Impact of maternally derived immunity on immune responses elicited by piglet early vaccination against the most common pathogens involved in porcine respiratory disease complex
Porcine Health Management volume 8, Article number: 11 (2022)
Newborn piglets can trigger an elementary immune response, but the acquirement of specific antibodies and/or cellular immunity against pathogens before they get infected post-natally is paramount to preserve their health. This is especially important for the pathogens involved in porcine respiratory disease complex (PRDC) as they are widespread, fairly resistant at environment, and genetically variable; moreover, some of them can cause intrauterine/early life infections.
Piglet protection can be achieved by either passive transfer of maternal derived immunity (MDI) and/or actively through vaccination. However, vaccinating piglets in the presence of remaining MDI might interfere with vaccine efficacy. Hence, the purpose of this work is to critically review the putative interference that MDI may exert on vaccine efficacy against PRDC pathogens. This knowledge is crucial to design a proper vaccination schedule.
MDI transferred from sows to offspring could potentially interfere with the development of an active humoral immune response. However, no conclusive interference has been shown regarding performance parameters based on the existing published literature.
Suidae species are characterized by a six-layered epitheliochorial placenta  that, unless it is damaged during gestation  prevents leaking of large molecules like immunoglobulins from the sow to the foetuses . However, foetuses can produce their own antibodies against antigens in the last third of gestation [4,5,6]. These antibodies are considered as part of the innate immune system  and are considered as “natural antibody repertoire”. Although they might play a protective role for the newborn pig , their response is weak  and little is known about their specificity and affinity . On the other hand, piglets are born with functional immune cells and extracellular components able to respond to infections [10, 11]. However, due to limited or no external antigenic stimuli during foetal life, these components are usually immature at birth. Therefore, neonates are not fully immunologically competent.
Since the complete adaptative protective immune response of the piglet needs around four weeks to be established [12, 13], the protection of the newborn piglet against infectious agents is dependent on the acquirement of maternally derived immunity (MDI) from colostrum and milk .
The amount of MDI transferred from sows to their offspring is determined by the sow’s immunity level at the time of parturition, the timing of colostrum intake and the volume of colostrum ingested . Strengthening sow herd immunity against specific diseases through exposure and/or vaccination is a useful management tool for ameliorating clinical effects in piglets and delaying infection until the piglet immune system is fully prepared to respond .
The duration of MDI is rather variable among pathogens. Under field conditions, it is usually measured considering only one arm of the immune system, the humoral response. In this regard, two terms are used in the literature to refer to the persistence of such MDI: the duration of maternally derived antibodies (MDA) detected by means of serological tests and the rate of MDA decay. The duration of MDA (Table 1) refers to the age of the piglet at which their MDA levels fall below the limit of detection of the test , whereas the rate of decay, also called “half-life”, indicates the time required for a 50% decrease in MDA levels . This latter measure is a constant value and would be the most appropriate one to compare data among studies. However, the MDA decay is reported in few studies and significant variation is provided depending on the study; for example, MDA half-life for Actinobacillus pleuropneumoniae was calculated as 11–15 days by Vigre et al.  and 28–42 days by Cruijsen et al. . Therefore, the duration of MDA is the most widely used parameter among published studies. Nevertheless, it is important to consider that the duration of MDA is dependent on the initial concentration of MDA and the threshold of the serologic test used .
If the level of MDI wane before piglets’ immune system has reacted against a given pathogen, there is a non-protected timeframe or time-window where the piglet is highly susceptible to infection. Therefore, the desirable scenario is to vaccinate piglets prior to natural infection although it implies that vaccination is performed in presence of MDI for most pathogens. Depending on the levels of such MDI, a potential interference of vaccine uptake may happen, jeopardizing vaccine seroconversion and efficacy [21,22,23,24,25].
The objective of this review was to compile information on how MDI can affect vaccine efficacy against the most common swine pathogens involved in porcine respiratory disease complex (PRDC), namely Swine Influenza viruses (SIV), Porcine reproductive and respiratory syndrome virus (PRRSV), Porcine circovirus 2 (PCV-2), Mycoplasma hyopneumoniae (M. hyopneumoniae) and Actinobacillus pleuropneumoniae (A. pleuropneumoniae).
Maternally derived immunity (MDI)
Components of MDI
Different antibody isotypes are present to varying proportions within colostrum and milk . Immunoglobulins G (IgG) and M (IgM) are the most common isotypes in colostrum, whereas immunoglobulin A (IgA) is the most common one in milk . Colostrum and milk also contain large numbers of cells that may vary depending on the mammary gland’s developmental stage and the sow’s physiologic and immunologic status . Many of them are leukocytes, such as neutrophils, other granulocytes, and mostly antigen-experienced lymphoid cells [29,30,31,32] that participate in the cell-mediated immune (CMI) response. In addition, there are also other components that are thought to play an immunomodulatory role, such as the antibacterial protein lactoferrin, lysozyme and cytokines [33, 34].
The newborn systemic and mucosal immune systems are immature, with limited peripheral lymphoid cells, underdeveloped lymph nodes, rudimentary jejunal Peyer’s patches and a low number of effector and memory T-lymphocytes [11, 35, 36]. As indicated above, the newborn piglet does not receive neither produce antibodies against a specific pathogen during gestation, unless a potential intrauterine infection or damage of placentation occurs during the immunocompetence period (from around 70–80 days of gestation onwards) . In such eventuality, the animal would be delivered already with antibodies against the specific pathogen. Noteworthy, one report suggested PCV-2 antibody placental barrier leakage from sow to fetus, mainly in those cases from which the sows had very high levels of antibody titers . These authors hypothesized that antibody crossing might be associated with small damage to the placental barrier during the gestational period. If this happens only with PCV-2 antibodies or with any type of antibody is presently unknown.
Antibodies and immune cells are transferred from sow to piglet by the ingestion of colostrum and milk, and these can cross the intestinal barrier and reach the peripheral blood for a limited period. This way they can reach lymphatic and non-lymphatic tissues including mesenteric lymph nodes, and a variety of other tissues such as the spleen, liver, lungs and the duodenum and jejunum’s lamina propria and submucosal spaces [33, 38, 39]. Nevertheless, this absorption process differs slightly between antibodies and cells [13, 40].
The peak of antibody transfer occurs immediately after birth. Therefore, it is critical to ensure piglet suckling for at least the first 6 h of life . Acquired antibodies remain intact in the neonatal digestive tract due to low proteolytic activity, which is further reduced by sow colostrum trypsin inhibitor . Antibodies (IgG but not IgA or IgM) can pass through the intestinal mucosa even if the maternal source or donor species is different from the own mother (for example, newborn pigs have been proven to absorb cow antibodies ). This absorption can be done by two transcytosis mechanisms to penetrate the intestinal barrier: non-specific endocytosis or antibody specific neonatal Fc-receptors [42,43,44,45]. The ability to absorb MDA by the proximal to the distal part of the small intestine lasts only for a short period of time. Specifically, Murata & Namioka  concluded that duodenum uptake stops 2 h after birth, while the jejunum’s and ileum uptake stop 48 and 72 h after birth, respectively. This post-natal loss of absorption capability is known as “gut closure”. Finally, within 9 days of birth, the mucosal epithelium is completely replaced by intestinal epithelial cells incapable of transcytosis [47, 48]. Colostral IgG are detectable in the neonatal circulatory system from 48 h after birth onwards [49, 50].
