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PEDIATRICS Vol. 107 No. 1 January 2001, pp. 67-72

Varicella Outbreak at a Summer Camp for Human Immunodeficiency Virus-Infected Children

Andrea G. Winquist, MD*, Dagger , Aaron Roome, PhD, MPHDagger , and James Hadler, MD, MPHDagger

From the * Epidemic Intelligence Service, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, Georgia; and Dagger  Connecticut Department of Public Health, Bureau of Community Health, Infectious Disease Division, Hartford, Connecticut.



    ABSTRACT
Top
Abstract
Background
Methods
Results
Discussion
References

Objectives.  Varicella can result in severe, persistent, or recurrent disease in human immunodeficiency virus (HIV)-infected children. In the summer of 1997, we were notified of a suspected varicella outbreak among attendees of a summer camp for HIV-infected children. We investigated this outbreak to determine the extent and sequelae of the outbreak, and to identify factors that contributed to the outbreak to identify measures for preventing such outbreaks at the camp in the future.

Design.  To identify varicella-susceptible persons and those developing varicella after camp and to evaluate the camp's varicella prevention measures, we reviewed camp records for the 110 campers and 96 staff at the implicated camp session, mailed questionnaires to the campers' parents/guardians and physicians, and interviewed susceptible staff. We defined a case as varicella in a person who attended the session with onset <= 21 days after the session ended.

Results.  Eleven of 31 susceptible children (36%) and 2 of 4 susceptible adults developed varicella. Two children were hospitalized. One developed cellulitis. Cases occurred among children in 5 of 15 cabins. The most likely index case was a child with active zoster at camp, reported to the camp after the session ended. The camp had varicella-prevention measures in place, but the varicella-susceptibility and exposure information provided to the camp was often incomplete or inaccurate. Staff with no varicella history underwent serologic testing, but susceptible staff members were not vaccinated.

Conclusions.  Widespread varicella transmission occurred at the camp. A case of zoster was the most likely source. The risk for such outbreaks can be minimized through vaccinating susceptible staff members, considering vaccination for asymptomatic or mildly symptomatic HIV-infected children according to Advisory Committee on Immunization Practices and American Academy of Pediatrics guidelines, rigorously collecting recent varicella and zoster exposure information, excluding anyone with active varicella or zoster or with recent varicella or zoster exposure, and considering varicella and zoster exposures at camp to be potentially camp-wide.varicella, human immunodeficiency virus infections, disease outbreaks, intravenous immunoglobulin.

Varicella is now a vaccine-preventable disease.1-4 However, among HIV-infected children, varicella vaccination currently can be considered only for those who are asymptomatic or mildly symptomatic, with CD4+ T-lymphocyte percentages of >= 25% (Centers for Disease Control and Prevention class N1 or A1).2,4 Before May 1999, varicella vaccination was not recommended for any children known to be HIV-infected.1,3 HIV-infected children who contract varicella have an increased risk for persistent, recurrent, or severe disease and commonly develop zoster at a young age.5-9

In the summer of 1997, the Connecticut Department of Public Health was notified of 5 HIV-infected children who contracted varicella after attending a summer camp in Connecticut. Initial interviews with camp staff and hospital group organizers revealed that 2 staff members and several additional campers from 3 states also had contracted varicella after camp, suggesting that varicella transmission had occurred at camp. In addition, after the camp session was over, the camp staff had been notified of a child who had active zoster while at camp. We investigated this outbreak to determine the extent and sequelae of the outbreak and to identify factors that contributed to the outbreak in order to identify measures for preventing such outbreaks at the camp in the future.


    BACKGROUND
Top
Abstract
Background
Methods
Results
Discussion
References

A total of 110 campers attended the implicated camp session, which was a special 5-day session for HIV-infected children. The children were from 4 states and most attended camp as part of groups organized through hospitals. Age range was 7 to 16 years. At camp, the children were grouped into 5 units according to age, with 3 cabins per unit.

