blood-borne viruses in the haemodialysis-dependent population attending top end northern territory...

Or ig ina l Ar t ic le

Blood-borne viruses in the haemodialysis-dependent populationattending Top End Northern Territory facilities 2000–2009nep_1603 501..507

JANE DAVIES,1 ZULFIKAR JABBAR,2 FIZZA GAGAN3 and ROBERT W BAIRD3

Departments of 1Infectious Diseases, 2Nephrology and 3Microbiology, Royal Darwin Hospital, Darwin, Northern Territory, Australia

KEY WORDS:dialysis, hepatitis B, infection control, Northern

Territory.

Correspondence:Dr Jane Davies, Department of Infectious

Diseases, Royal Darwin Hospital, Rocklands

Drive, Tiwi, Darwin, NT 0811, Australia. Email:

[email protected]

Accepted for publication 15 March 2012.

Accepted manuscript online 28 March 2012.

doi:10.1111/j.1440-1797.2012.01603.x

SUMMARY AT A GLANCE

This paper is an audit of viral infectious

serology in a predominantly Indigenous

dialysis service in the Northern Territory.

Its value relates to documentation of

previous exposure, HBcAb, and current

HBsAg positivity in a significant proportion

of this population and, on the other hand,

low seroconversion rates for haemodialysis

patients positive for HBsAg managed with

current non-isolation unit strategies.

ABSTRACT:

Aim: To describe the incidence and prevalence of blood-borne viruses(BBV) including: hepatitis B virus (HBV), hepatitis C virus (HCV), humanimmunodeficiency virus (HIV) and human T-cell leukaemia virus type-1(HTLV) in the haemodialysis-dependent population of the Top End of theNorthern Territory (TENT).Methods: We retrospectively reviewed the serology of BBV in a longitudinalfashion in the haemodialysis-dependent population treated in the TENT ofAustralia from 2000 to 2009 inclusive. HBV, HCV, HIV and HTLV serology oncommencement of dialysis and at exit or January 2010, whichever wasearlier, as well as demographic details were collected. Patients with a changein serological status had all serology reviewed.Results: Four-hundred and forty patients were included in the analysis. Ofthese, 84.3% were Indigenous and 55.4% female, with a median age of 50(IQR 43–59) years at the commencement of haemodialysis. Evidence of pastHBV infection was documented in 42.7% and 8.9% were hepatitis B surfaceantigen-positive. Positive serology for HTLV was documented in 2.2%, 1.6%were hepatitis C antibody-positive and no individual was HIV-positive.Three patients had a definite change in their HBV serology over time; thisequates to an absolute seroconversion risk of 0.1 per 100 person years or0.0006 per dialysis episode.Conclusions: In this cohort, there was a high rate of past and current hepa-titis B infection but low rates of seroconversion while on haemodialysis.

INTRODUCTION

The Top End of the Northern Territory (TENT) has a popu-lation with a high incidence of renal disease, predominantlyattributed to diabetes and hypertension. In 2008, the inci-dence and prevalence of dialysis-dependent individuals inthe Northern Territory (NT) was 405 and 1810 per millionpopulation, respectively; this is compared with national Aus-tralian figures of 116 and 471 per million population, respec-tively.1 Hepatitis B virus (HBV) infection is also common inthe NT; available data have suggested hepatitis B surfaceantigen (HBsAg) positivity rates of 8.5% in remote Indig-enous communities2 and 8.2% in Indigenous school children(14.8% in rural areas).3 Two recent antenatal surveysshowed Indigenous pregnant women to have HBsAg-positive rates of 5.5% and 3.7%, respectively,4,5 and oneretrospective review of existing serology in an East Arnhem-

land clinic showed 12% to have current and 63% past HBVinfection.6 Universal HBV vaccine coverage has been in placefor Indigenous children in the NT since 1988 and for allchildren since 1990 with coverage consistently in the regionof 95%.7 Hepatitis C virus (HCV), human T-cell lym-photrophic virus type-1 (HTLV) and human immunodefi-ciency virus (HIV) are less common with an overallprevalence in the NT of <2%, <0.5% and 0.1%, respectively(Dr P Markey, pers. comm., October 2011, NT Centre forDisease Control). HTLV is more prevalent in Central Austra-lia (13.9% in a 1994 serosurvey8) but is less common in theTop End.

