• View in gallery

    Adult patients admitted to a cholera treatment center in Haiti, June 2012–May 2013.

  • View in gallery

    Study flow diagram of adult patients admitted to a cholera treatment center in Haiti, June 2012–May 2013.

  • 1.

    Mintz ED, Tauxe RV, 2013. Cholera in Africa: a closer look and a time for action. J Infect Dis 208 (Suppl 1): S4S7.

  • 2.

    Luquero FJ, Grout L, Ciglenecki I, Sakoba K, Traore B, Heile M, Dialo AA, Itama C, Serafini M, Legros D, Grais RF, 2013. First outbreak response using an oral cholera vaccine in Africa: vaccine coverage, acceptability and surveillance of adverse events, Guinea, 2012. PLoS Negl Trop Dis 7: e2465.

    • Search Google Scholar
    • Export Citation
  • 3.

    Djomassi LD, Gessner BD, Andze GO, Mballa GA, 2013. National surveillance data on the epidemiology of cholera in Cameroon. J Infect Dis 208 (Suppl 1): S92S97.

    • Search Google Scholar
    • Export Citation
  • 4.

    Jenson D, Szabo V, Duke FHI Haiti Humanities Laboratory Student Research Team, 2011. Cholera in Haiti and other Caribbean regions, 19th century. Emerg Infect Dis 17: 21302135.

    • Search Google Scholar
    • Export Citation
  • 5.

    Ivers LC, Walton DA, 2012. The “first” case of cholera in Haiti: lessons for global health. Am J Trop Med Hyg 86: 3638.

  • 6.

    Weil AA, Ivers LC, Harris JB, 2012. Cholera: lessons from Haiti and beyond. Curr Infect Dis Rep 14: 18.

  • 7.

    UNAIDS, 2013. September 2013 Core Epidemiology Slides: Global Summary of the AIDS Epidemic 2012. Available at: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/201309_epi_core_en.pdf. Accessed September 2015.

    • Search Google Scholar
    • Export Citation
  • 8.

    UNAIDS, 2013. Global Report: UNAIDS Report on the Global AIDS Epidemic 2013. Available at: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 9.

    Cayemittes M, Busangu MF, Bizimana JDD, Cayemittes V, Charles E, 2012. Enquête Mortalité, Morbidité et Utilisation des Services HAÏTI 2012. Available at: http://mspp.gouv.ht/site/downloads/EMMUSVdocumentfinal.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 10.

    Ministère de la Santè Publique et de la Population, 2014. Rapport Journalier du MSPP. Available at: http://mspp.gouv.ht/site/downloads/Rapport%20Web_16.03_Avec_Courbes_Departementales.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 11.

    Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, 2012. Cholera. Lancet 379: 24662476.

  • 12.

    Sack DA, Sack RB, Nair GB, Siddique A, 2004. Cholera. Lancet 363: 223233.

  • 13.

    von Seidlein L, Wang XY, Macuamule A, Mondlane C, Puri M, Hendriksen I, Deen JL, Chaignat CL, Clemens JD, Ansaruzzaman M, Barreto A, Songane FF, Lucas M, 2008. Is HIV infection associated with an increased risk for cholera? Findings from a case-control study in Mozambique. Trop Med Int Health 13: 683688.

    • Search Google Scholar
    • Export Citation
  • 14.

    Rey J, Milleliri JM, Soares JL, Boutin JP, Desfontaine M, Merouze F, Van de Perre P, 1995. HIV seropositivity and cholera in refugee children from Rwanda. AIDS 9: 12031204.

    • Search Google Scholar
    • Export Citation
  • 15.

    Utsalo SJ, Eko FO, Umoh F, Asindi AA, 1999. Faecal excretion of Vibrio cholerae during convalescence of cholera patients in Calabar, Nigeria. Eur J Epidemiol 15: 379381.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization, 2015. Cholera. Available at: http://www.who.int/mediacentre/factsheets/fs107/en/index.html. Accessed September 2015.

    • Search Google Scholar
    • Export Citation
  • 17.

    World Health Organization, 2004. First Steps for Managing an Outbreak of Acute Diarrhoea. Available at: http://www.who.int/topics/cholera/publications/en/first_steps.pdf. Accessed September 2015

    • Search Google Scholar
    • Export Citation
  • 18.

