Focusing on the case law developed by the Court of Justice of the European Union since Van Gend en Loos, this article contends that three important shifts occurred concerning the effects of EU law in national courts since that case was decided. First, the existence of a particular category of (“direct effect”) EU norms, which implies a process of selection among EU law provisions, is no longer as problematic as the method of comparison and combination of norms in judicial reasoning that has become a vehicle for the penetration of EU law in courts. Second, the possibility for individuals to claim (subjective) rights on the basis of the Treaty is overshadowed by questions concerning obligations imposed by the Treaty on individuals, and more generally, on the methods through which this horizontal effect occurs. Third, the duty for national courts to apply EU law provisions directly (direct enforcement) is now coupled with one prior question that these courts have to address, and which has become much more sensitive than before in view of the growing centrality of fundamental rights’ protection in the EU system: the question of the applicability of EU and national (constitutional) law. Having examined these three shifts, the article concludes that it has become urgent to reconsider the effects of EU law in member states in order to avoid a decline of individual rights and freedoms resulting from EU law enforcement. Thus, “Revisiting Van Gend en Loos” leads to a reflection on the hypothesis, in which EU law should yield and national courts should be granted more discretion, when confronted with the resisting substance of national law (especially fundamental rights or freedoms protected by national constitutions).
No account of the development European Law misses the reference to Van Gend en Loos. This is not because the facts are exciting, captivating, or memorable: who would enjoy recounting the facts in Van Gend en Loos? Nor is it because the case addressed a cause, a socially sensitive issue. Rather, the reason for all this attention is because the European Court of Justice (ECJ) named and shaped a “new legal order,” which can still be characterized by “the direct effect of a whole series of provisions which are applicable to their nationals and to the Member States themselves.”1 For that reason, the decision is considered a moment of “passage,” one of these turning points that marked the history of European legal and political integration.2 Combined with Costa v. E.N.E.L.3 and the principle of primacy, Van Gend en Loos has allowed a considerable expansion of EU law effects, in national courts, an evolution that was fostered by the dialogue between these courts and the ECJ, through the channel of preliminary ruling.4
But what is the significance of the decision today? To be sure, the doctrine of “direct effect,” as affirmed in the decision, remains a powerful instrument through which EU law penetrates national legal systems. And the effectiveness of European treaties’ provisions owes a lot to the role assigned to national courts in the “new legal order” of the European Community (EC), namely to protect individual rights conferred by the treaty.
However, EU law has evolved in so many different ways since Van Gend en Loos was decided, and the “transformation of Europe”5 has been so profound, that one may doubt that the case can be of any help to face today’s challenges concerning the effects of EU law in national courts. To be sure, the doctrine of direct effect has not been called into question: it remains true, and it is an essential feature of the EU legal order, that some provisions of EU law can be relied on in national courts to claim subjective rights. But the effects of EU law in national courts have diversified and grown more complex to such an extent that Van Gend en Loos seems to grasp only a thin fragment of EU law enforcement issues. It seems, rather, that Van Gend en Loos no longer gives an accurate idea of the ways through which EU law penetrates member states through its enforcement in national courts. And it would be an error, I believe, to cling too rigidly to its doctrine, in trying to address the new challenges that the evolution of EU law has created.
The approach taken in this paper focuses on the case law developed by the ECJ. It is, indeed, a narrow angle: it looks at one particular scene, on which EU law is expressed, and developed, as if it could be isolated from the other “sources” of law development. Of course, I do not pretend that analyzing the court’s discourse and, in particular, the departures from expected repetitions and the moments when improvization occurs, thus making change possible, can be properly done without taking into account elements of legal, social, or political context. However, because the purpose of this reflection is to revisit a case decided by the ECJ fifty years ago, the choice to focus mainly on case law, existing and prospective, seems appropriate.
When I started to reconsider Van Gend en Loos, I asked myself the following question: what would be today’s version of that case? Or, rather, what situation(s), involving the effects of EU law in national courts, would be as challenging for the ECJ today as Van Gend en Loos was, in its time? The answer, I believe, is that the Court of Justice would have to rule in a case, or a series of cases, that would be substantially different from Van Gend en Loos. Three important shifts would characterize the action(s) before a national court as compared to the situation in Van Gend en Loos. First, the claim would be based, not on one particular provision of the Treaty on EU (TEU) or the Treaty on the Functioning of the European Union (TFEU) which satisfies the conditions to be given direct effect, but rather on a combination of norms, regardless of their respective direct effect. Second, instead of involving an individual requesting the benefit of a provision of the Treaty, the action would challenge an obligation imposed by the Treaty on a private actor, not the state, or contest a coercive measure applied to an individual, on the basis of EU law: the effects of the Treaty would be contested, not requested. Lastly, the case would imply a prior question on the applicability of the primary law. More precisely, the CJEU would be questioned on the applicability of the Charter of Fundamental Rights to the situation before it, and would have to consider, at the same time, the possibility for a national court to enforce fundamental rights protected by the constitution of the member state to which the court belongs.
Imagining in detail this abstract case is not the purpose of this article. But sketching out the kind of situations that are most problematic allows us to shed light on three essential outcomes of Van Gend en Loos that no longer constitute the major challenges concerning EU law enforcement in national courts: the existence of a particular category of (“direct effect”) EU norms, which implies a process of selection among EU law provisions; the possibility for individuals to claim (subjective) rights on the basis of the treaty; and the duty for national courts to apply EU law provisions directly (direct enforcement). That triad (selection, rights, application) has lost most of its mystery. As far as selection of direct effect norms is concerned, uncertainties have been reduced to a minimum. To be sure, not all questions on that matter have vanished in the course of EU law evolution, but they are somehow overshadowed by a phenomenon that Van Gend en Loos had ignored: comparison and combination of norms in judicial reasoning. Concerning subjective rights, without denying the fact that individuals have, since Van Gend en Loos, gained new rights from the treaty, and from other sources of EU law, there is more to say, today, on the obligations imposed by the Treaty on individuals, and more generally, on the methods through which this horizontal effect occurs (or does not occur). Lastly, the duty of national courts to apply EU law—the enduring importance of that function assigned to national courts—is now coupled with one prior question that these courts have to address, and which has become much more sensitive than before in view of the growing centrality of fundamental rights’ protection in the EU system: the question of the applicability of EU and national (constitutional) law.
Thus, following Van Gend en Loos, a dialectical approach can be constructed using a series of pairs: selection–combination (of norms); (individual) rights–obligations; and application–applicability of EU law. This article intends to use these dialectic pairs, successively (Sections 2 to 4), in order to examine the new questions concerning EU law enforcement in national courts. Unsurprisingly, the conclusions of these analyses are not straightforward. On the one hand, it is quite clear that there are more opportunities than before to mobilize EU law in national courts. This confirms what has been a constant evolution since the narrow concept of “direct effect” has been extended to allow a much larger variety of claims based on EU law: new forms of invoc ability of EU law have emerged and to some extent have transformed the notion of EU law effectiveness in national courts. On the other hand, the rigor of direct effect, in its original purity, has become problematic in some particular instances. This is the case when obligations binding on individuals stem from horizontal application of provisions of primary law—in particular, free-market rules which were not meant to apply to private actors. More broadly, the effectiveness of European Union law is too simple an answer, it seems, in cases, more numerous than before, in which EU law imposes obligations or constraints on individuals, rather than states. In 2013, the power of EU law to impose transformations of national policies should not be affirmed at all costs, without consideration to the impact of EU policies on individual rights and freedoms protected by national Constitutions. That is an important matter that “revisiting Van Gend en Loos” also invites us to think about, in guise of conclusion (Section 5).
2. From selection to combination
Among the various ways in which EU law norms are invoked before national courts, there is one which contrasts sharply with the Van Gend en Loos concept of direct effect: the combination of norms emanating from different sources of law. Indeed, in some cases, it seems as if effectiveness of European law depended not on the respective legal force of the norms invoked before the court, but on the relationship that they entertain. To be sure, this phenomenon is not specific to EU law,6 but it takes on specific forms in EU law, in light of the specific system of norms of that legal order.
Van Gend en Loos implied identification by judges of EU law norms possessing direct effect: such norms could be the basis for subjective rights. The case led to distinctions among, and the constitution of, different categories of norms, depending on their capacity to produce direct effect. Although this is not coming to an end, and the taxonomic enterprise must go on, since many new provisions of EU law come to life with an uncertain nature,7 the power accorded to normative combinations has made it less important than before to ascertain the exact effect of each provision of the law.
