Pandemic (H1N1) 2009 Surveillance in Marginalized Populations, Tijuana, Mexico

To detect early cases of pandemic (H1N1) 2009 infection, in 2009 we surveyed 303 persons from marginalized populations of drug users, sex workers, and homeless persons in Tijuana, Mexico. Six confirmed cases of pandemic (H1N1) 2009 were detected, and the use of rapid, mobile influenza testing was demonstrated.

. The virus responsible for the outbreak, identifi ed as a novel infl uenza A (H1N1) virus, now referred to as pandemic (H1N1) 2009, spread quickly. By the end of 2009, ≈70,000 cases were confi rmed and 944 deaths were recorded in Mexico (2), and >600,000 cases were reported worldwide (3).
When pandemic (H1N1) 2009 fi rst emerged there was concern that Mexico-US border cities, which have served as corridors for binational transmission of infectious diseases (4), might become overwhelmed by the disease before national surveillance resources could be mobilized. Of particular concern was the fact that traditional hospital-based disease surveillance would miss the emergence of pandemic (H1N1) 2009 in the dense, highly mobile (5), marginalized border populations. Furthermore, the poorest and most underserved border populations, composed of the homeless, commercial sex workers, and those with alcohol and drug abuse problems, have disproportionately high levels of diseases such as HIV (6) and tuberculosis (7), illnesses suspected of increasing vulnerability to acquiring and dying of pandemic (H1N1) 2009 (8,9). We report the results of an enhanced surveillance effort to detect early pandemic (H1N1) 2009 cases and assess perceptions of the pandemic and risk factors associated with acquiring the disease in marginalized populations in Tijuana, Mexico.

The Study
This surveillance project was a collaboration between Mexican public health offi cials, nongovernment organizations, and the University of California, San Diego (UCSD). The project was approved by the institutional review boards of Tijuana General Hospital and UCSD.
Our binational research team of US and Mexican researchers has been conducting prospective studies of populations at high risk for infectious diseases in the most vulnerable communities of Tijuana and Ciudad Juarez, Mexico, since 2004 (10,11). More than 2,500 drug users, sex workers, and homeless persons have been recruited to participate in those studies. From May 1 through November 20, 2009, we conducted active and passive infl uenza surveillance within our existing marginalized study populations in Tijuana. We used mobile outreach units and community clinics in the city's Zona Roja (red light zone) as magnet sites (Figure).
Active surveillance included contacting all known current and previous study participants, parking mobile health units in study zones ( Figure), and having outreach workers refer persons who reported feeling unwell for any reason. Passive recruitment, conducted by word-of-mouth advertising, was open to all persons in communities served by our mobile and fi xed-site clinics.
Persons seen by the surveillance team had their oral temperatures recorded and completed brief surveys documenting demographics, infl uenza risk factors, and clinical symptoms. Persons meeting inclusion criteria for infl uenza-like illness based on early Centers for Disease Control and Prevention guidelines (12) were considered pandemic (H1N1) 2009 suspected case-patients. Inclusion criteria were a subjective or objective fever (oral temperature >100°F [37.8°C]) and 1 of the following signs or symp- toms: cough, sore throat, severe headache, diarrhea, vomiting, or severe muscle/body aches and fatigue. Persons with infl uenza-like illness completed an indepth survey and underwent rapid infl uenza testing. Participants were compensated $5 US. In-depth surveys included questions on symptom duration, treatment choices, and pandemic (H1N1) 2009 knowledge.
Enrolled pandemic (H1N1) 2009 suspected case-patients provided a nasopharyngeal swab for rapid infl uenza testing with the BinaxNOW assay (Inverness Medical, Waltham, MA, USA). Suspected case-patients with positive rapid test results for type A infl uenza were considered probable pandemic (H1N1) 2009 case-patients and provided another nasopharyngeal swab for infl uenza A strain confi rmation and characterization. Persons with positive test results were transported to Tijuana General Hospital for evaluation and treatment. Suspected case-patients with negative rapid infl uenza test results were not evaluated further.
Nasal swab specimens were cultured on MDCK cells within 48 hours of fi eld collection. Positive cultures were detected by cytopathic effect and by hemabsorbtion. Viral isolates were characterized by hemagglutinin and neuraminidase type by using immunofl uorescent staining (ViroStat, Portland, ME, USA and eEnzyme, Gaithersburg, MD, USA) and confi rmed to be pandemic (H1N1) 2009 by real-time PCR (13).
From May 1 through November 20, 2009, a total of 303 persons were screened. Forty-three (15%) met inclusion criteria as pandemic (H1N1) 2009 suspected case-patients and were tested with the rapid infl uenza test. Six suspected case-patients (14%) had rapid test results positive for infl uenza A, and all 6 were confi rmed to have infl uenza A pandemic (H1N1) 2009 virus. One patient had a rapid test result positive for infl uenza B. Pandemic (H1N1) 2009 cases were not related and were detected at a rate of ≈1/ month during July-November.
Median age of screened persons was 35 years (interquartile range 29-43 years), and 62% were men (Table). Median oral temperature of patients with confi rmed pandemic (H1N1) 2009 was 37.9°C (IRQ 37-38.3). Six (86%) of 7 patients with infl uenza reported a cough and 5 (71%) reported sore throat or severe joint/muscle ache. Less than 10% of screened persons not identifi ed as infl uenza suspected case-patients had these symptoms. No patients with confi rmed infl uenza reported vomiting or diarrhea.
All patients with confi rmed pandemic (H1N1) 2009 received antiviral drug treatment within 24 hours of their positive rapid infl uenza test result; no pandemic (H1N1) 2009 related deaths were reported by completion of the study. One person with a negative rapid test result who was severely ill during the survey died within days of being re-ferred to Tijuana General Hospital but was diagnosed with end-stage tuberculosis after death, not infl uenza.
Awareness was high; 88% of screened persons (n = 264/300) who answered the question about prior knowledge reported hearing about the pandemic (H1N1) 2009 epidemic in Mexico before the time of screening. More than 80% heard about the epidemic from television broadcasts. All pandemic (H1N1) 2009 suspected case-patients (n = 43) reported that they would get a pandemic (H1N1) 2009 vaccine if available; most suspected case-patients (71%) preferred to be vaccinated in a hospital.