In contrast, transference of colostral cells needs a minimum period of suckling from 12 to 20 h, and the absorption is accomplished through the intercellular space between the epithelial cells of intestinal mucosa . Years ago it was considered that only maternally-derived cells from the biological mother could pass the intestinal mucosa of piglets [38, 39]. This assumption was supported by Bandrick et al.  who reported no evidence of immune cell reactivity in cross-fostered animals just after birth. Therefore, animals fostered by a substitute dam could be deficient in CMI . In contrast, new research has shown that piglets may absorb immune cells transferred by colostrum independently if they originate from their biological mother or from another sow .
Estimation of MDI transferred to the piglet by dams’ parameters
The most used technique to measure MDA levels in mammary secretions [26, 51,52,53] and/or antibodies in serum of sows and piglets  is the enzyme-linked immunosorbent assay (ELISA). Occasionally, this technique (commercial or in-house methods) has been also used to monitor the presence and quantity of immunoglobulins in other sample types like oral fluids [55, 56]. Alternatively, monitoring CMI is also feasible but mainly restricted to research purposes because the techniques used (for example, enzyme-linked immunosorbent spot [ELISPOT]) are labour-intensive, hard to read and rarely commercialized.
However, the results obtained from measuring antibody levels in the dam are not effective as a tool for estimating MDI transferred later through colostrum and milk . This is mainly because MDI levels in piglets depend on how effective the colostrum and milk intakes are in terms of quantity and timing.
Early life vaccination of piglets
Different vaccination strategies are used to immunize the populations of swine production (breeding animals, piglets, or both). The vaccination approach will be determined by the pathogenesis and epidemiology of each pathogen. Understanding the infection dynamics and herd immunological status for each infectious agent will be critical to determine the best vaccination strategy.
Early piglet vaccination might imply that piglets still have MDI. Therefore, a potential interference between residual immunity of maternal origin and the vaccine antigen uptake needs to be considered. Piglet MDI may come from natural infection, vaccination or both scenarios (natural infection and vaccination). In the latter case, and especially if sows are vaccinated by late gestation, the amount of measurable MDA transferred can be very high, increasing the risk of interference. Nevertheless, vaccinating sows and piglets in the appropriate timing may yield the best results in terms of herd protection and productivity.
Effect of MDA on the seroconversion and efficacy of the most used vaccines in the pig industry for pathogens involved in PRDC
Vaccine efficacy interference by MDA is defined as the ability of residual antibodies transferred to piglets by colostrum and/or milk to block or delay the active immunization of the piglet . This interference involves a number of possible mechanisms, including the neutralization of the immunizing antigen , the masking of B cell epitopes, and/or the down-regulation of neonatal Ig synthesis by means of the inhibition of B cell maturation and development . Importantly, this concept is mainly considered with intramuscularly (and probably intradermally) applied vaccines that generate systemic and, eventually, mucosal immune responses. However, the degree of potential vaccine efficacy interference due to MDA with vaccines delivered through mucosal surfaces remains unknown .
In the presence of high levels of systemic antibody titres at the time of intramuscular vaccination, the most typical interference effect is a reduced or lack of seroconversion [59,60,61]. However, the key issue would be if this interference in seroconversion translates into lower vaccine effectiveness. The most widely used method of measuring vaccination effectiveness in terms of productive parameters is the calculation of average daily weight gain (ADWG) .
Nowadays, piglets are usually vaccinated against several pathogens at early ages. The most common infectious agents involved in PRDC for which piglet vaccines have been developed are detailed in Table 2, including current data on potential interference with vaccine efficacy. Importantly, while interference with vaccine efficacy is often analyzed by comparing experimental vaccinated groups with different antibody titres, it may also be studied by comparing vaccinated groups of various ages.
Swine influenza viruses
Swine influenza viruses (SIV), generally of type A, are the causal agents of swine influenza and a major cause of acute respiratory disease outbreaks in pigs. Nowadays, different subtypes of SIV as H1N1, H1N2, H3N2, and pandemic H1N1 virus are co-circulating worldwide . Their infection can display different clinical forms, ranging from an acute outbreak to an endemic subclinical scenario . Although the epizootic presentation is more aggressive, the endemic one is more common within herds. The virus is spread primarily through direct contact with infectious oronasal secretions . In this scenario, newborn piglets that do not receive MDI are at a high risk of showing clinical signs.
Some studies describing the MDA duration against SIV reported a steadily decline until the age of 10 weeks [23, 65], with an average waning period of 7–8,5 weeks . However, other investigations have reported that MDA in piglets coming from vaccinated sows could persist up to 2–4 months of age under both experimental [66,67,68] and field  conditions.
Currently, the main strategy for controlling SIV infection is vaccination. Nevertheless, in the presence of high MDA levels, previous studies reported interference of early piglet vaccination in terms of reduced post-vaccination humoral response [23, 67] and worse respiratory clinical signs [23, 68]. Interestingly, Kitikoon et al.  found that piglet vaccination gave better protection (less fever, lower viral shedding and reduced pneumonia) than MDA against SIV, raising doubts on the common practice of immunizing sows to boost MDI. Information on the putative interference of MDA in vaccine efficacy in terms of production parameters has not been assessed so far.
Porcine reproductive and respiratory syndrome virus (PRRSV)
Porcine reproductive and respiratory syndrome (PRRS) is a common disease in pigs with one of the major economic impacts in porcine production worldwide . Its etiological agent is PRRSV, a virus that causes reproductive problems in sows and respiratory disorders in pigs of all ages, as well as slower growth and mortality in growing pigs . This virus can also cause a long-lasting infection, as animals can remain contagious even after clinical disease recovery [72, 73]. Since piglets can be infected congenitally or very early in life , it is critical to protect them as soon as possible after birth or also to protect against intrauterine infections.
Different studies showed that MDA has a significant protective effect against PRRSV infection in suckling piglets [75, 76], lasting between 2 and 11 weeks [71, 72, 77,78,79,80,81,82]. In fact, the highest rates of PRRSV detection in sera usually occur between 6 and 8 weeks of age, when MDA have achieved lowest levels in many cases [71, 72, 81]. Therefore, since high levels of MDI may offer a strong protection to the piglets in the first few weeks of life, one of the options is to protect the piglet through dam vaccination . However, piglets gradually lose passive immunity, resulting in a steady supply of PRRSV-susceptible piglets and allowing the virus to spread across pig herds. Under this scenario, piglet vaccination may strengthen the piglet’s own early humoral and cellular immune responses .
Since vaccination of sows and piglets is a common strategy for controlling PRRS, it is important to consider the effect the MDI may have on developing an active immune response after vaccination. In this regard, recent investigations have yielded contradictory results. According to Fablet et al.  and Renson et al. , piglets with high MDA at vaccination had a hindered post-vaccination immunological response for at least 4 weeks. In contrast, Balasch et al.  and Jeong et al.  showed that vaccines can overcome maternal immunity and piglets as young as one day old can generate a partially protective immune response. It may happen that different vaccines may have different ability to overcome MDI, but side-by-side comparisons in such regard have not been performed.
Noteworthy, up to now, interference of MDI on PRRSV vaccine efficacy in terms of productive parameters has not been studied.
Porcine circovirus 2 (PCV-2)
Porcine circovirus 2 (PCV-2) is the primary aetiologic agent of porcine circovirus diseases (PCVDs) , which include the systemic disease (PCV-2-SD), the reproductive disease (PCV-2-RD), porcine dermatitis and nephropathy syndrome (PDNS) and the subclinical infection (PCV-2-SI) [85,86,87]. Although PCV-2 is ubiquitous in domestic swine and wild boar, pigs younger than 4 weeks of age are very rarely affected by the disease . This suggest that certain levels of MDI prevent the development of PCV-2-SD in the offspring [89, 90]. However, early infections, including intrauterine infections, do occur in farms in presence or absence of subsequent PCV-2-SD in late nursery or growing pigs [91, 92].
