Vaccine Preventable Diseases in Australia, 2005 to 2007

3.16 Varicella-zoster virus infection

Page last updated: 24 December 2010

The varicella-zoster virus (VZV) is so named because it causes two distinct illnesses: varicella (chickenpox), following primary infection, and herpes zoster (shingles), following reactivation of latent virus. Varicella is a highly contagious infection with an incubation period of 10–21 days, most commonly 14–16 days, after which a characteristic rash appears. Acute varicella may be complicated by secondary bacterial skin infections, haemorrhagic complications, cerebellitis, encephalitis, and viral and bacterial pneumonia.1,2 About 5% of infections are subclinical.3

In unvaccinated populations, varicella is primarily a childhood illness with more than 80%–90% of the population in temperate countries developing clinical or serological infection by adolescence.4,5 Varicella is generally a benign, self-limiting illness in children, but morbidity and mortality rates are higher in adults,6 at the extremes of ages, and in the immunocompromised.7 Varicella also causes congenital disease that can severely affect newborns of non-immune women.8 Varicella-zoster virus has been responsible for a significant disease burden, including hospitalisations and deaths, in Australia and New Zealand.9 Routine use of varicella vaccine in childhood was first recommended in Australia in 2003, and, in November 2005, varicella vaccination was funded under the National Immunisation Program for all children using a single dose schedule at 18 months of age, and in a school-based catch-up program at 10–13 years of age for those with no history of disease or previous vaccination.

Herpes zoster or shingles is a sporadic disease, caused by reactivation of latent VZV in sensory nerve ganglia. It is usually self-limiting and is characterised by severe pain with dermatomal distribution, sometimes followed by post-herpetic neuralgia which can be chronic and debilitating in the elderly.10,11 Although herpes zoster can occur at any age, most cases occur after the age of 50 with the incidence of complications also increasing with age.12 However, children infected in utero or those who acquire varicella before the age of 1 year, and patients on immunosuppressive drugs or infected with human immunodeficiency virus, are also at increased risk of herpes zoster.13–15 A new herpes zoster vaccine which is over 60% effective in reducing the burden of herpes zoster and post-herpetic neuralgia16 has been available on the private market in Australia since 2008. The zoster vaccine is formulated from the same VZV strain (Oka-derived) as the licensed varicella (chickenpox) vaccines but is of higher potency (at least 14 times greater).

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Case definitions

Hospitalisations and deaths

The ICD-10-AM/ICD-10 code B01 (varicella [chickenpox]) was used to identify varicella hospitalisations and deaths. The ICD-10-AM/ICD-10 code B02 (zoster [shingles]) was used to identify herpes zoster hospitalisations and deaths.

South Australian notification data

Varicella, herpes zoster and unspecified VZV-related disease have been notifiable in South Australia since 2002, and became nationally notifiable in 2006 in all Australian jurisdictions except New South Wales. However, data was not received from all notifying states until early 2008. The methods of reporting vary among states and territories.

South Australian notification data are included in this report. Cases notified in South Australia meet the following case definition: Clinical diagnoses of chickenpox or herpes zoster by a medical practitioner, and/or laboratory diagnoses of varicella-zoster virus infection. Due to the dual notification system in South Australia, laboratory reports are initially classified as ‘Varicella virus (unclassified)’ until the corresponding medical notification, if available, allows further classification of the disease as either chickenpox or herpes zoster.

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Secular trends, varicella and herpes zoster

National notification data on varicella-zoster virus infections are not available for the reporting period of January 2006 to December 2007. (Notification data from South Australia are reported in a later section of this chapter.)

