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. 2022 Mar 4;17(3):e0264435. doi: 10.1371/journal.pone.0264435

Testing and healthcare seeking behavior preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: Directions for early-case finding

Ward P H van Bilsen 1,*, Janneke P Bil 1, Jan M Prins 2, Kees Brinkman 3, Eliane Leyten 4, Ard van Sighem 5, Maarten Bedert 1, Udi Davidovich 1,6, Fiona Burns 7, Maria Prins 1,2
Editor: Awachana Jiamsakul8
PMCID: PMC8896686  PMID: 35245293

Abstract

Objectives

To assess differences in socio-demographics, HIV testing and healthcare seeking behavior between individuals diagnosed late and those diagnosed early after HIV-acquisition.

Design

Cross-sectional study among recently HIV-diagnosed migrant and non-migrant individuals living in the Netherlands.

Methods

Participants self-completed a questionnaire on socio-demographics, HIV-testing and healthcare seeking behavior preceding HIV diagnosis between 2013–2015. Using multivariable logistic regression, socio-demographic determinants of late diagnosis were explored. Variables on HIV-infection, testing and access to care preceding HIV diagnosis were compared between those diagnosed early and those diagnosed late using descriptive statistics.

Results

We included 143 individuals with early and 101 with late diagnosis, of whom respectively 59/143 (41%) and 54/101 (53%) were migrants. Late diagnosis was significantly associated with older age and being heterosexual. Before HIV diagnosis, 89% of those with early and 62% of those with late diagnosis had ever been tested for HIV-infection (p<0.001), and respectively 99% and 97% reported healthcare usage in the Netherlands in the two years preceding HIV diagnosis (p = 0.79). Individuals diagnosed late most frequently visited a general practitioner (72%) or dentist (62%), and 20% had been hospitalized preceding diagnosis. In these settings, only in respectively 20%, 2%, and 6% HIV-testing was discussed.

Conclusion

A large proportion of people diagnosed late had previously tested for HIV and had high levels of healthcare usage. For earlier-case finding of HIV it therefore seems feasible to successfully roll out interventions within the existing healthcare system. Simultaneously, efforts should be made to encourage future repeated or routine HIV testing among individuals whenever they undergo an HIV test.

Introduction

In the Netherlands, the number of new HIV diagnoses decreased from 1,026 in 2013 to 580 in 2019. The majority of diagnoses were among men who reported sex with other men (61%) and a relatively large proportion was born outside the Netherlands (42%) [1]. Over the past years, efforts have been made to increase HIV testing uptake among specific subgroups. Individuals at higher risk, e.g. men who have sex with men (MSM) and sex workers, are offered free-of-charge HIV testing at Sexual Health Centers (SHC) of Public Health Services and during outreach activities. Individuals can also test for HIV at the general practitioner (GP), which costs approximately €10 as part of the deductible excess of one’s health insurance. Individuals without a health insurance or residence permit are also able to get tested for HIV at the GP or SHC.

Despite wide-spread availability of HIV tests in the Netherlands, still one out of every three individuals newly diagnosed with HIV received their diagnosis at a late stage of disease [1]. Late HIV diagnoses, i.e. having <350/mm3 CD4+-cells or an AIDS-defining illness at time of HIV diagnosis [2], have been defined as a major public health challenge in ending the HIV epidemic, as it contributes to ongoing HIV transmission [3]. On the individual level, late diagnosis is associated with adverse clinical outcomes [4, 5]. It is therefore important to identify and treat individuals with an HIV-infection as early as possible. For the development of effective interventions to increase earlier diagnosis, more knowledge is needed about factors associated with late diagnosis. Also, it is important to assess which opportunities for testing are currently being missed. In this study we aimed to assess whether socio-demographic characteristics, HIV testing and healthcare seeking behavior preceding HIV diagnosis differed between individuals with early and late diagnosis in the Netherlands.