The camp was aware of the need for precautions to prevent infections in immunocompromised children and specific varicella prevention measures were in place. The camp form asked about history of varicella, zoster, and varicella vaccination. Instructions to parents and guardians warned against sending children to camp if they had been recently exposed to varicella. A late changes form, to be submitted on arrival at camp if applicable, included questions about changes in laboratory tests and medications as well as the question, "Has the child had contact with varicella during the last 3 weeks?" To facilitate administration of prophylaxis if necessary, the camp compiled a list of varicella-susceptible children. The camp obtained a varicella history from all staff members before their employment. Any permanent staff member without a history of varicella underwent serologic testing. The camp had no recommendation regarding varicella vaccination for susceptible staff members.


    METHODS
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Abstract
Background
Methods
Results
Discussion
References

We reviewed the children's camp forms for demographic information, physician information, varicella and zoster history, medications, and information about recent varicella exposure. The camp form did not contain sufficient information to allow assessment of the overall clinical and immunologic status of the children. We reviewed staff members' camp forms for varicella susceptibility and interviewed susceptible staff members to determine whether they had developed varicella after the session. We also reviewed the infirmary's list of varicella-susceptible children and log of infirmary visits.

We mailed questionnaires to the parents or guardians of the children, requesting information about: 1) varicella history, 2) diagnosis of varicella after camp, 3) varicella exposure before camp, and 4) activities while at camp. Follow-up questionnaires were sent to nonrespondents. We also mailed questionnaires to each child's physician, requesting information about varicella and zoster history, diagnosis of varicella or zoster after camp, and history of varicella vaccination or receipt of varicella-zoster immune globulin (VZIG). Physicians who did not initially respond were contacted by phone. In some cases, information about varicella history and diagnosis of varicella after camp was obtained through the relevant state health department rather than directly from the physician. No other clinical information was collected from parents or physicians. Parents were contacted by telephone if there was discrepant information from various sources, if the physician reported development of varicella and the parents did not respond, or if only limited physician information could be obtained and the parents did not respond to the mailed questionnaire.

For the purposes of this investigation, we considered a child with no history of varicella or zoster from any source to be susceptible to varicella. The camp routinely performed serologic testing on permanent staff members who had no history of varicella. We considered a staff member to be susceptible to varicella if the person gave no history of varicella and had a negative serology (if it was performed). We defined a case as a report of varicella in a person who attended the implicated camp session, with rash onset within 21 days of the end of the session. The report could be from the parent, guardian or physician for a child, or from the staff members for themselves.

We analyzed the data by using EPI Info software.10 We used the method of Greenland and Robins 11 to calculate 95% confidence intervals (CIs) for relative risks (RRs). P values were calculated by using the Mantel-Haenszel adjusted chi 2 test.

This investigation was reviewed by the Centers for Disease Control and Prevention, Epidemiology Program Office, Assistant Director for Science and was deemed not to be research but to be a local disease control activity.12 Thus, the investigation was deemed not to require institutional review board review.


    RESULTS
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Abstract
Background
Methods
Results
Discussion
References

We reviewed the camp forms for all campers and staff. Questionnaires were returned for 57% of the children by parents/guardians and for 100% of the children by physicians (or by state health departments on behalf of physicians). All susceptible staff members were interviewed.

Thirty-one of the 110 children (28%) and 4 of the 96 staff members (4%) were susceptible to varicella. None of the children or susceptible staff members was known to have received varicella vaccine. Eleven cases of varicella were identified among 31 susceptible campers (attack rate: 35%), and 2 cases were identified among the 4 susceptible staff members (attack rate: 50%). Rash onset dates ranged from 9 to 17 days after the camp session ended (Fig 1). If exposure is assumed to have occurred on the last day of camp, the majority of cases had incubation periods of 12 to 17 days, similar to the usual incubation period for immunocompetent children.



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Fig. 1.   Distribution of rash onset dates for cases of varicella developing within 21 days of the end of the camp session in campers and staff who attended the summer camp session.