There were 2,787 hospitalisations (average annual hospitalisation rate 6.8 per 100,000) for varicella between July 2005 and June 2007. During this period, the median number of varicella hospitalisations per month was 132.5 (range 48–189) (Figure 3.16.1). The overall population rate and median monthly admissions were similar to that of the period July 2002 to June 2005 (rate 7.2 per 100,000; median 124 with range 60–197).17

Figure 3.16.1 shows that there were considerably more hospitalisations for herpes zoster than varicella. There were 10,506 hospitalisations (average annual hospitalisation rate 25.6 per 100,000 for all herpes zoster and 10.7 per 100,000 for herpes zoster as a principal diagnosis) between July 2005 and June 2007. The median number of hospitalisations per month with herpes zoster as one of the discharge diagnoses was 438 (range 363–501, excluding the last month of reporting with incomplete admission data) (Figure 3.16.1). The rate and median monthly admissions were similar to the period July 2002 to June 2005 (rate 25.0 per 100,000; median 410 with range 310–465).17

There is some pattern of disease peaks for varicella hospitalisations, particularly in more recent years, with most hospitalisations occurring between June and January (Figure 3.16.1).

Figure 3.16.1: Varicella and herpes zoster hospitalisations, Australia, 1993/1994 to 2006/2007,* by month of admission

Figure 3.16.1:  Varicella and herpes zoster hospitalisations, Australia, 1993/1994 to 2006/2007, by month of admission

* Hospitalisations where the date of admission was between July 1993 and June 2007.

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Severe morbidity and mortality, varicella

For hospitalisations with an ICD-10-AM code for chickenpox, 15,375 hospital bed days (average 7,688 per year) were recorded during the 2 years July 2005 to June 2007. Of the 2,787 varicella hospitalisations, 1,907 (68%) had a principal diagnosis of varicella (average annual rate 4.6 per 100,000) (Table 3.16.1). Complications arising from varicella infection were recorded for 897 hospitalisations (32%). Of all varicella hospitalisations, 136 (4.9%) were coded as having varicella encephalitis or meningitis, and 249 (8.9%) were coded as having varicella pneumonia (Table 3.16.2). There were 9 hospitalisation records where both varicella pneumonia and varicella encephalitis/meningitis were coded as diagnoses. Although the hospitalisation rate was highest in the youngest age group (age 0–4 years), hospitalisations coded as chickenpox in people aged ≥60 years had the longest median length of stay (Table 3.16.1). The hospitalisation rate for varicella in children aged 0–4 years (34.9 per 100,000) declined significantly in comparison with the period July 2002 to June 2005 (42.1 per 100,000).17

Table 3.16.1: Varicella hospitalisations and deaths, Australia, 2005 to 2007,* by age group

Age group
(years)
Hospitalisations
2 years
(July 2005–June 2007)
LOS per
admission
(days)
Deaths
2 years
(2005–2006)
n () Rate§ () Median () n Rate§
0–4
905
(631)
34.9
(24.3)
2.0
(2.0)
1
0.04
5–14
468
(324)
8.5
(5.9)
2.0
(2.0)
0
15–24
260
(182)
4.6
(3.2)
2.0
(2.0)
0
25–59
929
(653)
4.6
(3.3)
3.0
(2.0)
1
<0.005
60+
225
(117)
3.1
(1.6)
7.0
(6.0)
8
0.11
All ages
2,787
(1,907)
6.8
(4.6)
2.0
(2.0)
10
0.02

* Hospitalisations where the date of separation was between July 2005 and June 2007; deaths where the death was recorded between January 2005 and December 2006.

† LOS = length of stay in hospital.

‡ Principal diagnosis (hospitalisations).

§ Average annual age-specific rate per 100,000 population.

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Table 3.16.2: Selected indicators of severe morbidity* for hospitalised cases of varicella, Australia, 2005 to 2007,* by age group

Age group
(years)
Varicella encephalitis or meningitis Varicella pneumonia
n % of cases n % of cases
0–4
23
2.5
24
2.7
5–14
27
5.8
20
4.3
15–24
17
6.5
19
7.3
25–59
54
5.8
175
18.8
60+
15
6.7
11
4.9
All ages
136
4.9
249
8.9

* Based on National Hospital Morbidity data where the date of separation was between July 2005 and June 2007.

