Published online November 1, 2007
PEDIATRICS Vol. 120 No. 5 November 2007, pp. e1345-e1349 (doi:10.1542/peds.2004-1681)
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EXPERIENCE & REASON

Severe Varicella Caused by Varicella-Vaccine Strain in a Child With Significant T-Cell Dysfunction

Patrick Jean-Philippe, MDa,b, Abigail Freedman, MDa,b, Mary Wu Chang, MDa,c, Sharon P. Steinbergd, Anne A. Gershon, MDd, Philip S. LaRussa, MDd and William Borkowsky, MDa,b

a Department of Pediatrics
b Saul Krugman Division of Infectious Diseases and Immunology
c Ronald O. Perelman Department of Dermatology, New York University School of Medicine, New York, New York
d Division of Infectious Diseases, Department of Pediatrics, Columbia University Medical Center, New York, New York

ABSTRACT

In March 1995, the US Food and Drug Administration approved a live attenuated varicella vaccine for use in healthy children 12 months to 12 years old. We report here an 18-month-old girl with cell-mediated immunodeficiency who developed a severe vaccine-associated rash and clinical evidence of vaccine-associated pneumonia 1 month after inadvertent receipt of varicella vaccine.

Key Words: varicella • vaccine adverse reaction • immunodeficiency

Abbreviations: LAVV, live attenuated varicella vaccine • Ig, immunoglobulin • PCR, polymerase chain reaction • VZV, varicella-zoster virus • WT, wild type

In March 1995, after >20 years of testing, the US Food and Drug Administration approved a live attenuated varicella vaccine (LAVV) for prevention of varicella in susceptible healthy individuals 12 months of age or older.1 This vaccine, the Oka strain, was developed in Japan by Takahashi et al2 and had been used there since 1974.3 Because of the severe morbidity of varicella in immunocompromised persons, early US trials were conducted in leukemic patients as well as in healthy children, with excellent efficacy and safety profiles resulting.4,5 However, vaccine use in many immunocompromised populations has remained contraindicated or restricted because of fear that vaccine virus might cause disease in these patients.6–9 Here we report 1 such instance: a case of severe disseminated vaccine-strain varicella in a child with an uncharacterized cell-mediated immunodeficiency.

CASE REPORT

An 18-month-old black girl was admitted to Bellevue Hospital (New York, NY) with a 4-day history of fever and increasing numbers of papulovesicular/pustular skin lesions. The rash was first noted on the patient's trunk 6 days before admission when she began having intermittent fevers. At that time, she was seen by her primary physician as an outpatient and evaluated by a pediatric dermatologist. Since that time, the lesions had become generalized, and on admission they covered her entire body including her scalp, palms, and soles. A culture from blood drawn 4 days before admission did not grow any bacteria, but a culture from 1 of the pustules revealed infection with methicillin-resistant Staphylococcus aureus. Three days before admission, she was started on benzathine penicillin and erythromycin, but the rash continued to progress. On the evening before admission she was brought to the emergency department because of a fever of 103°F.

Medical History
This patient's medical history was significant for preterm delivery at 32 weeks' gestation via cesarean section, secondary to maternal prolactinoma and polyhydramnios. At birth she was noted to have choanal atresia and a patent ductus arteriosus; a choroid plexus cyst was also noted on computed tomography of the head, and bilateral renal calculi were seen on ultrasound. The result of prenatal testing of the patient's mother for HIV antibody was negative, and the result of testing of the patient for HIV antibody as part of the state's newborn screening program was also negative. In the early postnatal period she required both a tracheostomy and gastrostomy-tube placement. Although her anomalies suggested a congenital syndrome, a specific diagnosis was not established at birth or through subsequent investigation.