Two children were hospitalized for their illness. One child developed cellulitic lesions. None had reported evidence of visceral dissemination. The duration of the illness was provided for only 3 children, for whom reported durations were 10 to 12 days. Information about antiviral treatment for varicella was provided for 8 children, of whom 7 received antiviral treatment. The antiviral agent used was specified for 3 of the treated children, all of whom received acyclovir. The 2 staff members developing varicella had no complications.

Four children were reported as having developed varicella after camp but were not considered cases related to this outbreak. Two of these children had a previous history of varicella or zoster and 2 had onset >21 days after the end of the camp session. The first child had an episode of zoster 3 months before camp and had onset of new lesions ~6 days after camp ended, with a total of <10 lesions. The second child had an initial episode of varicella 5 months before camp, after a known exposure to a sibling with varicella. That child had onset of new lesions 22 days after camp ended, with lesions initially starting on the arm but later spreading to the rest of the body. The third child developed varicella 41 days after the end of the camp session. This child was regularly receiving intravenous immunoglobulin (IVIG) and had no known varicella exposure after camp. The fourth child developed varicella with onset at least 52 days after the end of the camp session. It is not known whether this child was receiving IVIG. These 4 children may have acquired varicella as a result of exposure at camp, but this cannot be determined with certainty.

The camp staff was not aware of any cases of varicella developing during the camp session. Review of infirmary records did not identify any visits for illnesses compatible with varicella or zoster. Three children were reportedly exposed to varicella before camp (2 reported only on the mailed parent questionnaires, 1 reported on the camp's late changes form). However, none of these exposed children developed varicella within 21 days of the end of the camp session, although 1 developed varicella at least 52 days after the end of the camp session.

After the camp session was over, the camp staff was notified of a child who had active zoster while at camp. The lesions involved 2 to 3 contiguous dermatomes on the chest (approximately T9, 10, and 11) and were unilateral. The child was admitted to the hospital for zoster within a day of leaving camp, and at that time, the child indicated that the lesions had been present at camp but were kept covered by clothing. There was no clinical evidence of disseminated disease. Camp staff members were not aware of the child's zoster during the camp session.

VZIG prophylaxis was not administered to children at the session. One child received VZIG shortly after the session for other reasons. However, several of the children were regularly receiving IVIG as part of their HIV treatment. The camp form asked whether the children were regularly receiving IVIG or blood transfusions as part of the assessment of the needs of the children at the camp. Only 1 of 9 susceptible children (11%) who were regularly receiving IVIG or blood transfusions developed varicella within 21 days of the end of the camp session, compared with 10 of 22 susceptible children (45%) who were not (RR: 4.09; 95% CI: .61-27.45; P = .07). If all susceptible children developing varicella after camp are included in the analysis (including the 2 children developing varicella >21 days after the camp session ended), 2 of 9 susceptible children (22%) who were regularly receiving IVIG or blood transfusions developed varicella, compared with 11 of 22 children (54%) who were not (RR: 2.25; 95% CI: .62-8.19; P = .16).

Among susceptible children, attack rates were higher among younger children than among older children. The attack rate among susceptible children was 86% (6/7) among children 7 to 8 years of age, 40% (4/10) among children 9 to 10 years of age, 14% (1/7) among children 11 to 12 years of age, and 0% among children 13 years of age and older (chi 2 for linear trend = 13.7; P < .001). Stratified analysis demonstrated that the differing attack rates by age were not attributable to differences in receipt of IVIG.

Examination of camp activities and living quarters did not suggest a single site where transmission occurred. No associations with camp activities were identified. Cases occurred in children in 3 of 5 units and 5 of 15 cabins (Fig 2). The kitchen worker who developed varicella stayed in a separate cabin area for staff only. Thus, varicella transmission at the camp seemed to be widespread.