† Nine hospitalisations with varicella pneumonia also had diagnostic codes of varicella encephalitis or meningitis.

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Among the 24 hospitalisations with a varicella code where death was the mode of separation during the period July 2005 to June 2007, varicella was the principal diagnosis for 7 (all had either varicella encephalitis or varicella pneumonia, together with underlying medical conditions in other diagnostic codes [data not shown]). All but one of them were aged ≥60 years. For the majority of the remaining 17 varicella hospitalisations resulting in death, the principal or other diagnoses included underlying immunocompromising medical conditions, in particular malignancies, and the age ranged from 33–92 years (median 61 years).

There were 10 deaths recorded with varicella as the underlying cause in the AIHW National Mortality Database in the calendar years 2005 and 2006; 8 (80%) of them were people aged ≥60 years. In children aged 0–4 years, 1 death was recorded during this period; this was a decline in comparison with the period 2003–2004, during which there were 3 recorded deaths in this age group.17

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Age and sex distribution, varicella

The highest rate of varicella hospitalisations continued to occur in the youngest age groups, especially the 0–4 years age group (Table 3.16.1; Figure 3.16.2), although the rate was reduced in this age group compared with the period July 2002 to June 2005. Within the 0–4 years age group (Figure 3.16.3), there was a sharp decrease in hospitalisations in the 12–23 months age group beginning in 2004/2005, a period which included the time when universal varicella immunisation at 18 months of age became recommended. This decreasing trend continued in 2005/2006 and 2006/2007. The hospitalisation rate decreased in infants aged <12 months during 2006/2007, but remained higher than in those aged 12–23 months, and was similar to the rate in infants <12 months of age in 2002/2003. Hospitalisation rates also declined in children aged 24–35 months over the 2-year period 2005/2006–2006/2007. The overall male:female ratio of hospitalisations was 1.2:1. Males predominated in all age groups, except young adults aged 15–29 years and elderly people aged ≥85 years, where there was a slight female predominance (data not shown). Of the 10 varicella deaths recorded in the AIHW National Mortality Database in 2005–2006, 9 were males.

Figure 3.16.2: Varicella hospitalisation rates, Australia, 2005/2006 to 2006/2007,* by age group and sex

Figure 3.16.2:  Varicella hospitalisation rates, Australia, 2005/2006 to 2006/2007, by age group and sex

* Hospitalisations where the date of separation was between July 2005 and June 2007.

Figure 3.16.3: Varicella hospitalisation rates, Australia, 2002/2003 to 2006/2007,* by age group (0–4 years) and year of separation

Figure 3.16.3:  Varicella hospitalisation rates, Australia, 2002/2003 to 2006/2007, by age group (0-4 years) and year of separation

* Hospitalisations where the date of separation was between July 2002 and June 2007.

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Geographical distribution, varicella

For the period 2005/2006–2006/2007, the Northern Territory had the highest average annual hospitalisation rate (12.7 per 100,000), with all other states recording average annual rates between 4.8 and 8.0 per 100,000. Hospitalisation rates were lowest in the Australian Capital Territory, South Australia and Tasmania (average annual rate 4.8, 4.8 and 4.9 per 100,000, respectively) (see also Appendix 6.3).

South Australian surveillance data, varicella

Figure 3.16.4 shows the notifications of varicella in South Australia by month of notification from January 2002 to December 2007. A total of 1,474 cases of chickenpox were notified in the period January 2006 to December 2007, an average annual rate of 46.8 per 100,000. Figure 3.16.5 shows the notifications by gender and age group for the current review period.

Figure 3.16.4: Varicella notifications, South Australia, 2002 to 2007,* by month of notification

Figure 3.16.4:  Varicella notifications, South Australia, 2002 to 2007, by month of notification

* Notifications where the date of notification was between January 2002 and December 2007.