Blood-borne viruses (BBV) including HBV, HCV, HIV andHTLV are recognized as important hazards for patients andstaff in haemodialysis units. It is acknowledged that theprevalence of BBV in a dialysis population tends to reflectthat of the community in which it is based and surveillance

Nephrology 17 (2012) 501–507

© 2012 The AuthorsNephrology © 2012 Asian Pacific Society of Nephrology 501

for BBV in the haemodialysis-dependent population islargely based on local policy. Guidelines from the UK renalassociation,9 Kidney Disease: Improving Global Outcomes,10

and US Centre for Disease Control11 have been variable inscreening recommendations, and there is no regional guide-line from Caring for Australasians with Renal ImpairmentGuidelines12,13 in this regard.

There is evidence that having a specific protocol for HBV-infected dialysis patients is associated with a decreased risk ofseroconversions while on dialysis therapy and that HBV-infected individuals have increased morbidity and mortalityboth on dialysis and after they have received a renaltransplant.14

The TENT, as of 1 January 2011, had 221 prevalent hae-modialysis patients served by the haemodialysis unit at RoyalDarwin Hospital and satellite units spread over 447 000 km2.HBV, of all the BBV, is an excellent indicator of the value ofparticular infection control practices, as seropositive HBsAgpatients are significant reservoirs of potential viral transmis-sion. An untreated percutaneous exposure to a hepatitisB-infected source carries a risk of seroconversion of up to30% dependent on the source’s viral load and the size of theinoculum.15

The aim of this study was to document the incidence andprevalence of BBV over the last decade, and in particulardocument episodes of haemodialysis associated seroconver-sion as a marker of the effectiveness of our infection controlprotocols. Based on our findings of the pattern of incidenceand prevalence of BBV, we hope to be able to devise strate-gies to optimize the need, nature and frequency of routinesurveillance in haemodialysis units across the region.

METHODS

Patients who received haemodialysis for at least 3 months at centres

in the TENT of Australia between the years of 2000 and 2009 were

identified through the renal register and serology results accessed via

the Labtrack public pathology laboratory database. HBV, HCV, HIV

and HTLV serology on commencement of dialysis and at exit or

January 2010, whichever was earlier, as well as demographic details

were collected. Patients with a change in serological status had all

serology reviewed.

Each patient was serologically tested approximately yearly; some

individual patients were tested up to 4 times/year.

Policies/protocols

Northern Territory vaccination policy states that haemodialysis

patients receive HBV immunization, if they have no evidence of

pre-existing HBV seromarkers (HBcAb, HBsAg, hepatitis B surface

antibody (HBsAb)), when commencing dialysis, and boosters

(National Health and Medical Research Council immunization

guidelines eighth edition 2008) as required. Vaccination is with

40 mg of i.m. hepatitis B vaccine administered into the deltoid region

at 0, 1 and 6 months. HBsAg titres are checked 4 weeks after the last

dose and non-responders (HBsAg titres <10 IU/mL) receive three

further 40 mg doses.

Dialysis protocols for Infection Control in the Unit are as per

‘Recommended Practices for the Prevention and Control of Infec-

tions in Dialysis Settings’.16 In the TENT, infection control practices

over the last 10 years have stipulated that patients with BBV are not

segregated within facilities and are not assigned dedicated dialysis

machines. Single patient use trolleys are provided for each dialysis

episode, no multi-dose vials are used and the machines are disin-

fected between patients, with single patient use lines and dialysers.

Serology investigations

Assays

HTLV-1, currently Abbott ARCHITECT rHTLV-I/II chemiluminescent

assay, previously Serodia passive particle agglutination; HCV, cur-

rently Abbott ARCHITECT anti-HCV, previously Abbott AXSYM

anti-HCV; HIV, currently Abbott ARCHITECT HIV Ag/Ab Combo

assay, previously Abbott AXSYM HIV; hepatitis B, currently Abbott

ARCHITECT HepBsAg, HepBsAb and HepBcAb assays, previously

Abbott AXSYM hepatitis B assays. HBV Abbott Real-Time HBV

Assay, dynamic range 10–109 IU/mL.

