Health issues of refugees attending an infectious disease refugee health clinic in a regional Australian hospital

BETWEEN 2007 AND 2012, Australia accepted 12,000–13,750 refugees each year under the Humanitarian Program.1 This has since risen to 17,555 refugees per year in 2016–17.2 Approximately 4000 of these refugees settle in Victoria annually and, of this number, 10–15% settle in rural and regional Victoria.3 Of all regional areas in Victoria, the greater Geelong region had the largest refugee settlement between January 2007 and December 2012.3 Prior to departure for Australia, all refugee entrants applying for permanent visas are required to undergo a pre-departure health assessment, including a physical examination, chest X-ray (those aged ≥11 years), and syphilis and human immunodeficiency virus (HIV) screening (those aged ≥15 years).4,5 Dependent on visa subclass, empirical treatment for intestinal helminths with a single dose of albendazole is offered, as is the measles, mumps and rubella vaccination (for those aged nine months to 54 years, unless pregnant).6 Polio and yellow fever vaccines are given on the basis of location of residence before departure.6 A comprehensive primary health assessment is recommended within one month of arrival in Australia.6 Medicare-funded initial health checks are available for refugees and humanitarian entrants who have been in Australia for less than 12 months.6–8 Standard refugee health assessments in Australia include testing for latent and active tuberculosis (TB) infections, parasitic infestation, iron deficiency, abnormal lipid profiles, blood-borne viruses, sexually transmitted infections and vitamin deficiencies. Individual risk factors, source and transit countries, and history and examination findings then guide tailored investigations.6 The assessment is intended to proactively focus on preventive health, catch-up immunisations, as well as diagnosis and treatment of any unmanaged chronic conditions, including mental health issues.6,7 General practitioners (GPs) typically provide the first point of access to healthcare for newly arrived refugees. Studies of refugee populations throughout Australia show that latent tuberculosis (LTBI), and parasitic and vector-borne diseases tend to be the most common infectious diseases among refugees, with vitamin deficiencies also commonly seen.6,7,9,10 These studies, largely on African refugees, have primarily highlighted the prevalence of infectious diseases screened in general practice or specialist migrant health units.11–14 The University Hospital Geelong (UHG) Refugee Health Clinic at Barwon Health is one of two centres to offer specialised refugee infectious disease healthcare in Western Victoria and receives referrals for refugees residing west of Melbourne, in Greater Peta J Masters, Penelope J Lanfranco, Emmy Sneath, Amanda J Wade, Sarah Huffam, James Pollard, Jane Standish, Kate McCloskey, Eugene Athan, Daniel P O’Brien, N Deborah Friedman


Background and objective
Refugees in Australia present with conditions different to those of the general population.The aim of this study was to review the reasons for referral, prevalence of conditions and treatment outcomes for refugee patients attending a specialist referral clinic in regional Victoria.

Methods
A retrospective review was undertaken of patients attending the refugee health clinic at University Hospital Geelong from January 2007 to December 2012.

Results
Two hundred and ninety-one refugee patients attended the clinic over the six-year period.Latent tuberculosis infection (LTBI) (54.6%), vitamin deficiencies (15.8%), hepatitis B (11%) and schistosomiasis (11%) were the most common diagnoses.Less than two-thirds of the patients completed LTBI treatment; 35.4% of patients attended all scheduled clinic appointments.

Discussion
LTBI, vitamin deficiencies, parasitic infections and hepatitis B were the most common diagnoses among refugees referred to the University Hospital Geelong (UHG) Refugee Health Clinic from January 2007 to December 2012.General practitioners play an important role in the care of refugees, guiding referral to specialist services when necessary and recognising the potential implications of suboptimal clinic attendance and treatment completion.
Geelong and from south-western Victoria.The weekly clinic is staffed by infectious disease (ID) physicians, paediatric consultants and registrars, and a clinical nurse consultant, assisted by foreign language interpreters.Most patients are referred by their GPs after positive screening or suspicion of other infections.Intra-hospital and inter-hospital referrals, as well as referrals from the Victorian Department of Health and Human Services, are also accepted.Patients requiring other services, including mental health services that are not available in the clinic, are referred on from the Refugee Health Clinic.
A clinical audit of refugees attending the UHG Refugee Health Clinic between 2007 and 2012 was undertaken.The aims were to: • determine the most common reasons for referral • ascertain the most common conditions present among refugees • analyse treatment outcomes with the objective of improving future patient management.

Methods
A retrospective review of patients' medical records between 1 January 2007 and 31 December 2012 was undertaken.Patients were identified by iPIMs coding software and patient data were extracted from the UHG electronic medical record.
Data collected included age at first visit, gender, country of origin, language, interpreter use, year of migration to Australia, last country of residence, and time spent in a refugee camp.The reason for referral, investigations performed, confirmed diagnoses, missed clinic appointments, treatment and the outcome of treatment were also collected.Patients were considered paediatric if aged <16 years.The Mantoux tuberculin skin test (TST), blood interferon gamma release assay (IGRA) test or acid-fast bacilli (AFB) smear were performed for investigation of LTBI and active TB.In accordance with recommendations by the Australasian Society for Infectious Diseases, 6 a positive TST was defined as induration ≥10 mm in adults and children from refugee-like backgrounds (Table 1).
Data analysis involved descriptive statistics.Comparisons between categorical variables were performed using the chi-squared test and odds ratios calculated using the Mantel-Haenszel test.Data was analysed using STATA 12 (StataCorp, Texas, US).
The Barwon Health human research and ethics committee reviewed and approved this study (reference 13/113) without the requirement of obtaining informed consent from the retrospective de-identified patient cohort.

