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Environmental factors as key determinants for visceral leishmaniasis in solid organ transplant recipients, Madrid, Spain.

Visceral leishmaniasis (VL) is an uncommon but potentially fatal complication for solid organ transplant (SOT) recipients (1,2). Beginning in July 2009, an outbreak of leishmaniasis affected the southwest area of Madrid (3). The outbreak was primarily located in Fuenlabrada, which has an annual VL incidence of 21.1 cases/100,000 population (4), notably higher than that estimated for the general population in Spain (0.5 cases/ 100,000 population) (5).

Spatial analysis revealed that the highest concentration of cases was in the residential area bordering the park (Bosque Sur) (6). A large population of Lepus granatensis hares, which serve as a reservoir for Leishmania infantum, was present in the area (7,8), and the Phlebotomus perniciosus sand fly in Spain can act as a vector and take blood meals from these hares (6,8,9). Thus, the parkland facilitated the transmission of the leishmaniasis pathogen, which led to the outbreak. This large, urban outbreak provided us the opportunity to analyze the incidence and specific risk factors of VL among SOT recipients.

The Study

The University Hospital 12 de Octubre in Madrid, Spain, acts as the reference hospital for SOT in South Madrid. We performed a retrospective study of all consecutive adult patients who underwent kidney, liver, or heart transplantation during January 1, 2005-January 1, 2013, and lived in the outbreak area. Patients who underwent SOT before January 1, 2005, were excluded because of the difficulty of ensuing long-term follow-up and the potential of heterogeneity in posttransplant practices. Patients who died or had moved to a different place of residence before outbreak onset were excluded (online Technical Appendix Figure 1, https://wwwnc.cdc.gov/EID/ article/23/7/15-1251-Techapp1.pdf).

The primary study outcome was the occurrence of VL, the diagnosis of which required confirmation of parasitemia (online Technical Appendix) (10). We recorded pretransplant, peritransplant and posttransplant variables and collected various environmental factors prospectively by unblinded, direct interview with the patients. Patients were considered to have frequent contact with dogs if patients reported having dogs at home or taking care of dogs and to have the habit of visiting the park if they reported visiting once a year. The distance between the place of residence and the park was obtained by locating the patient's home address and measuring the shortest linear distance to the nearest border of the parkland by means of an online mapping tool (Google Maps; Google Inc., Mountain View, CA, USA).

The beginning of the exposure period was set as July 2009 (outbreak onset) for patients who underwent SOT before the outbreak and as the transplant date for those who underwent SOT after outbreak onset. In both cases, the exposure period extended to the date of diagnosis of VL, death, or December 2013. We chose to end the study in December 2013 because the incidence of leishmaniasis decreased thereafter because of the implementation of control measures. The clinical research ethics committee of the University Hospital 12 de Octubre approved the study, and participants provided informed consent.

We analyzed 68 patients (Table 1) for a median follow-up of 4.4 (interquartile range 2.39-6.95) years. VL was diagnosed in 7 patients, yielding a cumulative incidence of 10.3% (95% CI 3.1%-17.5%) and an annual incidence of 2,997 (95% CI 1,213-6,161) cases per 100,000 population. Details on disease pathology and therapy were recorded (Table 2). The mean interval between transplant and diagnosis was 1.34 [+ or -] 0.89 years. No patients had visited highly VL-endemic countries.

Black sub-Saharan African SOT recipients were more likely than other recipients to become affected by VL (relative risk 6.40, 95% CI 1.76-23.29, p = 0.049) (Table 1). All 7 episodes of VL occurred in patients who underwent transplantation during the outbreak period (Figure 1).

The median distance between the place of residence and the park was significantly shorter for recipients with VL (399 m) than for those without (1,370 m; p = 0.001) (Figure 2; online Technical Appendix Figure 2). We explored the predictive accuracy of this variable by establishing the optimal cutoff value with the area under the receiving operating characteristic curve analysis. Recipients living <1,000 m from the park (26.1%, 6/23) had a higher incidence of VL than recipients living [greater than or equal to] 1,000 m away (2.2%, 1/45; relative risk, 11.74, 95% CI 1.50-91.78; p = 0.005). At 4 years, a lower percentage of the SOT recipients living <1,000 m from the park were free from VL than those living [greater than or equal to] 1,000 m away (61.0% vs 98%; p = 0.001 by log-rank test) (online Technical Appendix Figure 3).