2.1. Direct effect as a process of a selection
Van Gend en Loos raised the question whether a provision of the treaty (art. 12 TEU) could be a source of individual rights that national courts should protect. To answer this question, the Court of Justice insisted on the nature of the Community legal order, a nature justifying the capacity of provisions mentioned in the treaty to create rights and obligations for individuals, and not only for member states. At the same time, the Court clearly embraced the idea that not all treaty provisions had such effect: only under certain conditions, it indicated, can treaty provisions be invoked by individuals in national courts, in order to claim subjective rights. Since then, the Court of Justice has presided over the process of selection of direct-effect norms.
In Van Gend en Loos, the Court already mentioned the criteria to be taken into account in order to distinguish among EU law norms: to produce direct effect, the provisions concerned must be clear, precise, and unconditional. As the subsequent case law showed, these criteria were given extensive interpretation, particularly when treaty provisions were concerned, and the only true requirement became the possibility of effective enforcement, the “justiciability” of the law.8 This led, for example, to granting all free movement provisions direct effect.9
As was already mentioned, the issue of selection, i.e. the identification of directly applicable norms, is not an outdated question. The question of selection has re-emerged with great force concerning the provisions of the Charter of fundamental rights of the European Union. The distinction between “rights” and “principles” contained in that instrument resembles a modern and explicit version of the distinction among EU law provisions that was implicit in the TEU, and that the Court unveiled in Van Gend en Loos. As Advocate-General Cruz Villalón synthesized: the “principles,” in the Charter, determine the missions assigned to public authorities and are different from “rights,” the purpose of which is to protect the legal situation of individuals—a situation directly defined by the text itself.10 Public authorities, Cruz Villalón added, must respect the legal situation of individuals guaranteed by “rights,” but, as far as “principles” are concerned, their function is much more open: “principles” define not individual situations, but rather general matters and outcomes that condition the action of public authorities.11
There is a high chance that, in a number of future cases, national courts will turn to the Court of Justice to identify the Charter’s provisions which are a source of subjective rights that they have to protect. The French Cour de Cassation did exactly that, not too long ago:12 in the case of Association de médiation sociale, it questioned the Court of Justice, through the preliminary ruling procedure, on the direct effect of article 27 of the Charter.13
However, even if the identification of direct effect norms remains important, action (or defense) before national courts can also rest on a combination of legal references. Precisely this method is what Advocate-General Cruz Villalón relied on in Association de médiation sociale,14 once he had reached the conclusion that article 27 of the Charter belonged to the category of “principles” and was, on its own, deprived of direct effect.
2.2. Legal effects of normative combination
The rise of fundamental rights, which, in EU law, has been from the outset narrowly tied to the existence of a category of general principles, has shown—as has become more obvious with the Charter of Fundamental Rights—that seeking direct effect was not always the most appropriate, or the most effective, method of sustaining claims in situations covered by EU law. In comparison, normative combination could be described as a shift from application of the law to the interpretation of the law, if we set aside the fact that the two operations are tightly intertwined. Direct effect would lie on the side of “application,” where normative combination belongs to the realm of “interpretation.” Put differently, some references produce effects directly, while others are only “considered” or “taken into account” to construe other norms. Besides the fact that this does not correspond to all types of combinations that have emerged in the case law of the Court of Justice, the distinction, if any, between application and interpretation of the law is not the point I want to discuss in the following lines. What I would like to insist on, instead, is the legal force that the Court of Justice accords to different sorts of combination of norms, inasmuch as this solution differs radically from the process of selection of direct-effect norms that was the outcome of Van Gend en Loos.
To begin with, I must admit that “normative combination” is a very synthetic concept for a phenomenon including a large variety of cases, which only have in common that the solution derives from the use of a series of references, and that these references, taken separately, would be powerless. However, because what I want to show and question is the shift from direct effect to a radically different way to ensure EU law effectiveness, I am convinced that various types of combination should be mentioned. They differ according to the source of the norms combined (primary and secondary legislation; soft and hard law; and EU law, international or national law); the relationships between these norms; and the different effects produced by their interaction. To simplify, I will confine my remarks to a basic typology, distinguishing between two categories of combinations.
In the first one, all norms combined belong to EU law: a general principle or a fundamental right is coupled with a provision of derived legislation. Using such a combination, judges were able to satisfy individual claims, whereas neither of the norms, taken separately, could produce such effect.
In the more classical version of this association of norms, provisions of the Charter of Fundamental Rights, notwithstanding the uncertainty concerning their direct effect (in the language of the Charter, their identification as “rights” or “principles”) were used to interpret directives in such a way as to allow the rights to be protected by national courts to emerge. A good illustration is the Kamberaj case,15 in which the Court of Justice relied on the aim to ensure a decent existence for all those who lack sufficient resources, as defined in article 34(3) of the Charter, to decide that a third-country national should have the right to equal treatment in obtaining housing benefits, according to Directive 2003/109. Similarly, in Chatzi,16 the Court decided, referring to the “principle of equal treatment, which is one of the general principles of European Union law, and whose fundamental nature is affirmed in Article 20 of the Charter of Fundamental Rights,” that clause 2.1 of the Framework Agreement on Parental Leave17 “read in the light of the principle of equal treatment” obliges the national legislature to establish a parental leave regime which, according to the situation in the Member State concerned, ensures that the parents of twins receive treatment that takes due account of their particular needs.” It is incumbent upon national courts, the court added, to determine whether the national rules meet that requirement and, if necessary, to interpret those national rules, so far as possible, in conformity with European Union law.”18 To be sure, following Chatzi, the claim brought to court may not prove immediately successful; however, the reasoning, which relied on a combination of norms, implied that the national court and the legislator must ensure that the legitimate demand for equal treatment is satisfied.
This type of case, in which judges use fundamental rights to construe legislative provisions, is not uncommon, of course, in other legal orders. To take just one ex ample, German courts do not hesitate to resort to the German Constitution to interpret general provisions of the civil code. In a famous case, the Federal Labor Court decided that the interpretation of § 315 of the German Civil Code concerning the specification of performance by one party, and requiring that this specification be “equitable,” had to be consistent with article 4. I of the German Constitution, concerning freedom of thought. As a result, an employer was deprived of the right to oblige his employee to perform a duty conflicting with his freedom of thought (producing books glorifying war).19 In this case, as in the cases decided by the Court of Justice, the effect of fundamental rights does not depend on their direct effect, but it is the result of the interpretation of other norms, according to the doctrine of consistent interpretation.20
More original, and specific to EU law, are cases in which a directive and a general principle are combined to produce effects, the former being considered a mere “concretization” of the latter. This combination, as a method of compensating for the lack of implementation, or defective implementation, of directives, is an instrument specific to EU law that requires transposition in national law. A couple of well-known cases decided by the Court of Justice demonstrate, in particular, that derived legislation gains force when it can be considered as implementing a general principle of law or fundamental rights. In Mangold21 and Kücükdeveci,22 quite remarkably, the general principle of non-discrimination compensates for the absence of horizontal direct effect of Directive 2000/78/EC on Equal Treatment in Employment and Occupation.23 Conversely, the directive is necessary because the jurisdiction of EU law—and the applicability of the general principle in a given case—depends on it. The outcome of this clever duo, as the Court pointed out in Kücükdeveci, is that,
European Union law, more particularly the principle of non-discrimination on grounds of age as given expression by Directive 2000/78, must be interpreted as precluding national legislation, such as that at issue in the main proceedings, which provides that periods of employment completed by an employee before reaching the age of 25 are not taken into account in calculating the notice period for dismissal.24
Thus, coupled with the provisions of a directive, general principles of law can, eventually, have the same effect as rights that individuals can claim in national courts against other individuals. This method is the one that Advocate-General General Cruz Villalón suggests in its recent opinion in Association de médiation sociale:25 the principle contained in article 27 of the Charter, concretized in article 3 of Directive 2002/14,26 precludes, he contends, national legislation that excludes some workers from being taken into account when calculating the number of employees of the company in order to ensure information and consultation.
The virtue of the association of a general principle and the provisions of a directive can also lie in an extension of the field of application of the derived legislation. In Danosa,27 for instance, the scope of application of directives on equal treatment of men and women was extended to include a person whose status as a worker was uncertain. Referring to the principle of non-discrimination of men and women, and article 23 of the Charter of Rights, the Court decided that:
[I]t is of no consequence, whether Ms Danosa falls within the scope of Directive 92/85 or of Directive 76/207, or—to the extent that the referring court categorises her as “a self-employed person”—within the scope of Directive 86/613, which applies to self-employed person. . . .