Methods

Study design and population

Data was used from individuals living in the Netherlands who participated in the European advancing Migrant Access to health services in Europe (aMASE) study. Inclusion criteria and study procedures of the aMASE study are described elsewhere [6, 7]. Briefly, migrant and non-migrant individuals aged ≥18 years with an HIV diagnosis in the five years preceding recruitment were included between 2013–2015. Recruitment in the Netherlands was conducted at three HIV outpatient treatment clinics in Amsterdam and The Hague. Participants completed a self-administered computer-assisted questionnaire or personal interview on socio-demographics, and use of HIV-related services before and after HIV diagnosis (see S1 and S2 Appendices). Questionnaire items were mostly generated using existing survey instruments, and new questions were drafted by the aMASE research team and international experts and EuroCoord calloborators [6]. Validation of the questionnaire was done using cognitive testing by Latin American and black African migrants living in Spain and England who were recruited from community-based HIV service organizations [8]. Questionnaire items were available in 15 languages. Clinical data were obtained from the ATHENA (AIDS Therapy Evaluation in the Netherlands) HIV cohort database [1].

Study variables

Socio-demographic characteristics included age at study inclusion and HIV diagnosis, gender, sexual orientation, education level, income, migration background (defined as born outside the Netherlands), region of birth, self-defined ethnicity, injecting drug use and attending religious services at least once a year.

Variables related to HIV diagnosis included years since HIV diagnosis at study inclusion, location of HIV diagnosis, and CD4+-cell count and AIDS-defining illness at time of HIV diagnosis. Late HIV diagnoses was defined as having <350/mm3 CD4+-cells or an AIDS-defining illness at time of HIV diagnosis [2]. Among migrants, years between migration and HIV diagnosis and country of HIV diagnosis was additionally assessed. Variables on testing behavior preceding HIV diagnosis included ever having had an HIV test before diagnosis, and, among those with a previous HIV test, years between last negative HIV test and HIV diagnosis. Self-reported diagnosis of hepatitis B virus (HBV), hepatitis C virus (HCV) or bacterial sexually-transmitted infection (STI) preceding HIV diagnosis was additionally assessed.

Variables on access to healthcare preceding HIV diagnosis included registration at a GP in the Netherlands at time of HIV diagnosis, healthcare usage in the Netherlands in the two years preceding HIV diagnosis, and experienced difficulty accessing healthcare in the Netherlands. Among those with healthcare usage in the two years preceding HIV diagnosis, we assessed which healthcare professionals were visited and whether an HIV test was discussed during these visits.

Statistical analyses

First, we constructed a multivariable logistic regression model to explore whether socio-demographic characteristics were associated with late presentation. Variables with a p-value<0.2 in univariable analysis were included in a multivariable model, after which all non-significant variables were subsequently removed in a backwards-stepwise fashion. Second, variables on HIV diagnosis, and HIV testing and access to care preceding HIV diagnosis were compared between those with an early and late HIV diagnosis using Pearson’s χ2 test or Fisher’s exact test for categorical data and Mann-Whitney U test for continuous data. As sexual orientation and migrant background was shown to affect previous outcomes of aMASE studies [6, 9], participants were categorized in the following six groups: non-migrant men who have sex with men (MSM), migrant MSM, non-migrant heterosexual men, migrant heterosexual men, non-migrant women and migrant women.

All analyses were conducted in STATA IC v15.0. A p-value<0.05 was considered statistically significant.

Ethical considerations

The medical ethical committee of the University of Amsterdam approved the aMASE study in the Netherlands (2013_137#C20131038). Informed consent was obtained for all participants through a tick box in the questionnaire.