Statistical analysis

For continuous variables, normality of data was tested with the

Shapiro–Wilk test. Results were expressed as frequencies and per-

centages for categorical variables and median with inter-quartile

range (IQR) for continuous variables. Differences between groups

were tested using the non-parametric Mann–Whitney U-test for

continuous variables, and Fisher’s exact test and contingency table

chi-squared test for categorical variables where applicable. A two-

sided P-value of <0.05 was considered to be statistically significant.

All analyses were performed by using SPSS for Windows software

v16.0 (SPSS Inc., Chicago, IL, USA).

Ethics

This study was approved by the Human Research Ethics Committee

of the Northern Territory Department of Health and Menzies School

of Health Research HREC 2010-1478.

RESULTS

Four-hundred and forty patients were identified andincluded in the analysis, each individual usually receiveddialysis 3 times per week. This represents an analysis ofapproximately 2000 patient dialysis years, and represents anestimated 300 000 individual dialysis episodes. Demograph-ics of the study population are presented in Table 1. Themajority of patients were Indigenous (84.3%) with a slightpredominance of female subjects (55.4%). The age ofpatients at the time of commencing dialysis ranged between5 and 78 years. The age distribution of the patients is pre-sented in Figure 1. The median age of starting dialysis for allpatients was 50 years (IQR 43–59); this was 49 years (IQR43–57) for Indigenous patients and 58 years (IQR 47–68) for

J Davies et al.

© 2012 The AuthorsNephrology © 2012 Asian Pacific Society of Nephrology502

non-Indigenous patients (P = 0.0001). Median duration onhaemodialysis was 52 months (IQR 26–80).

Hepatitis B

Overall, 186 (42.7%) of patients had evidence of past HBVinfection (HBcAb-positive, HBsAg-negative 1 HBsAg >10).Thirty-eight (8.9%) had evidence of chronic HBV infection(HBsAg-positive and HBcAb-positive), 17 of these patientswere still receiving haemodialysis on 1 January 2011(Table 2).

Thirty-two (82.0%) of the chronic HBV group were hepa-titis B e antigen (HBeAg)-negative, hepatitis B e antibody(HBeAb)-positive. All in this group (who had viral loadsdetermined n = 12) had DNA levels less than 2000 IU/mL,hence in the immune control phase of their disease. Sixpatients (15.4%) were HBeAg-positive with high viral loads,so in the immune clearance phase of their disease. For onepatient, no e markers were available. Three of these patientshave passed away (one from hepatocellular carcinoma), two

were receiving treatment with entecavir and one was under-going assessment at the time of inclusion in this study.

Of the 70 patients with isolated HBcAb-positive infection,20 had a viral load performed; all of these were undetectable.

Two patients who were initially HBsAg-positive clearedtheir surface antigen and became surface antibody-positiveover the course of their period on dialysis.

Three patients significantly altered their HBV markers(Table 3). Two patients developed new HBcAb on dialysis;this could be indicative of dialysis-related seroconversion,although other modes of transmission of HBV are welldescribed. Viral isolates were not available for genotyping.One patient with known HBcAb developed HBsAg while ondialysis; this is indicative of HBV reactivation rather thandialysis-related seroconversion.

Hepatitis C

Seven patents were HCV antibody-positive; we did not haveRNA viral loads available to confirm infection status in thesepatients.

One patient with equivocal HCV serology for 3 years sero-converted to HCV antibody-positive; this represents a pos-sible haemodialysis-associated seroconversion. Genotypingwas not available for either the patient or others dialysingwith HCV-positive serology in the same time period.

HTLV

Ten (2.2%) of the patients had seromarkers of HTLV, con-firmed by western blot. Of the 10 patients with HTLV, nonehad co-existent HIV, one had co-existent HCV and HBVmarkers and eight patients had co-existent HBV markers.One patient had HTLV as an isolated infection.