Results
Two hundred and ninety-one patients were seen in the Refugee Health Clinic over the six-year period.The median age of clinic patients was 33 years, 53% were male, and one-third were from Myanmar (Table 2).GP referrals accounted for 251 (86%) of clinic attendees (Table 3).The remaining patients were referred from the UHG emergency department, Victorian Department of Health and Human Services, and other hospitals.The majority of clinic patients (83.2%) required interpreter services.Eighty-nine patients (29.9%) were diagnosed with two or more conditions.Analysis of attendance outcomes revealed that 35.4% of patients attended all scheduled appointments, and 32.7% missed three or more scheduled appointments (Table 2).

Tuberculosis
GP referrals of patients with positive or equivocal TST results were the most common reasons for referral (136 of 251 referrals).Of these, 116 patients had a confirmed diagnosis of LTBI made in the clinic.There were six confirmed diagnoses of active TB in the patient cohort; all six patients completed treatment according to Australian guidelines. 15he most common diagnosis at the clinic was LTBI (54.6%;Table 3).Of patients offered treatment, 63.5% completed a full course of LTBI therapy, 10.7% ceased treatment because of hepatotoxicity, and 11.4% of those suitable for LTBI treatment were lost to follow-up (Table 4).There was a significant association between the diagnosis of LTBI and country of origin, with patients from Afghanistan (odds ratio [OR]: 4.63; 95% confidence interval [CI]: 2.10-10.21;P <0.001) or the Democratic Republic of Congo (OR: 2.87; 95% CI: 1.10-7.49;P = 0.02) being more likely to have a diagnosis of LTBI when compared with patients from other countries of origin.Eighty-six of 133 patients (64.7%) who had lived in a refugee camp developed either active or latent TB.

Vitamin deficiencies
Vitamin deficiencies (A, B or D) were the second-most common conditions (15.5%; Table 3).Over half of these patients (52.2%) were from Africa.GPs referred 20 patients (including 18 paediatric patients) for management of vitamin D deficiency (Table 3).Forty of 45 patients (88.9%) with a diagnosis of vitamin deficiency received treatment according to standard treatment protocols.

Hepatitis B
A total of 32 patients (11.0%) were diagnosed with chronic hepatitis B (CHB) infection (Table 3), with the largest number being among refugees from Myanmar (43.7%).Fifty per cent of CHB cases were diagnosed in refugees who had migrated from Asia, while 40.6% were diagnosed in refugees of African origin.Two cases of acute hepatitis B infection (IgM+ to hepatitis B core antigen [Anti-HBc]) were detected.Ongoing follow-up of these patients was conducted in the UHG Liver Clinic.