Our study suggests that the incidence of VL in SOT recipients is notably higher than that in the general population (11). Acquisition of the parasite most likely occurred posttransplant because all but 1 recipient affected with VL (from whom serum samples could be recovered) were seronegative for Leishmania spp. before transplantation.

Our findings suggest that environmental factors might be crucial in modulating the incidence of VL in immunocompromised hosts, such as SOT recipients; the distance from the patient's residence to the focus of the outbreak (6,7) emerged as a key risk factor. The median distance between the park and the homes of recipients with posttransplant VL was <500 m; the maximum flight distance of female sand flies is 600 m (12,13). Therefore, persons living within this radius had a higher chance of being bitten by the VL vector. A similar association was described for the general population during this outbreak (6).

Undergoing transplantation during the outbreak period was another risk factor for VL. This finding suggests that, in the case of an outbreak in a country with low baseline incidence, pretransplant screening of patients listed for SOT for VL-specific antibodies should be considered and repeated during the posttransplant period for the prompt detection of de novo infection. Recipients should also receive specific counseling to reduce the risk of being bitten by sand flies. In addition, treating physicians must maintain a low threshold of suspicion for VL for persons on immunosuppressive therapy during a VL outbreak.

We found that 28% of posttransplant VL cases occurred in black recipients born in sub-Saharan Africa, even though this subgroup only represented 2.4% of the overall population in the affected area (14). An association between sub-Saharan African ethnicity and VL has also been reported in the general population (4). No apparent relationship was found between the race of the patient and the frequency of parkland visits. Both black recipients in question came from Equatorial Guinea, a country not considered endemic for leishmaniasis by the World Health Organization (15). Therefore, the potential association between genetic susceptibility and posttransplant VL warrants further investigation.

Limitations of this study include the small sample size and that interviewers were not blinded to the diagnosis of VL. However, the objective nature of the questionnaire minimized the potential risk for bias. When assessing degree of exposure to sand flies, we used only indirect variables (i.e., distance between the patient's residence and park, habit of visiting the park) as surrogate measures. Regarding the distance from the park, only linear distances were assessed without considering the potential presence of physical obstacles in the sand fly flight trajectory. Because of these limitations, our findings must be interpreted with caution.

Conclusions

Our study indicates several risk factors (being black and from sub-Saharan Africa, having an SOT during the outbreak, and living <1,000 m from the outbreak focus) useful for helping physicians treat SOT recipients during a VL outbreak. Doctors should select the patients with these risk factors for counseling to minimize their exposure to vectors and active monitoring for prompt diagnosis.

Acknowledgment

We thank Emiliano Aranguez Ruiz for his kind help providing the map included in this paper.

This study was co-funded by the World Health Organization (APW-2012/271093-O), the Spanish Ministry of Economy and Competitiveness, Instituto de Salud Carlos III (Proyecto Integrado de Excelencia 13/00045), and the European Regional Development Fund. M.F.R. holds a clinical research contract Juan Rodes (JR14/00036) from the Spanish Ministry of Economy and Competitiveness, Instituto de Salud Carlos III.

Dr. Carrasco-Anton is a specialist in internal medicine currently working at the Fundacion Jimenez Diaz in Madrid, Spain. Her research interests are leishmaniasis and other infections in immunocompromised hosts.

References

(1.) Clemente W, Vidal E, Girao E, Ramos AS, Govedic F, Merino E, et al. Risk factors, clinical features and outcomes of visceral leishmaniasis in solid-organ transplant recipients: a retrospective multicenter case-control study. Clin Microbiol Infect. 2015;21:89-95. http://dx.doi.org/10.1016/j.cmi.2014.09.002

(2.) Alves da Silva A, Pacheco-Silva A, de Castro Cintra Sesso R, Esmeraldo RM, Costa de Oliveira CM, Fernandes PF, et al. The risk factors for and effects of visceral leishmaniasis in graft and renal transplant recipients. Transplantation. 2013;95:721-7. http://dx.doi.org/10.1097/TP.0b013e31827c16e2