And it added:
[W]hichever directive applies, it is important to ensure, for the person concerned, the protection granted under EU law to pregnant women in cases where the legal relationship linking her to another person has been severed on account of her pregnancy.28
Eventually, it remained a mystery which directive should apply, but that did not matter to the Court: the claimant obtained the right to equal treatment.
Another category of combinations covers a variety of sources that do not all belong to the EU legal order. In the field of fundamental rights’ protection, this phenomenon reaches beyond the borders of EU law and, again, it is not our objective to demonstrate that EU law is singular in this respect. In terms of normative combination and the use of a variety of instruments that do not belong to its own legal order, the ECJ takes a path that a number of other courts sometimes follow. At the European Court of Human Rights, for example, the decision in Demir and Baykara v. Turkey29 is a perfect illustration of a reasoning involving a series of sources of different origin and nature.30
Most striking, in this category of cases, is the recourse to international law (by which I mean norms other than the European Convention on Human Rights (ECHR), which has a very specific status in EU law31). Of course, international law is often relied on, alongside EU norms, because in a number of instances it is binding on EU institutions. One recent example is N.S.,32 where the Court of Justice relied on “the duty of the Member States” to interpret and apply Regulation 343/2003 in a manner that ensures due respect of the Geneva Convention of July 28, 1951 and the Protocol of January 31, 1967 relating to the status of refugees, and other relevant treaties (as required by art. 78 of the TFEU). The more recent Ring33 and Commission v. Italy cases34 are other examples. In these cases, the Court of Justice decided that Directive 2000/78 on equal treatment in employment and occupation 35 had to be construed according to the UN Convention on the Rights of Persons with Disabilities ratified by the EU.36 Taking into account the UN Convention has led to an extension of the scope of EU legislation, and as a result, in Ring, rights could be claimed under the Directive. But as Ring also shows, even when international law is binding on the EU, the combination of EU and International law, is not at all a simple story.37 Without entering too much into this thorny problem, the Ring case gives an idea of this complex relationship and of the flexibility of the law that goes with it: “the primacy of international agreements concluded by the European Union over instruments of secondary law,” stated the Court, “means that those instruments must as far as possible be interpreted in a manner that is consistent with those agreements.” What happens if such consistent interpretation is not possible?38 International law is, at least temporarily, paralyzed. As we will see in more detail below (Section 3), the same is also true of the relationship between EU law and national law when the former does not have direct effect.
This situation, in which EU law is bound (although with some degree of flexibility) by international law, is different from one in which international law, without being part of the European legal order, is used in a comparative way, in order to show convergence towards a certain interpretation of a right or the recognition of a fundamental right.39 This “consensual” method,40 comparable to the method used by the Court of Human Rights in the Demir and Baykara v. Turkey case,41 was applied in the famous Viking42 and Laval43 cases, where the fundamental right to collective action was recognized. In these two cases, the Court quoted, among other references, the European Social Charter, signed at Turin on October 18, 1961 and Convention No. 87 concerning Freedom of Association and Protection of the Right to Organise, adopted on July 9, 1948 by the International Labour Organisation.44 More recently, in Commission v. Germany,45 concerning the right to collective bargaining, the Court relied, once again, on article 6 of the European Social Charter.
If this method remains exceptional, the fact that it is enforced in such important and difficult cases suggests that it must be taken seriously. To be sure, the cases do not give much force to the fundamental rights that they identify, based on convergence of a series of legal instruments. Rights are brought to life, but without any effect in the cases concerned. The effectiveness of EU law, as far as these rights are concerned appears illusory. But this does not dwarf the potential efficiency of the process of combination.
Considering the different categories of normative combinations that contribute to the development of EU law, it is no exaggeration to say that the effects of EU law in national courts no longer depend on the identification of norms capable of producing certain legal effects. Rather, it has become crucial to take into account the fact that EU law provisions are often effective when articulated with one another, or with norms borrowed from other legal systems, which are not necessarily binding, but can allow for an evolutive interpretation of the law. Although this phenomenon remains limited, considering the modest number of cases, especially when identifying new fundamental rights is at stake, it indicates that the effects of EU law norms can depend not on their intrinsic nature, but on their association with other references. As a result, there is space, I believe, for a theory of “combined effects” of norms in the EU legal order, a multifaceted model that would depart quite radically from the self-executing and self-sufficient norm celebrated in Van Gend en Loos. This new model can be a source of increased effectiveness of EU law in national courts. It can also be seen as the outcome of an adaptation of legal actors, faced with the congenital weakness or incompleteness that characterizes some provisions of European law: building constructive relationships between norms in order to compensate this weakness has become an essential part of legal reasoning.
3. From rights to obligations, and flexible effects of EU law in national courts
A second line that can be drawn from Van Gend en Loos comes from this essential element of the case: direct effect was defined as a mechanism, through which individuals could obtain rights in member states’ courts, based on EU law and, more precisely and more importantly, on provisions of primary law. Although this was not absent in Van Gend en Loos, the evolution of EU law, since the case was decided, has allowed that, in a larger number of hypotheses, individuals be brought before national courts, on the basis of obligations imposed on them by provisions of the treaties. With so-called horizontal direct effect, EU primary law has shifted away from the dominant concern that permeated Van Gend en Loos: submitting states to an orthopedic treatment aimed at reforming their public policies, along the lines of internal market’s requirements. In that respect, however, the evolution can still be seen as a continuation of Van Gend en Loos: the effectiveness of EU law could justify, to some extent, the submission of private actors to TFEU, and to internal market rules in particular. In comparison, it is no longer a mere extension of direct effect, when, in the absence of direct effect, national courts are required to interpret national law in conformity with European Union law: under the “indirect horizontal effect” doctrine, the effects of EU law become dependent on the capacity of national courts to tailor national law to European fashion, a made-to-measure approach contrasting with Van Gend en Loos uniform requirement for national courts to grant subjective rights.
3.1. Vertical direct effect as a source of subjective rights
As opposed to the French version of the case, the Italian version of Van Gend en Loos is explicit about the fact that individuals can claim subjective rights on the basis of treaty provisions. The case made it clear that the treaty was available to entertain private claims in municipal courts. As a result, not only would citizens of member states benefit directly from the treaty, but they would, as the court pointed out, exercise “an effective supervision” on member states to ensure that they respect EU law requirements. Individual rights derived from the Treaty were key, as through them EU law could penetrate national legal orders and transform them. And it did. In particular, when direct effect of common market rules was affirmed, it became clear that member states would have to face requests based on free movement of goods, persons, capital or free provision of services and, as a consequence, would have to reform their systems of regulation in many different fields.46
Although the Court also mentions in Van Gend en Loos that the treaty imposes obligations on individuals, the lesson from that particular case was that national courts had to protect individual rights, not that they had to make sure that obligations deriving from the treaty were enforced against individuals. At the time, the obligations binding on individuals were indeed quite limited. Competition law was an important source of such obligations, as antitrust rules and the prohibition of abuse of a dominant position were explicitly targeting the behavior of private companies. They still do, of course, and continue to frame the behavior of private economic actors. But what has been a major source of extension of obligations binding on private parties is the recognition of a horizontal direct effect47 to treaty provisions concerning the internal market. This evolution has raised new questions concerning the consequences of direct effect of treaty provisions.
3.2. Horizontal direct effect and the problem of submitting individuals to free market rules
The evolution that led to the recognition of horizontal direct effect to Treaty provisions, and, in particular, free movement rules has gone, until recently, largely unnoticed. One reason for this is that the extension was only apparent in rare cases (and not necessarily very clear in all of them). As a result, it did not seem to imply important changes at once. The story has been told many times,48 but recent examples have brushed away, it seems, obstacles or limits to the horizontal direct effect of free movement rules, even if the Court of Justice has, not so long ago, continued to suggest that free trade provisions of the EU treaty were public law rules.49
In spite of this inconsistency, the language used in Viking50 is unambiguous: “there is no indication” in case law, the Court of Justice said, that horizontal effect “applies only to associations or to organisations exercising a regulatory task or having quasi-legislative powers.” No distinction is made, in particular, between the different types of private actions, depending on their impact, a distinction that Advocate-General Maduro supported in his opinion in the case. In the subsequent Laval case,51 the Court simply pointed that the right of trade unions to take collective action, whereby undertakings established in other member states may be forced to sign a collective agreement, is liable “to make it less attractive, or more difficult, for such undertakings to carry out its activity in the State concerned,” and “therefore constitutes a restriction on the freedom to provide services within the meaning of Article 49 EC” (now art. 56 TFEU). In sum, according to these decisions, only the restriction, or potential restriction, on free exercise of economic freedom matters, regardless of the private action that induces it.