    Baron EJ, Miller JM, Weinstein MP, Richter SS, Gilligan PH, Thomson RB Jr, Bourbeau P, Carroll KC, Kehl SC, Dunne WM, Robinson-Dunn B, Schwartzman JD, Chapin KC, Snyder JW, Forbes BA, Patel R, Rosenblatt JE, Pritt BS, 2013. A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2013 recommendations by the Infectious Diseases Society of America (IDSA) and the American Society for Microbiology (ASM). Clin Infect Dis 57: e22e121.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mushayabasa S, Bhunu CP, 2012. Is HIV infection associated with an increased risk for cholera? Insights from a mathematical model. Biosystems 109: 203213.

    • Search Google Scholar
    • Export Citation
  • 20.

    Valcin CL, Severe K, Riche CT, Anglade BS, Moise CG, Woodworth M, Charles M, Li Z, Joseph P, Pape JW, Wright PF, 2013. Predictors of disease severity in patients admitted to a cholera treatment center in urban Haiti. Am J Trop Med Hyg 89: 625632.

    • Search Google Scholar
    • Export Citation
  • 21.

    Charles M, Delva GG, Boutin J, Severe K, Peck M, Mabou MM, Wright PF, Pape JW, 2014. Importance of cholera and other etiologies of acute diarrhea in post-earthquake Port-au-Prince, Haiti. Am J Trop Med Hyg 90: 511517.

    • Search Google Scholar
    • Export Citation
  • 22.

    Mehandru S, Poles MA, Tenner-Racz K, Horotwitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M, 2004. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200: 761770.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Clinical Features of Human Immunodeficiency Virus–Infected Patients Presenting with Cholera in Port-au-Prince, Haiti

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  • 1 Groupe Haïtien Etude pour le Sarcome de Kaposi et les Infections Opportunistes (GHESKIO), Port-au-Prince, Haiti.
  • 2 Center for Global Health, Weill Cornell Medical College, New York, New York.

Human immunodeficiency virus (HIV) infection has been postulated to alter the natural history of cholera, including increased susceptibility to infection, severity of illness, and chronic carriage of Vibrio cholerae. Haiti has a generalized HIV epidemic with an adult HIV prevalence of 1.9% and recently suffered a cholera epidemic. We conducted a prospective study at the cholera treatment center (CTC) of GHESKIO in Haiti to characterize the coinfection. Adults admitted at the CTC for acute diarrhea were invited to participate in the study. Vital signs, frequency, and volume of stools and/or vomiting were monitored, and single-dose doxycycline was administered. After counseling, participants were screened for HIV by enzyme-linked immunosorbent assay and for cholera by culture. Of 729 adults admitted to the CTC, 99 (13.6%) had HIV infection, and 457 (63%) had culture-confirmed cholera. HIV prevalence was three times higher in patients without cholera (23%, 63/272) than in those with culture-confirmed cholera (7.9%, 36/457). HIV prevalence in patients with culture-confirmed cholera (7.9%) was four times higher than the adult prevalence in Port-au-Prince (1.9%). Of the 36 HIV-infected patients with cholera, 25 (69%) had moderate/severe dehydration versus 302/421 (72%) in the HIV negative. Of 30 HIV-infected patients with weekly stool cultures performed after discharge, 29 (97%) were negative at week 1. Of 50 HIV-negative patients with weekly stool cultures, 49 (98%) were negative at week 1. In countries with endemic HIV infection, clinicians should consider screening patients presenting with suspected cholera for HIV coinfection.

Introduction

With recent cholera outbreaks in the Caribbean and sub-Saharan Africa, there is now significant geographic overlap of the human immunodeficiency virus (HIV)–1 and Vibrio cholerae epidemics. Cholera is a waterborne disease caused by V. cholerae that spread across the world from its original reservoir in the Ganges delta in India. More than 20 countries in Africa have reported cholera, with recent outbreaks reported in Cameroon, Democratic Republic of Congo, Ghana, Guinea, Niger, Sierra Leone, and Uganda.13 Cholera has also been reported in countries in South America and the Caribbean including Bolivia, Brazil, Ecuador, Guatemala, Nicaragua, and Peru.46 Most recently, the disease emerged in Haiti, the country with the highest rates of HIV-1 infection in the Western Hemisphere.79 The cholera outbreak in Haiti has been one of the largest in recent history with 745,588 cases reported to date.10

The natural history of cholera varies depending upon bacterial strain, inoculum, host genetics, and immune status.11 Most people infected with V. cholerae develop no symptoms or only mild disease, whereas 10–30% develop profuse diarrhea, rice-watery stools, nausea, and vomiting.12 The severe form is cholera gravis which can lead to shock and death in majority of cases without effective care. Appropriate treatment consists of rehydration by oral or intravenous fluids and antibiotics.