MDA against PCV-2 is known to last between 4 and 12 weeks of age [21, 60, 93,94,95,96], and can be fostered by sow vaccination at mid-late gestation. Although a strong maternal immunization is crucial for the newborn piglet protection against infection, when the piglet is vaccinated it may block the vaccine antigen. Indeed, high MDA titres against PCV-2 have been shown to impair an active seroconversion after vaccination [17, 21, 60, 95,96,97,98,99]. However, production parameters such as ADWG did not appear to be jeopardized in similar scenarios [21, 93, 96, 98, 100], suggesting that interference with seroconversion does not always imply a lack of protection. Of note, Feng et al.  highlighted that extremely high titres of MDA at vaccination may interfere with production parameters, although it was considered not economically relevant in practical conditions as it is rare to find such high MDA titres in the field. Alternatively, Haake et al.  concluded that, regardless the antibody titre at vaccination, immunization at 1 week of age can result in lower production parameters than immunizing later (3 weeks of age). However, in this study, 1 week-old vaccinated piglets had higher antibody values than those vaccinated at 3 weeks of age.
Mycoplasma hyopneumoniae is the main aetiological agent of enzootic pneumonia [101, 102]. Under experimental conditions, M. hyopneumoniae infection can last for up to 240 days . During that time, animals could still shed the pathogen in a slow and silent fashion, which explains the M. hyopneumoniae endemic and chronic behaviour on most farms.
The prevalence of M. hyopneumoniae infection in piglets at weaning has been, in some studies, correlated with the prevalence and severity of lung lesions in fattening pigs [104, 105]. For this reason, reducing vertical transmission from dams to piglets during lactation period is considered a critical point in M. hyopneumoniae control. In consequence, sow vaccination strategies have been proposed as a potential tool to reduce vertical transmission and induce specific antibodies and CMI in sow serum and colostrum. These components would be, in turn, transferred to their suckling piglets and play a role in piglet protection [14, 29, 106,107,108]. MDA against M. hyopneumoniae wane approximately between 2 and 9 weeks [20, 109]. Moreover, piglet vaccination is the most common practice, and it usually takes place around weaning, within the 4 first weeks of life. Nevertheless, some vaccines are licensed to be applied within the first week of life  and, consequently, such vaccination takes place in presence of MDI .
The influence of MDI on piglet’s vaccination has not been fully elucidated. Whereas some studies reported that the antibody response elicited by vaccination in face of MDI could be reduced or absent [112,113,114,115], some others do not describe it [109, 111, 116]. However, lack of seroconversion following vaccination has not been related to worse productive parameters of the piglet so far .
Actinobacillus pleuropneumoniae is the aetiological agent of porcine contagious pleuropneumonia. Virulent serotypes of this bacteria can cause respiratory distress, anorexia, and fever, with variable degrees of severity depending on the clinical form: peracute, acute, or subacute . Death is frequent in peracute and acute presentations. Subclinical infections can also take place with several A. pleuropneumoniae serotypes . This bacterium cannot survive in the environment for long periods of time ; therefore, transmission is mostly pig-to-pig via direct contact, both oral and nasal, and, to a lesser extent, via aerosols over short distances . In addition, infected pigs that carry the bacterium silently contribute to the pathogen’s spread . Therefore, a proportion of piglets are exposed to the bacterium early in life, mainly during the suckling period. Subsequently, when MDI wanes by end of the nursery period or during the growing phase, infection is further spread .
MDA against A. pleuropneumoniae-specific can persist from 2 to 12 weeks of age in the offspring [18, 19, 122,123,124]. Vaccinating dams against A. pleuropneumoniae can be an effective method for improving the herd serological status and, consequently, the amount of acquired colostral antibodies in piglets . Colostral immunity protects piglets against sudden death or peracute outbreaks, but not against infection, as piglet infection with A. pleuropneumoniae can occur from 10th day of life even in the presence of MDA . However, high levels of MDI against the pathogen are especially indicated for newborns as they remain seropositive for a longer period and enhances antibody response when they seroconvert due to natural infection . Indeed, Krejci et al.  found that the protection of the piglet could be even better if, in addition to having specific colostrum-derived antibodies, it was pre-infected with low infection doses.
Vaccine manufacturers recommend vaccination in late nursery and/or early fattening pigs for protection against A. pleuropneumoniae . However, vaccination at those ages is a concern due to interference of MDA that may still be present. Tumamao et al.  found that vaccinating piglets against A. plueropneumoniae in the presence of low levels of MDA induces a significant antibody response, but no comparison with animals with high MDA levels was made in the same study. On the other hand, Jirawattanapong et al.  found no antibody response after vaccination of pigs in presence of high MDA titres at 6 and 10 weeks of age. Therefore, it seems that vaccination against A. pleuropneumoniae should not be used during the first weeks of life to prevent an impairment of post-vaccinal antibody response .
Notably, evident interference of MDI on A. pleuropneumoniae vaccine effectiveness in terms of productive parameters has not been found in published studies. However, all marketed products against this pathogen indicate vaccination from 6 weeks of age onwards, which suggests vaccine efficacy interference if administered to earlier ages still with MDI (European Medicines Agency—https://ema.europa.eu).
Vaccination can be applied to sows, piglets or both populations. Sow immunization prior to farrowing enhances MDI transferred to offspring through colostrum and milk. Piglet vaccination at early ages is directed to immunize them before they become infected naturally. The optimal moment would be when MDA levels are high enough to protect the piglet, but low enough to minimize the interference with vaccine antigen. That is why the third alternative, vaccinating both collectives, is the one at a higher risk of interference with vaccine efficacy in the piglet.
Several studies have assessed the amount and duration of MDA to properly ascertain the best timing to apply the vaccine to the piglet. However, the exact duration of MDA for each pig or groups of pigs is virtually impossible to be assessed under field conditions, since it is dependent on the sow’s serological status at farrowing and on the piglet colostrum intake. Therefore, it is expectable to have high individual variability amongst sows and even within piglets from the same litter.
The most likely situation is that piglets are vaccinated in the presence of an unknown level of MDA. This scenario would imply a potential risk of interference between these antibodies and the vaccine antigen intake. In this regard, it is worth noting that interference might be assessed from two different perspectives: interference on seroconversion and interference on vaccine efficacy in terms of production parameters (mainly ADWG). Several studies on PRDC pathogens reviewed in this work have shown that MDA may interfere with seroconversion, particularly when the titres of systemic antibodies were high at the time of piglet vaccination. Therefore, it might be interesting in some cases to wait for MDA declining and vaccinate piglets beyond 3–4 weeks of age, or even later. In contrast, when vaccine efficacy was also evaluated, the interference was shown in terms of seroconversion elicited by the immunization, but it was rarely translated in worse productive parameters. However, it must be considered that lack of demonstrated commercial vaccine effectiveness is unlikely to be published in the literature. Furthermore, it would be also worthy to investigate if the existence of antigen-specific CMI of maternal origin in the neonatal piglet can influence the development of vaccine-induced immunity, particularly in those cases where the piglet is vaccinated very early .
All in all, based on the existing literature, early piglet vaccination could be considered as an option to protect the piglet in terms of reduction of clinical signs and improving performance parameters, notwithstanding the potential serological interference issue.
According to the literature, MDA transferred from sows to offspring could potentially interfere with the development of an active humoral immune response when vaccines are applied at the recommended age for most of the PRDC pathogens. However, no conclusive interference has been shown regarding performance parameters based on the existing published literature.
Availability of data and materials
All data used in this review work has been obtained from public scientific databases, available elsewhere.
Macdonald AA, Bosma AA. Notes on placentation in the Suina. Placenta. 1985;6(1):83–91. https://doi.org/10.1016/S0143-4004(85)80035-7.