Results

In total, 417 individuals diagnosed with HIV in the preceding 5 years were invited for study participation, of whom 252 (60%) agreed to participate. Eight participants were excluded from further analyses, as stage of HIV-infection at time of diagnosis could not be determined. Among the included 244 participants, 143 (59%) were classified as being diagnosed early and 101 (41%) as late. Of these, respectively 123/143 (86%) and 63/101 (62%) were identified as MSM, and 59/143 (41%) and 54/101 (53%) as migrants (Table 1). Those diagnosed late were older at time of study participation and HIV diagnosis compared to those diagnosed earlier (p<0.001 for both). Education level did not differ significantly between groups: 47% of participants with early and 36% of participants with late diagnosis reported to be highly educated (p = 0.08).

Table 1. Socio-demographic characteristics of aMASE-study participants in the Netherlands, 2013–2015, including uni- and multivariable logistic regression analysis of determinants associated with late diagnosis of HIV infection.

Early diagnosis* (N = 143) Late diagnosis* (N = 101) Association with late diagnosis*, univariable analyses Association with late diagnosis *, multivariable analysis
n/N % n/N % OR 95%-CI p-value aOR 95%-CI p-value
Age at HIV-diagnosis (median, IQR) 37 [29–48] 44 [37–50] 1.04 1.01–1.06 .001 1.04 1.01–1.06 .007
Male 130/143 91% 90/101 89% 0.82 0.35–1.91 .643
Sexual orientation according to migration status
 Non-migrant MSM 75/143 53% 37/101 37% Ref < .001 Ref < .001
 Migrant MSM 48/143 34% 26/101 26% 1.10 0.59–2.04 1.34 0.70–2.57
 Non-migrant heterosexual male 4/143 3% 10/101 10% 5.07 1.49–17.24 5.57 1.60–19.40
 Migrant heterosexual male 3/143 2% 17/101 17% 11.48 3.17–41.69 11.14 3.04–40.81
 Migrant heterosexual female 8/143 6% 11/101 11% 2.79 1.03–7.52 3.20 1.16–8.88
 Non-migrant heterosexual female 5/143 4% 0/101 0% - - - -
College degree or higher 67/143 47% 36/101 36% 0.63 0.37–1.06 .080
Lower income level (less than minimum wage) 43/134 32% 46/94 49% 2.03 1.18–3.49 .010
Region of birth † .001
 Europe, the Netherlands 84/143 59% 47/101 57% Ref
 Europe, other than the Netherlands 23/143 16% 10/101 10% 0.78 0.34–1.77
 Sub-Saharan Africa 7/143 5% 22/101 22% 5.61 2.23–14.13
 Latin America / Caribbean 15/143 10% 11/101 11% 1.31 0.56–3.08
 Other 14/143 10% 11/101 11% 1.40 0.59–3.34
Self-defined ethnicity † .008
 European 92/141 65% 54/101 54% Ref
 African 9/141 6% 22/101 22% 4.16 1.79–9.70
 American 4/141 3% 2/101 2% 0.85 0.15–4.81
 Asian 9/141 6% 8/101 8% 1.51 0.55–4.16
 Mixed 13/141 9% 9/101 9% 1.18 0.47–2.94
 Latin America / Caribbean 11/141 8% 2/101 2% 0.31 0.07–1.45
 Middle Eastern 3/141 2% 4/101 4% 2.27 0.49–10.53
Attending religious services at least once a year 42/138 30% 32/99 32% 1.09 0.63–1.90 .757
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95%-CI, 95% confidence interval; aOR, adjusted odds ratio; OR, odds ratio; IQR, interquartile range; NA, Not applicable.

* Late HIV diagnoses is defined as having had an AIDS-defining illness or a CD4 count <350 cells/mm3 at time of HIV diagnosis.

† Not included in the multivariable model due to collinearity with variable on sexual orientation according to migration status.

In multivariable analysis (Table 1), late diagnosis was associated with older age at time of HIV diagnosis (adjusted odds ratio [aOR] = 1.04 per year, 95%-CI = 1.01–1.06). Also, being heterosexual was associated with late diagnoses: compared to non-migrant MSM, the adjusted odds of being diagnosed late was 1.34 (95%-CI = 0.70–2.57) for migrant MSM, 5.57 (95%-CI = 1.60–19.40) for non-migrant heterosexual males, 11.14 (95%-CI = 3.04–40.81) for migrant heterosexual males, and 3.20 (95%-CI = 1.16–8.88) for migrant heterosexual females (p<0.001).