(3.) Gomez-Barroso D, Herrador Z, San Martin JV, Gherasim A, Aguado M, Romero-Mate A, et al. Spatial distribution and cluster analysis of a leishmaniasis outbreak in the south-western Madrid region, Spain, September 2009 to April 2013. Euro Surveill. 2015;20:pii=21037. http://dx.doi.org/10.2807/1560-7917. ES2015.20.7.21037

(4.) Horrillo L, San Martin JV, Molina L, Madronal E, Matia B, Castro A, et al. Atypical presentation in adults in the largest community outbreak of leishmaniasis in Europe (Fuenlabrada, Spain). Clin Microbiol Infect. 2015;21:269-73. http://dx.doi.org/ 10.1016/j.cmi.2014.10.017

(5.) Herrador Z, Gherasim A, Jimenez BC, Granados M, San Martin JV, Aparicio P. Epidemiological changes in leishmaniasis in Spain according to hospitalization-based records, 1997-2011: raising awareness towards leishmaniasis in non-HIV patients. PLoS Negl Trop Dis. 2015;9:e0003594. http://dx.doi.org/10.1371/journal.pntd.0003594

(6.) Aranguez Ruiz E, Arce Arnaez A, Moratilla Monzo L, Estirado Gomez A, Iriso Calle A, De la Fuente Urena S, et al. Spatial analysis of an outbreak of leishmaniasis in the south of Madrid's metropolitan area. 2009-2013 [in Spanish]. Rev Salud Ambient. 2014;14:39-53.

(7.) Molina R, Jimenez MI, Cruz I, Iriso A, Martin-Martin I, Sevillano O, et al. The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain. Vet Parasitol. 2012;190:268-71. http://dx.doi.org/10.1016/ j.vetpar.2012.05.006

(8.) Jimenez M, Gonzalez E, Iriso A, Marco E, Alegret A, Fuster F, et al. Detection of Leishmania infantum and identification of blood meals in Phlebotomus perniciosus from a focus of human leishmaniasis in Madrid, Spain. Parasitol Res. 2013;112:2453-9. http://dx.doi.org/10.1007/s00436-013-3406-3

(9.) Suarez Rodriguez B, Isidoro Fernandez B, Santos Sanz S, Sierra Moros MJ, Molina Moreno R, Astray Mochales J, et al. Review of the current situation and the risk factors of Leishmania infantum in Spain [in Spanish]. Rev Esp Salud Publica. 2012;86:555-64.

(10.) World Health Organization. Control of the leishmaniases. Report of a meeting of the WHO Expert Committee on the Control of Leishmaniases, Geneva, 22-16 March 2010. Geneva: WHO Press; 2010.

(11.) Arce A, Estirado A, Ordobas M, Sevilla S, Garcia N, Moratilla L, et al. Re-emergence of leishmaniasis in Spain: community outbreak in Madrid, Spain, 2009 to 2012. Euro Surveill. 2013;18:20546. http://dx.doi.org/10.2807/1560-7917. ES2013.18.30.20546

(12.) Dergacheva TI, Strelkova MV, Lapin VA, Karulin BE, Chabovskii AV The use of radioisotope labelling for studying the feeding of sandflies (Phlebotominae) and their move into colonies of the greater gerbil (Rhombomys opimus Licht.) [Russian]. Med Parazitol (Mosk). 1996;3:11-4.

(13.) Kamhawi S, Abdel-Hafez SK, Molyneux DH. The behaviour and dispersal of sandflies in Ras el Naqb, South Jordan with particular emphasis on Phlebotomus kazeruni. Parassitologia. 1991;33(Suppl):307-14.

(14.) City Council of Fuenlabrada. Population in Fuenlabrada, by sex and country of origin [Spanish]. 2016 Jan 5 [cited 2016 Mar 23]. http://ayto-fuenlabrada.es/index.do?MP=3&MS=27&MN=2&TR= A&IDR=1&iddocumento=17132

(15.) World Health Organization. Global Health Observatory data repository. Leishmaniasis [cited 2016 March 23]. http://apps.who. int/gho/data/node.main.NTDLEISH?lang=en

Address for correspondence: Nerea Carrasco-Anton, Unit of Infectious Diseases, Hospital Universitario 12 de Octubre, Centro de Actividades Ambulatorias, 2nd Fl, Section D, Avda de Cordoba, s/n, Postal Code 28041, Madrid, Spain; email: nereacarrascoanton@gmail.com