Discussion
This study provides comprehensive data on the reasons for referral, predominantly from general practice, to a refugee health clinic at a tertiary hospital in regional Victoria between 2007 and 2012.
LTBI was the most common diagnosis, in over half of the patients, which is comparable to 55% of referrals in Gibney's study of African immigrants attending an infectious diseases clinic in Melbourne. 11n analysis of African refugees attending the UHG clinic revealed that 51% were diagnosed with LTBI, accounting for 31.4% of those diagnosed with LTBI in the entire cohort.Other studies conducted within the primary healthcare setting found a lower percentage of LTBI (25%) among newly arrived refugees. 12,13The higher percentage in this study is likely  to be a reflection of local adherence of GPs to guidelines, which recommend referral of patients with positive TB screening to a specialist TB centre. 6,10hile the prevalence of active TB in this study was relatively low (2%), LTBI is recognised globally as a reservoir for active TB.Reactivation of LTBI occurs most commonly in the first five years post-migration. 6,16In countries where the disease is endemic, rates of reactivation can remain high (approximately 10%) for many years post-arrival. 6,16,17This has important implications, given that 63.5% of patients with LTBI who were offered treatment completed the full course of therapy, and 11.4% of those who were suitable for LTBI treatment in this study were lost to follow-up.Educating patients about symptoms of reactivation and the need for prompt medical assessment are priorities to reduce the spread of active TB.This study also found that 64.7% of patients with refugee camp exposure were diagnosed with either active TB or LTBI.The World Health Organization recognises the significant burden of TB infections within refugee camps, and estimates that each person with active TB will infect, on average, 10 to 15 people per year if left untreated. 17Prior refugee camp residents are a group in which early postarrival TB screening should be expedited.The second-most common diagnosis in this study was vitamin deficiency (affecting 15.5%), considerably lower than the 20-80% found in other studies. 9,12,13This lower prevalence may be attributed to appropriate management of vitamin deficiencies in general practice, resulting in fewer referrals.Of 20 referrals made by GPs to the clinic for vitamin deficiency, 18 were for paediatric patients, probably reflecting an inability to access the recommended higher dose vitamin D therapy 18 in the community.The smaller African population in this study (33.6%) may have contributed to the lower rate of vitamin deficiency when compared to other studies. 12,13HB accounted for 11.0% of diagnoses in this study population.Of 32 patients diagnosed with CHB, 19 (59.3%) were diagnosed by GPs prior to referral to the Refugee Health Clinic.The rate of CHB in African patients (12.6%) in this study is substantially lower than reported rates of 56.7% found in sub-Saharan African refugees attending a primary care Migrant Health Unit in Western Australia, 13 but is comparable to the 8% found in African patients attending general practice clinics throughout Melbourne, 12 and 19% in African immigrants at a referral ID unit. 11he rate of CHB among refugees is considerable compared to the Australian prevalence estimate of 1%, 19 highlighting the importance of detection of infection and vaccination of the non-immune in the initial refugee health assessment.
Schistosomiasis was present in 11.0% of referred patients, which is similar to the 6-12% found in African migrants in the primary healthcare setting 12,13 and the 17% found in a study involving refugees from various origins. 9The lower prevalence in this study, compared with the 41% detected among African immigrants attending an ID unit, 11 may be explained by the UHG clinic's smaller African population, in which schistosomiasis is endemic. 6Blood testing for schistosomiasis in general practice should be offered to patients who have lived in, or travelled through, endemic countries (including Africa, parts of South-East Asia and the Middle East). 6ttendance rates at the UHG clinic were poor: 35.4% of patients attended all scheduled appointments, and nearly half of patients missed two or more scheduled appointments (Table 2).This is significantly lower than the 81% attendance rate at the Migrant Health Unit in Western Australia. 13owever, the Migrant Health Unit is a primary healthcare service, while the UHG Refugee Health Clinic operates on a referral basis.Non-attendance rates may be due, at least in part, to problems such as competing priorities, unstable housing, poor health literacy, distance, and a lack of transport, especially for patients living in remote areas of South-Western Victoria.This underscores the important role of GPs in the provision of care closer to home, potentially in a shared care arrangement with specialists, and use of Telehealth.Language barriers, cultural responsiveness, appointment waiting times and cost are additional factors that have been shown to influence access and attendance of refugees. 20Further local research into reasons for poor clinic attendance and solutions to this challenge are required.Nearly 30% of patients attending the clinic were diagnosed with two or more conditions, demonstrating the complex variety of health conditions among newly arrived refugees.This highlights the need for comprehensive pre-departure and post-arrival health assessments and the important role of GPs in ongoing patient care.Comprehensive guidelines on refugee screening and management of common conditions are a useful resource. 6Ongoing patient care must focus on those needs of refugees unmet in the UHG clinic, including cancer screening, psychological support, improving health literacy, and referrals for dental and allied health.
Possible limitations of this study include reliance on the accuracy of information in medical records, potentially resulting in ascertainment bias.Incomplete screening and subjective practitioner evaluation may have also resulted in selection bias.Notwithstanding these limitations, the electronic record system used provides an accurate record of attendance, reasons for referral, and medical review.
This study confirms that LTBI, vitamin deficiency, parasitic infestation and hepatitis B are common among newly arrived refugees in Australia referred to a tertiary centre.In addition, this study uncovers the challenges of poor attendance at scheduled clinic appointments, suboptimal completion of treatment for LTBI, and a concerning loss to follow-up among refugees.In particular, awareness of potential LTBI reactivation is critical.Future research is required to understand the barriers to clinic attendance, adherence to LTBI treatment and how to best integrate services and follow-up in general practice for refugee patients in the Greater Geelong region.

Table 1 .
6ecommendations for screening and treatment of LTBI6 CXR, chest X-ray; HIV, human immunodeficiency virus; LBTI, latent tuberculosis infection; TB, tuberculosisAdapted with permission the Australasian Society for Infectious Diseases, from Denholm J, Bailes M, Francis J. Tuberculosis.In: Chaves NJ, Paxton G, Biggs BA, et al; on behalf of the Australasian Society for Infectious Diseases and Refugee Health Network of Australia Guidelines writing group.Recommendations for comprehensive post-arrival health assessment for people from refugee-like backgrounds.2ndedn.Surry Hills, NSW: Australasian Society for Infectious Diseases and Refugee Health Network ofAustralia, 2016.

Table 2 .
Characteristics of patients reviewed in the Refugee Health Clinic

Table 3 .
GP referrals to the refugee health clinic and diagnostic outcomes of all patients AFB, acid-fast bacilli; GP, general practitioner; IGRA, interferon gamma release assay; LBTI, latent tuberculosis infection; TB, tuberculosis; TST, tuberculin skin test

Table 4 .
Outcomes of patients with a confirmed diagnosis of latent tuberculosis