Affirmed by published opinion. Judge WILKINS wrote the opinion, in which Judge WILLIAMS and Judge LEE joined.
WILKINS, Circuit Judge:
James Curtis and Connie Rena Westberry brought this action against Gislaved Gummi AB (GGAB), claiming that GGAB was liable under South Carolina law for damages the Westberrys suffered as a result of the company's failure to warn of the danger of the talcum powder (talc) lubricant GGAB placed on rubber gaskets it
GGAB manufactured rubber products, including rubber gaskets used in window frames. Westberry's employer purchased gaskets produced by GGAB for use in manufacturing skylights and windows in the Greenwood, South Carolina plant where Westberry was employed. Because the rubber gaskets were difficult to handle without a protective lubricant, GGAB applied a coating of talc to the gaskets prior to shipping.
Westberry's first duties in the plant involved working on a production line adjacent to the area where the GGAB gaskets were cut. In January 1994, he changed to the position of gasket cutter, which required him to remove the gaskets from their boxes and to place them in the cutting machine. Although the evidence was conflicting, Westberry testified that these duties brought him into contact with high concentrations of airborne talc. Westberry received no warning that talc could be dangerous, and he wore no protective gear when performing his duties as a gasket cutter.
Following his change to the position of gasket cutter, Westberry began to experience unrelenting sinus problems. He was hospitalized for four days in July 1994 with a severe sinus infection and was treated with antibiotics by his physician, Dr. W. David Isenhower, Jr. Beginning in September 1994, Westberry underwent several sinus surgeries in an attempt to alleviate his sinus pain, including a procedure in which his frontal sinuses were obliterated.
Westberry brought the present action against GGAB, claiming that its failure to warn him of the dangers of breathing airborne talc proximately caused the aggravation of his pre-existing sinus condition. He alleged causes of action sounding in strict liability, breach of warranty, and negligence. Following a trial at which Westberry's treating physician, Dr. Isenhower, provided the principal evidence of causation, the jury returned a verdict in favor of Westberry. Although GGAB challenges the judgment on a number of grounds, the only one warranting extended discussion is its contention that the district court abused its discretion in admitting the opinion testimony of Dr. Isenhower concerning the cause of Westberry's sinus problems.
The introduction of expert opinion testimony is governed by Federal Rule of Evidence 702, which provides:
Expert testimony is admissible under Rule 702, then, if it concerns (1) scientific, technical, or other specialized knowledge that (2) will aid the jury or other trier of fact to understand or resolve a fact at issue. See Daubert v. Merrell Dow Pharms., Inc., 509 U.S. 579, 592, 113 S.Ct. 2786, 125 L.Ed.2d 469 (1993). The first prong of this inquiry necessitates an examination of whether the reasoning or methodology underlying the expert's proffered opinion is reliable—that is, whether it is supported by adequate validation to render it trustworthy. See id. at 590 & n. 9, 113 S.Ct. 2786. The second prong of the inquiry requires an analysis of whether the opinion is relevant to the facts at issue. See id. at 591-92, 113 S.Ct. 2786. Thus, an expert's testimony is admissible under Rule 702 if it "rests on a reliable foundation and is relevant." Kumho Tire Co. v. Carmichael, ___ U.S.
A district court considering the admissibility of expert testimony exercises a gate keeping function to assess whether the proffered evidence is sufficiently reliable and relevant. See id. at 1174. The inquiry to be undertaken by the district court is "a flexible one" focusing on the "principles and methodology" employed by the expert, not on the conclusions reached. Daubert, 509 U.S. at 594-95, 113 S.Ct. 2786. In making its initial determination of whether proffered testimony is sufficiently reliable, the court has broad latitude to consider whatever factors bearing on validity that the court finds to be useful; the particular factors will depend upon the unique circumstances of the expert testimony involved. See Kumho Tire Co., 119 S.Ct. at 1175-76.
This court reviews the decision of a district court to admit or exclude evidence for an abuse of discretion. See General Elec. Co. v. Joiner, 522 U.S. 136, 139, 118 S.Ct. 512, 139 L.Ed.2d 508 (1997). A district court abuses its discretion if its conclusion is guided by erroneous legal principles, see Koon v. United States, 518 U.S. 81, 100, 116 S.Ct. 2035, 135 L.Ed.2d 392 (1996), or rests upon a clearly erroneous factual finding, see United States v. Barber, 119 F.3d 276, 283(4th Cir.) (en banc), cert. denied, ___ U.S. ___, 118 S.Ct. 457, 139 L.Ed.2d 391 (1997). Further, even if a district court applies the correct legal principles to adequately supported facts, the discretion of the trial court is not boundless and subject to automatic affirmance. See Wilson v. Volkswagen of Am., Inc., 561 F.2d 494, 506 (4th Cir.1977) (noting "that an appellate court would be remiss in [its] duties if [it] chose only to rubber stamp . . . orders of lower courts" (internal quotation marks omitted) (first & second alterations in original)). This court is obligated to review the record and reasons offered by the district court and to reverse if the "court has a definite and firm conviction that the court below committed a clear error of judgment in the conclusion it reached upon a weighing of the relevant factors." Id. With these principles in mind, we turn to a consideration of the decision of the district court to permit Dr. Isenhower to testify that in his opinion the sinus problems experienced by Westberry were caused by the inhalation of airborne talc in the workplace.