Author affiliations: University Hospital 12 de Octubre of Complutense University of Madrid, Madrid, Spain (N. Carrasco-Anton, F. Lopez-Medrano, M. Fernandez-Ruiz, A. Garcia-Reyne, A. Perez-Ayala, C. Lumbreras, R. San-Juan, J.M. Aguado); Instituto de Salud Carlos III, Madrid (E. Carrillo, J. Moreno); Hospital General Universitario Gregorio Maranon, Madrid (M.L. Rodriguez-Ferrero); Drugs for Neglected Diseases Initiative, Geneva, Switzerland (J. Alvar)

DOI: https://dx.doi.org/10.3201/eid2307.151251

Caption: Figure 1. Distribution of VL among solid organ transplant recipients, Madrid, Spain, January 1,2005-January 1,2013. Columns represent the number of solid organ transplant procedures performed each year at the University Hospital 12 de Octubre among patients permanently residing in Fuenlabrada, the nearby city affected by the outbreak. Gray shading indicates outbreak period. SOT, solid organ transplant; VL, visceral leishmaniasis.

Caption: Figure 2. Spatial distribution of solid organ transplant recipients in the southwest area of Madrid, Spain, in relation to park that was focus of visceral leishmaniasis (VL) outbreak, January 1,2005-January 1,2013. Map inset shows the location of the outbreak in relation to the rest of Spain. VL, visceral leishmaniasis.
Table 1. Baseline and clinical characteristics of solid organ
transplant recipients in study of risk factors for VL, Madrid, Spain,
January 1, 2005-January 1, 2013 *

                                                     Overall cohort,
Characteristics                                           n = 68

Recipient age, y, mean [+ or -] SD                  51.1 [+ or -] 14.2
Male sex, no. (%)                                       48 (70.6)

Race, no. (%)
  White                                                 62 (91.2)
  Black, sub-Saharan African                             4 (5.9)
  Other                                                  2 (2.9)

Type of SOT, no. (%)
  Kidney                                                57 (83.8)
  Liver                                                  8 (11.8)
  Heart                                                  3 (4.4)

Donor age, y, mean [+ or -] SD                      46.1 [+ or -] 16.2
Cold ischemia time, min, median (IQR)               1,005 (630-1,354)
No. HLA mismatches, mean [+ or -] SD                 4.0 [+ or -] 1.2
DCD donor, no. (%)                                      18 (26.5)
Transplant during the outbreak, no. (%)                 41 (60.3)

Induction therapy, no. (%)
  Basiliximab                                           22 (32.4)
  Antithymocyte globulin                                24 (35.3)
  None                                                  22 (32.4)

Maintenance immunosuppression, no. (%)
  Steroids                                              56 (82.4)
  Calcineurin inhibitors                                60 (88.2)
  Mycophenolate mofetil/mycophenolic acid               47 (61.8)
  mTOR inhibitors                                       10 (14.7)

Complications in the first year after
    SOT, no. (%)
  Acute graft rejection                                 19 (27.9)
  CMV infection                                         21 (30.9)
  Bacterial infection                                   60 (88.2)

Environmental factors
  Frequent contact with dogs, no. (%)                   26 (38.2)
  Habit of visiting the park, no. (%) ([section])       19 (31.7)
  Distance from patient's residence to park, m,
    median (IQR)                                    1,220 (849-1,865)

Characteristics                                         VL, n = 7

Recipient age, y, mean [+ or -] SD                  53.0 [+ or -] 15.5
Male sex, no. (%)                                        6 (85.7)

Race, no. (%)
  White                                                  5(71.4)
  Black, sub-Saharan African                            2 (28.6) J
  Other                                                   0 (0)

Type of SOT, no. (%)
  Kidney                                                 6 (85.7)
  Liver                                                   0 (0)
  Heart                                                  1 (14.3)

Donor age, y, mean [+ or -] SD                      49.4 [+ or -] 17.4
Cold ischemia time, min, median (IQR)                795 (371-1,365)
No. HLA mismatches, mean [+ or -] SD                 5.0 [+ or -] 1.0
DCD donor, no. (%)                                       3 (42.8)
Transplant during the outbreak, no. (%)                 7 (100.0)