Saha D, Sacristán RDP, van Renne N, Huang L, Decaluwe R, Michiels A, Rodriguez AL, Rodríguez MJ, Durán MG, Declerk I, Maes D, Nauwynck HJ. Anti-porcine circovirus type 2 (PCV2) antibody placental barrier leakage from sow to fetus: impact on the diagnosis of intra-uterine PCV2 infection. Virologica Sinica. 2014;29(2):136. https://doi.org/10.1007/S12250-014-3432-Z.
Šinkora M, Šinkora J, Řeháková Z, Šplíchal I, Yang H, Parkhouse RME, Trebichavský I. Prenatal ontogeny of lymphocyte subpopulations in pigs. Immunology. 1998;95(4):595–603. https://doi.org/10.1046/J.1365-2567.1998.00641.X.
Redman DR, Bohl EH, Ferguson LC. Porcine parvovirus: natural and experimental infections of the porcine fetus and prevalence in mature swine. Infect Immun. 1974;10(4):718–23. https://doi.org/10.1128/IAI.10.4.718-723.1974.
Redman DR, Bohl EH, Cross RF. Intrafetal inoculation of swine with transmissible gastroenteritis virus. Am J Vet Res. 1978;39(6):907–11.
Sun J, Hayward C, Shinde R, Christenson R, Ford SP, Butler JE. Antibody repertoire development in fetal and neonatal piglets. I. Four VH genes account for 80 percent of VH usage during 84 days of fetal life. J Immunol. 1998;161(9):5070–8.
Ochsenbein AF, Zinkernagel RM. Natural antibodies and complement link innate and acquired immunity. Immunol Today. 2000;21(12):624–30. https://doi.org/10.1016/S0167-5699(00)01754-0.
Butler JE, Sun J, Weber P, Ford SP, Rehakova Z, Sinkora J, Lager K. Antibody repertoire development in fetal and neonatal piglets. IV. Switch recombination, primarily in fetal thymus, occurs independent of environmental antigen and is only weakly associated with repertoire diversification. J Immunol (Baltimore, Md: 1950). 2001;167(6):3239–49. https://doi.org/10.4049/JIMMUNOL.167.6.3239.
Butler JE, Zhao Y, Sinkora M, Wertz N, Kacskovics I. Immunoglobulins, antibody repertoire and B cell development. Dev Comp Immunol. 2009;33(3):321–33. https://doi.org/10.1016/J.DCI.2008.06.015.
Šinkora M, Sun J, Šinkorová J, Christenson RK, Ford SP, Butler JE. Antibody repertoire development in fetal and neonatal piglets. VI. B cell lymphogenesis occurs at multiple sites with differences in the frequency of in-frame rearrangements. J Immunol. 2003;170(4):1781–8. https://doi.org/10.4049/JIMMUNOL.170.4.1781.
Šinkora M, Butler JE. The ontogeny of the porcine immune system. Dev Comp Immunol. 2009;33(3):273–83. https://doi.org/10.1016/j.dci.2008.07.011.
Salmon H, Berri M, Gerdts V, Meurens F. Humoral and cellular factors of maternal immunity in swine. Dev Comp Immunol. 2009;33(3):384–93. https://doi.org/10.1016/j.dci.2008.07.007.
Poonsuk K, Zimmerman J. Historical and contemporary aspects of maternal immunity in swine. In: Animal health research reviews, vol 19, Issue 1. Cambridge University Press; 2018. p. 31–45. https://doi.org/10.1017/S1466252317000123.
Bandrick M, Ariza-Nieto C, Baidoo SK, Molitor TW. Colostral antibody-mediated and cell-mediated immunity contributes to innate and antigen-specific immunity in piglets. Dev Comp Immunol. 2014;43(1):114–20. https://doi.org/10.1016/j.dci.2013.11.005.
Klobasa F, Werhahn E, Butler JE. Regulation of humoral immunity in the piglet by immunoglobulins of maternal origin. Res Vet Sci. 1981;31(2):195–206. https://doi.org/10.1016/s0034-5288(18)32494-9.
Opriessnig T, Yu S, Thacker EL, Halbur PG. Derivation of porcine circovirus type 2-negative pigs from positive breeding herds. J Swine Health Prod. 2004;12(4):186–91.
Fort M, Sibila M, Pérez-Martín E, Nofrarías M, Mateu E, Segalés J. One dose of a porcine circovirus 2 (PCV2) sub-unit vaccine administered to 3-week-old conventional piglets elicits cell-mediated immunity and significantly reduces PCV2 viremia in an experimental model. Vaccine. 2009;27(30):4031–7. https://doi.org/10.1016/j.vaccine.2009.04.028.
Vigre H, Ersbøll AK, Sørensen V. Decay of Acquired Colostral Antibodies to Actinobacillus pleuropneumoniae in Pigs. J Vet Med Ser B Infect Dis Vet Public Health. 2003;50(9):430–5. https://doi.org/10.1046/j.0931-1793.2003.00700.x.
Cruijsen T, van Leengoed LAMG, Kamp EM, Bartelse A, Korevaar A, Verheijden JHM. Susceptibility to Actinobacillus pleuropneumoniae infection in pigs from an endemically infected herd is related to the presence of toxin-neutralizing antibodies. Vet Microbiol. 1995;47(3–4):219–28. https://doi.org/10.1016/0378-1135(95)00109-3.
Morris CR, Gardner IA, Hietala SK, Carpenter TE, Anderson RJ, Parker KM. Persistence of passively acquired antibodies to Mycoplasma hyopneumoniae in a swine herd. Prev Vet Med. 1994;21(1):29–41. https://doi.org/10.1016/0167-5877(94)90030-2.
Feng H, Segalés J, Fraile L, López-Soria S, Sibila M. Effect of high and low levels of maternally derived antibodies on porcine circovirus type 2 (PCV2) infection dynamics and production parameters in PCV2 vaccinated pigs under field conditions. Vaccine. 2016;34(27):3044–50. https://doi.org/10.1016/j.vaccine.2016.04.088.
Gava D, Souza CK, Mores TJ, Argenti LE, Streck AF, Canal CW, Bortolozzo FP, Wentz I. Dynamics of vanishing of maternally derived antibodies of Ungulate protoparvovirus 1 suggests an optimal age for gilts vaccination. Trop Anim Health Prod. 2017;49(5):1085–8. https://doi.org/10.1007/s11250-017-1301-0.
Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC, Sornsen SA, Thacker EL. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol. 2006;112(3–4):117–28. https://doi.org/10.1016/j.vetimm.2006.02.008.
Pomorska-Mól M, Markowska-Daniel I. Interferon-γ secretion and proliferative responses of peripheral blood mononuclear cells after vaccination of pigs against Aujeszky’s disease in the presence of maternal immunity. FEMS Immunol Med Microbiol. 2010;58(3):405–11. https://doi.org/10.1111/j.1574-695X.2010.00651.x.
Suradhat S, Damrongwatanapokin S, Thanawongnuwech R. Factors critical for successful vaccination against classical swine fever in endemic areas. Vet Microbiol. 2007;119(1):1–9. https://doi.org/10.1016/j.vetmic.2006.10.003.
Curtis J, Bourne FJ. Immunoglobulin quantitation in sow serum, colostrum and milk and the serum of young pigs. BBA Protein Struct. 1971;236(1):319–32. https://doi.org/10.1016/0005-2795(71)90181-4.
Dvorak CMT, Payne BJ, Seate JL, Murtaugh MP. Effect of maternal antibody transfer on antibody dynamics and control of porcine Circovirus type 2 infection in offspring. Viral Immunol. 2017;31(1):40–6. https://doi.org/10.1089/vim.2017.0058.