The effect of HIV-1 infection upon the natural history of cholera is not certain. A small study in Mozambique suggested that people with HIV-1 infection may be at higher risk of developing symptomatic cholera than HIV-uninfected people.13 A case series in a Rwandan orphanage suggested that HIV-1-infected children were more likely to develop severe cholera than uninfected children.14 Other case reports suggest that HIV-infected individuals may have longer duration of excretion of V. cholerae, with the pathogen detected in stools 6 months after initial diarrheal illness.15 Large-scale studies have not been conducted because cholera epidemics occur sporadically and unpredictably, and it is difficult to conduct research in the context of an emergency response.

Given the increasing geographic overlap between HIV-1 and cholera epidemics and the limited data on the effects of HIV-1 upon the natural history of cholera, we conducted a study in Haiti to characterize the coinfection. Our objectives were to determine the prevalence of HIV-1 in adult patients presenting with symptomatic cholera and to examine differences in disease severity and duration of excretion of V. cholerae between HIV-1 infected versus uninfected.

Methods

The study was approved by the institutional review boards of Weill Cornell Medical College and the GHESKIO Center. All participants provided written informed consent.

Study site.

The study was conducted at the GHESKIO Center in central Port-au-Prince, Haiti. GHESKIO is a clinical and research institution dedicated to service, research, and training in infectious diseases. It is located in downtown Port-au-Prince adjacent to large, densely populated slums with poor water supply and sanitation. Since the cholera epidemic began in 2010, GHESKIO has participated in the emergency response including provision of clean water, prevention programs in slums, and emergency care at an inpatient cholera treatment center (CTC) on its downtown campus.

Patients with acute diarrhea come to the GHESKIO CTC on their own, are brought by family, are referred by primary care clinics, or are transported to the CTC by ambulance. Patients are immediately evaluated, and medical staff determines the degree of dehydration (mild, moderate, or severe) based upon World Health Organization (WHO) guidelines.16 Patients with mild dehydration are provided oral rehydration fluids, observed for several hours, and admitted if symptoms worsen. Patients with moderate or severe dehydration are admitted immediately to the CTC for rehydration. At admission, sociodemographic information and medical history are routinely collected including age, gender, address, education, economic status, duration of diarrhea, antibiotic use, and other drugs taken before admission.

During hospitalization, patients who can take oral fluids are rehydrated with oral rehydration fluids (glucose, sodium, bicarbonate and potassium with osmolarity: 245 m osm/L). Other patients are provided intravenous fluids (Lactated Ringer's solution or when indicated normal saline or dextrose normal saline solutions). Vital signs and the frequency and volume of stools are monitored by medical staff to guide the volume of fluid resuscitation. An admission stool specimen is collected before administration of antibiotics, stored in a refrigerator at 4°C, and is available for microbiological examination. Serum electrolytes are monitored as per clinician's judgment (VITROS; Ortho Clinical Diagnostics, Raritan, NJ) and replacement electrolytes are provided as needed.16 Other laboratory tests are performed when clinically indicated. All patients are given doxycycline 300 mg as a single oral dose as per WHO recommendations.17

Study recruitment and procedures.

Patients 18 years or older, living in the Port-au-Prince metropolitan area, and admitted with diarrhea to the GHESKIO CTC were eligible to participate in the current study. Approximately 12–24 hours after admission and emergency rehydration, a study nurse explained the study and procedures to potential participants and obtained written informed consent.

All study participants had an HIV test. Pretest and posttest counseling were provided, and at discharge, all HIV-1-infected participants were referred for outpatient HIV-1 care to the GHESKIO HIV unit located on the same campus. Data from the participant's medical chart was abstracted for research purposes including demographic information, disease severity, and fluid intake and output. A subset of participants with positive stool cultures for V. cholerae was invited to participate in a longitudinal study to determine the length of V. cholerae excretion. At discharge, 30 HIV-infected individuals with a positive stool culture and 50 HIV-uninfected people with a positive stool culture were followed up weekly. Both groups received sterile containers and were asked to return to GHESKIO with a stool specimen weekly. Counseling was provided to the participants on collection procedures following the recommendations of the American Society for Microbiology.18 We performed weekly study visits and stool culture until two consecutive negative cultures were obtained.