Induction therapy, no. (%)
  Basiliximab                                             0 (0)
  Antithymocyte globulin                                 4 (57.1)
  None                                                   3 (42.8)

Maintenance immunosuppression, no. (%)
  Steroids                                              7 (100.0)
  Calcineurin inhibitors                                 6 (85.7)
  Mycophenolate mofetil/mycophenolic acid                4 (57.1)
  mTOR inhibitors                                        1 (14.3)

Complications in the first year after
    SOT, no. (%)
  Acute graft rejection                                  2 (28.6)
  CMV infection                                          4 (57.1)
  Bacterial infection                                    6 (85.7)

Environmental factors
  Frequent contact with dogs, no. (%)                    3 (42.8)
  Habit of visiting the park, no. (%) ([section])        3 (50.0)
  Distance from patient's residence to park, m,
    median (IQR)                                      399 (261 -985)

Characteristics                                       No VL, n = 61

Recipient age, y, mean [+ or -] SD                  51.0 [+ or -] 13.5
Male sex, no. (%)                                       42 (68.9)

Race, no. (%)
  White                                                 57 (93.4)
  Black, sub-Saharan African                             2 (3.3)
  Other                                                  2 (3.3)

Type of SOT, no. (%)
  Kidney                                                51 (83.6)
  Liver                                                  8 (13.1)
  Heart                                                  2 (3.3)

Donor age, y, mean [+ or -] SD                      46.3 [+ or -] 16.3
Cold ischemia time, min, median (IQR)               1,020 (660-1,360)
No. HLA mismatches, mean [+ or -] SD                 4.0 [+ or -] 1.2
DCD donor, no. (%)                                      15 (24.6)
Transplant during the outbreak, no. (%)                 34 (55.7)

Induction therapy, no. (%)
  Basiliximab                                           22 (36.1)
  Antithymocyte globulin                                20 (32.8)
  None                                                  19 (31.1)

Maintenance immunosuppression, no. (%)
  Steroids                                              49 (80.3)
  Calcineurin inhibitors                                54 (88.5)
  Mycophenolate mofetil/mycophenolic acid               43 (70.5)
  mTOR inhibitors                                        9 (14.8)

Complications in the first year after
    SOT, no. (%)
  Acute graft rejection                                 17 (27.9)
  CMV infection                                         17 (27.9)
  Bacterial infection                                   54 (88.5)

Environmental factors
  Frequent contact with dogs, no. (%)                   23 (37.7)
  Habit of visiting the park, no. (%) ([section])       16 (29.6)
  Distance from patient's residence to park, m,
    median (IQR)                                    1,370 (974-1,880)

Characteristics                                     p value ([dagger])

Recipient age, y, mean [+ or -] SD                        0.721
Male sex, no. (%)                                         0.664

Race, no. (%)
  White                                                   0.112
  Black, sub-Saharan African                              0.049
  Other                                                   1.000

Type of SOT, no. (%)
  Kidney                                                  1.000
  Liver                                                   0.587
  Heart                                                   0.282

Donor age, y, mean [+ or -] SD                            0.596
Cold ischemia time, min, median (IQR)                     0.370
No. HLA mismatches, mean [+ or -] SD                      0.265
DCD donor, no. (%)                                        0.370
Transplant during the outbreak, no. (%)                   0.037

Induction therapy, no. (%)
  Basiliximab                                             0.087
  Antithymocyte globulin                                  0.233
  None                                                    0.673

Maintenance immunosuppression, no. (%)
  Steroids                                                0.338
  Calcineurin inhibitors                                  1.000
  Mycophenolate mofetil/mycophenolic acid                 0.668
  mTOR inhibitors                                         1.000

Complications in the first year after
    SOT, no. (%)
  Acute graft rejection                                   1.000
  CMV infection                                           0.189
  Bacterial infection                                     0.190

Environmental factors
  Frequent contact with dogs, no. (%)                     1.000
  Habit of visiting the park, no. (%) ([section])         0.369
  Distance from patient's residence to park, m,
    median (IQR)                                          0.001

* CMV, cytomegalovirus; DCD, donation after circulatory death; HLA,
human leukocyte antigen; IQR, interquartile range; mTOR, mammalian
target of rapamycin; SOT, solid organ transplant; VL, visceral
leishmaniasis.