Magnusson U, Rodriguez-Martinez H, Einarsson S. A simple, rapid method for differential cell counts in porcine mammary secretions. Vet Rec. 1991;129(22):485–90. https://doi.org/10.1136/vr.129.22.485.
Biebaut E, Beuckelaere L, Boyen F, Haesebrouck F, Gomez-Duran CO, Devriendt B, Maes D. Transfer of Mycoplasma hyopneumoniae-specific cell mediated immunity to neonatal piglets. Vet Res. 2021;52(1):96. https://doi.org/10.1186/S13567-021-00968-0.
Hlavova K, Stepanova H, Faldyna M. The phenotype and activation status of T and NK cells in porcine colostrum suggest these are central/effector memory cells. Vet J (London, England: 1997). 2014;202(3):477–82. https://doi.org/10.1016/J.TVJL.2014.09.008.
Oh Y, Seo HW, Han K, Park C, Chae C. Protective effect of the maternally derived porcine circovirus type 2 (PCV2)-specific cellular immune response in piglets by dam vaccination against PCV2 challenge. J Gen Virol. 2012;93(Pt 7):1556–62. https://doi.org/10.1099/vir.0.041749-0.
Oliver-Ferrando S, Segalés J, Sibila M, Díaz I. Comparison of cytokine profiles in peripheral blood mononuclear cells between piglets born from Porcine circovirus 2 vaccinated and non-vaccinated sows. Vet Microbiol. 2018;214:148–53. https://doi.org/10.1016/j.vetmic.2017.12.011.
Nechvatalova K, Kudlackova H, Leva L, Babickova K, Faldyna M. Transfer of humoral and cell-mediated immunity via colostrum in pigs. Vet Immunol Immunopathol. 2011;142(1–2):95–100. https://doi.org/10.1016/j.vetimm.2011.03.022.
Nguyen TV, Yuan L, Azevedo MSP, Jeong K-I, Gonzalez A-M, Saif LJ. Transfer of maternal cytokines to suckling piglets: in vivo and in vitro models with implications for immunomodulation of neonatal immunity. Vet Immunol Immunopathol. 2007;117:236–48. https://doi.org/10.1016/j.vetimm.2007.02.013.
Butler JE, Sun J, Weber P, Navarro P, Francis D. Antibody repertoire development in fetal and newborn piglets, III. Colonization of the gastrointestinal tract selectively diversifies the preimmune repertoire in mucosal lymphoid tissues. Immunology. 2000;100(1):119–30. https://doi.org/10.1046/J.1365-2567.2000.00013.X.
Talker SC, Käser T, Reutner K, Sedlak C, Mair KH, Koinig H, Graage R, Viehmann M, Klingler E, Ladinig A, Ritzmann M, Saalmüller A, Gerner W. Phenotypic maturation of porcine NK- and T-cell subsets. Dev Comp Immunol. 2013;40(1):51–68. https://doi.org/10.1016/j.dci.2013.01.003.
Salmon H. Immunité chez le foetus et le nouveau-né : modèle porcin Immunité chez le foetus et le nouveau-né: modèle porcin summary. Immunity of the fetus and the newborn: a porcine model. Reproduction Nutrition Développement. 1984;24(2):197–206.
Tuboly S, Bernáth S, Glávits R, Medveczky I. Intestinal absorption of colostral lymphoid cells in newborn piglets. Vet Immunol Immunopathol. 1988;20(1):75–85. https://doi.org/10.1016/0165-2427(88)90027-X.
Williams PP. Immunomodulating effects of intestinal absorbed maternal colostral leukocytes by neonatal pigs. Can J Vet Res. 1993;57(1):1–8.
Bandrick M, Pieters M, Pijoan C, Baidoo SK, Molitor TW. Papers: effect of cross-fostering on transfer of maternal immunity to Mycoplasma hyopneumoniae to piglets. Vet Record. 2011;168(4):100. https://doi.org/10.1136/vr.c6163.
Jensen PT. Trypsin inhibitor in sow colostrum and its function. In INRA editions, vol 9, Issue 2; 1978. https://hal.archives-ouvertes.fr/hal-00900993.
Bush LJ, Staley TE. Absorption of colostral immunoglobulins in newborn calves. J Dairy Sci. 1980;63(4):672–80. https://doi.org/10.3168/jds.S0022-0302(80)82989-4.
Cervenak J, Kacskovics I. The neonatal Fc receptor plays a crucial role in the metabolism of IgG in livestock animals. Vet Immunol Immunopathol. 2009;128(1–3):171–7. https://doi.org/10.1016/J.VETIMM.2008.10.300.
Leary HL, Lecce JG. Uptake of macromolecules by enterocytes on transposed and isolated piglet small intestine. J Nutr. 1976;106(3):419–27. https://doi.org/10.1093/jn/106.3.419.
Pácha J. Development of intestinal transport function in mammals. In Physiological reviews, vol 80, Issue 4. American Physiological Society; 2000. p. 1633–1667. https://doi.org/10.1152/physrev.2000.80.4.1633.
Murata H, Namioka S. The duration of colostral immunoglobulin uptake by the epithelium of the small intestine of neonatal piglets. J Comp Pathol. 1977;87(3):431–9. https://doi.org/10.1016/0021-9975(77)90032-9.
Moog F. Endocrine influences on the functional differentiation of the small intestine. J Anim Sci. 1979;49(1):239–49. https://doi.org/10.2527/jas1979.491239x.
Smith MW, Jarvis LG. Growth and cell replacement in the new-born pig intestine. Proc Roy Soc Lond Biol Sci. 1978;203(1150):69–89. https://doi.org/10.1098/rspb.1978.0092.
Watson DL. Immunological functions of the mammary gland and its secretion-comparative review. Aust J Biol Sci. 1980;33(4):403–22. https://doi.org/10.1071/BI9800403.
Wilson AD, Stokes CR, Bourne FJ. Effect of age on absorption and immune responses to weaning or introduction of novel dietary antigens in pigs. Res Vet Sci. 1989;46(2):180–6. https://doi.org/10.1016/s0034-5288(18)31142-1.
Nielsen R. Detection of antibodies against Actinobacillus pleuropneumoniae, serotype 2 in porcine colostrum using a blocking enzyme-linked immunosorbent assay specific for serotype 2. Vet Microbiol. 1995;43(4):277–81. https://doi.org/10.1016/0378-1135(94)00112-A.
Sibila M, Fraile L, Ticó G, López-Soria S, Nofrarías M, Huerta E, Llorens A, López-Jiménez R, Pérez D, Segalés J. Humoral response and colostral antibody transfer following “one-dose” pre-mating vaccination of sows against porcine circovirus type-2. Vet J (London, England: 1997). 2013;197(3):881–3. https://doi.org/10.1016/j.tvjl.2013.04.014.
Song Q, Stone S, Drebes D, Greiner LL, Dvorak CMT, Murtaugh MP. Characterization of anti-porcine epidemic diarrhea virus neutralizing activity in mammary secretions. Virus Res. 2016;226:85–92. https://doi.org/10.1016/J.VIRUSRES.2016.06.002.
Christopher-Hennings J, Erickson GA, Hesse RA, Nelson EA, Joy Scaria SR, Slavic D. Diagnostic tests, test performance, and considerations for interpretation. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J, editors. Diseases of Swine. 11th ed. Wiley; 2019. p. 75–97.
Hernandez-Garcia J, Robben N, Magnée D, Eley T, Dennis I, Kayes SM, Thomson JR, Tucker AW. The use of oral fluids to monitor key pathogens in porcine respiratory disease complex. Porcine Health Manag. 2017. https://doi.org/10.1186/S40813-017-0055-4.