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The highest rate of varicella notifications continued to occur in the youngest age groups, especially the 0–4 years age group (Figure 3.16.5), although there was a decline in the overall rate of notifications in the 0–4 years age group during 2006–2007 (306.9 per 100,000 during 2006–2007 compared with 377.1 per 100,000 during 2003–2005).

Figure 3.16.5: Varicella notifications and rates, South Australia, 2006 to 2007,* by age group and sex

Figure 3.16.5:  Varicella notifications and rates, South Australia, 2006 to 2007, by age group and sex

* Notifications where the date of notification was between January 2006 and December 2007.

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Severe morbidity and mortality, herpes zoster

For patients with an ICD-10-AM code for herpes zoster, 122,987 hospital bed days (average 61,494 per year) were recorded. Of the 10,506 herpes zoster hospitalisations, 4,410 (42%) had a principal diagnosis of herpes zoster (average annual rate 10.7 per 100,000) (Table 3.16.3). Complications arising from herpes zoster infection were recorded for 46% (4,783 of 10,506) of all hospitalisations with a herpes zoster diagnosis, and 58% (2,557 of 4,410) of hospitalisations where the principal diagnosis was herpes zoster. Of all the 10,506 herpes zoster hospitalisations, 169 (1.6%) were coded as having zoster encephalitis or meningitis, 105 (1.0%) were coded as having disseminated herpes zoster, and 1,172 (11.2%) were coded as having ocular complications (Table 3.16.4); <4% of the 4,783 hospitalisations with zoster complications had multiple diagnostic codes for zoster complications in their records. By far the greatest number of hospitalisations was in the oldest age group, who also had the longest median length of stay. There were 34 deaths recorded with herpes zoster as the underlying cause in the calendar years 2005 and 2006; 33 of them were people aged ≥60 years. The highest death rate was also recorded in people aged ≥60 years.

Table 3.16.3: Herpes zoster hospitalisations and deaths, Australia, 2005 to 2007,* by age group

Age group
(years)
Hospitalisations
2 years
(July 2005–June 2007)
LOS per admission
(days)
Deaths
2 years
(2005–2006)
n () Rate§ () Median () n Rate§
0–4
56
(41)
2.2
(1.6)
3.0
(3.0)
0
5–14
179
(109)
3.3
(2.0)
3.0
(2.0)
0
15–24
179
(91)
3.1
(1.6)
2.0
(2.0)
1
0.02
25–59
1,812
(841)
9.0
(4.2)
4.0
(3.0)
0
60+
8,280
(3,328)
114.2
(45.9)
7.0
(5.0)
33
0.46
All ages
10,506
(4,410)
25.6
(10.7)
6.0
(4.0)
34
0.08

* Hospitalisations where the date of separation was between July 2005 and June 2007; deaths where the death was recorded between January 2005 and December 2006.

† LOS = length of stay in hospital.

‡ Principal diagnosis (hospitalisations).

§ Average annual age-specific rate per 100,000 population.

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Table 3.16.4: Indicators of severe morbidity* for hospitalised cases of herpes zoster, Australia, 2005 to 2007,* by age group

Age group
(years)
Zoster encephalitis or meningitis Zoster with other nervous system involvement (without encephalitis or meningitis) Disseminated zoster Ocular complications of herpes zoster
n % of cases n % of cases n % of cases n % of cases
0–4
4
7.1
2
3.6
2
3.6
13
23.2
5–14
5
2.8
10
5.6
1
0.6
26
14.5
15–24
9
5.0
16
8.9
2
1.1
20
11.2
25–59
58
3.2
306
16.9
33
1.8
215
11.9
60+
93
1.1
2,419
29.2
67
0.8
898
10.8
All ages
169
1.6
2,753
26.2
105
1.0
1,172
11.2

* Based on National Hospital Morbidity data where the date of separation was between July 2005 and June 2007.

