Detection of antibodies against flavivirus over time in wild non-human primates from the lowlands of Costa Rica

Abstract

Two-hundred-nine free ranging non-human primates from 31 locations throughout Costa Rica were captured and released between 1993 and 2012, and blood samples, sera or plasma were collected, to detect antigens and antibodies, and so assess the distribution of active and passive flavivirus infections over time. A competitive enzyme-linked immunoassay for the detection of antibodies was used to determine the distribution of past flavivirus infections over time, while Reverse Transcriptase Polymerase Chain Reaction (RT-PCR) was used to detect active West Nile Virus (WNV) and Dengue virus (DENV) infections. The first serological evidence of flavivirus in these animals was determined in 1993, at the same time when DENV re-emerged in humans from Costa Rica. An increase in the number of seropositive wild monkeys to flavivirus was determined over time in the country (11.3% seropositivity in 1993–1996, 20.7% in 2001–2008, and finally 52.9% in 2010–2012). Furthermore, the presence of DENV2 was detected in samples from four howler monkeys collected in 2001–2002, whereas DENV2, DENV3, and DENV4 were found in samples from four white-faced monkeys, and WNV in three howler monkeys living in the Pacific coast of Costa Rica during 2010–2012. The habitat where the positive PCR individuals lived were characterized as fragmented forests, having temperatures ranging from 26°C to 28°C, altitudes below 250 meters above sea level, high precipitation during 7 to 9 months (1500–4000 mm), and a marked dry season of 3 to 5 months. All these animals were living near mangroves; however, they did not show clinical signs of illness at the time of sampling. Results obtained show that the number of seropositive wild non-human primates to flavivirus were increasing during time in the country, longitudinal studies are needed to investigate their role as sentinels of these viruses and to determine if flavivirus infections can affect these species.

Animals as potential reservoirs for dengue transmission: A systematic review

“…There was significant intra-group heterogeneity in the serology group (I 2 : 97.82%), and pooling of results from both serology and RT-PCR methods was not supported as given significant inter-group heterogeneity was noted ( p = 0.000). There were 15 studies involving a forest setting [ 22 , [24] , [25] , [26] , [27] , [28] , [29] , [30] , [31] , [32] , [33] , [34] , [35] , [36] , [37] ], 12 of which were based solely in a forest. Of 7 studies involving the urban/rural setting [ 26 , 31 , [38] , [39] , [40] , [41] , [42] ], only 5 were exclusively based at such.…”

“… [ 31 ] Argentina Unknown Unknown 0/4 NHP, Monkeys Costa Rica 31 Lowlands locations Forest & Urban/rural (Private land) 1993–1996, 2000–2012 8/155 (5.2); D2,3,4 (C/prM) 53/209 (25.4) (Tested against flavivirus) ELISA Co-circulation of D1,2,3,4 since re-emergence in 1993. [ 26 ] NHP, Monkeys Malaysia Unknown Forest 1962–1964 139/221 (62.9); D2 PRNT; Tested for D2 only [ 35 ] NHP, Monkeys French Guiana Petit Saut Hydroelectric Dam Forest 1994–1995 0/145 PRNT; Tested for D2 only Dramatic increase in cases over the past 30 years, epidemic in 1991–1992 with up to 3000 cases. [ 37 ] Mandrill Gabon Lope National Park Forest 1998–2006 2/25 (8); D2 PRNT; Tested for D2 only [ 30 ] NHP, Monkeys Congo Basin; Uganda, Democratic Republic of Congo & Rwanda Bwindi forest, Park National of the Volcanoes, Kinigi & Unknown locations Forest 2001–2009 0/44 NHP, Monkeys Panama Localities near the Canal zone (unknown setting) Urban/rural 1954–1955 2/105 (1.9); D1,2 HI; Tested against D1/2 only (Only 2 positive samples further tested using PRNT) Dengue epidemic in 1904, 1912, late 1941 to early 1942.…”

Worldwide dynamic biogeography of zoonotic and anthroponotic dengue

“…However, spillback cases with primates acting as reservoirs for urban dengue serotypes could also occur [ 116 ], and this might be happening in South America [ 33 , 34 ]. Seropositivity to the dengue virus has been documented in species from the genus Alouatta in north-eastern Argentina [ 117 ] and Costa Rica [ 118 ], from Cebus in Costa Rica [ 118 ], and from Leontopithecus in south-eastern Brazil [ 119 ]. Precisely, south-eastern Brazil, specifically the Atlantic forests surrounding Bahia, is highlighted by our model as an area at risk of zoonotic transmission to humans ( Fig 4 ).…”

Serosurvey of Nonhuman Primates in Costa Rica at the Human–Wildlife Interface Reveals High Exposure to Flaviviruses

“…ZIKV and DENV circulate in anthroponotic cycles, which has facilitated their rapid spread throughout the Americas [10], with no recognized sylvatic cycle. Nevertheless, possible maintenance through sylvatic cycles has been suggested in the Americas for NPs of different species, i.e., Alouatta spp., Cebus spp., Ateles spp., by serological and molecular detections [11][12][13]. However, these detections may be due to spillback, i.e., humans being the primary source of the virus and spilling the virus into wildlife [7,11,14,15].…”