Turlewicz-Podbielska H, Włodarek J, Pomorska-Mól M. Noninvasive strategies for surveillance of swine viral diseases: a review. J Vet Diagnost Investig. 2020;32(4):503–12. https://doi.org/10.1177/1040638720936616.
Siegrist CA. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine. 2003;21(24):3406–12. https://doi.org/10.1016/S0264-410X(03)00342-6.
Wilson HL, Obradovic MR. Evidence for a common mucosal immune system in the pig. Mol Immunol. 2015;66(1):22–34. https://doi.org/10.1016/J.MOLIMM.2014.09.004.
Kim J, Kim T, Hong J-K, Lee H-S, Lee K-N, Jo HJ, Choi J, Choi J, Lee SH, Lee M-H, Kim B, Park J-H. The interference effect of maternally-derived antibodies on the serological performance of pigs immunized with a foot-and-mouth disease oil emulsion vaccine. Vaccine. 2020;38(7):1723–9. https://doi.org/10.1016/J.VACCINE.2019.12.043.
Martelli P, Saleri R, Ferrarini G, de Angelis E, Cavalli V, Benetti M, Ferrari L, Canelli E, Bonilauri P, Arioli E, Caleffi A, Nathues H, Borghetti P. Impact of maternally derived immunity on piglets’ immune response and protection against porcine circovirus type 2 (PCV2) after vaccination against PCV2 at different age. BMC Vet Res. 2016;12:77. https://doi.org/10.1186/s12917-016-0700-1.
Pyo HM, Hlasny M, Zhou Y. Influence of maternally-derived antibodies on live attenuated influenza vaccine efficacy in pigs. Vaccine. 2015;33(31):3667–72. https://doi.org/10.1016/J.VACCINE.2015.06.044.
Poulsen B, van Vlaenderen I, Mah C, Angulo J. Do high levels of maternally derived antibodies interfere with the vaccination of piglets against porcine circovirus type 2? A literature review and data analysis. Vaccines. 2021;9(8):923. https://doi.org/10.3390/VACCINES9080923.
Mancera Gracia JC, Pearce DS, Masic A, Balasch M. Influenza A virus in Swine: epidemiology, challenges and vaccination strategies. Front Vet Sci. 2020;7:647. https://doi.org/10.3389/fvets.2020.00647.
Simon-Grifé M, Martín-Valls GE, Vilar MJ, Busquets N, Mora-Salvatierra M, Bestebroer TM, Fouchier RA, Martín M, Mateu E, Casal J. Swine influenza virus infection dynamics in two pig farms; results of a longitudinal assessment. Vet Res. 2012;43(1):24. https://doi.org/10.1186/1297-9716-43-24.
Loeffen WLA, Heinen PP, Bianchi ATJ, Hunneman WA, Verheijden JHM. Effect of maternally derived antibodies on the clinical signs and immune response in pigs after primary and secondary infection with an influenza H1N1 virus. Vet Immunol Immunopathol. 2003;92(1–2):23–35. https://doi.org/10.1016/S0165-2427(03)00019-9.
Cador C, Hervé S, Andraud M, Gorin S, Paboeuf F, Barbier N, Quéguiner S, Deblanc C, Simon G, Rose N. Maternally-derived antibodies do not prevent transmission of swine influenza A virus between pigs. Vet Res. 2016;47(1):86. https://doi.org/10.1186/s13567-016-0365-6.
Markowska-Daniel I, Pomorska-Mól M, Pejsak Z. The influence of age and maternal antibodies on the postvaccinal response against swine influenza viruses in pigs. Vet Immunol Immunopathol. 2011;142(1–2):81–6. https://doi.org/10.1016/j.vetimm.2011.03.019.
Rajao DS, Sandbulte MR, Gauger PC, Kitikoon P, Platt R, Roth JA, Perez DR, Loving CL, Vincent AL. Heterologous challenge in the presence of maternally-derived antibodies results in vaccine-associated enhanced respiratory disease in weaned piglets. Virology. 2016;491:79–88. https://doi.org/10.1016/J.VIROL.2016.01.015.
Rose N, Hervé S, Eveno E, Barbier N, Eono F, Dorenlor V, Andraud M, Camsusou C, Madec F, Simon G. Dynamics of influenza a virus infections in permanently infected pig farms: evidence of recurrent infections, circulation of several swine influenza viruses and reassortment events. Vet Res. 2013;44:1. https://doi.org/10.1186/1297-9716-44-72.
Nathues H, Alarcon P, Rushton J, Jolie R, Fiebig K, Jimenez M, Geurts V, Nathues C. Cost of porcine reproductive and respiratory syndrome virus at individual farm level—an economic disease model. Prev Vet Med. 2017;142:16–29. https://doi.org/10.1016/J.PREVETMED.2017.04.006.
Fablet C, Renson P, Eono F, Mahé S, Eveno E, le Dimna M, Normand V, Lebret A, Rose N, Bourry O. Maternally-derived antibodies (MDAs) impair piglets’ humoral and cellular immune responses to vaccination against porcine reproductive and respiratory syndrome (PRRS). Vet Microbiol. 2016;192:175–80. https://doi.org/10.1016/j.vetmic.2016.07.014.
Chung WB, Lin MW, Chang WF, Hsu M, Yang PC. Persistence of porcine reproductive and respiratory syndrome virus in intensive farrow-to-finish pig herds. Can J Vet Res. 1997;61(4):292–8.
Stevenson GW, van Alstine WG, Kanitz CL, Keffaber KK. Brief communications: endemic porcine reproductive and respiratory syndrome virus infection of nursery pigs in two swine herds without current reproductive failure. J Vet Diagn Invest. 1993;5(3):432–4. https://doi.org/10.1177/104063879300500322.
Pileri E, Mateu E. Review on the transmission porcine reproductive and respiratory syndrome virus between pigs and farms and impact on vaccination. Vet Res. 2016;47(1):1–13. https://doi.org/10.1186/S13567-016-0391-4.
Lopez OJ, Oliveira MF, Garcia EA, Kwon BJ, Doster A, Osorio FA. Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin Vaccine Immunol. 2007;14(3):269–75. https://doi.org/10.1128/CVI.00304-06.
Loving CL, Osorio FA, Murtaugh MP, Zuckermann FA. Innate and adaptive immunity against porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol. 2015;167(1–2):1–14. https://doi.org/10.1016/J.VETIMM.2015.07.003.
Albina E, Madec F, Cariolet R, Torrison J. Immune response and persistence of the porcine reproductive and respiratory syndrome virus in infected pigs and farm units. Vet Rec. 1994;134(22):567–73. https://doi.org/10.1136/VR.134.22.567.
Balasch M, Fort M, Taylor LP, Calvert JG. Vaccination of 1-day-old pigs with a porcine reproductive and respiratory syndrome virus (PRRSV) modified live attenuated virus vaccine is able to overcome maternal immunity. Porcine Health Manag. 2018;4(1):1–11. https://doi.org/10.1186/s40813-018-0101-x.
Dee SA, Morrison RB, Joo H. Eradicating porcine reproductive and respiratory syndrome (PRRS) virus using two-site production and nursery depopulation. Swine Health Prod. 1993;1:20–3.
Houben S, van Reeth K, Pensaert MB. Pattern of infection with the porcine reproductive and respiratory syndrome virus on Swine farms in Belgium. J Vet Med. 1995;42:209–2015.
Nodelijk G, van Leegoed LAMG, Schoevers EJ, Korese AH, de Jong MCM, Wensvoort G, Verheijden JHM. Seroprevalence of porcine reproductive and respiratory syndrome virus in Dutch weaning pigs. Vet Microbiol. 1997;56:21–32.