† A small proportion of hospitalisations had multiple diagnostic codes for zoster complications.

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Age and sex distribution, herpes zoster

The highest number and rate of herpes zoster hospitalisations occurred in the oldest age groups, especially in the ≥60 years age group, where the rate was over 114 per 100,000 (Table 3.16.3). Across all ages, the male:female rate ratio of hospitalisations was 0.7:1. The male:female rate ratio for deaths due to herpes zoster was 0.7:1.

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Geographical distribution, herpes zoster

For the period 2005/2006–2006/2007, South Australia had the highest crude average annual hospitalisation rate for herpes zoster (32.6 per 100,000), followed by Tasmania (27.7 per 100,000). The Northern Territory and the Australian Capital Territory had the lowest rates at around 20.6 per 100,000 (Appendix 6.3).

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South Australian surveillance data, herpes zoster

Figure 3.16.6 shows the notifications of herpes zoster by month from January 2002 to December 2007. A total of 1,188 cases were notified during 2006–2007, an average annual rate of 37.7 per 100,000. Figure 3.16.7 shows the notifications by gender and age group for the current review period.

Figure 3.16.6: Herpes zoster notifications, South Australia, 2002 to 2007,* by month of notification

Figure 3.16.6:  Herpes zoster notifications, South Australia, 2002 to 2007, by month of notification

* Notifications where the date of notification was between January 2002 and December 2007.

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Figure 3.16.7: Herpes zoster notifications and rates, South Australia, 2006 to 2007,* by age group and sex

Figure 3.16.7:  Herpes zoster notifications and rates, South Australia, 2006 to 2007, by age group and sex

* Notifications where the date of notification was between January 2006 and December 2007.

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Comment

The burden of disease caused by primary infection and reactivation of VZV is substantial. Severe herpes zoster occurs predominantly in the elderly, resulting in more hospitalisations than severe varicella, which is most common in young children, even when only the principal diagnosis is considered. The median length of stay for herpes zoster is also longer than for varicella, by 4 days.

Although most varicella hospitalisations were in the youngest age group (905 episodes with a rate of 34.9 per 100,000 among those aged 0–4 years), hospitalisations coded as chickenpox in people aged ≥60 years (rate 3.1 per 100,000) had the longest median length of stay of 7 days (6 days for those with varicella as the principal diagnosis). Hospitalisations of patients aged ≥60 years coded as primary varicella infection may be more likely from re-activation of VZV, rather than primary disease, due to the prevalence of underlying medical conditions in this age group. The observation that the majority of varicella hospitalisations that eventuated in death occurred in older persons with underlying immunocompromising medical conditions supports this. The finding that the Northern Territory has the lowest overall hospitalisation rates for herpes zoster and the highest for varicella presumably reflects the younger age structure of the population of the Northern Territory.

During 2005/2006–2006/2007, 32% of hospitalised varicella cases had at least one recorded complication. For herpes zoster hospitalisations, 46% of those with zoster as any one of the diagnoses, and 58% of hospitalisations where zoster was the principal diagnosis, had at least one complication. This routine data is in agreement with a more detailed study that found that over 50% of hospitalisation episodes with a principal diagnosis of herpes zoster had documented complications, the majority of which were neurological.18 In that study, 16% had ophthalmic zoster, which is a serious complication that threatens vision.18

Early data suggested an impact of vaccine use in children aged 1–4 years in 2004/2005, the period during which vaccination was recommended but not funded.9 This trend continued in 2005/2006 and 2006/2007, particularly in children aged 18–23 months, whose hospitalisation rate became lower than that of the <1 year age group, and in those aged 24–35 months, of whom some would have been eligible for the funded vaccine. Varicella hospitalisations do not appear to have declined substantially in other age groups, including those <12 months of age. This suggests there is not yet evidence of a herd immunity effect, which was observed in the USA from approximately 5 years after commencement of their universal immunisation program in 1995. The decline in the incidence of varicella in the USA, using active surveillance, was in all age groups, but most marked in those aged 1–4 years.19