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Fig. 2.   Diagram of cabin area of camp, illustrating the cabin locations of susceptible children, children developing varicella, children regularly receiving IVIG or blood transfusions, the counselor who developed varicella, and the case of active zoster at camp. Children developing varicella within 21 days after the camp session ended and those developing varicella >21 days after the camp session ended are represented separately. Two reported cases of varicella that developed in children with a history of previous zoster are also represented.

Assessment of the camp's varicella prevention measures documented that information regarding recent exposure to varicella had been completed for only 36 of the children (33%). One late changes form indicated that a susceptible child who attended camp had been exposed to varicella in the 3 weeks before camp. That child developed varicella at least 52 days after camp ended and was not counted as a case related to this outbreak. The infirmary's list of susceptible children omitted 6 susceptible children (19%) and listed 19 nonsusceptible children (24%). The majority of these discrepancies were caused by the camp receiving incomplete or incorrect information.


    DISCUSSION
Top
Abstract
Background
Methods
Results
Discussion
References

Widespread varicella transmission occurred at the camp session with an attack rate of 35% among susceptible children and 50% among susceptible staff. Because varicella susceptibility was determined based on parental and physician-provided history, the number of susceptible children may have been overestimated, and, thus, the attack rate among susceptible children underestimated, especially among older children. In a study of healthy children 7 to 12 years of age with negative or uncertain parent-provided varicella histories, 31% had positive varicella serologic tests.13 In the case of this outbreak, the percentage of nonsusceptible children among children with negative varicella histories was likely lower than this figure, because of the close medical attention that these children likely receive and the inclusion of physician-provided varicella histories in addition to parent-provided histories. However, we were not able to obtain further validation of susceptibility status.

Few of the affected children had immediate serious complications of varicella. One child was hospitalized and one developed cellulitis. None had evidence of visceral dissemination. Our finding of few immediate serious complications is consistent with the findings of most previous studies of groups of HIV-infected children with varicella.5-7,14-16 However, 2 reports have suggested a higher frequency of serious complications of varicella among HIV-infected children.8,9 One was a study of 38 HIV-infected Romanian children with varicella, of whom 14 developed complications, including superinfection of the skin, pneumonia, and thrombocytopenia.8 The other was a report of 8 HIV-infected children with varicella, of whom 7 developed serious complications, including pneumonia, hepatitis, involvement of the brain and pancreas, and death.9 Both of these studies included only cases for which complete clinical information was retrospectively available and may have preferentially included more severe cases. It is possible that the group of HIV-infected children at this camp was a relatively healthy population, compared with other populations of HIV-infected children with varicella; however, we did not assess the overall clinical and immunologic status of the children.

Studies of varicella in groups of HIV-infected children have found recurrence (as either recurrent varicella or zoster) and persistence to be a more frequent problem than immediate complications.5-7,15 The duration of illness and long-term consequences, such as recurrent varicella or zoster, were not assessed in our cohort. Thus, the full extent of the consequences of this outbreak is not known.

There were no known cases of varicella at the camp session. The child with the earliest known varicella onset had rash onset 9 days after the camp session ended and would have unlikely been infectious before leaving camp. One child with a history of zoster developed varicella 6 days after the end of the camp session. Even if this case were truly a reinfection rather than a reactivation, the child would have unlikely been infectious 6 days before rash onset. Based on the available information, the most likely index case was the case of active zoster at camp.

