antibodies using a standard ELISA technique. How does measles infection present in HIV-infected individuals? : Severe measles may occur in patients with compromised or deficient cellular immunity such as those with HIV infection. Kaplan et al. looked at measles cases occurring in immunocompromised patients from 1989-1990. They also combined this with cases recorded in the literature. They found that the case fatality rate for severe measles in children and young adults was calculated to be 70% in 40 oncology patients and 40% in 11 HIV-infected patients. In the oncology patients, 40 percent had no rash, 58 percent had pneumonitis, and 20 percent had encephalitis. In the HIV-infected population, 27 percent had no rash and 82 percent had pneumonitis. (12) In addition, measles virus can cause 3 major CNS syndromes. Acute encephalitis is thought to be an autoimmune process occurring during recovery from measles and involves a recrudescent fever, headaches, seizures, and changes in mental status. Subacute sclerosing panencephalitis (SSPE) presents after a latent period and presents with the insidious onset of mental deterioration and later of motor dysfunction. Symptoms progress to seizures, coma, and death within 1-2 years. Finally, acute encephalitis of the delayed type (also called subacute measles encephalitis, SME) is usually seen in immunocompromised patients. Encephalitic signs and symptoms such as seizures, myoclonus, stupor, and coma usually develop 1 to 10 months after measles infection. (13, 14) Should HIV-infected individuals be vaccinated for measles? : Recognizing the potential for serious complications from measles infection in HIV-infected people, the Advisory Committee on Immunization Practices (ACIP) addressed this in their report in 1998. (15) Among HIV-infected patients with no evidence of severe immunosuppression (see Table 1), there have been no reported serious adverse events after measles vaccination. (16) The current recommendation, therefore, is that MMR vaccination is recommended for all asymptomatic HIV-infected patients who do not have evidence of severe immunosuppression. Also, MMR vaccination should be considered for all symptomatic HIV-infected patients who do not have evidence of severe immunosuppression. Table 1. Age-specific CD4 T-lymphocyte count and percent of total lymphocytes as criteria for severe immunosuppression in persons infected with human immunodeficiency virus (HIV) Total CD4 T-lymphocytes or CD4 T-lymphocytes (as % of total lymphocytes) <12 mos <750/uL or <15% 1-5 yrs <500/uL or <15% Age 6-12 yrs <200/uL or <15% ≥13 yrs <200/uL or <14% Of note, transient increases in HIV viral load have been observed after administration of other vaccines to HIV-infected patients. (18, 19) This hasn’t been studied in reference to the MMR vaccination, so the clinical significance of this observation is not known. Measles vaccine is not recommended for HIV-infected persons with evidence of severe immunosuppression (as outlined in Table 1) for several reasons. This includes a case of progressive measles pneumonitis in patient with HIV and severe immunosuppression to whom the MMR vaccine was administered. (18) In this case, on September 3, 1992, a 20 year-old man with hemophilia A and HIV infection received the MMR vaccination to fulfill a college prematriculation vaccination requirement for a second dose of measles vaccine. He had gotten a previous dose of measles vaccine in 1973. His CD4 count was reported as “too few to enumerate” as of August of the same year. Also, at the time of the second dose, he did not have any HIVrelated symptoms, was not taking any antiretroviral therapy, or taking prophylaxis for Pneumocystis carinii. On August 31, 1993, he was hospitalized for worsening dyspnea, fever, nonproductive cough, and weight loss. Eventually, he underwent an open-lung biopsy on October 6 that revealed numerous multinucleate giant cells, and some contained both intranuclear and cytoplasmic eosinophilic inclusions suggestive of viral infection. On October 22, measles virus was identified from tissue-culture cells inoculated with the lung biopsy tissue. The patient was started on ribavirin therapy on October 23, and his condition slowly stabilized. He later was discharged home. He was readmitted on November 12th for increasing shortness of breath and found to have bilateral pulmonary infiltrates. Following the onset of encephalopathic changes, he died on December 17th. Although the reported immediate cause of death was cytomegalovirus (CMV) encephalitis, pulmonary measles and Mycobacterium avium complex (MAC) infection were listed as contributing causes. Also, further analysis of the measles virus isolate recovered from the lung biopsy tissue showed a high degree of similarity between the patient’s virus isolate and the Moraten vaccine virus strain. Summary: 1. Atypical measles is a syndrome described in people that were administered the killed measles vaccine and then years later were exposed to wild measles virus. The symptoms differed from classic measles, and the clinical course could be prolonged, possibly even fatal. 