The finding of persistent lymphopenia on serial lymphocyte count and the absence of a thymic shadow on chest radiograph raised the suspicion of DiGeorge anomaly, but results of a fluorescent in situ hybridization study to detect the 22q11.2 deletion were negative. However, initial determination of lymphocyte subsets revealed severe depletion of both CD4 and, particularly, CD8 subsets, with normal or increased B cells (CD19) and natural killer cells (CD56). Lymphocyte-proliferation assays also revealed absent proliferation to standard mitogens. This trend would persist, albeit with some normalization of CD4 percentage, until this admission (Table 1). In addition to her deficits in cellular immunity, the patient also had severe humoral dysregulation. Although her immunoglobulin (Ig)G, IgM, and IgA concentrations were within normal limits for her age, she failed to produce protective antibody titers to tetanus toxoid and Haemophilus influenza type B after immunization. Further workup of her immunodeficiency included testing for genotypes of severe combined immunodeficiency, such as ZAP-70 deficiency and associated promoter mutations, all of which were unremarkable. Because of the nursing care her tracheostomy required, she was placed in a chronic care facility.


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  		TABLE 1 Longitudinal Immunologic Data

 
Before this admission, the patient had been hospitalized multiple times. During several admissions for exacerbations of chronic reactive airway disease, test results of nasopharyngeal aspirates were positive for respiratory syncytial virus. On 1 of these admissions, at 9 months of age, the patient suffered an exacerbation of her chronic ichthyosiform rash that was manifested by diffuse erythroderma, alopecia, and electrolyte disturbances. Quantitative Igs at that time revealed markedly elevated serum IgE (36000 IU); however, her clinical course was not felt to be compatible with Job syndrome because of absent history of deep organ abscess. A diagnosis of Netherton syndrome was considered but not supported by the results of skin biopsy and hair-shaft examination. Furthermore, molecular testing results were negative for mutation on SPINK5. The diagnosis of Omenn syndrome was also considered, but testing for RAG1 and RAG2 was not performed. Despite the gastrostomy tube, she continued to suffer from failure to thrive and weighed only 8.6 kg at 18 months of age, with profound developmental delay. No cause for her immunodeficiency was ever elucidated, but because of this condition, her physician advised that she receive no live vaccines. Nevertheless, 5 weeks before her admission, she was given Varivax (Merck and Co, West Point, PA), the LAVV.

Hospital Course
On admission, the patient was awake, alert, responsive, and moving all extremities. She was afebrile but hypertensive, tachycardic, and tachypneic and had a blood pressure of 120/80 mmHg, a heart rate of 150 beats per minute, and respiratory rate of 45/minute on 28% O2 via a tracheostomy collar. There were generalized erythematous-based vesicles and pustules, including on her palms, soles, scalp, and trunk, with the highest concentration being in the genital area. Her breath sounds were coarse, with occasional wheezes; her liver was palpable 3 cm below the costal margin, but laboratory testing on admission revealed a normal complete blood count, chemistry, and liver function.

The patient was admitted with a preliminary diagnosis of staphylococcal pustulosis, but because of the mixed nature of the lesions and the history of varicella immunization, treatment was begun with intravenous vancomycin, intravenous ceftriaxone, and intravenous acyclovir. A 3-mm punch biopsy was performed by the pediatric dermatology service, 2 vesicles on the dorsum of the left foot were unroofed for bacterial, fungal, and viral cultures, and a Tzanck smear was obtained; the results of these tests were negative. On hospital day 4, fluid obtained from 1 of the vesicles was sent to Columbia University for a diagnostic polymerase chain reaction (PCR) and viral strain determination.

New lesions continued to appear for >1 week, for a total of >14 days after initial appearance of the rash, and the patient continued to have low-grade fevers and mild respiratory distress. A chest radiograph on hospital day 4 revealed bilateral patchy consolidation. Two punched-out ulcers appeared on her left flank and another on her left frontal scalp; all 3 were >1 cm in diameter and surrounded by 3 to 4 cm of erythema and induration. On hospital day 4, the pathology report on the biopsy reported results consistent with a herpesvirus infection, although differentiation between herpes simplex virus and varicella-zoster virus (VZV) was not possible. On the 4th hospital day, the PCR was reported positive for vaccine-strain (Oka) varicella. After the 9th hospital day, new lesions gradually diminished, and by the 17th hospital day, the punched-out ulcers began to fill with granulation tissue. Although the patient's hospital course was complicated by S aureus bacteremia and candidemia, as well as methicillin-resistant S aureus superinfection of the primary lesions, her varicella continued to improve after this point. After a lengthy and difficult hospital course, she was discharged back to her chronic care facility on the 55th hospital day.