Localized zoster is considered less contagious than varicella or disseminated zoster because the respiratory tract is not involved. However, zoster in immunocompromised patients, even if it is apparently localized, is considered to be potentially disseminated and potentially infectious by the airborne route.17 Previous outbreaks of varicella have been reported for which the source patient was a patient with apparently localized zoster. In one report, an outbreak occurred in a day care center for which the index case was a previously healthy 3-year-old boy with typical localized zoster.18 In that case, transmission was thought to have been facilitated by the child's not keeping the lesions covered. Another report described a nosocomial outbreak for which the index patient was a 68-year-old woman with localized zoster who was being treated with dexamethasone.19 In that case, susceptible nurses who had not been in the index patient's room were infected, supporting the conclusion that airborne spread of virus had occurred. The possibility of airborne spread of virus from immunocompromised patients with zoster is also supported by a study that demonstrated that varicella-zoster virus (VZV) DNA could be isolated by polymerase chain reaction from air samples taken from the rooms of immunocompromised patients with localized zoster whose lesions were in areas normally covered by clothing.20 The potential for spread of infection from patients with zoster was also emphasized in a report on the 5-year experience at one hospital with nosocomial transmission from cases of varicella and zoster. The study documented that nosocomial transmission from zoster was more common than nosocomial transmission from varicella, possibly because less stringent or less prompt infection control measures were implemented for cases of zoster. In addition, they identified 2 patients who acquired varicella from other patients with zoster.21 Our findings support the conclusion that apparently localized zoster in an HIV-infected child can be the source of infection for other susceptible children and that covering the lesions with clothing is not adequate for prevention of spread of infection.

VZIG should be administered, within 96 hours of exposure, to susceptible HIV-infected children who are known to have had close contact with a person with varicella or shingles.22 In this outbreak, prophylaxis was not administered. However, in the case of previous known varicella exposures at the camp, only children in the same unit as the affected child were considered to require prophylaxis. Current recommendations for identifying persons exposed to a patient with varicella or zoster use the criterion of at least 1 hour of direct contact with an infectious person while indoors.1 However, some have argued that periods of face-to-face contact as short as 5 minutes indoors may warrant prophylaxis.23 In a summer camp setting, in which children may interact with several other children and durations of exposure can be difficult to assess, identifying the group of exposed children to receive prophylaxis can be difficult. In the case of this camp, children from various units and cabins participated together in several all-camp activities, and meals were eaten together in a single large dining hall. Thus, there were several opportunities for children from various cabins and units to be exposed to each other, and the extent of such exposures would be very difficult to assess. No single camp activity associated with development of chickenpox could be identified. The results of this investigation show that varicella exposures at camp are potentially camp-wide, and camp-wide prophylaxis should be considered.

IVIG can reduce the incidence of minor bacterial infections, viral infections, and serious bacterial infections in certain groups of HIV-infected children.24,25 Prophylactic use of IVIG or trimethoprim-sulfamethoxazole is recommended for HIV-infected children who have recurrent invasive bacterial infections.22 Prophylactic use of IVIG is also recommended for HIV-infected children who have hypogammaglobulinemia (immunoglobulin G <400 mg/dL).22 Thus, in a large cohort of HIV-infected children, one would expect to find several children regularly receiving IVIG, as was true in this outbreak. Although VZIG preparations have higher VZV antibody titers than IVIG preparations, VZV antibody titers have been found to be equivalent at 4 weeks after administration of either IVIG or VZIG, likely because of the larger volume of IVIG administered and incomplete absorption of intramuscularly administered VZIG.26 Thus, IVIG may offer protection against development of varicella in exposed persons. Current recommendations state that VZIG should be administered to children routinely receiving IVIG if the last dose of IVIG was administered >21 days before the exposure.22 However, the effectiveness of IVIG in preventing varicella in exposed HIV-infected children has been questioned because of several reports of HIV-infected children developing varicella after exposure despite regular receipt of IVIG.6,7,15,27,28 Development of varicella in exposed HIV-infected children despite receipt of VZIG has also been reported.14,15

In this outbreak, regular receipt of IVIG or blood transfusions seemed to offer some protection against development of varicella, although this association was not statistically significant. Detection of a significant association may have been hindered because of the small number of children, incomplete reporting of receipt of IVIG or blood transfusions, lack of information on the timing of last receipt of IVIG, and the fact that although most of the children reported on the camp form to be regularly receiving IVIG or blood transfusions were likely receiving IVIG, some may have been receiving other blood products. One child known to be regularly receiving IVIG developed varicella within 21 days of the end of the camp session. One other child known to be regularly receiving IVIG developed varicella 41 days after the end of the camp session. VZIG can cause a prolonged incubation period for varicella,6,29 and this may also be true of receipt of IVIG. Thus, this child may have been infected while at camp.