Even more striking is the comparison of two cases, one decided in 2000 and the other in 2012. In Ferlini,52 it seems, the Court limited to certain hypothesis the horizontal application of the non-discrimination rule in a case of free movement of workers: “article 6 of the Treaty also applies in cases where a group or organisation exercises a certain power over individuals and is in a position to impose on them conditions which adversely affect the exercise of the fundamental freedoms guaranteed under the Treaty.”53 In Erny,54 in contrast, the Court went much further, bluntly affirming that the prohibition of discriminations laid down in article 45(2) TFEU on free movement of workers “applies not only to the actions of public authorities, but also to all agreements intended to regulate paid labour collectively, as well as to contracts between individuals.”55 As in a previous case,56 one must admit, this solution only concerns the prohibition of discriminations based on nationality, which may well be a limit to the extension of horizontal effect of free movement rules, and could be justified by the particular status of the principle of non-discrimination, as a general principle of EU law.
This possible restriction of horizontal direct effect of free market rules does not call into question the observation that, in the course of EU law development, private parties have been subject to certain provisions of the treaty concerning the realization of the internal market, that were considered to be binding only on governments at the time of Van Gend en Loos. Through horizontal direct effect, these provisions of the treaty stepped into the realm of private law. The “constitutionalization of private law” that this evolution achieves creates a series of problems that the Court of Justice has not yet addressed in its case law.57 Rather, although the transposition of a reasoning designed for cases involving states or other public entities is not necessarily appropriate, where private law relationships are concerned, the Court of Justice had, until now, ignored the need for a separate doctrine when obligations binding on individuals are derived from free market rules. This is particularly striking in Erny,58 which addressed the justification of restrictive measures: “neither the scope nor the content of those grounds of justification is in any way affected by the public or private nature of the disputed provisions,” the court contended. Yet, it is clear that justification of restrictions by reason of general interest or public good can hardly be available when private actors are responsible for a restriction to free movement. The crucial issue of justification of free movement restrictions, to which the Court and legal scholars have devoted enormous attention after Cassis the Dijon,59 remains a virgin land, when private restrictive conducts are at stake.
In addition, the types of actions and remedies available, in cases of treaty violations resulting from the behavior of individuals, need to be adapted to the particular situation of private actors.60 While making states liable for free movement restrictions is the inevitable, and acceptable, outcome of their commitments at the EU level, the same is not true for private actors. In particular, when the latter fulfill a particular economic or social function, which is the case for trade unions or other non-governmental organizations, making them liable under free movement provisions may jeopardize their very existence. This is not only because of potentially high damages. The unpredictability generated by the introduction of constitutional arguments (the reference to fundamental freedoms) in private law disputes is also problematic. Indeed, uncertainty may deter the organizations concerned from taking action, although this action can be considered socially useful. Along the same lines, when fundamental freedoms reach the sphere of contractual relations, the resulting disruption in the parties’ commitments should also be taken into account. Until now, “insufficient attention was paid to the way in which private law has already sought to balance competing rights through its legal doctrines and rules.”61
In comparison, the requirement of consistent interpretation of EU law, a source of indirect horizontal effect, seems more respectful of existing settlements between competing rights.62 The questions it raises are of a different kind, but still closely related to the effectiveness of EU law in national courts: the issue is not the overbroad conception of what the effectiveness of EU internal market law requires (imposing obligations on individuals), but the variability of this effectiveness when it applies to private relationships, depending on the possible interpretations of national law according to national courts. This solution is a far cry from the recognition of direct effect to a treaty provision, which allowed individuals to claim the same right before all national courts.
3.3. Indirect horizontal effect and the challenge of variable effectiveness
The doctrine of indirect effect requires national courts to interpret national law “in the light” of EU law.63 Indirect effect is a method of ensuring the effect of EU law when direct effect is missing. As the Court of Justice has stated: “this obligation to interpret national law in conformity with European Union law is inherent in the system of the Treaty on the Functioning of the European Union, since it permits national courts, for the matters within their jurisdiction, to ensure the full effectiveness of European Union law when they determine the disputes before them.”64 If this requirement is “inherent in the system of the Treaty,” as the Court has mentioned, it is also part of a more general trend: recently, domestic courts have, outside any European obligation, relied on the doctrine of indirect effect to give force to international law.65 This method of internalization of international law, transcending the distinction between monist and dualist systems, has retained much attention, and concern, beyond the frontiers of EU law.66
In EU law, consistent interpretation was used in applying EU law in disputes between private parties: individuals were subject to EU law provisions, even when those provisions had no horizontal direct effect. The requirement of a consistent interpretation implies consideration of EU law in many cases in which it generates no subjective rights that can be claimed by an individual, but may still result in unexpected duties or burdens for individuals. Thus, indirect effect contributes, when applied horizontally, to increased obligations on individuals, resulting from EU law developments.
The progress of harmonization in many fields of private law,67 criminal law, or tax law,68 has resulted in new rights and duties for member states’ citizens, which, in most instances, did not need the doctrine of direct effect, nor any theory about the effects of EU law in national courts, to be enforced: these obligations, having their source in EU directives, only applied after implementation through internal law. However, the impact of directives themselves in private disputes has become more and more obvious over time. But, having accepted long ago that directives could have vertical direct effect,69 the Court of Justice has, continuously, refused to give horizontal direct effect to their provisions.70 As a result, directives are still considered not to be binding on individuals, and should not be a source of obligations for them, the Court continuously confirmed.71 However, at the same time, the ECJ’s case law has constructed bypasses, allowing directives to produce effects in private disputes.72 And these bypasses, including indirect horizontal effect,73 have proved, prima facie, to be as powerful as direct horizontal effect.74
At first, consistent interpretation seems to be a very basic demand, in line with the principle of sincere cooperation laid down at article 4(3) TFEU. But, looking closer, it is not so trivial as it seems.75 Consistent interpretation compels judges to overrule previous interpretations, if needed. This means, possibly, to introduce, without notice, an unexpected change in the law.76 Of course, overruling also happens in member states’ courts, without EU commanding it. But the disruption it creates, depriving citizens of their legitimate expectations, should make it exceptional. As a method prescribed by EU law to give effect to a directive when states have failed to implement it properly, overruling loses its marginality. This is not, to say the least, a satisfying way for EU law to penetrate national legal systems.
However, the most problematic aspect of consistent interpretation, related to EU law effectiveness in national courts, lies elsewhere. The outcome of the order to interpret national law in conformity with EU law very much depends on the flexibility of national law. When the provisions of national legislation that are inconsistent with EU law are very clear and precise, according to their interpreters, EU law will have little impact, because interpreting contra legem is not required.77 When, on the contrary, the fabric of national law is soft, malleable, or at least considered so by those in charge of its enforcement, the impact of EU law will be potentially much stronger. As a result, the penetration of EU law into national legal orders depends on national legislators, national legislative styles, and national techniques of interpretation. To be sure, the Court of Justice does not leave entire discretion to national courts, and requires that they try as hard as they can to achieve consistent interpretation, which implies, for instance, that they take “the whole body of domestic law into consideration” and make use of the interpretative methods recognized by domestic law with a view to ensuring that EU law is fully effective. Eventually, however, it remains clear that such interpretation is not always possible.78
The resulting flexibility concerning the effects of EU law throughout the Union contrasts with Van Gend en Loos, a case in which the Court decided what the effect of an EU law norm was going to apply in all states and before all courts. This flexibility could be considered as an aspect of procedural autonomy, a concept that describes and justifies the limited effectiveness of EU law, in the absence of a complete system of justice and procedural rules. Because procedural autonomy concerns remedies, it may indeed result in differences in the enforcement of EU law. But the various consequences of consistent interpretation, which depend on national substantive law, would imply a considerable extension of that concept. Indeed, the hypothesis is one in which the variation in the implementation of EU law does not depend on the system of justice and procedures, but on the legal force given to the EU provisions concerned, in each national court: the variation concerns the binding force of the norm. The doctrine of consistent interpretation admits, contrary to Van Gend en Loos, that it is not possible, for every individual, to expect that EU law will have a pre-determined effect, in national courts.
As a result of consistent interpretation, individual claims will thrive in some national courts, and obligations will be imposed on individuals as a result, whereas, in others, they will be unsuccessful because of the limits in the courts’ power to interpret national law. This solution seems quite remote from the idea of direct application and full effectiveness of EU law: beyond procedural autonomy, EU law effectiveness is made dependent on the specificity of national substantive laws and methods of interpretation.