In 1952, Hope-Simpson proposed the hypothesis that exposure to varicella may boost immunity against herpes zoster.20 There is increasing evidence to support that hypothesis, with two observational studies showing lower rates of herpes zoster in groups who have been exposed to varicella.21,22 If exposure to wild varicella provides boosting and protection against activation of herpes zoster, universal infant varicella vaccination and the subsequent decline in wild varicella may result in an increase in herpes zoster incidence among those previously infected.23 Mathematical modelling has also suggested that widespread infant varicella vaccination might result in a significant increase in the incidence of herpes zoster, possibly over a 40-year period.23 An Australian study, performed to assess the potential impact of universal varicella vaccination based on this hypothesis, suggested that total morbidity due to varicella and herpes zoster in Australia would decrease for the first 7 years of a population program, but, for 8–51 years after vaccination commenced, total morbidity was predicted to be higher than pre-vaccination levels.24 However, this model assumed 90% vaccination coverage and 93% vaccine effectiveness. These predictions might not be correct, particularly given that overall vaccine coverage and effectiveness are now estimated to be less than that originally used in the model. Currently, surveillance data from the USA, where varicella immunisation has been recommended for over a decade, indicates a large reduction in varicella morbidity with no increase in zoster disease yet demonstrated.25

The South Australian notification data show a declining notification rate among those aged 0–4 years, consistent with the decline in hospitalisations reported in this age group nationally. The reduction in reported cases may also have been on the background of an increase in the tendency to report cases which often occurs due to increasing awareness of disease among clinicians following introduction of recommendations for vaccination. Varicella cases were more frequently detected than herpes zoster cases through the South Australian surveillance system, in contrast to the national hospitalisation data. The gender-specific and age-specific notification data from South Australia show a similar epidemiology to the hospitalisation data, suggesting that hospitalisation data provides a useful measure of trends in varicella and herpes zoster.

The decline in hospitalisations and notifications in young children who are in the cohort eligible for funded varicella vaccine suggests an early impact of the vaccination program. This needs to be confirmed over time and in more age groups as vaccine coverage rises. Additionally, trends in disease epidemiology will need to be reviewed through notification data from other Australian states and territories, and via other mechanisms, such as reporting to the Australian Paediatric Surveillance Unit of data on neonatal, congenital and severe varicella infections.

The epidemiology of herpes zoster, as reflected in the national hospitalisation data and notification data from South Australia, does not appear to have changed over this review period. Surveillance for herpes zoster across all jurisdictions, together with ongoing monitoring of hospitalisation trends over time, should assist in identifying any changes in disease burden associated with ongoing use of the varicella vaccine and with the anticipated increase in uptake of the zoster vaccine over time in older Australians.

Acknowledgement: Dr Ann Koehler, Communicable Diseases Control Branch, Department of Health, South Australia, for provision of the South Australian notification data for varicella-zoster virus infections.

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References

1. Chickenpox/Herpes zoster. In: Heymann DL, ed. Control of Communicable Diseases Manual. 19th edn. Washington, DC: American Public Health Association, 2008.

2. Gershon AA, Takahashi M, Seward JF. Varicella vaccine. In: Plotkin SA, Orenstein WA, Offit PA, eds. Vaccines. 5th edn. Philadelphia, PA: Saunders Elsevier, 2008.

3. Hambleton S, Gershon AA. Preventing varicella-zoster disease. Clin Microbiol Rev 2005;18(1):70–80.

4. Preblud SR, Orenstein WA, Bart KJ. Varicella: clinical manifestations, epidemiology and health impact in children. Pediatr Infect Dis 1984;3(6):505–509.

5. Gidding HF, MacIntyre CR, Burgess MA, Gilbert GL. The seroepidemiology and transmission dynamics of varicella in Australia. Epidemiol Infect 2003;131(3):1085–1089.