The patient was subsequently readmitted on several occasions for ulcerated skin lesions and respiratory illness. VZV was never isolated from any specimen. Her lymphocyte-proliferation responses remained severely depressed, and she eventually died at 2 years, 2 months of age from respiratory failure.

DISCUSSION

In March 1995, the US Food and Drug Administration approved an LAVV (Varivax) after almost 2 decades of clinical trials had shown it to be safe, effective, and immunogenic.4,10 The Advisory Committee on Immunization Practices initially recommended that the use of this vaccine be restricted to healthy children 12 months to 12 years of age.1 Subsequent updated recommendations of the Advisory Committee on Immunization Practices allowed its use to be considered in asymptomatic or mildly symptomatic HIV-infected children in Centers for Disease Control and Prevention class N1 or A1 with an age-specific CD4+ T-lymphocyte percentage of ≥25%,11 and it was recently shown to be safe and immunogenic in HIV-infected children with a CD4 percentage between 15% and 24%.12

Although the genetic basis of vaccine-strain attenuation is still being elucidated, specific phenotypic correlates have been proposed. In experiments using the human severe combined immunodeficiency mouse model, the vaccine strain has shown decreased ability to replicate in skin compared with the wild-type (WT) strain.13 It has also demonstrated decreased transmissibility compared with WT; secondary transmission of varicella-vaccine strain from a vaccine recipient with rash to close contacts has been documented in only a few instances14–17 and has been significantly less than what would be expected from WT strain. Finally, evidence indicates decreased propensity to reactivate as herpes zoster,18,19 although such cases have been reported.17,20

The mechanism by which the vaccine strain confers protection has yet to be elucidated conclusively; however, it has been speculated that production of nonreplicating immunogenic viral particles at the site of inoculation, as well as decreased infectivity for the skin compared with the WT strain, allows time for the induction of an adaptive VZV-specific cell-mediated immune response before viremia occurs.21 Previous studies have shown that the extent of VZV-specific T-cell response 3 days into the course of the disease determines the extent of the rash in WT infection.22,23 Patients with impaired cellular immune responses can have viremia after vaccine administration. However, in most clinical studies performed before and after licensure, varicella vaccine has proved to be safe and effective in healthy recipients.4,17,24,25 A recent study performed in 3 active surveillance sites showed significant reduction in the number of new cases of varicella after introduction of the vaccine.25 Subsequent studies have also demonstrated a substantial health care impact of the vaccine, including significant reduction in VZV-related hospitalizations,26,27 emergency department visits,26 medical expenditures,27 and mortality in all age groups.28 The latter effect was highest in the 1- to 4-year-old age group, with 92% reduction in varicella-induced mortality.

LAVV has also shown a favorable profile in some categories of immunocompromised patients, especially leukemic children for whom most of the data are available. As in healthy children, the most common adverse event after immunization is a mild vaccine-associated rash, usually maculopapular and vesicular, that occurs ~1 month after immunization in 5% of vaccine recipients who are not receiving chemotherapy and in up to 50% of leukemic children who are receiving chemotherapy at the time of immunization.29,30 It also protected 86% of leukemic vaccine recipients from household exposure to chickenpox.31,32 Using Varilrix (SmithKline Beecham, Rixensart, Belgium), Leung et al33 reported a good safety and immunogenicity profile on pediatric patients with hematologic cancers in maintenance phase or solid tumors 3 to 6 months after discontinuation of chemotherapy.34 Recent data on a limited number of pediatric solid organ (kidney, liver, and intestine) transplant recipients suggested that varicella vaccine is also safe and immunogenic in this immunosuppressed population.34,35