If this is acceptable, and the effect of EU law in national courts can differ depending on the substance of national law and the techniques of interpretation available to national courts, there may be a case for more flexibility in other instances, in particular when applicability of constitutional rights is concerned.
4. From application to applicability
According to Van Gend en Loos, national courts “must” apply treaty provisions, and protect individual rights that they create. The mission entrusted to national courts in that case imposed “role splitting”:79 national judges were required to act both as organs of national and European judiciary, and apply the rules emanating from two different legal orders. Fifty years after Van Gend en Loos, it is still not absolutely sure that all national courts have fully understood, and accepted, that role. Looking, for instance, at the variations in the use of the preliminary ruling procedure among national courts80 suffices to indicate that national contexts have some influence on the impact of EU law in national courts. However, in terms of effective application of EU law norms in national courts, there is little doubt that direct effect, coupled with preliminary references, contributed extensively to effective application of EU law. The “collaboration” of national courts with the Court of Justice81 was rightly considered a decisive source of EU law effective enforcement.
Today, the issue of EU law enforcement in national courts is faced with another major challenge: the uncertainty concerning the applicability of EU law. In recent times, this question has been particularly visible, and strenuous, in the field of fundamental rights’ protection. On one side, the question is one of applicability of EU law provisions protecting fundamental rights. It has, indeed, become a more acute issue since the Charter of Fundamental Rights has gained the same legal value as the Treaties with the Lisbon Treaty,82 and at a time when it is settling in the EU legal environment. To be sure, this does not mean that applicability has not been a major concern in other fields, such as free movement of citizens, as the Zambrano saga illustrated,83 but the issue concerning the applicability of the Charter of Fundamental Rights has a much broader scope. On the other hand, fundamental rights’ protection by national courts depends on the applicability of national constitutions protecting these rights and freedoms. In this respect, the question that arises, and that national courts have to face, concerns the restriction to the protection of fundamental rights granted by national constitutions, which is, or should be, required in order to ensure effectiveness of EU law. The ever-growing impact of EU policies on fundamental rights has brought to the fore the question of the limits to the effectiveness of EU law which would leave room for national constitutions. This issue touches on a tension deeply rooted in the history of EU federalism.
Considered from these two angles, the protection of fundamental rights appears as one of the most important domains, if not the most important, in which EU law effect iveness is challenged, these days, in relation with the issue of applicability of EU and national law. This has been illustrated in recent important cases. Correlatively, “role splitting” is no longer the new frontier for national courts, but their mission to ensure a distribution of roles, when confronted with a plurality of sources of protection of fundamental rights and freedoms. Some of the hardest questions, for national courts, are no longer whether EU law contains rights that they have to protect, but rather, on the one hand, whether fundamental rights embedded in EU law can apply in the case before them (a question of applicability of fundamental rights protected by the EU) and, on the other hand, whether they have power, and to what extent, to guarantee a higher degree of protection of fundamental rights on the basis, for example, of their own constitution, even if the situation lies within the scope of EU law (a question of applicability of constitutional or international law, in situations falling under EU law).
The answers to both questions are crucial for the enforcement of EU law in member states’ courts. The applicability of fundamental rights protected by EU law would be a mundane question, although no less tricky, for that matter, on the jurisdiction of EU law, if the question had not given rise to recent developments in the case law of the Court of Justice that need to be confronted with the doctrine of EU law effectiveness in national courts. As far as the applicability of national constitutional rights is concerned (or rather, as the case law shows, the refusal, by the Court, to accept this applicability), recent developments do not only show that the need to ensure EU law effectiveness, an heritage of Van Gend en Loos, resists the passage of time: the question concerning there being room for national law when the fabric of EU law is only loosely woven, has become more crucial than ever.
4.1. Applicability of fundamental rights protected by the EU
Since the Charter of Fundamental Rights has been proclaimed, and, even more so, since the Lisbon Treaty conferred the status of primary law on that instrument, the delimitation of its scope of application has been a major concern and a source of uncertainty in national courts in charge of enforcing EU law, as Van Gend en Loos
Evaluating the buffering vs. direct effects hypotheses of emotional social support on inflammatory markers: The Multi-Ethnic Study of Atherosclerosis
Briana Mezuk, PhD,1Ana V. Diez Roux, PhD MD,2 and Teresa Seeman3
4Department of Epidemiology and Community Health, Virginia Commonwealth University
5Center for Integrative Approaches to Health Disparities, University of Michigan School of Public Health
6School of Medicine, Division of Geriatrics, University of California – Los Angeles
Corresponding author: Briana Mezuk, PhD, Virginia Commonwealth University School of Medicine, Department of Epidemiology and Community Health, PO Box 980212, Richmond, VA 23298, ude.ucv@kuzemb, Phone: 804-628-2511, Fax: 804-628-2510
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Brain Behav Immun. Author manuscript; available in PMC 2011 Nov 1.
Published in final edited form as:
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Social support is associated with cardiovascular disease mortality, however the physiologic mechanisms underlying this relationship remains unspecified. This study evaluated the association of social support with inflammatory markers associated with cardiovascular risk: C-reactive protein (CRP), interleukin-6 (IL-6), and fibrinogen. We evaluated two competing models of the support-inflammation relationship: first, that low social support is directly associated with inflammation, and second, that high support acts to buffer the effect of stress on inflammation. Using data from the baseline interview of the Multi-Ethnic Study of Atherosclerosis (N = 6,814, 53% female, age 45–84 years) we assessed the independent and interacting associations of social support and stress with inflammation. Social support was measured by the Emotional Social Support Index. Stressors in multiple domains (work, family, finances, interpersonal) were assessed. Serum CRP, IL-6, and fibrinogen were analyzed from fasting samples using high-sensitivity assays. Multivariate linear regression, including models stratified by gender and age group (45 – 64 and 65 – 84 years), was used to assess the direct and buffering relationships between social support, stress, and inflammation. In bivariate analyses low social support was associated with higher levels of all three markers. In adjusted models, low support was associated with higher lnCRP (B: 0.15, 95% CI: 0.01, 0.30) among men but not women. High social support buffered the relationship between stress and CRP among middle-aged women only (P for interaction 0.042). Overall, social support was only modestly associated with inflammation in this relatively healthy sample, and these relationships varied by age and gender.
Keywords: social support, inflammation, aging, gender differences
Investigations of the interrelationships between the social environment and health have established that low social support, poor social integration and social isolation are associated with increased mortality, particularly from cardiovascular disease (CVD) (Berkman et al., 2003; Brummett et al., 2001; Frasure-Smith et al., 2000). Despite this epidemiologic evidence, the physiologic mechanisms underlying these relationships remain unspecified (Berkman et al., 2003; Knox & Uvnas-Moberg, 1998). Several researchers have speculated that alterations in immune function may be a mechanism by which psychosocial exposures, including social support, affect health. In particular, low social support has been associated with elevated levels of circulating inflammatory markers, including cytokines (e.g., interleukin-6 (IL-6), TNF-α), acute phase proteins (e.g., C-reactive protein), and clotting factors (e.g., fibrinogen) (Seeman, Berkman, Blazer, & Rowe, 1994; B. N. Uchino, Holt-Lunstad, Uno, Betancourt, & Garvey, 1999) that have been implicated in risk of CVD. However, not all studies have reported a significant association between social support and systemic inflammation (McDade, Hawkley, & Cacioppo, 2006); and even in those instances where support is associated with inflammation, it is unclear whether this relationship is due to a direct (i.e., independent) influence on physiology, or if support simply buffers (i.e., moderates) the effect of negative experiences (e.g., daily hassles, caregiving, stressful life events) which have direct effects on physiology (Cohen & Wills, 1985).
An integrative framework of the ways social experiences influence health should address the potential that the relationship between social support and physiologic indicators such as inflammation may vary by age and sex (Seeman and Crimmins 2001). As social roles evolve over the life course (i.e., marriage, parenthood), the influence of social experiences on health may also change. As with other psychosocial characteristics, social support may have cumulative effects over time, as well as acute effects in the context of events that affect social life (i.e., divorce, retirement) (Uchino et al. 1999). Also, many aspects of the receipt and provision of social support vary by sex (i.e., women are more likely to experience widowhood and are more likely to be caretakers than men) (Moen, 2001), and thus the implications for social relations to health may likewise differ for men and women (Ajrouch, Blandon, & Antonucci, 2005) Consistent with this general framework, there is suggestive evidence that the physiologic correlates of social integration and support vary by age and gender (Ford, Loucks, & Berkman, 2006; Hughes, 2007). For example, Ford and colleagues (2006) reported that low social integration was associated with elevated C-reactive protein among older men, but not among women or younger men (Ford et al., 2006). Loucks and colleagues (2006) also reported a significant association between CRP levels and social integration among older men but not older women (Loucks, Berkman, Gruenewald, Seeman 2006). However, relatively few studies have systematically examined variation by age and gender in this relationship, and most have only examined a single indicator of immune function. Thus, a systematic investigation of whether the relationship between social support and inflammatory indicators of CVD risk varies by age and gender is warranted.