Conclusions
Of ≈1,200 persons and their families who were contacted directly during the course of this survey, 303 selfidentifi ed as "feeling unwell" during May 1-November 20, 2009. Six persons had confi rmed pandemic (H1N1) 2009 virus, but given that the rapid infl uenza test used for screening in this study has only moderate sensitivity (14), this is likely an underestimate of cases. Confi rmed cases represented ≈0.7% of the 826 pandemic (H1N1) 2009 cases recorded in Tijuana during April-November 2009 (15), suggesting that isolation of these populations from the general population might have been protective.
All case-patients were treated with antiviral medication within 24 hours of a rapid infl uenza A positive test result, but access to antiviral drugs was through nontraditional means requiring many levels of negotiation by study staff and medical professionals in Tijuana that would not have been practical if more cases had been detected. The antiviral medication, oseltamivir, although plentiful in the United States, was only available in limited quantities in Tijuana, indicating that there are major hurdles to overcome in binational distribution of medical resources in an early pandemic setting.
Although rapid infl uenza tests are relatively insensitive, especially for pandemic (H1N1) 2009 (14), these tests can identify persons for PCR confi rmation in an effi cient and cost-effective fashion for early detection of cases. If pandemic (H1N1) 2009 were to develop more extensively in this population, changing inclusion criteria to objective fever (>100°F [37.8°C]) plus sore throat and/or cough would likely be effective for identifying pandemic (H1N1) 2009 cases with greater precision. Despite the limited health, financial resources, and unstable housing in our study population, it appears that television broadcasts were effective in distributing early messages about pandemic (H1N1) 2009. This enhanced surveillance survey, planned and executed safely and effi ciently within 4-6 weeks of the initial pandemic (H1N1) 2009 cases in Mexico, demonstrated the potential of binational academic/public health collaborations to respond to emerging health threats in Mexico/US border regions in real time.

Acknowledgments
We thank the staff of Patronato Pro-COMUSIDA for their assistance with data collection and Melanie Rusch for the production of the map.