The patient described in this report had profound impairment of cellular immune function as well as impaired humoral responses. Intensive genetic and immunologic workup never identified an etiology for her immunodeficiency. At 17 months of age the patient inadvertently received LAVV and, 28 days later, developed a vesicular eruption that consisted of hundreds of new lesions that appeared as late as 2 weeks after onset of the eruption despite antiviral therapy. The appearance and evolution of these lesions, described above, were consistent with the appearance of WT VZV in immunocompromised patients; although the patient had lesions of variable sizes, the eruption was monomorphic (ie, lesions evolved synchronously), in contrast to varicella in a normal individual on whom the lesions evolve asynchronously (new lesions mixed with healing, older lesions). In addition, the concurrent tachypnea, oxygen requirement, and appearance on a chest radiograph of bilateral patchy infiltrates are suggestive of varicella pneumonia. Previous reports have used similar criteria for diagnosis of varicella pneumonia in immunosuppressed patients.36 A VZV PCR using restriction fragment length polymorphism revealed a pattern consistent with Oka vaccine virus strain: presence of a novel BglI site in gene 53 and absence of a PstI site in gene 38.37

Review of the literature reveals few reports of serious adverse effects associated with varicella-vaccine strain in immunocompromised patients: a 19-year-old adolescent with primary sclerosing cholangitis and lymphopenia who developed a severe varicella-vaccine–induced vesicular eruption after receipt of varicella vaccine38; a 13-month-old boy subsequently diagnosed with adenosine deaminase deficiency who developed hepatitis and a generalized vesicular eruption caused by the Oka vaccine strain39; a 16-month-old boy with HIV infection and a CD4 count of 8 cells per mm who developed Oka vaccine-strain–induced pneumonitis40; a 5-year-old boy with cerebral palsy and reactive airway disease who received a dose of varicella vaccine 7 days after completing a steroid taper and restarted on steroid therapy 8 days after receiving the vaccine who developed a rash and pneumonia, with the Oka vaccine strain recovered from his endotracheal secretions; an 11-year-old girl diagnosed with a natural killer T cell deficiency who developed rash and severe pneumonitis caused by Oka-strain infection 5 weeks after receipt of LAVV41; and a 1-year-old boy vaccinated with the Oka strain shortly before diagnosis with a neuroblastoma that required intensive chemotherapy. Although the 1-year-old boy did not contract acute varicella, he subsequently developed chronic disseminated herpes zoster that was shown to be caused by the vaccine strain.42 A 24-year-old resident of a developmental center with panhypopituitarism who was receiving physiologic doses of daily steroids developed a diffuse febrile vesicular rash and roentgenographic evidence of right basilar pneumonia 18 days after receipt of varicella vaccine, although the presence of vaccine strain was not demonstrated.43

CONCLUSIONS

This case report illustrates the fact that, although VZV vaccine has been proven to be safe in immunocompetent patients, it is potentially dangerous in patients with altered immunity, especially those with severely suppressed cell-mediated immunity, in whom it can produce long-lasting severe generalized eruption or organ dissemination. Although it may not be cost-effective to perform routine immunodeficiency screening in all apparently healthy children who present for vaccination with LAVV, particular attention should be paid to clues such as abnormal anthropomorphic data to detect patients who might be at increased risk of immunodeficiency and, therefore, at increased risk of adverse effects from vaccination with LAVV. This case also highlights the fact that if immunodeficiency is suspected, assessment of function in addition to phenotype should be conducted before excluding it.

FOOTNOTES

Accepted Apr 23, 2007.

Address correspondence to Patrick Jean-Philippe, MD, Henry M. Jackson Foundation for the Advancement of Military Medicine, National Institute of Allergy and Infectious Diseases/Department of Defense Liason Office, 6700A Rockledge Dr, 2nd Floor, Bethesda, MD 20892. E-mail: jeanphilippep{at}niaid.nih.gov

Address reprints requests to William Borkowsky, MD, Department of Pediatrics, Division of Infectious Diseases and Immunology, New York University School of Medicine, 550 First Ave, New York, NY 10016. E-mail: borkow01{at}gcrc.med.nyu.edu

Dr Freedman's current affiliation is Pediatric Center for Special Studies, New York Presbyterian Hospital/Weill Cornell Medical Center, New York, NY.

Dr Chang's current affiliation is Connecticut Children's Medical Center, Pediatric Dermatology, Hartford, CT.

Financial Disclosure: Dr Gershon consults and lectures for Merck and GlaxoSmithKline on varicella vaccine. The other authors have indicated they have no financial relationships relevant to this article to disclose.

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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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