The goal of this paper is to explore the relationship between social support and three markers of inflammation that have been implicated in CVD, interleukin-6, fibrinogen, and C-reactive protein, using the Multi-Ethnic Study of Atherosclerosis (MESA). The MESA sample was free of clinical atherosclerotic disease at baseline, and thus it is well-suited for examining the relationship between social support and physiologic changes isolated from the confounding effects of pre-existing CVD that may mask true associations or create spurious ones. While alterations in these inflammatory markers may not have immediate clinical significance, they may be early indicators of cardiovascular disease risk.
We investigated two main questions: (1) Is low social support directly associated with these inflammatory markers? and (2) Does high social support buffer the relationship between stress and inflammation? We hypothesized that if buffering is predominant, the association between stress and inflammation will be stronger among those experiencing lower social support than among those experiencing higher social support. However, if the direct model is predominant, the association of chronic stress with inflammation will not vary by level of support (and the association of social support with inflammation will not vary by stress level). In addition, we investigated whether these associations varied by age and gender.
MESA is an on-going population-based multi-site study of the predictors of subclinical cardiovascular disease. Participants aged 45–84 years and free of clinical CVD at baseline (e.g., never experienced a heart attack, stroke, transient ischemia attack, heart failure, angina, atrial fibrillation, or cardiovascular procedures) were recruited from six study sites (Baltimore City and Baltimore County, MD; Chicago, IL; Forsyth County, NC; Los Angeles County, CA; New York City, NY; and St. Paul, MN). The final sample was 53% female, 40% non-Hispanic white, 30% African American, 20% Hispanic, and 10% Asian. Details of the sampling design and study procedures have been discussed previously (Bild et al., 2002). This report is restricted to the baseline MESA sample with complete data on the measures of social support, stress, and markers of inflammation (N = 6,153, 90% of the baseline sample). Participants excluded from the analysis (N = 611) were older than those included (mean age 66.0 vs. 61.9 years, p < 0.02), but otherwise did not differ from the remaining sample in terms of race, gender, education, employment, income, marital status, body mass index (BMI), smoking status, or experience of stress (data not shown).
This study was approved by the Institutional Review Board at each site and all participants provided informed consent.
The primary independent variable was perceived emotional social support (ESS), indicated by the Emotional Social Support Index (ESSI, range: 6 – 30, Cronbach’s alpha: 0.88) which consists of six 5-point likert-scored items concerning availability of emotional support (e.g., Is there someone available to you whom you can count on to listen to you when you need to talk? 1 = None of the time, 2 = A little of the time, 3 = Some of the time, 4 = Most of the time, 5 = All of the time), with higher values indicating more available emotional support (ENRICHD, 2000; Mitchell et al., 2003). The ESSI has modest correlations with other indices of social support (i.e., Perceived Social Support Scale) (Mitchell et al., 2003). Because exploratory analyses indicated that the relationship between social support and inflammation was non-linear, the summed scale score was categorized to indicate low (score <12), moderate (score 12 – 24) or high (score ≥ 25) levels of ESS based on previous literature on social support and health in later life. In addition, each item was dichotomized as indicating low (score ≤ 2 or below) or moderate/high ESS (score ≥ 3).
Stress was measured by a composite of five items concerning contemporaneous, on-going stressors in five domains (i.e., personal health, health of a friend/relative, work-life, financial matters, and relationships with friends/relatives), with higher values indicating more stressors (Bromberger & Matthews, 1996). Each item that was endorsed was rated on a three-point scale in terms of stressfulness (1 = Not very stressful, 2 = Moderately stressful, 3 = Very stressful) (range: 0 – 5 very stressful events). The scores on this scale were strongly left-skewed, with 66% of the sample reporting only experiencing zero or one very stressful events, and therefore these responses were then combined into a dichotomous variable indicating presence of at least one very stressful event. In addition, to categorize stressors as either recent-onset or long-standing, participants were also asked if each of the stressors endorsed had been going on for 6 months or longer. If a participant responded positively to this duration question for at least on stressor, they were classified as experiencing chronic stress.
The main factors investigated as moderators of the relationship between ESS and the markers of inflammation were gender and age group, dichotomized as middle- age (45 – 64 years, N = 3543) and older adults (65 – 84 years, N = 2648).
Additional factors included as covariates were age (centered on the sample mean, 61.9 years), sex, race/ethnicity (modeled as an indicator variable with non-Hispanic whites as the reference group), educational attainment (dichotomized as at least some college versus high school or less (reference)), employment status (dichotomized as currently working versus other (reference)), annual gross household income (categorized as <$20,000 (reference), $20,000 to <$40,000, $40,000 to < $75,000, and ≥$75,000), and marital status (categorized as current married (reference), divorced/separated, never married, and widowed). Three additional factors known to influence inflammatory markers, current smoking status (with former/never smoker as the reference), BMI (kg/m2), and number of alcohol drinks per week were included. Two health conditions, hypertension and diabetes, were also included. Hypertension was dichotomously indicated as systolic blood pressure ≥ 140 mm Hg or diastolic ≥ 90 mm Hg from the average of three resting blood pressure readings, or use of antihypertensive medications. Diabetes was determined by the American Diabetes Association 2003 fasting glucose criteria (≥ 7.0mmol/L) or use of insulin or other hypoglycemic medications (American Diabetes Association, 2006). Consistent with previous MESA reports using these inflammatory markers, recent infection status was dichotomously coded based on self-report of cold or flu, sinus infection, urinary tract infection, tooth infection, bronchitis, or pneumonia in the preceding two weeks and accounted for in the regression models (Ranjit et al., 2007). Use of non-steroidal anti-inflammatory drugs (NSAIDs) was also recorded.
All variables were assessed at the baseline MESA interview concurrently with the measurement of serum inflammatory markers.
The primary outcomes were three markers of inflammation, interleukin-6 (IL-6, pg/mL), C-reactive protein (CRP, mg/L), and fibrinogen antigen (mg/dL) which have been shown to be associated with risk of cardiovascular morbidity and mortality. We conducted separate analyses with each marker as an evaluation of the robustness of the relationships to inflammation more generally. The standardized procedures for the collection, processing, shipping, and storage of blood samples have been previously described (Bild et al., 2002). Fasting venous blood samples were taken from participants at baseline and processed at a centralized laboratory. IL-6 was measured using ultrasensitive enzyme-linked immunosorbant assay (ELISA) (R&D Systems, Minneapolis, MN). High-sensitivity CRP was measured by nephelometry (BNII nephelometer, Dade-Behring Inc., San Mateo, CA). Fibrinogen antigen was also measured by nephelometery (BNII N antiserum to human fibrinogen, Dade-Behring, San Mateo, CA).
Initially we used multivariate analysis of variance (MANOVA) to compare mean levels of the three inflammatory markers by emotional social support and investigate interactions between ESS, gender, and age group. We used the non-parametric Wilcoxon rank-sum test for linear trend to evaluate whether covariates varied across levels of ESS (categorized as low, moderate and high, described above). We used a series of linear regression models to assess the independent association between levels of ESS and the three markers of inflammation as the outcomes. Values of the inflammatory markers were log-transformed in order to normalize their distributions to better meet the model assumptions. High ESS was the most prevalent category (55.2% of the sample), and was used as the reference group for the analyses evaluating the direct associations between low and moderate emotional support and inflammation (Hypothesis 1). In order to evaluate whether high levels of ESS buffered the association between stress and inflammation, we dichotomized support as high versus moderate/low, with the latter as the reference group (Hypothesis 2). We evaluated the statistical significance of the interaction between this dichotomous indicator of high ESS with the dichotomous indicator of stress (both recent onset and chronic) in order to determine whether the relationship between social support and inflammation varied by exposure to stress.