HIV diagnosis and HIV/STI-testing preceding HIV diagnosis

The majority of migrant participants were diagnosed with HIV in the Netherlands (93% of those diagnosed early and 91% of those diagnosed late; p = 0.87; Table 2). Years between migration to the Netherlands and HIV diagnosis did not differ between those diagnosed early or late (median 8 [IQR = 2–24] vs. 6 [IQR = 1–14] years; p = 0.17).

Table 2. HIV-diagnosis characteristics, HIV/STI-testing and access to healthcare preceding HIV-diagnosis among aMASE-study participants in the Netherlands, 2013–2015, stratified by early versus late HIV presenters.

Early diagnosis* (N = 143) Late diagnosis* (N = 101) p-value
n/N % n/N %
HIV-diagnosis
Years since HIV-diagnosis (median, IQR) 2 [1–3] 2 [1–4] .070
Location of HIV-diagnosis < .001
 Sexual health clinic / HIV testing clinic 80/139 58% 25/96 26%
 Hospital 22/139 16% 40/96 42%
 GP 30/139 22% 26/96 27%
 Other† 7/139 5% 5/96 5%
Years between migration to the Netherlands and HIV diagnosis (median, IQR) ‡ 8 [2–24] 6 [1–14] .168
Country of HIV diagnosis ‡ .874
 The Netherlands 55/59 93% 49/54 91%
 Country of birth 3/59 5% 4/54 7%
 Other country 1/59 2% 1/54 2%
HIV and STI-testing preceding HIV-diagnosis
Ever had a negative HIV-test before HIV-diagnosis 127/143 89% 63/101 62% < .001
Years between previous negative HIV-test and HIV-diagnosis (median, IQR) Ϟ 1 [0–3] 4 [2–9] < .001
Country of previous HIV negative test ‡,Ϟ .112
 The Netherlands 33/51 65% 14/30 47%
 Another country 18/51 35% 16/30 53%
Ever had a positive HBV test before HIV diagnosis 22/143 15% 13/101 13% .581
Ever had a positive HCV test before HIV diagnosis 19/143 13% 4/101 4% .014
Ever had a STI before HIV diagnosis 96/143 67% 39/101 39% < .001
Access to healthcare preceding HIV-diagnosis
Registered at a GP in the Netherlands 141/143 99% 98/101 97% .393
Healthcare usage in the Netherlands two years before HIV-diagnosis Ψ 121/130 93% 78/85 92% .793
 Antenatal care 1/130 1% 0/85 0% .999
 Dentist 90/130 69% 53/85 62% .296
 Drug treatment center 1/130 1% 2/85 2% .564
 General practitioner 89/130 69% 61/85 72% .606
 Hospital, emergency room 24/130 19% 12/85 14% .404
 Hospital, inpatient admission 17/130 13% 17/85 20% .174
 Hospital, outpatient clinic 36/130 28% 14/85 17% .057
 Medical care at refugee center 0/130 0% 1/85 1% .215
 Mental health facility 14/130 11% 5/85 6% .217
 Sexual health clinic or HIV testing clinic 59/130 45% 9/85 11% < .001
HIV-testing discussed during healthcare attendance in the two years before HIV-diagnosis ¢ 61/118 52% 19/75 25% < .001
 Antenatal care 0/1 0% 0/0 NA NA
 Dentist 2/90 2% 1/53 2% .999
 Drug treatment center 1/1 100% 2/2 100% NA
 General practitioner 26/89 29% 12/61 20% .187
 Hospital, emergency room 1/24 4% 0/12 0% .999
 Hospital, inpatient admission 1/17 6% 1/17 6% .999
 Hospital, outpatient clinic 6/36 17% 3/14 21% .697
 Medical care at refugee center 0/0 NA 0/1 0% NA
 Mental health facility 3/14 21% 0/5 0% .530
 Sexual health clinic or HIV testing clinic 46/59 78% 4/9 44% .048
Experienced difficulties accessing healthcare in the Netherlands 13/143 9% 13/100 13% .332
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IQR, interquartile range; GP, general practitioner; HBV, hepatitis B virus; HCV, hepatitis C virus; STI, sexually transmittable infection.