Laboratory procedures.

Serum samples were tested for HIV-1 antibodies by the Determine HIV1/2 assay (Abbott, Abbott Park, IL) and confirmed by HIV (1 + 2) Antibody (Shanghai Kehua Bioengineering Co. Ltd., Shanghai, China).

Stool specimens were inoculated in alkaline peptone water and plated on thiosulfate citrate bile sucrose for identification of V. cholerae. Suspicious colonies were selected for further identification on MacConkey or blood agar.18

Data analysis.

Data were entered into an ACCESS database (Microsoft, Redmond, WA). We determined the prevalence of HIV infection in all adult patients who presented with watery diarrhea. We compared clinical characteristics of patients with and without HIV. For comparison of proportions, we used Fisher's exact test. For comparison of means and medians, we used Student's t test and Wilcoxon rank-sum test, respectively. Excretion duration was measured in HIV-positive and HIV-negative patients and compared using the log rank test. All statistical tests were two sided with a P value of 0.05 for significance.

Results

Study enrollment.

In the 1-year period from June 1, 2012, to May 31, 2013, 888 patients of age ≥ 18 years from Port-au-Prince were admitted to the GHESKIO CTC with acute diarrhea. There was a peak in hospitalizations in November 2012 with 156 cases admitted; this corresponded to the rainy season (Figure 1).

Figure 1.
Figure 1.

Adult patients admitted to a cholera treatment center in Haiti, June 2012–May 2013.

Citation: The American Society of Tropical Medicine and Hygiene 95, 5; 10.4269/ajtmh.16-0105

Of the 888 adult patients, 72 (8%) did not consent to participate in the current study, 65 (7%) did not want HIV testing, 22 (2%) were discharged home before study enrollment, and 729 (83%) were enrolled in the current study (Figure 2). Of the 729 participants, 99 (13.6%) tested HIV seropositive. Of the 99 HIV-infected patients, 63 (64%) did not know their HIV status upon admission; the diagnosis of HIV infection was new. CD4+ T-cell counts were obtained for 72 HIV-infected patients. The median CD4 T-cell count was 222 (interquartile range = 79–530). Forty-nine of 72 (68%) had a CD4 count < 500 cells, and were eligible for antiretroviral therapy initiation under WHO guidelines at the time of the study.

Figure 2.
Figure 2.

Study flow diagram of adult patients admitted to a cholera treatment center in Haiti, June 2012–May 2013.

Citation: The American Society of Tropical Medicine and Hygiene 95, 5; 10.4269/ajtmh.16-0105

The characteristics of the 729 study participants, stratified by HIV status, are provided in Table 1. HIV-infected patients were older with a median age of 36 years versus 31 years for the HIV uninfected. HIV-infected patients also had a significantly lower educational and economic status than the HIV-uninfected patients.

Table 1

Characteristics of patients admitted to a cholera treatment center in Haiti

 HIV+N = 99HIVN = 630Total N = 729
Age**
 Median age363132
 Age range18–7018–8718–87
Gender
 Male50 (50.5%)329 (52.2%)379 (51.9%)
 Female49 (49.5%)301 (47.8%)350 (48.1%)
Education*
 None17 (17.2%)87 (13.8%)104 (14.3%)
 Primary school33 (33.3%)159 (25.2%)192 (26.3%)
 Secondary school47 (47.5%)357 (56.7%)404 (55.4%)
 Other1 (1.0%)16 (2.5%)17 (2.3%)
 Unavailable1 (1.0%)11 (1.7%)12 (1.6%)
Economy*
 None47 (47.5%)269 (42.7%)316 (43.4%)
 1.55–110 USD32 (32.3%)163 (25.9%)195 (26.7%)
 111–440 USD18 (18.1%)179 (28.4%)197 (27.0%)
 ≥ 441 USD1 (1.0%)8 (1.3%)9 (1.2)
 Unavailable1 (1.0%)11 (1.7%)12 (1.6%)
Stool cholera culture*** (positive)36 (36.4%)421 (66.8%)457 (62.7%)

HIV = human immunodeficiency virus. The P value comparing HIV+ vs. HIV are indicated by asterisks (*).