One patient had a seroconversion to HTLV infection whileon dialysis. This is not considered dialysis-related, due to theabsence of other patients with HTLV in the unit at the time.

Table 1 Patient demographics and causes of renal failure

Primary renal disease

Diabetes Presumed GN Hypertension IgA nephropathy Reflux Other† Uncertain Total

Sex

Male 82 (40) 17 (34) 25 (61) 10 (71.4) 6 (42.9) 26 (53.1) 30 (44.8) 196 (44.6)

Female 123 (60) 33 (66) 16 (39) 4 (28.6) 8 (57.1) 23 (46.9) 37 (55.2) 244 (55.4)

Total 205 (46.6) 50 (11.4) 41 (9.3) 14 (3.2) 14 (3.2) 49 (11.1) 67 (15.2) 440 (100)

Ethnicity

Indigenous 186 (90.7) 46 (92) 32 (78.1) 7 (50) 9 (64.3) 35 (71.4) 56 (83.6) 371 (84.3)

Caucasian 15 (7.3) 2 (4) 8 (19.5) 5 (35.7) 3 (21.4) 13 (26.5) 7 (10.4) 53 (12.1)

Other 4 (2) 2 (4) 1 (2.4) 2 (14.3) 2 (14.3) 1 (2) 4 (6) 16 (36)

Data are no. (%) of patients, unless otherwise indicated. Percentages may not equal to 100% because of rounding. †Focal sclerosing GN (9), obstructive (8),

mesangiocapillary GN (5), mesangioproliferative (3), renal cell carcinoma (3), paraproteinaemia (3), Goodpasture’s (2), SLE (2), cortical necrosis (2), membranous

GN (2), scleroderma (1), amyloidosis (1), Alport’s (1), polycystic (1), primary focal segmental glomerulosclerosis (1) and other GN (5). GN, glomerulonephritis; SLE,

systemic lupus erythematosus.

>70

60–69

50–59

40–49

30–39

20–29

10–19

Percentage

Age

ran

ge (

year

s)

0 5 10 15 20 25 30 35

<10

Fig. 1 Age distribution of Top End haemodialysis-dependent patients. ( )

Haemodialysis-dependent patients; ( ) 2006 Northern Territory population

(Australian Bureau Statistics).

BBV haemodialysis-dependent population


HIV

No patients in the cohort were HIV-positive.

Seroconversion

Eleven of the 440 patients had a change in their sera statusduring their period on haemodialysis. Six of the patientswere not considered in this analysis, as minor HBV markerchanges occurred or patients had alternating positive, nega-tive or equivocal results near the assay cut-offs. The serologi-cal features of the remaining five patients are detailed inTable 3.

DISCUSSION

Epidemiological data regarding HBV in the general popula-tion of Australia are sparse with prevalence estimates of0.49–0.87%.17 HBsAg positivity rates among the Indigenouspopulation in the NT are estimated to be between 3% and15%.2–6 We have documented a high prevalence of HBVinfection in this study population. Other renal units havereported widely diverse rates of surface antigen positivity, forexample, Turkey, Brazil, and USA and Europe of 13.3%,18

2.4–10%19 and 0.6–6%,14 respectively. The Asia Pacificreview of HBV and HCV infection in haemodialysis and peri-

toneal dialysis patients contained limited data regarding HBVwith a wide range of prevalence estimates between 1.3% and14%.20 There are no other published reports from Australiandialysis units to our knowledge.

We note the high percentage of the Indigenous haemodi-alysis population in our study, 84% compared with 10%nationally21 and the younger age of starting dialysis com-pared with non-Indigenous Australians 49 years versus58 years (P = 0.0001). The Australian mean age of startinghaemodialysis is 60 years.22