6. Guess HA, Broughton DD, Melton LJ 3rd, Kurland LT. Population-based studies of varicella complications. Pediatrics 1986;78(4 Pt 2):723–727.

7. Brody MB, Moyer D. Varicella-zoster virus infection: the complex prevention-treatment picture. Postgrad Med 1997;102(1):187–190, 192–194.

8. Burgess MA, Forrest JM. Congenital varicella. J Paediatr Child Health 1995;31(6):564.

9. Macartney KK, Burgess MA. Varicella vaccination in Australia and New Zealand. J Infect Dis 2008;197(Suppl 2):S191–S195.

10. Bowsher D. The lifetime occurrence of Herpes zoster and prevalence of post-herpetic neuralgia: a retrospective survey in an elderly population. Eur J Pain 1999;3(4):335–342.

11. Schmader K. Herpes zoster in older adults. Clin Infect Dis 2001;32(10):1481–1486.

12. Lin F, Hadler JL. Epidemiology of primary varicella and herpes zoster hospitalizations: the pre-varicella vaccine era. J Infect Dis 2000;181(6):1897–1905.

13. Guess HA, Broughton DD, Melton LJ 3rd, Kurland LT. Epidemiology of herpes zoster in children and adolescents: a population-based study. Pediatrics 1985;76(4):512–517.

14. Gershon AA. Prevention and treatment of VZV infections in patients with HIV. Herpes 2001;8(2):32–36.

15. Forrest JM, Mego S, Burgess MA. Congenital and neonatal varicella in Australia. J Paediatr Child Health 2000;36(2):108–113.

16. Oxman MN, Levin MJ, Johnson GR, Schmader KE, Straus SE, Gelb LD, et al. A vaccine to prevent herpes zoster and postherpetic neuralgia in older adults. N Engl J Med 2005;352(22):2271–2284.

17. Brotherton J, Wang H, Schaffer A, Quinn H, Menzies R, Hull B, et al. Vaccine Preventable Diseases and Vaccination Coverage in Australia, 2003 to 2005. Commun Dis Intell 2007;31(Suppl):S1–S152.

18. MacIntyre CR, Chu CP, Burgess MA. Use of hospitalization and pharmaceutical prescribing data to compare the prevaccination burden of varicella and herpes zoster in Australia. Epidemiol Infect 2003;131(1):675–682.

19. Seward JF, Watson BM, Peterson CL, Mascola L, Pelosi JW, Zhang JX, et al. Varicella disease after introduction of varicella vaccine in the United States, 1995–2000. JAMA 2002;287(5):606–611.

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20. Hope-Simpson RE. Infectiousness of communicable diseases in the household (measles, chickenpox, and mumps). Lancet 1952;260(6734):549–554.

21. Thomas SL, Wheeler JG, Hall AJ. Contacts with varicella or with children and protection against herpes zoster in adults: a case-control study. Lancet 2002;360(9334):678–682.

22. Brisson M, Gay NJ, Edmunds WJ, Andrews NJ. Exposure to varicella boosts immunity to herpes-zoster: implications for mass vaccination against chickenpox. Vaccine 2002;20(19–20):2500–2507.

23. Brisson M, Edmunds WJ, Gay NJ, Law B, De Serres G. Modelling the impact of immunization on the epidemiology of varicella zoster virus. Epidemiol Infect 2000;125(3):651–669.

24. Gidding HF, Brisson M, MacIntyre CR, Burgess MA. Modelling the impact of vaccination on the epidemiology of varicella zoster virus in Australia. Aust N Z J Public Health 2005;29(6):544–551.

25. Reynolds MA, Chaves SS, Harpaz R, Lopez AS, Seward JF. The impact of the varicella vaccination program on herpes zoster epidemiology in the United States: a review. J Infect Dis 2008;197(Suppl 2):S224–S227.

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