* P < 0.05; ** P < 0.01; *** P < 0.001.

Clinical characteristics during hospitalization.

In total, 457 (63%) of the 729 participants had a positive stool culture for V. cholerae. Of the 272 subjects without cholera, 63 (23%) were HIV infected. Of the 457 culture-confirmed cholera cases, 36 (7.9%) were HIV infected, (95% confidence interval = 5.6–10.7%). This is four times higher than the 1.9% estimated adult HIV seroprevalence in Port-au-Prince.

Demographic and clinical characteristics of the 36 HIV-infected patients with culture-confirmed cholera and the 421 HIV-negative patients with culture-confirmed cholera are presented in Table 2. The HIV-infected patients had similar disease severity as HIV-uninfected patients upon admission. There was no significant difference in length of hospital stay or stool output. Only one patient died. One HIV-infected patient with cholera died 1 week after discharge.

Table 2

Clinical characteristics of patients admitted to a cholera treatment center in Haiti and with positive Vibrio cholerae cultures

 HIV+N = 36HIVN = 421P value
Age (years)  0.8291
 Mean ± SD35.23 ± 8.9734.74 ± 13.1 
 Median3531.5 
 Interquartile range28–4024–43 
Sex  0.9911
 Male20 (56%)228 (54%) 
 Female16 (44%)193 (46%) 
Clinical severity on admission  0.9926
 Light11 (31%)119 (28%) 
 Moderate21 (58%)255 (61%) 
 Severe4 (11%)47 (11%) 
Systolic BP on admission  0.0971
 Too weak to measure7 (19%)38 (9%) 
 < 905 (14%)89 (21%) 
 90–12023 (64%)283 (67%) 
 > 1201 (3%)11 (3%) 
Hospitalization duration (hours)  0.2327
 Mean ± SD65 ± 3773 ± 39 
 Median5569 
 Interquartile range43–9049–91 
Total stool output (mL)  0.2192
 Mean ± SD14,123 ± 14,65217,288 ± 14,596 
 Median9,90013,400 
 Interquartile range5,900–17,5006,200–23,300 
Rate of stool output (mL/hour)  0.613
 Mean ± SD206 ± 113218 ± 139 
 Median166198 
 Interquartile range131–249125–268 

BP = blood pressure; HIV = human immunodeficiency virus; SD = standard deviation.

Longitudinal follow-up.

A total of 80 patients with culture-confirmed cholera were followed weekly to determine the length of V. cholerae excretion. This included 50 HIV-uninfected patients and 30 HIV-infected patients. Of note, all participants had received a single oral dose of doxycycline before discharge from the hospital as per WHO recommendation. There was no significant difference in the length of excretion of V. cholerae between the HIV infected versus uninfected. In 49 of 50 HIV-uninfected patients, all follow-up stool cultures were negative. One HIV-uninfected patient had a negative culture at week 1, a positive culture at week 2, and then all negative cultures. In 29 of 30 HIV-infected patients, all follow-up stool cultures were negative. One HIV-infected patient had a positive stool culture at week 1; the next two weekly cultures were found negative.

Discussion

This study demonstrates that a high percentage of patients presenting to a CTC in Haiti were HIV infected. In our study, ∼13% of the adults presenting with acute watery diarrhea were HIV infected; the prevalence of HIV in the general population is only 1.9%. Therefore, we recommend that in countries with endemic HIV, clinicians should consider screening patients presenting with acute diarrhea to a CTC for HIV infection.

Our findings of an association between cholera and HIV are supported by prior studies. A case-control study in 2008 in Mozambique suggested that HIV patients might be more at risk to present with cholera than in the general population.13 In a mathematical modeling study examining the correlation of HIV and cholera, Mushayabasa and others also suggested that cholera appears to be more frequent in HIV-endemic areas than areas without HIV.19 In our prospective study, even among patients with culture-documented V. cholerae, we found that the HIV prevalence (8%) was significantly higher than in the general population (2%).20,21

Furthermore, many HIV-infected patients with diarrhea but without cholera sought care at our CTC. This would suggest that HIV-infected patients with acquired immunodeficiency syndrome diarrhea may seek care at CTCs. We also found that two-thirds of the HIV-infected patients were newly diagnosed with a CD4 T-cell count that satisfied guidelines to start antiretroviral therapy. This provides a unique opportunity to diagnose HIV and initiate antiretroviral therapy.