The Gastroenterological Society of Australia ConsensusGuidelines23 produced in 2008 and the National Hepatitis BStrategy24 (2010) both list Indigenous Australians as a high-risk group for HBV screening and vaccination where needed.Only five patients were young enough to be part of theuniversal HBV vaccination programme, of these two hadevidence of past HBV infection (HBcAb-positive), two ofeffective immunization (HBsAb-positive) and one was nega-tive for all HBV markers, that is, non-immune at the com-mencement of dialysis. It is too early to assess the full impactof universal vaccination on the haemodialysis-dependentpopulation; however, we note that two of five individualsborn after its commencement have evidence of past HBVinfection and one was non-immune at entry to dialysis.25

It is standard practice to establish an individual’s BBVstatus prior to first dialysis and vaccinate them against HBV if

Table 2 Patient demographics and HBV serological markers

HBV markers

Negative HBsAb Isolated HBcAb HBsAg & HBcAb HBcAb & HBsAb > 10 P-value† Total‡

Sex

Male 42 (48.8) 62 (49.6) 25 (35.7) 19 (48.7) 45 (38.8) 0.0433 193 (44.3)

Female 44 (51.2) 63 (50.4) 45 (64.3) 20 (51.3) 71 (61.2) 243 (55.7)

Ethnicity

Indigenous 57 (66.3) 101 (80.8) 66 (94.2) 37 (94.9) 107 (92.2) <0.0001 368 (84.4)

Caucasian 25 (29.1) 20 (16) 2 (2.9) 0 (0) 5 (4.3) 52 (11.9)

Other 4 (4.6) 4 (3.2) 2 (2.9) 2 (5.1) 4 (3.5) 16 (3.7)

Renal disease

Diabetes 39 (45.3) 49 (39.2) 39 (53.8) 21 (53.8) 56 (48.3) 0.0439 204 (46.8)

Presumed GN 9 (10.5) 16 (12.8) 8 (11.4) 1 (2.5) 16 (13.8) 50 (11.5)

Hypertension 11 (12.8) 15 (12) 6 (8.6) 1 (2.5) 7 (6) 40 (9.1)

IgA nephropathy 2 (2.3) 6 (4.8) 1 (1.4) 2 (5.1) 3 (2.6) 14 (3.2)

Reflux 3 (3.5) 5 (4) 3 (4.3) 0 (0) 3 (2.6) 14 (3.2)

Uncertain 11 (12.8) 19 (15.2) 10 (14.3) 8 (20.5) 17 (14.7) 65 (14.9)

Other 11 (12.8) 15 (12) 3 (4.3) 6 (15.4) 14 (12.1) 49 (11.2)

Age ranges (years)

<40 12 (13.9) 21 (16.8) 10 (14.3) 4 (10.3) 31 (26.7) 0.3046 78 (17.9)

�40–50 21 (24.4) 43 (34.4) 27 (38.6) 12 (30.8) 30 (25.9) 133 (30.5)

�50–60 18 (20.9) 37 (29.6) 18 (25.7) 15 (38.5) 31 (26.7) 119 (27.3)

�60 35 (40.7) 24 (19.2) 15 (21.4) 8 (20.5) 24 (20.7) 106 (24.3)

Total 86 (19.7) 125 (28.7) 70 (16.1) 39 (8.9) 116 (26.6) 436 (100)

Data are no. (%) of patients, unless otherwise indicated. Percentages may not equal to 100% because of rounding. †Differences between groups were tested by

contingency table chi-squared test and Fischer’s exact test for categorical values. Pastor current HBV infections (HBcAb, HBsAg/HBcAb and HBcAb/HBsAb > 10)

were compared with no evidence of natural prior HBV infection (negative and HBsAb), with respect to sex, ethnicity (Indigenous vs other), renal disease (diabetes

vs other) and all age ranges, respectively. ‡Four patients had co-existent HCV and HBcAb. These four patients are not included in the table. GN, glomerulonephritis;

HBcAb, hepatitis B core antibody; HBsAb, hepatitis B surface antibody; HBsAg, hepatitis B surface antigen; HBV, hepatitis B virus; HCV, hepatitis C antibody.