* Late HIV diagnosis is defined as having had an AIDS-defining illness or a CD4 count <350 cells/mm3 at time of HIV diagnosis.

† Other includes: antenatal care (n = 3), refugee center (n = 3), fertility clinic (n = 1), dentist (n = 1), self-test (n = 1), medical examination (n = 1), private clinic (n = 1), unknown (n = 1).

‡ Among migrants.

Ϟ Only participants were included who had a previous negative HIV test before diagnosis.

Ψ Only participants were included who lived in the Netherlands for two years or more and who were diagnosed with HIV in the Netherlands.

¢ Only participants were included who lived in the Netherlands for two years or more, who were diagnosed with HIV in the Netherlands and who had used healthcare in the Netherlands in the previous two years before HIV diagnosis.

Before HIV diagnosis, 89% of participants diagnosed early and 62% who were diagnosed late had previously been tested for HIV-infection (p<0.001). Among those previously tested, median time between last negative HIV test and HIV diagnosis was 1 [IQR = 0–3] year for participants diagnosed early and 4 [IQR = 2–9] years for participants diagnosed late (p<0.001). In total, 67% of participants diagnosed early and 39% of participants diagnosed late had been diagnosed with a STI prior to their HIV diagnosis (p<0.001). Preceding HIV diagnosis, HCV was also more frequently diagnosed in participants with early diagnosis (13% vs. 4%, p = 0.014).

Access to healthcare preceding HIV diagnosis

Difficulty accessing healthcare preceding HIV diagnosis was reported by 9% of participants with early and 13% of participants with late diagnosis (p = 0.33) (Table 2). Also when analyses were restricted to migrants only, there was no difference in experienced difficulty accessing healthcare between groups (17% vs. 23%, p = 0.45). Healthcare use in the two years preceding HIV diagnosis was reported by the majority whether diagnosed early or late (93% vs. 92%, respectively; p = 0.79). The GP and dentist were the most frequently visited healthcare professionals. Those with early diagnosis more frequently visited a sexual health clinic (SHC) preceding diagnosis compared to those with late diagnosis (45% vs. 11%, respectively; p<0.001). During SHC visits, HIV testing was discussed with 78% of participants with early and 44% of participants with late diagnosis (p = 0.048). There was no difference between groups in the extent to which HIV testing was discussed during visits at other healthcare locations.

Discussion

In this study, late diagnosis of HIV was associated with older age and being heterosexual in both migrants and non-migrants living with HIV in the Netherlands. We additionally show that preceding HIV diagnosis, a relatively large proportion of people diagnosed late had previously tested for HIV and had high levels of healthcare usage, suggesting missed opportunities for early HIV diagnosis in this group.

Our association between late HIV diagnosis and older age and being heterosexual is in line with previous studies conducted in the Netherlands and other high-income countries [10, 11]. Several other studies additionally showed that late diagnosis is associated with a low HIV risk perception, which was not measured in our study, and being born in a country outside the one of current residence [12]. We previously demonstrated that disparities in access to and use of HIV-related health services and experiences exist by migrant status but also by sexual orientation [7].

Although late stage HIV-infections were associated with being heterosexual, it must be noted that the majority of people diagnosed late in the current study were MSM, reflecting the HIV epidemic in many high-income countries including the Netherlands where most newly-diagnosed infections occur among MSM [13]. This suggests that late diagnosis of HIV should be addressed in both groups, and that different strategies are needed to increase timely HIV testing. Our data showing that 62% of participants diagnosed late had previously tested for HIV test is reassuring, as it suggests that most individuals are not averse to HIV testing per se. Ways should be found to encourage more frequent HIV testing among these individuals, as time between last negative HIV test and HIV diagnosis was relatively long in the current study. This might be achieved by discussing the importance of routine HIV testing with individuals whenever they undergo an HIV test.