There are several possible explanations for the high rate of HIV among cholera patients. Both cholera and HIV are diseases of poverty and those at risk for one may be at risk for the other. HIV-infected patients may be more accustomed to seeking medical care and therefore more likely to seek care when they develop symptomatic diarrhea. Alternatively, HIV-infected patients may be more likely to develop symptomatic disease when exposed to V. cholerae. HIV preferentially infects gut-associated lymphoid tissue and impairs gastrointestinal mucosal immunity.22 This decreased mucosal immunity may render HIV-infected hosts more susceptible to V. cholerae. However, future studies to explore a causal relationship between HIV and symptomatic cholera are warranted.

Our study also compared the clinical features of cholera between patients with and without HIV infection. HIV-infected individuals seem to have the same level of severity of illness on presentation. Our findings also demonstrate that HIV-infected patients receiving doxycycline as recommended by WHO did not have longer duration of excretion than expected in the general population. Case studies have suggested that HIV-1-infected patients may be at higher risk of chronic carriage.15 Our study demonstrated that a single dose of doxycycline is effective at preventing chronic carriage.

One limitation of our study is that children were not evaluated. A study conducted in Rwanda demonstrated that HIV-infected children are also more likely to acquire cholera than HIV-uninfected patients.14 Further research is needed to explore the correlation in children. The study also did not measure host mucosal immunity to V. cholerae; further research is needed.

Recommendations.

In endemic HIV countries, clinicians should consider screening patients presenting with acute diarrhea for HIV infection. Education should be reinforced among HIV-infected patients to prevent other causes of diarrhea related to waterborne disease, especially during the rainy season when water supplies may be contaminated. HIV-infected patients in endemic countries may also benefit from cholera vaccination.

  • 1.

    Mintz ED, Tauxe RV, 2013. Cholera in Africa: a closer look and a time for action. J Infect Dis 208 (Suppl 1): S4S7.

  • 2.

    Luquero FJ, Grout L, Ciglenecki I, Sakoba K, Traore B, Heile M, Dialo AA, Itama C, Serafini M, Legros D, Grais RF, 2013. First outbreak response using an oral cholera vaccine in Africa: vaccine coverage, acceptability and surveillance of adverse events, Guinea, 2012. PLoS Negl Trop Dis 7: e2465.

    • Search Google Scholar
    • Export Citation
  • 3.

    Djomassi LD, Gessner BD, Andze GO, Mballa GA, 2013. National surveillance data on the epidemiology of cholera in Cameroon. J Infect Dis 208 (Suppl 1): S92S97.

    • Search Google Scholar
    • Export Citation
  • 4.

    Jenson D, Szabo V, Duke FHI Haiti Humanities Laboratory Student Research Team, 2011. Cholera in Haiti and other Caribbean regions, 19th century. Emerg Infect Dis 17: 21302135.

    • Search Google Scholar
    • Export Citation
  • 5.

    Ivers LC, Walton DA, 2012. The “first” case of cholera in Haiti: lessons for global health. Am J Trop Med Hyg 86: 3638.

  • 6.

    Weil AA, Ivers LC, Harris JB, 2012. Cholera: lessons from Haiti and beyond. Curr Infect Dis Rep 14: 18.

  • 7.

    UNAIDS, 2013. September 2013 Core Epidemiology Slides: Global Summary of the AIDS Epidemic 2012. Available at: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/201309_epi_core_en.pdf. Accessed September 2015.

    • Search Google Scholar
    • Export Citation
  • 8.

    UNAIDS, 2013. Global Report: UNAIDS Report on the Global AIDS Epidemic 2013. Available at: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 9.

    Cayemittes M, Busangu MF, Bizimana JDD, Cayemittes V, Charles E, 2012. Enquête Mortalité, Morbidité et Utilisation des Services HAÏTI 2012. Available at: http://mspp.gouv.ht/site/downloads/EMMUSVdocumentfinal.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 10.

    Ministère de la Santè Publique et de la Population, 2014. Rapport Journalier du MSPP. Available at: http://mspp.gouv.ht/site/downloads/Rapport%20Web_16.03_Avec_Courbes_Departementales.pdf. Accessed November 2015.

    • Search Google Scholar
    • Export Citation
  • 11.

    Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, 2012. Cholera. Lancet 379: 24662476.