2. HIV-infected adults have a level of immunity to measles that appears to be comparable to that found in non-HIV-infected populations. Once measles immunity (as determined by the presence of protective antibodies) is established in the HIV-infected patient, it is maintained despite progression of HIV-related immunodeficiency. 3. The presentation of measles in HIV-infected patients can be severe and include complications such as giant cell pneumonitis and subacute measles encephalitis (SME). 4. Current recommendations for measles vaccination of HIV-infected patients is based on the degree of immunosuppression. It is not recommended for HIV-infected patients with evidence of severe immunosuppression. References: 1. Ramh LW. Schmidt R. Measles immunization with killed virus vaccine. Am J Dis Child. 1965;109:232. 2. Fulginiti. VA, Eller JJ, Downie AW, et al. Altered reactivity to measles virus. JAMA. 1967;202:1075. 3. Frey HM, Krugman S. Atypical measles syndrome: unusual hepatic, pulmonary, and immunologic aspects. Am J Med. 1981:281:55. 4. Centers for Disease Control. Measles- United States, 1990. MMWR 1991;40:369-72. 5. Glaser JB. DeCorato Dr. Greifinger R. Measles antibody status of HIV-infected prison inmates. J AIDS 1991;4:540-1. 6. Zolopa AR. Kemper CA. Shiboski S., et al. Progressive immunodeficiency virus does not lead to waning immunity to measles in a cohort of homosexual men. Clin Infect Dis 1994;18:636-8. 7. Brunell PA. Vimal V. Courville TM., et al. Abnormalities of measles antibody response in human immunodeficiency virus type 1 (HIV-1) infection. J Acquired Immune Defic Syndr Hum Retroviral 1995; Dec 15;10(5):540-8. 8. Zolopa AR. Kemper CA. Shiboski S., et al. Progressive immunodeficiency virus does not lead to waning immunity to measles in a cohort of homosexual men. Clin Infect Dis 1994;18:636-8. 9. Sha BE, Harris AA, Benson CA, et al. Prevalance of measles antibodies in asymptomatic human immunodeficiency virus-infected adults. J Infect Dis 1991; 164:973-5. 10. Kemper CA, Ganger M, Arias G, Kane C, et al. The prevalence of measles antibody in human immunodeficiency virus-infected patients in northern California. J Infect Dis 1998 Oct;178(4):1177-80. 11. Wallace MR, Hooper DG, Graves SJ, et al. Measles seroprevalence and vaccine response response in HIV-infected adults. Vaccine 1994 Oct;12(13):1222-4. 12. Kaplan LJ, Daum RS, Smaron M, et al. Severe measles in immunocompromised patients. JAMA 1992 Mar 4;267(9):1237-41. 13. Gazzola P., MD, Cocito L., MD, Capello E., et al. Subacute measles encephalitis in a young man immunosuppressed for ankylosing spondylitis. Neurology 1999;52:107480. 14. Mustafa MM, Weitman SD, Winick NJ, et al. Subacute measles encephalitis in the young immunocompromised host: report of two cases diagnosed by polymerase chain reaction and treated with ribavirin and review of the literature. Clin Infect Dis 1993 May;16(5):654-60. 15. Centers for Disease Control: Recommendations of the Advisory Committee on Immunization Practices (ACIP). Measles, Mumps, and Rubella- Vaccine Use and Strategies for Elimination of Measles, Rubella, and Congenital Rubella Syndrome and Control of Mumps: MMWR 1998:47:1-57. 16. Sprauer MA. Markowitz LE. Nicholson JKA, et al. Response of human immunodeficiency-infected adults to measles-rubella vaccination. J AIDS 1993; 6: 10131016. 17. Centers for Disease Control: Recommendations of the Advisory Committee on Immunization Practices (ACIP). Measles, Mumps, and Rubella- Vaccine Use and Strategies for Elimination of Measles, Rubella, and Congenital Rubella Syndrome and Control of Mumps: MMWR 1998:47:21. 18. Centers for Disease Control: Recommendations of the Advisory Committee on Immunization Practices (ACIP). Measles Pneumonitis Following Measles- MumpsRubella Vaccination of a Patient with HIV infection, 1993: MMWR 1996:45(28):603606.