GGAB argues that the district court erred in failing to undertake a determination of the reliability and relevance of the evidence as required by Rule 702 because it believed such an analysis was applicable only to novel scientific opinions. We agree. As the Supreme Court recently made clear, the obligation of a district court to determine whether expert testimony is reliable and relevant prior to admission applies to all expert testimony. See Kumho Tire Co., 119 S.Ct. at 1174. Nevertheless, because we can affirm the evidentiary ruling of the district court on a ground different from that employed below, we consider whether Dr. Isenhower's testimony was sufficiently reliable and relevant to warrant admission. See Dorsey, 45 F.3d at 814 (concluding that decision of district court to exclude expert testimony was proper despite failure of district court to conduct analysis of reliability and relevance required by Rule 702).
GGAB contends that Dr. Isenhower's testimony was inadmissible because it was not based on reliable scientific methodology. This is so, it argues, because Dr. Isenhower had no epidemiological studies, no peer-reviewed published studies, no animal studies, and no laboratory data to support a conclusion that the inhalation of talc caused Westberry's sinus disease. Further, GGAB continues, Dr. Isenhower did not have any tissue samples indicating that talc was found in Westberry's sinuses, nor did he have studies showing that talc, at any threshold level, causes sinus disease. Instead, Dr. Isenhower merely relied on a differential diagnosis— supported in part by the temporal relationship between Westberry's exposure to talc and the problems he experienced with his sinuses—in reaching the conclusion that Westberry's sinus problems were caused by his exposure to talc from GGAB's gaskets. GGAB maintains that neither a differential diagnosis nor a temporal relationship between exposure and onset or worsening of symptoms is sufficient to establish the reliability of Dr. Isenhower's opinion. We disagree.
Differential diagnosis, or differential etiology, is a standard scientific technique of identifying the cause of a medical problem by eliminating the likely causes until the most probable one is isolated. See Baker v. Dalkon Shield Claimants Trust, 156 F.3d 248, 252-53 (1st Cir.1998). A reliable differential diagnosis typically, though not invariably, is performed after "physical examinations, the taking of medical histories, and the review of clinical tests, including laboratory tests," and generally is accomplished by determining the possible causes for the patient's symptoms and then eliminating each of these potential causes until reaching one that cannot be ruled out or determining which of those that cannot be excluded is the most likely. Kannankeril v. Terminix Int'l, Inc., 128 F.3d 802, 807 (3d Cir.1997) (explaining that "[d]ifferential diagnosis is defined for physicians as `the determination of which of two or more diseases with similar symptoms is the one from which the patient is suffering, by a systematic comparison and contrasting of the clinical findings'") (quoting Stedman's Medical Dictionary 428 (25th ed.1990)); see McCullock v. H.B. Fuller Co., 61 F.3d 1038, 1044 (2d Cir. 1995) (describing differential etiology as an analysis "which requires listing possible causes, then eliminating all causes but one"); Glaser v. Thompson Med. Co., 32 F.3d 969, 978 (6th Cir.1994) (recognizing that differential diagnosis is "a standard diagnostic tool used by medical professionals to diagnose the most likely cause or causes of illness, injury and disease"). This technique "has widespread acceptance in the medical community, has been subject to peer review, and does not frequently lead to incorrect results." Brown v. Southeastern Penn. Transp. Auth. (In re Paoli R.R. Yard PCB Litig.), 35 F.3d 717, 758 (3d Cir.1994); see Heller v. Shaw Indus., Inc., 167 F.3d 146, 154-55 (3d Cir.
GGAB next maintains that, assuming a differential diagnosis may provide a trustworthy foundation for an opinion on causation, Dr. Isenhower's differential diagnosis did not. According to GGAB, Dr. Isenhower's differential diagnosis was unreliable because he could not "rule in" talc as a possible cause of sinus disease. See Raynor v. Merrell Pharms., Inc., 104 F.3d 1371, 1374-76 (D.C.Cir.1997) (holding that expert opinion that exposure to Bendectin caused birth defects based in part on differential diagnosis was not admissible in light of "overwhelming body of contradictory epidemiological evidence" (internal quotation marks omitted)). Further, GGAB contends that Dr. Isenhower's differential diagnosis was not reliable because he failed to "rule out" all other possible causes.