Renson P, Fablet C, Andraud M, Normand V, Lebret A, Paboeuf F, Rose N, Bourry O. Maternally-derived neutralizing antibodies reduce vaccine efficacy against porcine reproductive and respiratory syndrome virus infection. Vaccine. 2019;37(31):4318–24. https://doi.org/10.1016/j.vaccine.2019.06.045.
Jeong J, Kim S, Park KH, Kang I, Park SJ, Yang S, Oh T, Chae C. Vaccination with a porcine reproductive and respiratory syndrome virus vaccine at 1-day-old improved growth performance of piglets under field conditions. Vet Microbiol. 2018;214:113–24. https://doi.org/10.1016/j.vetmic.2017.12.023.
Allan GM, McNeilly F, Kennedy S, Daft B, Clarke EG, Ellis JA, Haines DM, Meehan BM, Adair BM. Isolation of porcine circovirus-like viruses from pigs with a wasting disease in the USA and Europe. J Vet Diagn Invest. 1998;10(1):3–10. https://doi.org/10.1177/104063879801000102.
Chae C. A review of porcine circovirus 2-associated syndromes and diseases. Vet J. 2005;169(3):326–36. https://doi.org/10.1016/j.tvjl.2004.01.012.
Pejsak Z, Kusior G, Pomorska-Mól M, Podgórska K. Influence of long-term vaccination of a breeding herd of pigs against PCV2 on reproductive parameters. Pol J Vet Sci. 2012;15(1):37–42. https://doi.org/10.2478/v10181-011-0111-y.
Segalés J. Circovirosis porcina. Guía de Enfermedades Porcinas figura. 2019;2:1–30.
Segalés J, Domingo M. Postweaning multisystemic wasting syndrome (PMWS) in pigs. A review. Vet Quart. 2002;24(3):109–24. https://doi.org/10.1080/01652176.2002.9695132.
Allan G, McNeilly F, McNair I, Meehan B, Marshall M, Ellis J, Lasagna C, Boriosi G, Krakowka S, Reynaud G, Boeuf-Tedeschi L, Bublot M, Charreyre C. Passive transfer of maternal antibodies to PCV2 protects against development of post-weaning multisystemic wasting syndrome (PMWS): experimental infections and a field study. Pig J. 2002;50:59–67.
Calsamiglia M, Fraile L, Espinal A. Sow porcine circovirus (PCV2) status effect on litter mortality in postweaning multisystemic wasting syndrome (PMWS). Res Vet Sci. 2007;82:299–304.
Shen H, Wang C, Madson D, Opriessnig T. High prevalence of porcine circovirus viremia in newborn piglets in five clinically normal swine breeding herds in North America. Prev Vet Med. 2010;97(3–4):228–36. https://doi.org/10.1016/J.PREVETMED.2010.09.020.
Sibila M, Calsamiglia M, Segalés J, Blanchard P, Badiella L, le Dimna M, Jestin A, Domingo M. Use of a polymerase chain reaction assay and an ELISA to monitor porcine circovirus type 2 infection in pigs from farms with and without postweaning multisystemic wasting syndrome. Am J Vet Res. 2004;65(1):88–92. https://doi.org/10.2460/AJVR.2004.65.88.
Fachinger V, Bischoff R, Jedidia S, Saalmüller A, Elbers K. The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex. Vaccine. 2008;26(11):1488–99. https://doi.org/10.1016/j.vaccine.2007.11.053.
Kiss J, Szigeti K, Homonnay Z, Tamás V, Smits H, Krejci R. Maternally derived antibody levels influence on vaccine protection against PCV2d challenge. Animals. 2021;11:8. https://doi.org/10.3390/ANI11082231.
Martelli P, Ferrari L, Morganti M, de Angelis E, Bonilauri P, Guazzetti S, Caleffi A, Borghetti P. One dose of a porcine circovirus 2 subunit vaccine induces humoral and cell-mediated immunity and protects against porcine circovirus-associated disease under field conditions. Vet Microbiol. 2011;149(3–4):339–51. https://doi.org/10.1016/j.vetmic.2010.12.008.
Opriessnig T, Patterson AR, Elsener J, Meng XJ, Halbur PG. Influence of maternal antibodies on efficacy of porcine circovirus type 2 (PCV2) vaccination to protect pigs from experimental infection with PCV2. Clin Vaccine Immunol. 2008;15(3):397–401. https://doi.org/10.1128/CVI.00416-07.
Fraile L, Grau-Roma L, Sarasola P, Sinovas N, Nofrarías M, López-Jimenez R, López-Soria S, Sibila M, Segalés J. Inactivated PCV2 one shot vaccine applied in 3-week-old piglets: improvement of production parameters and interaction with maternally derived immunity. Vaccine. 2012;30(11):1986–92. https://doi.org/10.1016/j.vaccine.2012.01.008.
Fraile L, Sibila M, Nofrarías M, López-Jimenez R, Huerta E, Llorens A, López-Soria S, Pérez D, Segalés J. Effect of sow and piglet porcine circovirus type 2 (PCV2) vaccination on piglet mortality, viraemia, antibody titre and production parameters. Vet Microbiol. 2012;161(1–2):229–34. https://doi.org/10.1016/j.vetmic.2012.07.021.
Haake M, Palzer A, Rist B, Weissenbacher-Lang C, Fachinger V, Eggen A, Ritzmann M, Eddicks M. Influence of age on the effectiveness of PCV2 vaccination in piglets with high levels of maternally derived antibodies. Vet Microbiol. 2014;168(2–4):272–80. https://doi.org/10.1016/j.vetmic.2013.11.012.
Figueras-Gourgues S, Fraile L, Segalés J, Hernández-Caravaca I, López-Úbeda R, García-Vázquez FA, Gomez-Duran O, Grosse-Liesner B. Effect of Porcine circovirus 2 (PCV-2) maternally derived antibodies on performance and PCV-2 viremia in vaccinated piglets under field conditions. Porcine Health Manag. 2019;5:1. https://doi.org/10.1186/s40813-019-0128-7.
Opriessnig T, Giménez-Lirola LG, Halbur PG. Polymicrobial respiratory disease in pigs. Anim Health Res Rev. 2011;12(2):133–48. https://doi.org/10.1017/s1466252311000120.
Pieters M, Maes D. Mycoplasmosis. In: Zimmerman J, Karriker J, Ramirez L, Schwartz A, Stevenson K, Zhang G, editors. Diseases of Swine. 11th ed. Wiley; 2019. p. 863–83.
Pieters M, Pijoan C, Fano E, Dee S. An assessment of the duration of Mycoplasma hyopneumoniae infection in an experimentally infected population of pigs. Vet Microbiol. 2009;134(3–4):261–6. https://doi.org/10.1016/j.vetmic.2008.08.016.
Fano E, Pijoan C, Dee S, Deen J. Effect of Mycoplasma hyopneumoniae colonization at weaning on disease severity in growing pigs. Can Vet J Res. 2007;71:195–200.
Sibila M, Nofarías M, López-Soria S, Segalés J, Valero O, Espinal A, Calsamiglia M. Chronological study of Mycoplasma hyopneumoniae infection, seroconversion and associated lung lesions in vaccinated and non-vaccinated pigs. Vet Microbiol. 2007;122:97–107.
Arsenakis I, Michiels A, Schagemann G, Gomez-Duran CO, Boyen F, Haesebrouck F, Maes DGD. Effects of pre-farrowing sow vaccination against Mycoplasma hyopneumoniae on offspring colonisation and lung lesions. Vet Rec. 2019;184(7):222. https://doi.org/10.1136/vr.104972.
Ruiz A, Utrera V, Pijoan C. Effect of Mycoplasma hyopneumoniae sow vaccination on piglet colonization at weaning. J Swine Health Prod. 2003;11:131–5.