  • 12.

    Sack DA, Sack RB, Nair GB, Siddique A, 2004. Cholera. Lancet 363: 223233.

  • 13.

    von Seidlein L, Wang XY, Macuamule A, Mondlane C, Puri M, Hendriksen I, Deen JL, Chaignat CL, Clemens JD, Ansaruzzaman M, Barreto A, Songane FF, Lucas M, 2008. Is HIV infection associated with an increased risk for cholera? Findings from a case-control study in Mozambique. Trop Med Int Health 13: 683688.

    • Search Google Scholar
    • Export Citation
  • 14.

    Rey J, Milleliri JM, Soares JL, Boutin JP, Desfontaine M, Merouze F, Van de Perre P, 1995. HIV seropositivity and cholera in refugee children from Rwanda. AIDS 9: 12031204.

    • Search Google Scholar
    • Export Citation
  • 15.

    Utsalo SJ, Eko FO, Umoh F, Asindi AA, 1999. Faecal excretion of Vibrio cholerae during convalescence of cholera patients in Calabar, Nigeria. Eur J Epidemiol 15: 379381.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization, 2015. Cholera. Available at: http://www.who.int/mediacentre/factsheets/fs107/en/index.html. Accessed September 2015.

    • Search Google Scholar
    • Export Citation
  • 17.

    World Health Organization, 2004. First Steps for Managing an Outbreak of Acute Diarrhoea. Available at: http://www.who.int/topics/cholera/publications/en/first_steps.pdf. Accessed September 2015

    • Search Google Scholar
    • Export Citation
  • 18.

    Baron EJ, Miller JM, Weinstein MP, Richter SS, Gilligan PH, Thomson RB Jr, Bourbeau P, Carroll KC, Kehl SC, Dunne WM, Robinson-Dunn B, Schwartzman JD, Chapin KC, Snyder JW, Forbes BA, Patel R, Rosenblatt JE, Pritt BS, 2013. A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2013 recommendations by the Infectious Diseases Society of America (IDSA) and the American Society for Microbiology (ASM). Clin Infect Dis 57: e22e121.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mushayabasa S, Bhunu CP, 2012. Is HIV infection associated with an increased risk for cholera? Insights from a mathematical model. Biosystems 109: 203213.

    • Search Google Scholar
    • Export Citation
  • 20.

    Valcin CL, Severe K, Riche CT, Anglade BS, Moise CG, Woodworth M, Charles M, Li Z, Joseph P, Pape JW, Wright PF, 2013. Predictors of disease severity in patients admitted to a cholera treatment center in urban Haiti. Am J Trop Med Hyg 89: 625632.

    • Search Google Scholar
    • Export Citation
  • 21.

    Charles M, Delva GG, Boutin J, Severe K, Peck M, Mabou MM, Wright PF, Pape JW, 2014. Importance of cholera and other etiologies of acute diarrhea in post-earthquake Port-au-Prince, Haiti. Am J Trop Med Hyg 90: 511517.

    • Search Google Scholar
    • Export Citation
  • 22.

    Mehandru S, Poles MA, Tenner-Racz K, Horotwitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M, 2004. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200: 761770.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Grace Seo, Center for Global Health, Weill Cornell Medical College, 402 East 67th Street, 2nd Floor, New York, NY 10065. E-mail: grs2013@med.cornell.edu

Authors' addresses: Karine Sévère, Stravinsky B. Anglade, Claudin Bertil, and Alexandra Deroncenay, Infectious Diseases, Les Centres GHESKIO, Port-au-Prince, Haiti, E-mails: karinesevere@gheskio.org, sanglade@gheskio.org, claudinbertil@gmail.com, and aderoncenay@gmail.com. Aynsley Duncan, Oksana Ocheretina, Lindsey Reif, Grace Seo, Jean W. Pape, and Daniel W. Fitzgerald, Center for Global Health, Joan and Sanford I Weill Medical College of Cornell University, New York, NY, E-mails: ayd2001@med.cornell.edu, oko2001@med.cornell.edu, lir2020@med.cornell.edu, grs2013@med.cornell.edu, jwpape@gheskio.org, and dwf2001@med.cornell.edu. Patrice Joseph and Marie M. Mabou, Les Centres GHESKIO, Port-au-Prince, Haiti, E-mails: pjoseph@gheskio.org and mmabou@gheskio.org.

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