We monitored MERS-CoV–specific antibody levels in 11 pairs of camel dams and their calves at monthly intervals over the course of 1 year postparturition. These animals were born and raised on a closed commercial camel dairy farm in the United Arab Emirates that had a strict animal health and biosecurity program. The total number of camels on the farm was ≈4,500. Animals are kept in open paddocks and are grouped according to the age of their calves and production stage. Despite high standards of hygienic husbandry and biosecurity, the transmission of pathogens within the farm cannot be completely eliminated. Therefore, the entire farm is 1 epidemiologic unit. The 11 dam–calf pairs investigated in this study were kept in different fenced compartments within 100–150 m from each other. However, all these animals were kept together with other dam–calf pairs in the same paddock throughout lactation. All camel calves were born during June 3–15, 2014.

Nasal swab specimens were taken from all 11 mothers and calves, and serum samples were obtained through jugular vein puncture. Blood cells were removed immediately after collection, and samples were stored at −20°C until testing. Serum samples and nasal swabs were taken at the day of parturition, at 1 week and 1 month postparturition, and then at monthly intervals until June 2015. MERS-CoV RNA was detected through amplification of gene targets as described previously (12). Virus isolation was performed on Vero cells. MERS-CoV–specific IgG and neutralizing antibodies were determined by ELISA and microneutralization test as described previously (5,10).

Figure

Figure. MERS-CoV–specific IgG antibody levels in dromedary camel dam–calf pairs, United Arab Emirates, 2014–2015. A) MERS-CoV spike protein S1-domain–based ELISA ratios of individual samples (dots) plus mean (horizontal line) and SD (error...

In general, maternal IgG antibodies in camels are not acquired via the transplacental route but through the intake of colostrum during the first 24 hours postparturition (13). After 24 hours, antibody levels in the dam’s milk decrease rapidly, and IgG levels in calves’ serum cease to rise (13). This pattern is reflected for MERS-CoV in this study. On the day of parturition, samples were collected from 5 of 11 dam–calf pairs studied. High levels of MERS-CoV–specific antibodies were observed in all dams, whereas no antibodies were detected in calves (Figure, panel A). At day 7 postparturition, however, all 11 camel calves had high MERS-CoV–specific antibody levels. These levels declined during the first 6 months postparturition, whereas IgG in dams remained constantly at high levels. The neutralizing activity of IgG was confirmed by microneutralization tests on serum samples from calves collected 2–3 months, 5–6 months, and 1 year after birth (Figure, panel B). After 5–6 months, serum from 6 of 11 calves had completely lost their neutralizing activity. The remaining 5 calves had low neutralizing titers, ranging from 1:20 to 1:40 (Figure, panel B).

To examine possible correlations between antibodies and MERS-CoV infection, we examined shedding of MERS-CoV in nasal swab specimens. During the first 5 months postparturition, MERS-CoV RNA was detected sporadically on days 7 and 30 (Table). Infectious virus was isolated only from calves but not dams. At 6 months postparturition, when calves showed the lowest antibody titers, MERS-CoV RNA was detected in 2 of 11 calves (Table), indicating active MERS-CoV infection. All calves seroconverted during the following weeks (Figure, panel A); 1 calf had meanwhile been euthanized because of a congenital forelimb deformity. All calves showed high reciprocal neutralizing titers of >640 at 11–12 months postparturition.

This longitudinal study of natural MERS-CoV infections in camels confirms assumptions from preliminary cross-sectional studies in camels (4,5,11). MERS-CoV infection appears to predominantly affect young, immunologically naive animals. Serum antibodies might not have been sufficient to mediate protective immunity in the respiratory tract because dams and calves were sporadically infected even as maternal antibodies peaked at day 7 postparturition. These findings are consistent with earlier reports of MERS-CoV reinfection in seropositive camels (4,11). Nevertheless, our findings of virus isolation from calves but not dams are in line with earlier observations of reduced viral load in seropositive camels on reinfection (11,14), indicating that neutralizing antibodies might not provide sterile immunity but could still reduce the viral replication level. The predominance of infection in young animals is better explained by the absence of immunity than by other factors, such as social group density, because the number of newborn camels in our study was negligible compared with the overall size of the herd at the farm. Moreover, young camels were not kept in a contiguous group but in small compartments, where they had more contact with their mothers than with other young animals. Calves are likely to have been infected through fomites or through adult animals shedding low quantities of virus.

Our findings have important implications for the prevention of human infections through camel herd management and camel vaccination. Camel breeding, even if involving a small number of newborn animals, should be classified as a risk for human acquisition of MERS-CoV. The greatest risk should be assumed for the time after the fourth month of life until the first wave of natural infections, which should occur during the first year of life in camels raised in MERS-CoV–endemic regions. Measures for the prevention of infection, such as personal protective equipment, hand hygiene, and environmental sanitation, as applied on the farm in our study, should be sufficient for protection, given that no human MERS-CoV illnesses occurred among staff and only 2 of 300 workers with regular contact with camels had detectable MERS-CoV–specific IgG antibodies. Because persons with underlying disease and the elderly show the most severe outcomes of MERS-CoV infection, these groups should generally avoid farms where camel calves are being raised.

Our results also suggest that studies dealing with application and efficacy of MERS-CoV vaccines should be modified. A first study involving immunologically naive animals showed a sharp decline in virus secretion after vaccination (14). However, future vaccination trials should also investigate the effect of preexisting maternal antibodies on vaccine efficacy (15).