GGAB asserts that Dr. Isenhower could not "rule in" talc because he had no means of accurately assessing what level of exposure was adequate to produce the sinus irritation Westberry experienced. In order to carry the burden of proving a plaintiff's injury was caused by exposure to a specified substance, the "plaintiff must demonstrate `the levels of exposure that are hazardous to human beings generally as well as the plaintiff's actual level of exposure.'" Mitchell v. Gencorp Inc., 165 F.3d 778, 781 (10th Cir.1999) (quoting Wright v. Willamette Indus., Inc., 91 F.3d 1105, 1106 (8th Cir.1996)); see Allen v. Pennsylvania Eng'g Corp., 102 F.3d 194, 199 (5th Cir.1996) (concluding that "[s]cientific knowledge of the harmful level of exposure to a chemical, plus knowledge that the plaintiff was exposed to such quantities, are minimal facts necessary to sustain the plaintiffs' burden in a toxic tort case"); cf. Black v. Food Lion, Inc., 171 F.3d 308,
Federal Judicial Center, Reference Manual on Scientific Evidence 187 (1994). Consequently, while precise information concerning the exposure necessary to cause specific harm to humans and exact details pertaining to the plaintiff's exposure are beneficial, such evidence is not always available, or necessary, to demonstrate that a substance is toxic to humans given substantial exposure and need not invariably provide the basis for an expert's opinion on causation. See Heller, 167 F.3d at 157 (noting "that even absent hard evidence of the level of exposure to the chemical in question, a medical expert could offer an opinion that the chemical caused plaintiff's illness").
Although GGAB is correct that Dr. Isenhower had no scientific literature on which to rely to "rule in" talc as a possible basis for Westberry's sinus condition, it was undisputed that inhalation of high levels of talc irritates mucous membranes.
Additionally, Dr. Isenhower testified that he relied in part on the temporal proximity of Westberry's exposure to talc in his workplace to the onset and worsening of Westberry's sinus problems to conclude that talc was the cause. GGAB makes no serious argument that a strong temporal relationship between Westberry's exposure to talc and his sinus disease did not exist, but contends that the temporal relationship between Westberry's exposure to talc and his sinus problems was not a proper basis for an expert opinion on causation. Again, we disagree.
Of course, the mere fact that two events correspond in time does not mean that the two necessarily are related in any causative fashion. See Heller, 167 F.3d at 154. But, depending on the circumstances, a temporal relationship between exposure to a substance and the onset of a disease or a worsening of symptoms can provide compelling evidence of causation. See id.; Zuchowicz, 140 F.3d at 385, 390; Cavallo v. Star Enter., 892 F.Supp. 756, 774 (E.D.Va.1995) (explaining that "there may be instances where the temporal connection between exposure to a given chemical and subsequent injury is so compelling as to dispense with the need for reliance on standard methods of toxicology," for example, if one were exposed to a substantial amount of "chemical X and immediately thereafter developed symptom Y"); see also 2 Stephen A. Saltzburg et al., Federal Rules of Evidence Manual 1233-34 (7th ed.1998). But see Moore, 151 F.3d at 278 (holding that "[i]n the absence of an established scientific connection between exposure and illness, or compelling circumstances such as those discussed in Cavallo, the temporal connection between exposure to chemicals and an onset of symptoms, standing alone, is entitled to little weight").
Here, Dr. Isenhower testified that Westberry's sinus disease began shortly after Westberry began working as a gasket cutter. Furthermore, during the time he was treating Westberry, Dr. Isenhower experimented with keeping Westberry out of work and noticed that his sinus condition improved when he was not working but worsened when he returned. Under these circumstances, we conclude that the temporal relationship between Westberry's exposure and the onset and worsening of his sinus disease provided support for Dr. Isenhower's opinion that talc was the source of the problem.
GGAB also argues that Dr. Isenhower's differential diagnosis was unreliable because he failed to "rule out" all potential causes other than talc because he did not explain why a cold Westberry developed in May 1994 and water skiing he did over the summer of 1994 could not have accounted for his sinus problems. A differential diagnosis that fails to take serious account of other potential causes may be so lacking that it cannot provide a reliable basis for an opinion on causation. See In re Paoli R.R. Yard PCB Litig., 35 F.3d at 758-61. However, "[a] medical expert's causation conclusion should not be excluded because he or she has failed to rule out every possible alternative cause of a plaintiff's illness." Heller, 167 F.3d at 156. The alternative causes suggested by a defendant "affect the weight that the jury should give the expert's testimony and not the admissibility of that testimony," id. at 157, unless the expert can offer "no explanation for why she has concluded [an alternative cause offered by the opposing party] was not the sole cause," id. at 156. See also Kannankeril, 128 F.3d at 808 (explaining that "[i]n attacking the differential diagnosis performed by the plaintiff's expert, the defendant may point to a plausible cause of the plaintiff's illness other than the defendant's actions" and "[i]t
Dr. Isenhower's testimony made clear that he considered and excluded other potential causes for Westberry's sinus disease. Furthermore, on cross-examination Dr. Isenhower explained why he did not believe that the cold Westberry developed in 1994 or the waterskiing he did over that summer accounted for his sinus problems. Accordingly, Dr. Isenhower's alleged failure to account for all possible alternative causes for Westberry's sinus problems did not prohibit the admissibility of his opinion as to causation.
In sum, we reject GGAB's contention that Dr. Isenhower's testimony was invalid and untrustworthy. A reliable differential diagnosis provides a valid basis for an expert opinion on causation. And, Dr. Isenhower's differential diagnosis was sufficiently reliable. Because Dr. Isenhower's testimony satisfied the reliability and relevance standards of Rule 702, the district court properly admitted this testimony.