([dagger]) The p values refer to the comparison between patients with
and without visceral leishmaniasis. Significant values are in bold.

([dagger]) The country of birth of both patients with posttransplant
VL was Equatorial Guinea.

([section]) Data available for 60 patients.

Table 2. Disease characteristics, demographics, clinical
characteristics, therapy, and outcomes of 7 solid organ transplant
recipients with VL, Madrid, Spain, January 1, 2005-January 1,
2013 *

                                        Patient no.

Characteristics                       1              2

Sex                                   M              M
Race                                Black          Black
Linear distance from
  patient's residence to
  park, m                            794            399
Age at transplant, y                 35             34
Type of SOT                        Kidney         Kidney
Donor Leishmania spp.
  serostatus                      Negative          NP
Pretransplant recipient
  Leishmania spp. serostatus         NP             NP
Date of transplant               2011 Feb 11    2010 Jan 22
Interval from transplant to
  VL diagnosis, y                   1.17           2.44
Fever at admission                   Yes            Yes
Pancytopenia                         Yes            Yes
Splenomegaly                         Yes            Yes
Serologic testing results for
  Leishmania spp.                 Positive       Negative
Presence of amastigote forms
  in bone marrow sample           Positive       Positive
PCR assay results of bone
  marrow sample                      NP             NP
NNN culture results of bone
  marrow sample                   Positive          NP
Initial therapy                     L-AmB          L-AmB
Relapse                              Yes            No
Outcome                         Renal failure   Graft loss

                                             Patient no.

Characteristics                      3            4             5

Sex                                  M            M             M
Race                               White        White         White
Linear distance from
  patient's residence to
  park, m                           261         1,240          985
Age at transplant, y                76            55           68
Type of SOT                       Kidney        Kidney       Kidney
Donor Leishmania spp.
  serostatus                     Negative         NP        Negative
Pretransplant recipient
  Leishmania spp. serostatus     Negative      Positive     Negative
Date of transplant              2010 Mar 10   2010 Jul 7   2009 Dec 29
Interval from transplant to
  VL diagnosis, y                  0.25          1.4          0.17
Fever at admission                  No           Yes           Yes
Pancytopenia                        Yes          Yes           Yes
Splenomegaly                        Yes          Yes           Yes
Serologic testing results for
  Leishmania spp.                Negative      Positive     Negative
Presence of amastigote forms
  in bone marrow sample          Positive      Positive     Positive
PCR assay results of bone
  marrow sample                     NP         Negative        NP
NNN culture results of bone
  marrow sample                  Positive      Negative     Negative
Initial therapy                    L-AmB        L-AmB         L-AmB
Relapse                             Yes          Yes           No
Outcome                            Cured      Graft loss      Cured

                                     Patient no.

Characteristics                     6             7

Sex                                 F             M
Race                              White         White
Linear distance from
  patient's residence to
  park, m                          233           358
Age at transplant, y                49           52
Type of SOT                       Heart        Kidney
Donor Leishmania spp.
  serostatus                     Negative     Negative
Pretransplant recipient
  Leishmania spp. serostatus     Negative     Negative
Date of transplant              2010 Sep 5   2010 Apr 15
Interval from transplant to
  VL diagnosis, y                  1.81         2.21
Fever at admission                 Yes           Yes
Pancytopenia                       Yes           Yes
Splenomegaly                       Yes           Yes
Serologic testing results for
  Leishmania spp.                Positive     Negative
Presence of amastigote forms
  in bone marrow sample          Positive     Positive
PCR assay results of bone
  marrow sample                     NP           NP
NNN culture results of bone
  marrow sample                  Positive     Negative
Initial therapy                   L-AmB         L-AmB
Relapse                             No           No
Outcome                           Cured         Cured

* L-AmB, liposomal amphotericin B; NNN, Novy-McNeal-Nicolle; NP, not
performed; SOT, solid organ transplant; VL, visceral leishmaniasis.
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Title Annotation:DISPATCHES
Author:Carrasco-Anton, Nerea; Lopez-Medrano, Francisco; Fernandez-Ruiz, Mario; Carrillo, Eugenia; Moreno, J
Publication:Emerging Infectious Diseases
Geographic Code:4EUSP
Date:Jul 1, 2017
Words:3536
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