The initial multivariate regression model was adjusted for age, gender, race/ethnicity, educational attainment, income, employment status, and marital status. The second model was additionally adjusted for additional behavioral and biomedical risk factors for inflammation including smoking status, alcoholic drinks per week, body mass index, hypertension, diabetes, NSAID use, and recent infection status. We also conducted post-hoc sensitivity analyses by (1) adjusting for depressive symptoms as indicated by the Centers for Epidemiologic Studies Depression (CESD) scale (Radloff 1977; Ranjit et al., 2007); (2) adjusting for self-reported arthritis; and (3) excluding participants who reported a recent infection from the analysis, in order to better account for residual effects these exposures may have on inflammation. We examined whether the direct and stress-buffering association between support and inflammation varied by age and gender in stratified analyses. Any substantial differences were tested by including appropriate interaction terms in the regression models. All analyses were conducted using STATA v.9 software (StataCorp, College Station, TX). All p-values refer to two-tailed tests.
The sample overall reported high levels of emotional social support, and level of ESS was similar for men and women (M = 24.7 (SD = 5.2) for men, M = 23.8 (SD 5.2) for women out of a possible score of 30). Approximately one-third of the sample reported experiencing a very stressful event, whether recent onset or chronic. Women reported substantially more recent onset (M: 1.35 vs. 1.05, p<0.001) and chronic (M: 1.21 vs. 0.95, p<0.001) stress than men. Lower levels of support were associated with younger age, being male, having lower household income, marital status, being a current smoker, and prevalence of both recent onset and chronic stress. The three inflammatory makers were moderately correlated with each other (r2 = 0.41 to 0.46, all p < 0.001). Mean levels of all inflammatory markers were higher among those reporting low ESS relative to high, although this pattern was only statistically significant for fibrinogen (Table 1). Mean levels of inflammatory markers were higher in women than in men and increased with age.
Participant characteristics by emotional social support, Multi-Ethnic Study of Atherosclerosis (2000 – 2002)
MANOVA indicated no relationship between the continuous measure of emotional support and the three inflammatory markers. However, levels of the markers did vary according to the categories of low, moderate, and high levels of ESS (F = 2.42, p<0.024), consistent with the exploratory analysis indicating the relationship was non-linear. Interaction terms between ESS levels and gender and ESS and age were not statistically significant (data not shown).
Evaluating the Direct Hypothesis
Bivariate regression indicated that low levels of ESS were associated with elevated levels of all three inflammatory markers in the sample overall (Tables 2 – 4), consistent with the direct hypothesis. After adjustment for demographic and socioeconomic characteristics, low ESS remained significantly associated with elevated CRP and fibrinogen, but not IL-6 (Model 1, Tables 2 – 4). After additional adjustment for health behaviors and biomedical factors, only CRP remained significantly associated with low support (Model 2, Tables 2 – 4). Stratification by sex indicated that the association of ESS with CRP was stronger and more likely to be statistically significant in men than in women (p for interaction 0.039 in fully-adjusted model). Within each gender there was no evidence that the association between low ESS differed significantly by age for CRP, IL-6 or fibrinogen (p for interaction > 0.05 for all markers).
Evaluating the direct model: Mean difference in log-IL-6 by categories of emotional social support
Evaluating the direct model: Mean difference in log-Fibrinogen by categories of emotional social support
We conducted sensitivity analyses to determine whether depressive symptoms, arthritis, or recent infection were strong confounders in the stress-social support relationship. When CESD score was included in the models presented in Tables 3 – 5 the results did not change appreciably, and the interpretation that social support is only weakly directly associated with inflammation was upheld (data available upon request). Neither additional adjustment for arthritis, nor excluding participants who had experienced a recent infection (N = 1,467), substantially influenced the results (data available upon request)
Evaluating the direct model: Mean difference in log-CRP by categories of emotional social support
Evaluating the buffering model: Mean difference in log-CRP associated with emotional social support, chronic stress, and their interaction
Evaluating the Buffering Hypothesis
Stress was consistently associated with elevated levels of all inflammatory markers in main effect models (data not shown). However, there was no support for the stress-buffering hypothesis in the full sample or sex stratified analyses, either in bivariate or multivariable regression models for any of the inflammatory markers (Table 5 shows results for CRP only. The other inflammatory markers revealed similar patterns and are not shown). In age- and sex-stratified analyses, interactions terms were consistently negative, consistent with a buffering, but the magnitude of the heterogeneity was small and it was not statistically significant except in the case of 45–64 year old women. In this group, there was evidence that high ESS buffered the association between high stress and CRP in the fully-adjusted models (p for interaction 0.042). There was no evidence of buffering for the other two markers among middle-age women. Additional analyses focused on chronic stress (lasting 6 months or longer) produced similar results (data not shown).
Sensitivity analysis: Marriage as a proxy for emotional social support
Marriage is a key source of social support, particularly for older adults, and ESS and levels of IL-6, CRP and fibrinogen varied significantly by marital status (all p < 0.001). We therefore conducted a series of post-hoc analyses to evaluate whether marital status moderated the association between stress and inflammation. In multivariate regression analyses, the relationship between stress and inflammation did not significantly differ by marital status in the sample overall, indicated by the non-significant interaction terms between marital status and stress (data not shown). Similar results were obtained in the age- and sex-stratified analyses.
The main finding from this study is that perceived emotional social support has little influence, either through direct or stress-buffering pathways, on inflammatory markers in this diverse sample of adults free of prevalent CVD. These findings are broadly consistent with recent reports that indicate only modest associations between perceived social support and integration with inflammation after accounting for perceived stress (McDade et al., 2006). There was modest evidence that the relationship between ESS and inflammation differed for men and women and by age. Among men, there was evidence to support the direct hypothesis of social support but only for CRP. In adjusted models there was evidence that high ESS buffered the association between high stress and CRP, but only for middle-age women. However, because these relationships were only observed with one of the three inflammatory markers examined, they should be interpreted with caution.
In fully-adjusted analyses, there was no evidence to support either the direct or buffering hypotheses for IL-6 or fibrinogen. The inconsistency in the relationships among ESS and the three inflammatory markers is noteworthy because it suggests that the association between social support and inflammation is not equivalent across physiologic systems. These markers were only moderately correlated, and each has different responsiveness to social stressors (Ranjit et al., 2007) and may be influenced by health behaviors, particularly smoking and obesity, to differing degrees (Ozbay, Fitterling, Charney, & Southwick, 2008; Piché et al., 2005).
These findings are somewhat consistent with previous reports suggesting that the relationship between social support and health differs for women and men over the life span (Akiyama & Antonucci, 1996; Loucks, Berkman, Gruenewald, & Seeman, 2006), but suggest that in adults free from major health problems such as CVD these differences are less pronounced. Several studies have reported gender differences in the associations between social integration with inflammatory markers (Ford et al., 2006; Loucks et al., 2006; Loucks et al., 2006) or measures of cardiovascular activity (Hughes, 2007). In particular, similar to our findings, several previous studies have found a direct association between measures of support or integration and inflammatory markers among men but not women. The reasons for this gender difference are unclear, although there is suggestive evidence that men and women differentially utilize social support as a coping strategy in the face of ongoing stress and may appraise stress differently (Chaplin, Hong, Bergquist, & Sinha, 2008; Gerin, Milner, Chawla, & Pickering, 1995; Unger, McAvay, Bruce, Berkman, & Seeman, 1999). Future research should work towards identifying the specific contexts and points in the life course in which gender differences in social support and health are expected to be most relevant.
The primary strength of this study is the sample composition and measures of inflammation. The MESA sample was free of CVD at baseline, thus reducing the likelihood that poor health status confounded the relationship between inflammation and support (i.e., individuals who report low support may do so because they have limited functioning due to health problems that are themselves associated with inflammation). Data on inflammatory markers were available on over 90% of the baseline sample and samples were collected using a standardized protocol in clinical settings.
The findings should be interpreted in light of the study limitations. Foremost, this study only explored the relationship between systemic inflammation and emotional social support, and it is possible that other aspects of social life, such as caregiving and social integration, which are also associated with morbidity and mortality, are more strongly associated with these markers. For example, a growing body of evidence suggests that perceived loneliness is associated with inflammatory markers (Hawkley & Cacioppo, 2003; Steptoe, Owen, Kunz-Ebrecht, & Brydon, 2004). These contrasting findings indicate that high levels of emotional social support cannot be conceptualized or treated as equivalent to low levels of loneliness (and vice versa) in terms of the relationship to physiology, despite similarities in these constructs. Also, other measures of social support, such as instrumental (i.e., assistance with specific tasks) or provision of support may also be more relevant to inflammation. In addition, the relatively high levels of ESS reported in the sample, and the relatively low variance in the inflammatory markers may have contributed to the failure to detect significant relationships. Finally, the measure of chronic stress may not have captured all meaningful aspects of the stress process that are relevant to health (e.g., we could not examine stress appraisal or coping, nor other aspects of stress exposure including daily hassles). The measure of chronic stress may be confounded with low ESS since some of the events included in this measure referenced social relationships, a salient limitation particularly in light of the cross-sectional nature of the study.