An effective live attenuated varicella virus vaccine is available. At the time of this outbreak, varicella vaccine was not recommended for HIV-infected children. This vaccine has recently been determined to be safe and effective for HIV-infected children who are asymptomatic or mildly symptomatic and have age-specific CD4+ lymphocyte percentages of >= 25%.2,4 The current recommendations of the Advisory Committee on Immunization Practices and the American Academy of Pediatrics state that varicella vaccine (2 doses 3 months apart) should be considered for this subgroup of HIV-infected children after weighing the potential risks and benefits.2,4 However, this vaccine is not currently recommended for other HIV-infected persons because of the possible risk for developing disease related to the vaccine virus and the lack of definitive studies of the safety and efficacy of the vaccine in this population.2 We were not able to assess exactly how many of the children attending this camp session would have been eligible to receive the vaccine under the new recommendations. However, based on available information, it is clear that many would not have been eligible.

Varicella vaccine is recommended for people who have close contact with immunocompromised persons, including health care workers and household contacts.1 At camps serving immunocompromised children, staff should prove immunity to varicella by providing a positive history of varicella, providing a positive serology, or receiving vaccination. Assessment of immunity status alone, without vaccination of staff members who are eligible, leaves open the risk of their developing varicella and potentially exposing immunocompromised children.

As part of a varicella prevention strategy, in addition to vaccination of susceptible staff, camps such as this one should implement as fully as possible policies like those already developed at this camp, designed to minimize the potential for varicella to be introduced and to facilitate quick VZIG administration, if necessary. These policies include collection of information regarding recent exposure to varicella or zoster, with exclusion or rescheduling of all recently exposed children, and maintenance of an accurate list of susceptible children. In addition, because zoster is not uncommon among HIV-infected children, parents and children should be informed that zoster can be infectious and that children with active zoster should not attend camp. However, the effectiveness of such policies is dependent on the camp being given accurate information regarding varicella susceptibility and exposure. In the case of this outbreak, children came to camp from out of state with groups from hospitals. Parents or guardians did not accompany most of the children when they arrived at camp. Many of the children were under the care of guardians or foster parents who may not have been able to provide accurate varicella history information. Thus, collection of complete and accurate information about varicella susceptibility and exposure was not always possible.

As vaccination rates in the community increase, the likelihood of an outbreak like this one occurring among the subset of HIV-infected children who cannot be vaccinated will be expected to decrease. However, the risk of such outbreaks occurring as a result of exposure to zoster will likely persist for some time in the absence of vaccination in this population. Thus, although careful infection control measures currently remain the most effective means of preventing such outbreaks, these measures cannot be expected to completely prevent outbreaks such as this one.


    ACKNOWLEDGMENTS

We thank Matthew Cartter, MD, MPH, for guidance during this investigation and review of the manuscript, and Howard Pearson, MD, FAAP, for assistance with the investigation and review of the manuscript.


    FOOTNOTES

This investigation was presented in part at the 47th Epidemic Intelligence Service Conference; April 20-24,1998; Atlanta, GA.

Received for publication May 11, 1999; accepted May 1, 2000.

Reprint requests to (A.G.W.) Centers for Disease Control and Prevention, 1600 Clifton Rd, MS D-18, Atlanta, GA 30333. E-mail: aiw1{at}cdc.gov


    ABBREVIATIONS

HIV, human immunodeficiency virus; VZIG, varicella-zoster immune globulin; CI, confidence interval; RR, relative risk; IVIG, intravenous immunoglobulin; VZV, varicella-zoster virus.


    REFERENCES
Top
Abstract
Background
Methods
Results
Discussion
References
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Pediatrics (ISSN 0031 4005). Copyright ©2001 by the American Academy of Pediatrics

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