Our findings additionally support the need to increase healthcare provider-initiated testing, as recommended by the European Centre for Disease Prevention and Control [14]. In our study sample, 92% of participants diagnosed late visited a healthcare provider in the two years preceding HIV diagnosis, in which an HIV test was not often discussed. Efforts have been made in recent years to increase pro-active testing by GPs across Europe, which focus on testing based on indicator disease, sexual orientation, migration background and residence area [15, 16]. The impact of such interventions on testing behavior of GPs is mixed [17–19]. This might be attributable to several wide-spread barriers among GPs including competing priorities in general practice, difficulties with the organizational implementation of HIV testing, fear to discuss or offer HIV testing to patients, lack of registration of sexual orientation and migration background in patient files, and concerns regarding the impact that an HIV test can have on patients [16, 20]. These barriers should be addressed, and other opportunities within the existing healthcare system should be explored. For example, participants of the current study also frequently visited a dentist and were admitted to a hospital preceding HIV diagnosis. Providing HIV testing in these settings are likely hindered by similar barriers as described for GPs, although the majority of dentists in several high-income countries seem willing to conduct rapid HIV tests in their practice [21], which could be useful in cases of oral candidiasis or oral hairy leukoplakia, and intervention to increase targeted HIV testing in hospitals, especially emergency rooms, show promising results in some settings [22, 23].

A limitation of the current study was the lack of detailed information on motives and barriers for HIV testing among our participants. This limited us from exploring reasons why HIV testing was not performed earlier among people diagnosed late. These issues will need greater consideration in future studies. Furthermore, healthcare systems and characteristics of risk populations might differ across countries. Our results should therefore be generalized to other countries with caution. Finally, the generalizability of our study might be subject to selection bias, as 40% of individuals invited for study participation refused to participate. A previous study using aMASE data from Dutch recruitment sites showed that especially migrants from Latin America/Caribbean, non-migrant women and heterosexual men were less likely to participate, and therefore are likely underrepresented in the current study [7].

In conclusion, interventions to increase HIV testing are needed to diagnose and treat HIV-infections in an early stage. As most people diagnosed late used healthcare preceding their HIV diagnosis in which HIV testing was not discussed, it seems feasible to successfully roll out interventions to increase testing within the existing healthcare system. Simultaneously, efforts should be made to encourage future repeated or routine HIV testing among individuals whenever they undergo an HIV test.

Supporting information

S1 Appendix. aMASE clinic questionnaire, Dutch version.

(PDF)

Click here for additional data file. (899.7KB, pdf)
S2 Appendix. aMASE clinic questionnaire, English version.

(PDF)

Click here for additional data file. (412.1KB, pdf)

Data Availability

The Medical Ethical Committee of the University of Amsterdam put restrictions on publicly sharing data of the aMASE study as it contains potentially identifying information of human subjects. The data that support the findings of this study are however available upon reasonable request from the corresponding author (wvbilsen@ggd.amsterdam.nl) or the aMASE study group (amatser@ggd.amsterdam.nl). Data requests will be reviewed by the aMASE study group.

Funding Statement

The author(s) received no specific funding for this work.

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Decision Letter 0

Justyna Dominika Kowalska

26 Oct 2021

PONE-D-21-18622Testing and healthcare seeking behavior preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: directions for early-case findingPLOS ONE

Dear Dr. van Bilsen,

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Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The presented analysis touches on a very important topic in Europe Testing and healthcare seeking behaviour preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: directions for early-case finding.