While the finding that ESS was generally not associated with inflammation, in either the directly or stress-buffering models, is surprising in light of the consistent epidemiologic relationships between social support and heath, these results indicate that other mechanisms may underlie the relationship between social support and health (Hawkley & Cacioppo, 2003; B. Uchino, 2006). For example, ESS may operate on health through other pathways such as improved access to services (i.e., having supportive ties may facilitate treatment seeking), through the relationship between ESS and health-related behaviors (i.e., smoking, diet, exercise), via psychological states such as depression, or through stress-linked biological mechanisms not involving inflammation. In addition, other dimensions of social life such as integration and isolation and perceived loneliness may be stronger predictors of inflammation (Ford et al., 2006; Seeman et al., 1994) than the ESS measure we studied.
Overall our results suggest that ESS is modestly associated with levels of CRP in men and that it may buffer the effects of stress in women. Given the large number of comparisons we performed these results need to be confirmed in other large samples. Consistently with prior work, these findings illustrate the utility of examining how factors such as gender and age influence the relationship between social life and health.
This research was supported by the Robert Wood Johnson Health and Society Scholars program and the Michigan Center for Integrative Approaches to Health Disparities, P60 MD002249 funded by the National Center on Minority Health and Health Disparities, and by contracts N01-HC-95159 through N01-HC-95169 from the National Heart, Lung, and Blood Institute. The authors thank the other investigators, the staff, and the participants of the MESA study for their valuable contributions.
List of Abbreviations
|BMI||Body mass index|
|ELISA||enzyme-linked immunosorbant assay|
|MESA||Multi-Ethnic Study of Atherosclerosis|
|NSAID||Non-steroidal anti-inflammatory drug|
|PSS||Perceived social support|
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Competing interests: All authors declare they have no conflicting interests.
- Ajrouch K, Blandon A, Antonucci TC. Social networks among men and women: The effects of age and socioeconomic status. J Gerontol Ser B Psychol Sci Soc Sci. 2005;60B:S311–S317.[PubMed]
- Akiyama H, Antonucci TC. Same-sex and cross-sex relationships. J Gerontol Ser B Psychol Sci Soc Svi. 1996;51:374–382.[PubMed]
- American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2006;29:S43–S48.[PubMed]
- Berkman LF, Blumenthal J, Burg M, Carney RM, Catellier D, Cowan MJ, et al. Effects of treating depression and low perceived social support on clinical events after myocardial infarction: The enhancing recovery in coronary heart disease patients (ENRICHD) randomized trial. JAMA. 2003;289:3106–3116.[PubMed]
- Bild DE, Bluemke DA, Burke GL, Detrano R, Diez Roux AV, Folsom AR, et al. Multi-ethnic study of atherosclerosis: Objectives and design. Am J Epidemiol. 2002;156:871–881.[PubMed]
- Bromberger JT, Matthews KA. A longitudinal study of the effects of pessimism, trait anxiety, and life stress on depressive symptoms in middle-aged women. Psychol Aging. 1996;11:207–213.[PubMed]
- Brummett B, Barefoot J, Siegler I, Clapp-Channing N, Lytle B, Bosworth H, et al. Characteristics of socially isolated patients with coronary artery disease who are at elevated risk for mortality. Psychosom Med. 2001;63:267–272.[PubMed]
- Chaplin TM, Hong K, Bergquist K, Sinha R. Gender differences in response to emotional stress: An assessment across subjective, behavioral, and physiological domains and relations to alcohol craving. Alcohol Clin Exp Res. 2008;32:1242–1250.[PMC free article][PubMed]
- Cohen S, Wills T. Stress, social support, and the buffering hypothesis. Psychol Bull. 1985;98:310–357.[PubMed]
- ENRICHDInvestigators. Enhancing recovery in coronary heart disease patients (ENRICHD): Study design and methods. Am Heart J. 2000;139:1–9.[PubMed]
- Ford ES, Loucks EB, Berkman LF. Social integration and concentrations of C-reactive protein among US adults. Ann Epidemiol. 2006;16:78–84.[PubMed]
- Frasure-Smith N, Lesperance F, Gravel G, Masson A, Juneau M, Talajic M, et al. Social support, depression, and mortality during the first year after myocardial infarction. Circulation. 2000;101:1919–1924.[PubMed]
- Gerin W, Milner D, Chawla S, Pickering T. Social support as a moderator of cardiovascular reactivity in women: A test of the direct effects and buffering hypotheses. Psychosom Med. 1995;57:16–22.[PubMed]
- Hawkley LC, Cacioppo JT. Loneliness and pathways to disease. Brain Behav Immun. 2003;17:98–105.[PubMed]
- Hughes B. Social support in ordinary life and laboratory measures of cardiovascular reactivity: Gender differences in habituation-sensitization. Ann Behav Med. 2007;34:166–176.[PubMed]
- Knox SS, Uvnas-Moberg K. Social isolation and cardiovascular disease: An atherosclerotic pathway? Psychoneuroendocrinology. 1998;23:877–890.[PubMed]
- Loucks EB, Berkman LF, Gruenewald TL, Seeman TE. Relation of social integration to inflammatory marker concentrations in men and women 70 to 79 years. Am J Cardiol. 2006;97:1010–1016.[PubMed]
- Loucks EB, Sullivan LM, D'Agostino RB, Larson MG, Berkman LF, Benjamin EJ. Social networks and inflammatory markers in the Framingham heart study. J Biosoc Sci. 2006;38:835–842.[PubMed]
- McDade TW, Hawkley LC, Cacioppo JT. Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: The Chicago health, aging, and social relations study. Psychosom Med. 2006;68:376–381.[PubMed]
- Mitchell PH, Powell L, Blumenthal J, Norten J, Ironson G, Pitula CR, et al. A short social support measure for patients recovering from myocardial infarction: The ENRICHD social support inventory. J Cardiopulm Rehabil. 2003;23:398–403.[PubMed]
- Moen P. The gendered life course. In: Binstock RH, George LK, editors. Handbook of aging: Social sciences. San Diego CA: Academic Press; 2001. pp. 176–196.
- Ozbay F, Fitterling H, Charney D, Southwick S. Social support and resilience to stress across the life span: A neurobiologic framework. Cur Psychiatry Rep. 2008;10:304–310.[PubMed]
- Piché ME, Lemieux S, Weisnagel SJ, Corneau L, Nadeau A, Bergeron J. Relation of high-sensitivity C-reactive protein, interleukin-6, tumor necrosis factor-alpha, and fibrinogen to abdominal adipose tissue, blood pressure, and cholesterol and triglyceride levels in healthy postmenopausal women. Am J Cardiol. 2005;96:92–97.[PubMed]
- Radloff L. The CES-D scale: a self-report depression scale for research in the general population. Applied Psychological Measurement. 1977;1:385–401.
- Ranjit N, Diez Roux AV, Shea S, Cushman M, Seeman T, Jackson S, et al. Psychosocial factors and inflammation in the multi-ethnic study of atherosclerosis. Arch Intern Med. 2007;167:174–181.[PubMed]
- Seeman T, Berkman LF, Blazer D, Rowe J. Social ties and support and neuroendocrine function: The MacArthur studies of successful aging. Ann Behav Med. 1994;16:95–106.
- Seeman TE, Crimmins E. Social environment effects on health and aging; Integrating epidemiologic and demographic approaches and perspectives. Ann NY Acad Sci. 2001;954:88–117.[PubMed]
- Steptoe A, Owen N, Kunz-Ebrecht SR, Brydon L. Loneliness and neuroendocrine, cardiovascular, and inflammatory stress responses in middle-aged men and women. Psychoneuroendocrinology. 2004;29:593–611.[PubMed]
- Uchino B. Social support and health: A review of physiological processes potentially underlying links to disease outcomes. J Behav Med. 2006;29:377–387.[PubMed]
- Uchino BN, Holt-Lunstad J, Uno D, Betancourt R, Garvey TS. Social support and age-related differences in cardiovascular function: An examination of potential mediators. Ann Behav Med. 1999;21(2):135–142.[PubMed]
- Unger JB, McAvay G, Bruce ML, Berkman LF, Seeman T. Variation in the impact of social network characteristics on physical functioning in elderly persons: MacArthur studies of successful aging. J Gerontol Ser B Psychol Sci Soc Sci. 1999;54B:S245–S251.[PubMed]