Sibila M, Bernal R, Torrents D, Riera P, Llopart D, Calsamiglia M, Segalés J. Effect of sow vaccination against Mycoplasma hyopneumoniae on sow and piglet colonization and seroconversion, and pig lung lesions at slaughter. Vet Microbiol. 2008;127(1–2):165–70. https://doi.org/10.1016/j.vetmic.2007.07.027.
Martelli P, Terreni M, Guazzetti S, Cavirani S. Antibody response to Mycoplasma hyopneumoniae infection in vaccinated pigs with or without maternal antibodies induced by sow vaccination. J Vet Med Ser B Infect Dis Vet Public Health. 2006;53(5):229–33. https://doi.org/10.1111/j.1439-0450.2006.00952.x.
Maes D, Sibila M, Kuhnert P, Segalés J, Haesebrouck F, Pieters M. Update on Mycoplasma hyopneumoniae infections in pigs: knowledge gaps for improved disease control. Transbound Emerg Dis. 2018;65:110–24. https://doi.org/10.1111/tbed.12677.
Wilson S, van Brussel L, Saunders G, Runnels P, Taylor L, Fredrickson D, Salt J. Vaccination of piglets up to 1 week of age with a single-dose Mycoplasma hyopneumoniae vaccine induces protective immunity within 2 weeks against virulent challenge in the presence of maternally derived antibodies. Clin Vaccine Immunol. 2013;20(5):720. https://doi.org/10.1128/CVI.00078-13.
Hodgins D, Shewen P, Dewey C. Influence of age and maternal antibodies on antibody responses of neonatal piglets vaccinated against Mycoplasma hyopneumoniae. J Swine Health Prod. 2004;12:10–6.
Bandrick M, Theis K, Molitor TW. Maternal immunity enhances Mycoplasma hyopneumoniae vaccination induced cell-mediated immune responses in piglets. BMC Vet Res. 2014. https://doi.org/10.1186/1746-6148-10-124.
Grosse-Beilage E, Screiber A. Vaccination of sows against Mycoplasma hyopneumoniae with hyoresp. Dtsch Tierarztl Wochenschr. 2005;112:256–61.
Maes D, Deluyker H, Verdonck M, Castryck F, Miry C, Lein A, Vrijens B, de Kruif A. The effect of vaccination against Mycoplasma hyopneumoniae in pig herds with a continuous production system. J Vet Med. 1998;45:495–5050.
Reynolds SC, St Aubin LB, Sabbadini LG, Kula J, Vogelaar J, Runnels P, Peters AR. Reduced lung lesions in pigs challenged 25 weeks after the administration of a single dose of Mycoplasma hyopneumoniae vaccine at approximately 1 week of age. Vet J. 2009;181(3):312–20. https://doi.org/10.1016/j.tvjl.2008.03.012.
Sassu EL, Bossé JT, Tobias TJ, Gottschalk M, Langford PR, Hennig-Pauka I. Update on Actinobacillus pleuropneumoniae—knowledge, gaps and challenges. Transbound Emerg Dis. 2018;65:72–90. https://doi.org/10.1111/tbed.12739.
Sibila M, Aragón V, Fraile L, Segalés J. Comparison of four lung scoring systems for the assessment of the pathological outcomes derived from Actinobacillus pleuropneumoniae experimental infections. BMC Vet Res. 2014. https://doi.org/10.1186/1746-6148-10-165.
Gottschalk M, Broes A. Actinobacillosis. In: Zimmerman J, Karriker J, Ramirez L, Schwarts A, Stevenson K, Zhang G, editors. Diseases of Swine. 11th ed. Wiley; 2019. p. 749–66.
Tobias TJ, Bouma A, van den Broek J, van Nes A, Daemen AJJM, Wagenaar JA, Stegeman JA, Klinkenberg D. Transmission of Actinobacillus pleuropneumoniae among weaned piglets on endemically infected farms. Prev Vet Med. 2014;117(1):207–14. https://doi.org/10.1016/j.prevetmed.2014.07.017.
Savoye C, Jobert JL, Berthelot-Hérault F, Keribin AM, Cariolet R, Morvan H, Madec F, Kobisch M. A PCR assay used to study aerosol transmission of Actinobacillus pleuropneumoniae from samples of live pigs under experimental conditions. Vet Microbiol. 2000;73(4):337–47. https://doi.org/10.1016/S0378-1135(00)00181-4.
Chiers K, Donné E, van Overbeke I, Ducatelle R, Haesebrouck F. Actinobacillus pleuropneumoniae infections in closed swine herds: infection patterns and serological profiles. Vet Microbiol. 2002;85(4):343–52. https://doi.org/10.1016/S0378-1135(01)00518-1.
Jirawattanapong P, Stockhofe-Zurwieden N, van Leengoed L, Binnendijk G, Wisselink HJ, Raymakers R, Cruijsen T, van der Peet-Schwering C, van Nes A, Nielen M. Efficacy of a subunit vaccine against Actinobacillus pleuropneumoniae in an endemically infected swine herd. J Swine Health Prod. 2008;16(4):193–9.
Sjölund M, Zoric M, Persson M, Karlsson G, Wallgren P. Disease patterns and immune responses in the offspring to sows with high or low antibody levels to Actinobacillus pleuropneumoniae serotype 2. Res Vet Sci. 2011;91(1):25–31. https://doi.org/10.1016/j.rvsc.2010.07.025.
Kristensen CS, Andreasen M, Ersbøoll AK, Nielsen JP. Antibody response in sows and piglets following vaccination against Mycoplasma hyopneumoniae, toxigenic Pasteurella multocida, and Actinobacillus pleuropneumoniae. Can J Vet Res. 2004;68(1):66.
Vigre H, Angen Ø, Barfod K, Lavritsen DT, Sørensen V. Transmission of Actinobacillus pleuropneumoniae in pigs under field-like conditions: emphasis on tonsillar colonisation and passively acquired colostral antibodies. Vet Microbiol. 2002;89(2–3):151–9. https://doi.org/10.1016/S0378-1135(02)00149-9.
Krejci J, Nechvatalova K, Kudlackova H, Faldyna M, Kucerova Z, Toman M. Systemic and Local Antibody Responses after experimental infection with actinobacillus pleuropneumoniae in piglets with passive or active immunity. J Vet Med Ser B. 2005;52(4):190–6. https://doi.org/10.1111/J.1439-0450.2005.00844.X.
Tumamao JQ, Bowles RE, van den Bosch H, Klaasen H, Fenwick BW. An evaluation of the role of antibodies to Actinobacillus pleuropneumoniae serovar 1 and 15 in the protection provided by sub-unit and live streptomycin-dependent pleuropneumonia vaccines. Aust Vet J. 2004;82:773–80.
Kraft C, Hennies R, Dreckmann K, Noguera M, Rathkjen PH, Gassel M, Gereke M. Evaluation of PRRSv specific, maternally derived and induced immune response in Ingelvac PRRSFLEX EU vaccinated piglets in the presence of maternally transferred immunity. PLoS ONE. 2019;14(10): e0223060. https://doi.org/10.1371/journal.pone.0223060.
Núria Martínez is holder of an Industrial Doctorat grant from the Catalan Government (Spain), with the reference No. 2020 DI 59.
IRTA-CReSA funds are partially supported by the CERCA program from the Generalitat de Catalunya.
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Martínez-Boixaderas, N., Garza-Moreno, L., Sibila, M. et al. Impact of maternally derived immunity on immune responses elicited by piglet early vaccination against the most common pathogens involved in porcine respiratory disease complex. Porc Health Manag 8, 11 (2022). https://doi.org/10.1186/s40813-022-00252-3