The prepared material lacks the broader context of the situation described in the INTRODUCTION. There is no information about the epidemiological situation. There is even a lack of basic information on the number of infected people per year of tests, the proportion of HIV migrants and the specificity of HIV infection in the country described. Therefore, it is difficult to relate the obtained results to the general situation in the described country.

There is also a lack of information about the testing system, is it open to the public, paid / free of charge, do the migrants have the same access for testing as other residents? Is there any barriers: eg language, knowledge.

The METHODS: There is no explanation why 90% of the study was male? Do they test themselves more often, why is there such a small percentage of women both on tests and among migrants? Is it a national specificity or a deliberate selection for the study. If so, what was the decision made.

40% of the respondents refused to take part in the survey, there is no comment on this relatively large percentage

The DISSCUSION part also needs improvement. There are few references to research on similar topics. Whether the obtained results are consistent with the previous research on testing, or are they different in terms of characteristics.

It is worth comparing the obtained results to other studies on testing among migrants in Europe.

The whole article is very interesting, but actually how it was written was the lack of detailed information on motives and barriers for HIV testing among our participants. This could be an interesting issue for further analysis.

Reviewer #2: On my mind the objectives of this article is extremely important, because late HIV diagnostic remains as a huge problem not only for Western Europe but for Eastern Europe as well, where I am from.

Cross-sectional study design and statistical analysis using multivariable logistic regression were good conducted. Previously, I did not find the criteria inclusion for late diagnosis in methods. But I found them in Table 1: Late HIV diagnoses is defined as having had an AIDS-defining illness or a CD4 less than 350 cells/mm3 at time of HIV diagnosis. I think it is better include to methods. Manuscript presented in an intelligible fashion and written in standard English. Authors made all data underlying the findings in their manuscript fully available.

In conclusion, interventions to increase HIV testing are needed to diagnose and treat HIV-infections in an early stage. As most people diagnosed late used healthcare preceding their HIV diagnosis in which HIV testing was not discussed, it seems feasible to successfully roll out interventions to increase testing within the existing healthcare system. Simultaneously, efforts should be made to encourage future repeated or routine HIV testing among individuals whenever they undergo an HIV test.

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Reviewer #1: Yes: Magdalena Ankiersztejn-Bartczak

Reviewer #2: Yes: Tetiana Kyrychenko

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PLoS One. 2022 Mar 4;17(3):e0264435. doi: 10.1371/journal.pone.0264435.r002

Author response to Decision Letter 0

12 Jan 2022

Reviewers’ comments:

Reviewer #1

The presented analysis touches on a very important topic in Europe Testing and healthcare seeking behaviour preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: directions for early-case finding.

The prepared material lacks the broader context of the situation described in the INTRODUCTION. There is no information about the epidemiological situation. There is even a lack of basic information on the number of infected people per year of tests, the proportion of HIV migrants and the specificity of HIV infection in the country described. Therefore, it is difficult to relate the obtained results to the general situation in the described country.

There is also a lack of information about the testing system, is it open to the public, paid / free of charge, do the migrants have the same access for testing as other residents? Is there any barriers: eg language, knowledge.

Response: We acknowledge that the introduction was fairly brief and that additional information on the HIV epidemiology and testing services in the Netherlands is useful for the interpretation of our data. In the introduction section of the revised manuscript, we therefore elaborated on these topics.

The METHODS: There is no explanation why 90% of the study was male? Do they test themselves more often, why is there such a small percentage of women both on tests and among migrants? Is it a national specificity or a deliberate selection for the study. If so, what was the decision made.

40% of the respondents refused to take part in the survey, there is no comment on this relatively large percentage

Response: In the Netherlands, most new HIV infections occur in men who have sex with men (61% in 2019). Also in our study, the majority of participants were MSM (87%), which resulted in a relatively high proportion of men in the study. In table 1, the proportion of males in our study is specified, as well as the proportion of MSM and heterosexual individuals.

With regard to the response rate, we added a comment on this in the limitation section of the revised manuscript.