J Davies et al.


required and to monitor HBsAb levels on an annual basis.However, the low number of individuals who have anychange in their serology during their dialysis career in ourstudy population suggests that annual serology for all BBV isperhaps not needed. In an era of increasingly available andefficacious hepatitis B treatments,23 it would seem to be ben-eficial to focus on HBV DNA testing for all those who areHBsAg-positive and potentially those who have an isolatedcore antibody with the aim of detecting those with high viralloads. These are not only the most infectious individuals butalso those who will benefit most from further evaluation andpotential antiviral treatment. It is important to note thehepatocellular carcinoma screening recommendations thatapply to populations with similar prevalence data, that is,6 monthly ultrasound scans and alpha-fetoprotein measure-ments;18 there are no current guidelines for the AustralianIndigenous population.

Current infection control practices in the TENT for HBV-infected individuals in a unit with endemic levels of HBV areeffective as there were no episodes of HBsAg acquisitiondirectly attributable to dialysis. If we assume that the twoindividuals who changed their core antibody status didacquire their HBcAb as a direct consequence of dialysis that

would give an absolute risk of HBV acquisition of 0.0006 perdialysis session or 0.1 per 100 patient years. This is muchlower than published data from European and US unitswhere baseline prevalence of HBV is much lower andcommon practice is to have dedicated machines for all HBV-positive individuals (0.4–1.1 per 100 patient years).20 We arenot aware of any comparable Australian data.

The major limitation of this study is the retrospectivenature of the data collection. This particularly impacts on theaccuracy of attributing changes in patients’ serology to theirhaemodialysis-associated risk; if data had been collected pro-spectively root cause analyses could have been conductedinto each event and these data taken into consideration. Thismeans we may have overestimated the risk of HBV acquisi-tion from haemodialysis in the study population.

Our recommendations based on these data would be forno change in our infection control practices, for initialscreening and vaccination as appropriate followed by a moreindividualized approach to BBV testing (Fig. 2).

The TENT dialysis population has a high prevalence ofHBV infection with low levels of other BBV. Current infec-tion control practices appear to be effective in limitingdialysis-related seroconversions. Screening practices can

Table 3 Immunoserology details of patients who seroconverted to blood-borne virus while on haemodialysis in Top End facilities

Patient Number Date of assay HTLV-l HCV HBsAg HBcAb HBsAb

Patient 1 4/5/2000 ND ND ND <10

11/9/2000 ND

18/9/2000 ND

52 year-old female 5/4/2001 ND

Indigenous 5/9/2001 D ND ND D 302

3/3/2003 D

4/2/2005 D ND D 404

Patient 2 9/10/2001 ND EQ ND D >1000

8/4/2002 EQ

1/10/2002 EQ

29 year-old female 22/1/2003 EQ

Indigenous 2/4/2003 ND EQ

10/7/2003 ND ND D >1000

12/4/2004 D

Patient 3 5/2/2004 ND ND ND D <10

7/4/2004 ND

46 year-old male 11/4/2005 ND

Indigenous 10/5/2006 D

8/8/2008 ND ND D D <10

Patient 4 27/10/2000 ND ND ND ND <10

4/9/2001 ND

51 year-old female 10/2/2003 ND


13/12/2007 ND D <10

11/4/2008 ND ND ND D <10

Patient 5 20/12/2007 ND ND ND <10

5/2/2008 D

59 year-old female 2/5/2008 D


3/2/2010 ND ND ND D 15

HBV abbreviations as per Table 2. D, detected; EQ, equivocal; ND, not detected. HBsAb level >10 considered protective.



now be adjusted based on this epidemiological informationto enable the care of HBV patients to be optimized as well ascontinuing to maintain low levels of BBV seroconversionsacross dialysis units in the TENT.

ACKNOWLEDGEMENTS

Thanks to Kevin Freeman, Senior Scientist, Seroimmunol-ogy Royal Darwin Hospital. This work was supported by theAustralian and New Zealand Society of Nephrology (ANZSN)Amgen Quality Assurance Grant.

COMPETING INTERESTS’ STATEMENT

Dr Jane Davies received financial support in 2009 fromBristol-Myers-Squibb to attend an international conference.Dr Jane Davies has received payment for lectures deliveredon behalf of the Australian Society for HIV Medicine (ASHM)on the topics of hepatitis B & C. There are no other conflictsof interest.

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