The DISSCUSION part also needs improvement. There are few references to research on similar topics. Whether the obtained results are consistent with the previous research on testing, or are they different in terms of characteristics.

It is worth comparing the obtained results to other studies on testing among migrants in Europe.

The whole article is very interesting, but actually how it was written was the lack of detailed information on motives and barriers for HIV testing among our participants. This could be an interesting issue for further analysis.

Response: We agree with the reviewer that our discussion section lacked comparison between our study findings and that of previous studies or data of other high-income countries. In the revised version of our manuscript, we added information on this topic. We moreover mention that it would be interesting to further investigate motives and barriers for HIV testing among those with a late HIV diagnosis.

Reviewer #2

On my mind the objectives of this article is extremely important, because late HIV diagnostic remains as a huge problem not only for Western Europe but for Eastern Europe as well, where I am from.

Cross-sectional study design and statistical analysis using multivariable logistic regression were good conducted. Previously, I did not find the criteria inclusion for late diagnosis in methods. But I found them in Table 1: Late HIV diagnoses is defined as having had an AIDS-defining illness or a CD4 less than 350 cells/mm3 at time of HIV diagnosis. I think it is better include to methods. Manuscript presented in an intelligible fashion and written in standard English. Authors made all data underlying the findings in their manuscript fully available.

In conclusion, interventions to increase HIV testing are needed to diagnose and treat HIV-infections in an early stage. As most people diagnosed late used healthcare preceding their HIV diagnosis in which HIV testing was not discussed, it seems feasible to successfully roll out interventions to increase testing within the existing healthcare system. Simultaneously, efforts should be made to encourage future repeated or routine HIV testing among individuals whenever they undergo an HIV test.

Response: We thank the reviewer for this feedback. As suggested, we added the definition of late HIV diagnosis to the Method section of the revised manuscript.

Decision Letter 1

Awachana Jiamsakul

11 Feb 2022

Testing and healthcare seeking behavior preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: directions for early-case finding

PONE-D-21-18622R1

Dear Dr. van Bilsen,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kind regards,

Awachana Jiamsakul, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The article deals with a very important problem in Europe. The comments made in the first review have been incorporated in the revised version of the article. The additions added by the authors help to better understand the context of the HIV epidemic in the country.

Reviewer #2: I am very satisfied with results of the research and findings that late diagnosis was significantly associated with older age and being heterosexual.

It very interesting that a large proportion of people diagnosed late had previously tested for HIV and had high levels of healthcare usage. Really, efforts should be made to encourage future repeated or routine HIV testing among individuals whenever they undergo an HIV test. In Ukraine we have late diagnosis of HIV, some patients were diagnosed with HIV more than15 years and they did not visit doctor until feel worse. I think we can collaborate for future research. Please, feel free to send me your proposal on email tanakyrychenko@gmail.com

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Magdalena Ankiersztejn-Bartczak

Reviewer #2: Yes: Tetiana Kyrychenko

Acceptance letter

Awachana Jiamsakul

22 Feb 2022

PONE-D-21-18622R1

Testing and healthcare seeking behavior preceding HIV diagnosis among migrant and non-migrant individuals living in the Netherlands: directions for early-case finding

Dear Dr. van Bilsen:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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on behalf of

Dr. Awachana Jiamsakul

Academic Editor

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Appendix. aMASE clinic questionnaire, Dutch version.

    (PDF)

    Click here for additional data file. (899.7KB, pdf)
    S2 Appendix. aMASE clinic questionnaire, English version.

    (PDF)

    Click here for additional data file. (412.1KB, pdf)

    Data Availability Statement

    The Medical Ethical Committee of the University of Amsterdam put restrictions on publicly sharing data of the aMASE study as it contains potentially identifying information of human subjects. The data that support the findings of this study are however available upon reasonable request from the corresponding author (wvbilsen@ggd.amsterdam.nl) or the aMASE study group (amatser@ggd.amsterdam.nl). Data requests will be reviewed by the aMASE study group.

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